TAG REMOVAL FROM PROTEINS EXPRESSED IN PRO- AND EUKARYOTIC HOSTS

20180195056 ยท 2018-07-12

Assignee

Inventors

Cpc classification

International classification

Abstract

The present invention belongs to the field of biotechnology. More specifically, the present invention provides a protease, a non-naturally occurring fusion protein comprising a corresponding protease recognition site, expression vectors encoding same, host cells comprising said expression vectors, kit of parts as well as methods applying the protease, fusion protein, and uses thereof, as defined in the claims. The presently disclosed protease/protease recognition site is particularly useful in methods requiring an orthogonal set of proteases, and is suitable for use in both prokaryotic and selected eukaryotic expression systems

Claims

1. A protease comprising an amino acid sequence with at least 80% identity over amino acids 25-384 of SEQ ID NO: 1 (xlAtg4B), with the proviso that the protease is not the protease of SEQ ID NO: 1, wherein said protease is capable of cleaving the protease recognition site (PRS) according to SEQ ID NO: 2 (xlLC3B) with at least 20% activity as compared to the parent protease with the amino acid sequence of SEQ ID NO: 1, if tested using a native substrate protein shown in SEQ ID NO: 3 (His.sub.14-xlLC3B-MBP) and 500 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT and/or wherein said protease is capable of cleaving the protease recognition site (PRS) according to SEQ ID NO: 4 (xlGATE16) with at least 20% activity as compared to the parent protease with the amino acid sequence of SEQ ID NO: 1, if tested using 500 nM of said protease and a native substrate protein shown in SEQ ID NO: 5 (His.sub.14-xlGATE16-MBP) at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

2. The protease of claim 1, wherein the protease comprises an amino acid sequence with at least 80% identity to amino acids 14-384 of SEQ ID NO: 1 (xlAtg4B).

3. The protease of claim 1 or 2, wherein the protease comprises an amino acid sequence with at least 80% identity over the full length of SEQ ID NO: 1 (xlAtg4B).

4. The protease of any one of claims 1-3, wherein the protease comprises the amino acid sequence of amino acids 25-384 of SEQ ID NO: 1 (xlAtg4B).

5. The protease of any one of claims 1-4, wherein the protease comprises the amino acid sequence of amino acids 14-384 of SEQ ID NO: 1 (xlAtg4B).

6. The protease of any one of claims 1-5, wherein the protease consists of the amino acid sequence of amino acids 14-384 of SEQ ID NO: 1 (xlAtg4B).

7. The protease of any one of claims 1-5, wherein the protease consists of the amino acid sequence of amino acids 25-384 of SEQ ID NO: 1 (xlAtg4B).

8. The protease of any one of claims 1-7, wherein the protease is capable of cleaving (i) at least 90% of a 100-fold, preferably 150-fold, more preferably 200-fold molar excess of a native substrate protein shown in SEQ ID NO: 3 (His.sub.14-xlLC3B-MBP); and/or (ii) at least 90% of a 150-fold, preferably 200-fold, more preferably 300-fold molar excess of a native substrate protein shown in SEQ ID NO: 5 (His.sub.14-xlGATE16-MBP); at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

9. The protease of any one of claims 1-8, wherein the protease is capable of cleaving (i) at least 90% of a 500-fold, preferably 1000-fold, more preferably 1500-fold, most preferably 2000-fold molar excess of a native substrate protein shown in SEQ ID NO: 3 (His.sub.14-xlLC3B-MBP); and/or (ii) at least 90% of a 2000-fold, preferably 3000-fold, more preferably 4000-fold, even more preferably 5000-fold, still more preferably 6000-fold, most preferably 6600-fold molar excess of a native substrate protein shown in SEQ ID NO: 5 (His.sub.i4-xlGATE16-MBP); at conditions of 1 hour incubation at 25 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

10. The protease of any one of claims 1-9, wherein the protease is capable of cleaving at least 90% of a 100-fold molar excess of native substrate protein variants in which only residue 152 in SEQ ID NO: 3 (the P.sub.1 position of His.sub.14-xlLC3B-MBP) has been mutated to Met, Tyr, Arg or Glu relative to SEQ ID NO: 3 at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

11. The protease of any one of claims 1-10, wherein the protease is capable of cleaving at least 50% of a 200-fold molar excess of a native substrate protein as shown in SEQ ID NO: 3 (His.sub.14-xlLC3B-MBP) within one hour at 0 C. at high-salt conditions of 100 M initial concentration of substrate protein in a buffer consisting of 1.5 M NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

12. The protease of any one of claims 1-11, wherein the protease cleaves at stringent conditions any of the substrates shown in SEQ ID NO: 6 (His.sub.10-ZZ-TEV-MBP), SEQ ID NO: 7 (His.sub.14-bdNEDD8-MBP), SEQ ID NO: 8 (His.sub.14-bdSUMO-MBP), SEQ ID NO: 9 (His.sub.14-xlUb-MBP), or SEQ ID NO: 22 (His.sub.14-SUMOstar-MBP) at least 10 000 fold less efficiently than the substrate shown in SEQ ID NO: 3 (His.sub.14-xlLC3B-MBP), wherein stringent conditions are defined as 3 hour incubation at 25 C., 20 M protease, 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

13. The protease of any one of claims 1-12, wherein the protease, if the protease does not comprise a polyHis-tag, is capable of cleaving a substrate protein as shown in SEQ ID NO: 25 (His.sub.14-IF2d1-xlLC3B-MBP) immobilized on a Ni(II) chelate resin with at least 10% efficiency as compared to the non-immobilised substrate at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

14. The protease of any one of claims 1-13, wherein the protease retains at least 50% of its activity when pre-incubated for 16 h at 42 C. in the absence of oxygen in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 20 mM DTT, as compared to said non-treated protease, if tested using a native substrate protein shown in SEQ ID NO: 3 (His.sub.14-xlLC3B-MBP) and 500 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

15. The protease of any one of claims 1-14, wherein the protease further comprises an affinity tag, preferably a poly-His tag, a MBP-tag or a ZZ-tag.

16. A non-naturally occurring fusion protein, comprising a protease recognition site (PRS), which PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 2 (xlLC3B); or (ii) a derivative of (i) with an amino acid sequence having at least 75% identity over the full length of SEQ ID NO: 2 (xlLC3B), wherein the protease shown in SEQ ID NO: 1 (xlAtg4B) is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the amino acid sequence of SEQ ID NO: 2 (xlLC3B), under identical conditions of 1 hour incubation at 0 C., 500 nM protease, 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

17. A non-naturally occurring fusion protein, comprising a protease recognition site (PRS), which PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 4 (xlGATE16); or (ii) a derivative of (i) with an amino acid sequence having at least 75% identity over the full length of SEQ ID NO: 4 (xlGATE16), wherein the protease shown in SEQ ID NO: 1 (xlAtg4B) is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the amino acid sequence of SEQ ID NO: 4 (xlGATE16), under identical conditions of 1 hour incubation at 0 C., 200 nM protease, 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

18. The fusion protein of claim 16 or 17, further comprising an affinity tag, wherein the affinity tag is located in the fusion so that it is cleaved off if the fusion protein is incubated with the protease shown in SEQ ID NO: 1 (xlAtg4B), preferably wherein the affinity tag is N-terminal from the PRS.

19. An expression vector, comprising a multiple cloning site in functional linkage with a nucleic acid sequence encoding the protease recognition site as defined in claim 16 or 17.

20. The expression vector of claim 19, wherein the nucleic acid sequence further encodes an affinity tag as defined in claim 18.

21. An expression vector, comprising a nucleic acid sequence encoding the fusion protein according to any one of claims 16-18.

22. A host cell, comprising an expression vector according to any one of claims 19-21.

23. The host cell of claim 22, wherein the host cell is a eukaryotic host cell, wherein the eukaryotic cell is a fungal cell, or a plant cell.

24. The host cell of claim 23, wherein the host cell is a fungal cell, preferably a yeast cell, more preferably wherein the cell is of the genus Saccharomyces, even more preferably wherein the host cell is a cell of Saccharomyces cerevisiae.

25. The host cell of claim 23, wherein the host cell is a plant cell, preferably wherein said plant cell is a cell of the order Poales, more preferably wherein said cell is of the family Poaceae, even more preferably wherein said cell is of the subfamily Pooideae, still more preferably wherein said cell is of the tribe Triticeae, and most preferably, wherein said cell is of the genus Triticum.

26. The host cell of claim 22, wherein the host cell is a cell of E. coli.

27. The host cell of any one of claims 22-26, wherein the host cell further expresses a protease as defined in any one of claims 1-15.

28. Use of the protease according to any one of claims 1-15 for removing a protein tag, preferably wherein the protein tag is an affinity tag.

29. The use of claim 28, wherein the protease is used for on-column cleavage in an affinity chromatographic purification step.

30. Use of an expression vector according to claims 19-21 or of a host cell according to any one of claims 22-26 in the production of a fusion protein in a eukaryotic expression system.

31. A method for purifying a stoichiometric protein complex composed of at least two subunits from a mixture, said mixture comprising said protein complex and monomers of said at least two subunits, wherein said at least two subunits comprised in said mixture each comprise an N-terminal affinity tag (AT) separated from the subunit by a protease recognition site (PRS), wherein the ATs of each of said at least two subunits differ from each other and allow affinity chromatography being selective for each AT, and wherein the PRS of each of said at least two subunits is cleavable by a protease, which protease is orthogonal to the PRS of the other subunit(s), wherein the method comprises the steps of a) subjecting the mixture to a first affinity chromatography selective for the AT of the first of said at least two subunits, whereby (i) the protein complex binds to the affinity resin via the AT of the first subunit, and (ii) impurities are washed off the column, and (iii) the protein complex is eluted from the column and the AT of the first subunit is cleaved off, or the protein complex is eluted by on-column cleavage, using said orthogonal protease which is specific for the PRS of said first subunit, and (iv) optionally removing the cleaved off AT of the first subunit; and b) subjecting the eluate from step a) to a second affinity chromatography selective for the AT of the second of said at least two subunits, whereby (i) the protein complex binds to the affinity resin via the AT of the second subunit, and (ii) impurities are washed off the column, and (iii) the protein complex is eluted from the column and the AT of the second subunit is cleaved off, or the protein complex is eluted by on-column cleavage, using said orthogonal protease which is specific for the PRS of said second subunit, and (iv) optionally removing the cleaved off AT of the second subunit; characterized in that one PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 2 (xlLC3B); or (ii) a derivative of (i) with an amino acid sequence having at least 75% identity over the full length of SEQ ID NO: 2 (xlLC3B), wherein the protease shown in SEQ ID NO: 1 (xlAtg4B) is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the amino acid sequence of SEQ ID NO: 2 (xlLC3B), under identical conditions of 500 nM protease, 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; or (i) an amino acid sequence as shown in SEQ ID NO: 4 (xlGATE16); or (ii) a derivative of (i) with an amino acid sequence having at least 75% identity over the full length of SEQ ID NO: 4 (xlGATE16), wherein the protease shown in SEQ ID NO: 1 (xlAtg4B) is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the amino acid sequence of SEQ ID NO: 4 (xlGATE16), under identical conditions of 200 nM protease, 1 hour incubation at 0 C., 100 M io initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; and wherein the AT of the subunit comprising said PRS is cleaved off using a protease according to any one of claims 1-15.

32. The method of claim 31, wherein one PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 2 (xlLC3B); or (ii) a derivative of (i) with an amino acid sequence having at least 75% identity over the full length of SEQ ID NO: 2 (xlLC3B), wherein the protease shown in SEQ ID NO: 1 (xlAtg4B) is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the amino acid sequence of SEQ ID NO: 2 (xlLC3B), under identical conditions of 500 nM protease, 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; preferably wherein one PRS comprises, more preferably consists of an amino acid sequence as shown in SEQ ID NO: 2 (xlLC3B).

33. The method of claim 31 or 32, wherein in step a) (iii) and/or step b) (iii) the protein complex is eluted by on-column cleavage.

34. The method of any one of claims 31-33, wherein the method further comprises the step of c) removing the protease from the eluate originating from the last affinity chromatography.

35. The method of any one of claims 31-34, wherein one PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 9 (bdSUMO); or (ii) a PRS derivative of (i) with an amino acid sequence having at least 60% identity over the full length of SEQ ID NO: 10 (bdSUMO), wherein the protease shown in SEQ ID NO: 11 (bdSENP1.sup.248-481) is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the parent PRS with the amino acid sequence of SEQ ID NO: 10, under identical conditions of 30 nM protease, 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; and wherein the AT of the subunit comprising said PRS is cleaved off using (i) a protease comprising, preferably consisting of the amino acid sequence shown in amino acids 1-224 of SEQ ID NO: 11 (bdSENP1.sup.248-481), or (ii) a protease derivative of (i) having an amino acid sequence with at least 45% identity over the full length of SEQ ID NO: 11, wherein said protease derivative is capable of cleaving the PRS according to ID NO: 10 (bdSUMO) with at least 20% activity as compared to the parent protease as defined in (i), if tested using a native substrate protein shown in SEQ ID NO: 8 (His.sub.ia-bdSUMO-MBP) and 30 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; preferably wherein the subunit is eluted from the column using (i) the protease shown in in amino acids 1-224 of SEQ ID NO: 11 (bdSENP1.sup.248-481).

36. The method of any one of claims 31-35, wherein one PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 12 (bdNEDD8); or (ii) a PRS derivative of (i) with an amino acid sequence having at least 85% identity over the full length of SEQ ID NO: 12, wherein the protease shown in SEQ ID NO: 13 (bdNEDP1) is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the parent PRS with the amino acid sequence of SEQ ID NO: 12 under identical conditions of 300 nM protease, 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; and wherein the AT of the subunit comprising said PRS is cleaved off using (i) a protease comprising, preferably consisting of the amino acid sequence shown in SEQ ID NO: 13 (bdNEDP1), or (ii) a protease derivative of (i) having an amino acid sequence with at least 35% identity over the full length of SEQ ID NO: 13 (bdNEDP1), wherein said protease derivative, cleaves the PRS according to SEQ ID NO: 12 (bdNEDD8) with at least 20% activity as compared to the parent protease as defined in (i), if tested using a native substrate protein shown in SEQ ID NO: 7 (His.sub.14-bdNEDD8-MBP) and 300 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; preferably wherein the subunit is eluted from the column using the protease comprising, preferably consisting of the amino acid sequence shown in SEQ ID NO: 13 (bdNEDP1).

37. The method of any one of claims 31-36, wherein at least one PRS comprises, preferably consists of the TEV protease recognition site shown in SEQ ID NO: 14; and wherein the AT of the subunit comprising said PRS is cleaved off using (i) a protease comprising, preferably consisting of the amino acid sequence shown in SEQ ID NO: 15 or 16 (TEV protease), or (ii) a protease derivative of (i) having an amino acid sequence with at least 80% identity over the full length of SEQ ID NO: 15 or 16, wherein said protease derivative is capable of cleaving the PRS according to SEQ ID NO: 14 (TEV) with at least 20% activity as compared to the parent protease as defined in (i), if tested using a native substrate protein shown in SEQ ID NO: 6 (His.sub.to-ZZ-TEV-MBP) and 10 M of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

38. The method of any one of claims 31-37, wherein at least one PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 17 (xlUb); or (ii) a PRS derivative of (i) with an amino acid sequence having at least 80% identity over the full length of SEQ ID NO: 17, wherein the protease shown in SEQ ID NO: 18 (xlUsp2), is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the parent PRS with the amino acid sequence of SEQ ID NO: 17 under identical conditions of 1 M protease, 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; and wherein the AT of the subunit comprising said PRS is cleaved off using (i) a protease comprising, preferably consisting of the amino acid sequence shown in SEQ ID NO: 18 (xlUsp2), or (ii) a protease derivative of (i) having an amino acid sequence with at least 80% identity over the full length of SEQ ID NO: 18, wherein said protease derivative is capable of cleaving the PRS according to ID NO: 17 (xlUb) with at least 20% activity as compared to the parent protease as defined in (i), if tested using a native substrate protein shown in SEQ ID NO: 9 (His.sub.14-xlUb-MBP) and 1 M of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

39. The method of any one of claims 31-38, wherein at least one PRS comprises, preferably consists of (i) an amino acid sequence as shown in SEQ ID NO: 23 (SUMOstar); or (ii) a PRS derivative of (i) with an amino acid sequence having at least 80% identity over the full length of SEQ ID NO: 23, wherein the protease shown in SEQ ID NO: 24 (SUMOstar protease), is capable of cleaving said PRS derivative with at least 20% activity as compared to when using the parent PRS with the amino acid sequence of SEQ ID NO: 23 under identical conditions of 30 nM protease, 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; and wherein the AT of the subunit comprising said PRS is cleaved off using (i) a protease comprising, preferably consisting of the amino acid sequence shown in SEQ ID NO: 24 (SUMOstar protease), or (ii) a protease derivative of (i) having an amino acid sequence with at least 80% identity over the full length of SEQ ID NO: 24, wherein said protease derivative is capable of cleaving the PRS according to ID NO: 23 (SUMOstar) with at least 20% activity as compared to the parent protease as defined in (i), if tested using a native substrate protein shown in SEQ ID NO: 22 (His.sub.14-SUMOstar-MBP) and 30 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT.

40. The method of any one of claims 31-39, wherein the protein complex is composed of 2 different subunits, preferably with a stoichiometry of 1:1; or wherein the protein complex is composed of 3 different subunits, preferably with a stoichiometry of 1:1:1; or wherein the protein complex is composed of 4 different subunits, preferably with a stoichiometry of 1:1:1:1.

41. The method of any one of claims 31-40, wherein the mixture originates from a suitable fungal expression host cell, preferably wherein the host cell is a yeast cell, more preferably wherein the cell is of the genus Saccharomyces, most preferably wherein the host cell is a cell of Saccharomyces cerevisiae.

42. The method of claim 41, wherein one subunit comprises the PRS xlLC3B or a PRS derivative thereof as defined in claim 31, and wherein the elution is carried out using the protease as defined in claim 31; and wherein the other subunit comprises the PRS bdNEDD8 or a PRS derivative thereof as defined in claim 36 and wherein the elution is carried out using the protease as defined in claim 36.

43. The method of claim 41, wherein one subunit comprises the PRS xlLC3B or a PRS derivative thereof as defined in claim 31, and wherein the elution is carried out using the protease as defined in claim 31; and wherein the other subunit comprises the PRS SUMOstar or a PRS derivative thereof as defined in claim 39 and wherein the elution is carried out using the protease as defined in claim 39.

44. The method of claim 41, wherein one subunit comprises the PRS xlLC3B or a PRS derivative thereof as defined in claim 31, and wherein the elution is carried out using the protease as defined in claim 31; wherein a second subunit comprises the PRS bdNEDD8 or a PRS derivative thereof as defined in claim 36 and wherein the elution is carried out using the protease as defined in claim 36; and wherein a third subunit comprises the PRS SUMOstar or a PRS derivative thereof as defined in claim 39 and wherein the elution is carried out using the protease as defined in claim 39.

45. The method of any one of claims 31-40, wherein the mixture originates from a suitable plant expression host cell, preferably wherein said plant cell is a cell of the order Poales, more preferably wherein said cell is of the family Poaceae, even more preferably wherein said cell is of the subfamily Pooideae, still more preferably wherein said cell is of the tribe Triticeae, and most preferably, wherein said cell is of the genus Triticum.

46. The method of claim 45, wherein one subunit comprises the PRS or a PRS derivative thereof as defined in claim 31 or 32, and wherein the elution is carried out using the protease as defined in claim 31; and wherein the other subunit comprises the PRS SUMOstar or a PRS derivative thereof as defined in claim 39 and wherein the elution is carried out using the protease as defined in claim 39.

47. The method of any one of claims 31-46, wherein the one subunit comprises a poly-His tag, and preferably wherein the other subunit comprises a ZZ tag.

48. The method of any one of claims 31-47, wherein the mixture originates from a single lysate or supernatant or a pre-purified solution comprising all subunits of the protein complex.

49. The method of any one of claims 31-48, wherein the mixture originates from a mixture of lysates and/or supernatants and/or pre-purified solutions.

50. The method of any one of claims 31-49, wherein step c) is an affinity chromatography, a size exclusion chromatography, or a precipitation step.

51. The method of any one of claims 31-50, wherein the protease from the eluate originating from the last affinity chromatography prior to step c) comprises an affinity tag, preferably a poly-His tag or a ZZ tag, and wherein step c) is an affinity chromatography step, whereby the protease binds to the affinity resin, and the protein complex is collected in the flow-through.

52. The method of any one of claims 31-51, wherein the subunit(s) further comprise a spacer between the AT and the PRS, and/or between the PRS and the subunit; preferably wherein the subunit(s) further comprise a spacer between the AT and the PRS.

53. A kit of parts, comprising (i) the protease according to any one of claims 1-15, and (ii) an expression vector according to any one of claims 19-21 or a host cell according to any one of claims 22-27.

54. A kit of parts, comprising (i) the protease according to any one of claims 1-15, and at least one protease selected from the group of proteases consisting of (ii) a protease having an amino acid sequence with at least 45% identity over the full length of SEQ ID NO: 11 (bdSENP1), wherein said protease is capable of cleaving the PRS according to ID NO: 10 (bdSUMO) with at least 20% activity as compared to the parent protease of SEQ ID NO: 10 (bdSENP1), if tested using a native substrate protein shown in SEQ ID NO: 8 (His.sub.u-bdSUMO-MBP) and 30 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; preferably wherein the protease comprises the amino acid sequence shown as amino acids 1-224 in SEQ ID NO: 11 (bdSENP1.sup.248-481); more preferably wherein the protease consists of the amino acid sequence shown as amino acids 1-224 in SEQ ID NO: 11 (bdSENP1.sup.248-481); (iii) a protease having an amino acid sequence with at least 35% identity over the full length of SEQ ID NO: 13 (bdNEDP1), wherein said protease cleaves the PRS according to SEQ ID NO: 12 (bdNEDD8) with at least 20% activity as compared to the parent protease of SEQ ID NO: 13 (bdNEDP1), if tested using a native substrate protein shown in SEQ ID NO: 7 (His.sub.14-bdNEDD8-MBP) and 300 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; preferably wherein the protease comprises the amino acid sequence as shown in SEQ ID NO: 13 (bdNEDP1); more preferably wherein the protease consists of the amino acid sequence as shown in SEQ ID NO: 13 (bdNEDP1); (iv) a protease having an amino acid sequence with at least 80% identity over the full length of SEQ ID NO: 15 or 16, wherein said protease is capable of cleaving the PRS according to SEQ ID NO: 14 (TEV) with at least 20% activity as compared to the parent protease of SEQ ID NO: 15 or 16, if tested using a native substrate protein shown in SEQ ID NO: 6 (His.sub.10-ZZ-TEV-MBP) and 10 M of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; preferably wherein the protease comprises the amino acid sequence as shown in SEQ ID NO: 15 or 16, more preferably wherein the protease consists of the amino acid sequence as shown in SEQ ID NO: 15 or 16; (v) a protease having an amino acid sequence with at least 80% identity over the full length of SEQ ID NO: 18 (xlUsp2), wherein said protease is capable of cleaving the PRS according to ID NO: 17 (xlUb) with at least 20% activity as compared to the parent protease of SEQ ID NO: 18 (xlUsp2), if tested using a native substrate protein shown in SEQ ID NO: 9 (His.sub.14-xlUb-MBP) and 1 M of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT. preferably wherein the protease comprises the amino acid sequence as shown in SEQ ID NO: 18 (xlUsp2); more preferably wherein the protease consists of the amino acid sequence as shown in SEQ ID NO: 18 (xlUsp2); (vi) a protease having an amino acid sequence with at least 80% identity over the full length of SEQ ID NO: 24 (SUMOstar protease), wherein said protease is capable of cleaving the PRS according to ID NO: 23 (SUMOstar) with at least 20% activity as compared to the parent protease as defined in (i), if tested using a native substrate protein shown in SEQ ID NO: 22 (His.sub.14-SUMOstar-MBP) and 30 nM of said protease at standard conditions of 1 hour incubation at 0 C., 100 M initial concentration of substrate protein in a buffer consisting of 250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT; preferably wherein the protease comprises the amino acid sequence as shown in SEQ ID NO: 24 (SUMOstar protease); more preferably wherein the protease consists of the amino acid sequence as shown in SEQ ID NO: 24 (SUMOstar protease).

55. The kit of parts of claim 54, wherein at least one protease further comprises an affinity tag, preferably a poly-His tag or a ZZ tag.

56. The kit of parts of claim 54 or 55, which comprises the proteases as defined in (i) and (ii).

57. The kit of parts of claim 54 or 55, which comprises the proteases as defined in (i) and (iii).

58. The kit of parts of claim 54 or 55, which comprises the proteases as defined in (i) and (vi).

59. Use of a kit of parts as defined in any one of claims 54-58 in a method of purifying stoichiometric protein complexes comprising at least two subunits, preferably wherein the method is further defined as in any one of claims 31-52.

60. Use of a kit of parts as defined in any one of claims 54-58 for on-column cleavage in an affinity chromatography.

61. Use of a kit of parts as defined in any one of claims 56-58 in a method of purifying stoichiometric protein complexes comprising at least two subunits from a mixture originating from a eukaryotic expression host cell, preferably wherein said eukaryotic cell is a fungal cell or plant cell.

62. The use of claim 61, wherein the host cell is a fungal cell, preferably wherein the host cell is a yeast cell, more preferably wherein the cell is of the genus Saccharomyces, most preferably wherein the host cell is a cell of Saccharomyces cerevisiae.

63. The use of claim 61, wherein the host cell is a plant cell, preferably wherein said plant cell is a cell of the order Poales, more preferably wherein said cell is of the family Poaceae, even more preferably wherein said cell is of the subfamily Pooideae, still more preferably wherein said cell is of the tribe Triticeae, and most preferably, wherein said cell is of the genus Triticum.

Description

DESCRIPTION OF THE FIGURES

[0195] FIG. 1: Alignment of human and Xenopus laevis Atg4, LC3 and GATE16 homologs. A, Phylogenetic tree of human (hs) and Xenopus laevis (xl) Atg4 homologs. The alignment is based on the ClustalW algorithm. Note that isoforms A to D can be clearly separated in both organisms. B, Sequence alignment of human and Xenopus laevis Atg4B homologs. Exchanges with regard to hsAtg4B are underlined. Boxed areas correspond to N- and C-terminal extensions based on the solved structures of human Atg4B (Kumanomidou, T., Mizushima, T., Komatsu, M., Suzuki, A., Tanida, I., Sou, Y. S., Ueno, T., Kominami, E., Tanaka, K. and Yamane, T. (2006) J Mol Biol 355, 612-618; Sugawara, K., Suzuki, N. N., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2005) J Biol Chem 280, 40058-40065; Satoo, K., Noda, N. N., Kumeta, H., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2009) EMBO J 28, 1341-1350). C, Phylogenetic tree of human and Xenopus laevis LC3 and GATE16 homologs. Note that GATE16 forms a separate branch and can be clearly separated from the LC3 isoforms. D and E, Sequence alignment of human and Xenopus laevis LC3B and GATE16 orthologs, respectively. Exchanges with regard to the human proteins are underlined. Mature human and Xenopus laevis GATE16 proteins share identical primary sequences.

[0196] FIG. 2: Expression level and solubility of His.sub.14-UBL-tagged GFP. Proteins sketched in (A) were over-expressed as described in the section Methods in the Examples section below from appropriate expression vectors in E. coli strain NEB Express for 16 h at 18 C. Equal amounts of resuspended cells, total lysate and soluble material were analyzed by SDS-PAGE (B). GFP present in the soluble fraction was quantified via its absorbance at 488 nm. Note that scAtg8 promotes significantly lower expression levels than the other UBLs.

[0197] FIG. 3: Purification of xlAtg4B protease fragments. A, Schematic illustration of expression constructs used for (B) and (C). B, Exemplary purification of xlAtg4B.sup.14-384. His.sub.14-TEV-xlAtg4B.sup.14-384 was over-expressed from an appropriate expression vector in E. coli strain NEB Express. After cell lysis and centrifugation, the soluble material was applied to a Ni.sup.2+ chelate resin. Bound proteins were eluted with imidazole and treated with polyHis-tagged TEV protease over night at 4 C. before loading on a Superdex 200 gel filtration column. The pooled peak fractions mainly containing cleaved xlAtg4B.sup.14-384 and TEV protease were subjected to a reverse Ni.sup.2+ chromatography step (rev. Ni.sup.2+). Here, the polyHis-tagged TEV protease bound to the resin while pure xlAtg4B.sup.14-384 was found in the non-bound fraction. Purification of other xlAtg4B fragments was done identically. The remaining degradation bands (*) are specific for protease fragments containing the full-length C-terminus. C, Purity of xlAtg4B protease fragments. 40 pmol (1.6 g) of purified protease fragments were analyzed by SDS-PAGE and Coomassie-staining.

[0198] FIG. 4: In-vitro assay for xlAtg4B activity. A, Schematic representation of the protease substrates xlLC3B-MBP (top) and xlGATE16-MBP (bottom). Both fusion proteins contain an N-terminal polyHis-tag, a protease recognition site (xlLC3B or xlGATE16) and MBP (E. coli maltose binding protein, MBP) as a model target protein. To ensure a comparable accessibility, the scissile bond is followed by the identical tri-peptide (AGT; Ala-Gly-Thr) in both substrate proteins. For simplicity, substrate names do not contain the polyHis-tag. B, Protease titration. The substrate xlLC3B-MBP (100 M) was incubated for 1 h at 0 C. (left) or 25 C. (right) in the presence of a defined concentrations of indicated proteases. Cleavage products were separated by SDS-PAGE and stained with Coomassie G250. Shown are full-length substrate proteins (fl) and the C-terminal cleavage products (ccp). C, Time course. 100 M of xlLC3B-MBP was incubated at 0 C. with 500 nM of indicated protease fragments. At indicated time points, aliquots were withdrawn and analyzed as described in (C). D and E, Protease titration and time course with the xlGATE16-MBP substrate were performed in parallel to the corresponding experiments described in (C) and (D).

[0199] FIG. 5: Salt sensitivity and temperature dependence. A, Salt sensitivity. 100 M of xlLC3B-MBP (left) or xlGATE16-MBP (right) were incubated for one hour at 0 C. with 500 nM protease fragments at NaCl concentrations ranging from 0.2 to 1.5 M. B, Temperature dependence. Indicated xlAtg4B fragments were incubated with 100 M of xlLC3B-MBP (left) or xlGATE16-MBP (right) for 1 h at defined temperatures. Note that in comparison to the xlGATE16-MBP substrate, twice as much protease was used for cleavage of the xlLC3B-MBP substrate.

[0200] FIG. 6: Substrate recognition. A, Cleavage efficiency at limiting substrate concentrations. The concentration of indicated protease fragments and the substrates xlLC3B-MBP (left) or xlGATE16-MBP (right) was titrated at constant protease: substrate ratio (1:1000 or 1:2000, respectively). After cleavage (1 h at 0 C.), a fraction of each reaction corresponding to 1.2 g (20 pmol) of substrate protein was analyzed by SDS-PAGE. Due to the different substrate concentrations, the absolute volume of the cleavage reaction analyzed by SDS-PAGE had to be adjusted accordingly. B, Competitive binding of xlAtg4B fragments to immobilized xlLC3B and xlGATE16. An equimolar mixture of full-length xlAtg4B and indicated fragments (10 M each) was incubated with immobilized xlLC3B or xlGATE16. A resin without bait protein (right panel) served as a specificity control. Bound proteins were analyzed by SDS-PAGE. xlAtg4B degradation products lacking parts of the C-terminal extension are marked with an asterisk (*) in the input fractions. Note that binding is markedly reduced for protease fragments harboring C-terminal deletions. The pull-down efficiency is generally higher when using xlLC3B instead of xlGATE16 as a prey.

[0201] FIG. 7: Thermal stability. A, Long-term temperature stability. xlAtg4B fragments were pre-incubated for 16 h at indicated temperatures in the presence of 20 mM DTT under argon to protect the active site cysteines from oxidation. The remaining activity was then assayed by treating 100 M of xlLC3B or xlGATE16 substrate with each protease for 1 h at 0 C. B, Thermal denaturation of xlAtg4B fragments followed by dynamic light scattering. C, Long-term DLS measurement of xlAtg4B.sup.25-384. DLS signals were acquired for 20 h while incubating xlAtg4B.sup.25-384 at 37 C. with protection from oxidation. Note that at this temperature the protease appears rather stable for 2 h. At longer incubation, a gradual increase in average particle size is observed, indicating slow denaturation and aggregate formation.

[0202] FIG. 8: P.sub.1 preference of xlAtg4B.sup.14-384. A, Protease substrates used to analyze the P.sub.1 preference of xlAtg4B.sup.14-384 follow the general outline shown in FIG. 4A. Here, however, the P.sub.1 position of the P.sub.1-P.sub.1 scissile bond had been mutated to the potentially non-preferred residues methionine (Met), tyrosine (Tyr), arginine (Arg), glutamic acid (Glu), or proline (Pro). B, Solution cleavage assay with P.sub.1 substrates sketched in (A). Bands marked with an asterisk (*) refer to the protease.

[0203] FIG. 9: On column cleavage using xlAtg4B.sup.14-384. A, Schematic representation of substrate proteins used in (B)-(E). The N-terminal domain of E. coli IF2 (IF2d1 (58, 59)) serves as a spacer. B and C, A silica-based Ni.sup.2+ chelate resin was pre-loaded with similar amounts of His.sub.14-bdNEDD8-mCherry and either His.sub.14-IF2d1-xLC3B-GFP (B) or His.sub.14-IF2d1-xlGATE16-GFP (C). 50 l aliquots were treated with indicated concentrations xlAtg4B.sup.14-384 for 1 h at 4 C. Control incubations were performed with 4 M bdNEDP1 or with buffer containing 400 mM imidazole. Resins and eluates were photographed while illuminated at 366 nm. GFP and mCherry in the eluate fractions were quantified via their specific absorption. Quantification results are given below the respective eluate fractions. D and E, Protein purification using on-column cleavage by xlAtg4B.sup.14-384. Indicated substrates were over-expressed from appropriate expression vectors in E. coli strain NEB Express. After lysis and ultracentrifugation, the soluble material was incubated with a Ni.sup.2+ chelate resin. The resin was washed and treated with 500 nM xlAtg4B.sup.14-384 at 4 C. At indicated time points, the concentration and purity of the released MBP was determined using the calculated absorption coefficient at 280 nm (OD.sub.280) and SDS-PAGE, respectively. Proteins remaining on the resin after 60 min were eluted by 500 mM imidazole. The time course of elution is shown in (D), the OD.sub.280 reading at 60 min elution time was set to 100%. Relevant steps of the purifications are shown in (E).

[0204] FIG. 10: In-vitro cross-reactivity with other tag cleaving proteases. A, Schematic representation of substrates used for (B) and (C). The TEV protease substrate contains an N-terminal His.sub.10-ZZ tag preceding the TEV protease recognition site. All other substrates follow the scheme described in FIG. 4A, the protease recognition site, however, is replaced by the respective ubiquitin-like protein (UBL). B, Cross-reactivity between recombinant tag-cleaving proteases. bd, Brachypodium distachyon; tr, Triticum aestivum (summer wheat). 100 M of indicated substrates were incubated with indicated proteases for 3 h at 25 C. in LS-S buffer. Bands marked with an asterisk (*) originate from the respective protease. C, Detailed titration analysis of cross-reactivity between Xenopus laevis (xl), S. cerevisiae (sc) and wheat (tr) Atg4 homologs. 100 M of indicated substrates were incubated with various concentrations of indicated proteases for 1 h at 25 C. in LS-S buffer.

[0205] FIG. 11: Stability of UBL fusions in eukaryotic lysates and in S. cerevisiae. A, Schematic representation of substrates used for (B). B, Stability of protease substrates in cell extracts. C, Schematic representation of substrates used expression in S. cerevisiae (D) harboring an N-terminal ZZ-tag, a ubiquitin-like protein (UBL) and a C-terminal Citrine. D, In-vivo stability of protease substrates in S. cerevisiae. Indicated protease substrates were over-expressed in a S. cerevisiae strain constitutively expressing H2B-CFP as described in the section Methods in the Examples section below. Total cell lysates were analyzed by Western blot with an antibody recognizing the ZZ-tag (upper panel) or both Citrine and CFP (middle panel), respectively. Equal loading was confirmed by staining the membrane after blotting (lower panel). Bands marked with an asterisk to (*) originate from ZZ-tagged proteins cross-reacting with the anti-Citrine/CFP antibody. E, Cleavage of UBL substrates in extracts and in S. cerevisiae. ++, highly efficient cleavage; +, cleavage; , traces cleaved; , no cleavage; n.d.: not determined; .sup.1 data not shown.

[0206] FIG. 12: One-step protein purification from S. cerevisiae. ZZ-UBL-Citrine is fusions sketched in (A) were over-expressed in S. cerevisiae as described in the section Methods in the Examples section below. Cells were lysed and the soluble material was incubated with an anti-ZZ affinity resin. After washing off non-bound material, highly pure Citrine was eluted by treatment with 0.1 M SUMOstar protease (B), 1 M xlAtg4B.sup.14-384 (C) or 1 M bdNEDD8 (D) for 1 h at 4 C. Material remaining on the resin was analyzed after elution with SDS sample buffer. The asterisk (*) denotes the full-length xlLC3B fusion protein. The filled circle (*) marks band partially corresponding to low levels of free Citrine originating from in-vivo cleavage of the respective SUMOstar and bdNEDD8 fusion proteins.

DESCRIPTION OF THE SEQUENCES

[0207]

TABLE-US-00002 (XenopuslaevisAtg4B(xlAtg4B)) SEQIDNO:1 MDAATLTYDTLRFADTPDFPETAEPVWVLGRKYSALTEKEQLLNDITSRL WFTYRRNFQAIGGTGPTSDTGWGCMLRCGQMIFAQALICRHVGRDWRWDK QKPKGEYLNILTAFLDKKDSYYSIHQIAQMGVGEGKYIGQWYGPNTVAQV LRKLAVFDQWSSIAVHIAMDNTVVVDEIRRLCRAGSGESSDAGALSNGYT GDSDPSCAQWKPLVLLIPLRLGLSEINEAYIETLKHCFMVPQSLGVIGGR PNSAHYFIGYVGDELIYLDPHTTQLSVEPSDCSFIEDESFHCQHPPCRMH VSEIDPSIAVGFFCSSQEDFEDWCQHIKKLSLSGGALPMFEVVDQLPLHL SNPDVLNLTPDSSDADRLDRFFDSEDEEFEILSL (XenopuslaevisLC3B(xlLC3B)) SEQIDNO:2 MPSEKTFKQRRSLEQRVEDVRLIREQHPTKIPVIIERYKGEKQLPVLDKT KFLVPDHVNMSELIKIIRRRLQLNSNQAFFLLVNGHSMVSVSTPISEVYE REKDEDGFLYMVYASQETFG (His.sub.14-xlLC3B-MBP) SEQIDNO:3 MSKHHHHSGHHHTGHHHHSGSHHHTGGSSGSESSEKTFKQRRSLEQRVED VRLIREQHPTKIPVIIERYKGEKQLPVLDKTKFLVPDHVNMSELIKIIRR RLQLNSNQAFFLLVNGHSMVSVSTPISEVYEREKDEDGFLYMVYASQETF GAGTKTEEGKLVIWINGDKGYNGLAEVGKKFEKDTGIKVTVEHPDKLEEK FPQVAATGDGPDIIFWAHDRFGGYAQSGLLAEITPDKAFQDKLYPFTWDA VRYNGKLIAYPIAVEALSLIYNKDLLPNPPKTWEEIPALDKELKAKGKSA LMFNLQEPYFTWPLIAADGGYAFKYENGKYDIKDVGVDNAGAKAGLTFLV DLIKNKHMNADTDYSIAEAAFNKGETAMTINGPWAWSNIDTSKVNYGVTV LPTFKGQPSKPFVGVLSAGINAASPNKELAKEFLENYLLTDEGLEAVNKD KPLGAVALKSYEEELAKDPRIAATMENAQKGEIMPNIPQMSAFWYAVRTA VINAASGRQTVDEALKDAQTNGTGC (XenopuslaevisGATE16(xlGATE16)) SEQIDNO:4 MKWMFKEDHSLEHRCVESAKIRAKYPDRVPVIVEKVSGSQIVDIDKRKYL VPSDITVAQFMWIIRKRIQLPSEKAIFLFVDKTVPQSSLTMGQLYEKEKD EDGFLYVAYSGENTFG (His.sub.14-xlGATE16-MBP) SEQIDNO:5 MSKHHHHSGHHHTGHHHHSGSHHHTGGSSGSESSMKWMFKEDHSLEHRCV ESAKIRAKYPDRVPVIVEKVSGSQIVDIDKRKYLVPSDITVAQFMWIIRK RIQLPSEKAIFLFVDKTVPQSSLTMGQLYEKEKDEDGFLYVAYSGENTFG AGTKTEEGKLVIWINGDKGYNGLAEVGKKFEKDTGIKVIVEHPDKLEEKF PQVAATGDGPDIIFWAHDRFGGYAQSGLLAEITPDKAFQDKLYPFTWDAV RYNGKLIAYPIAVEALSLIYNKDLLPNPPKTWEEIPALDKELKAKGKSAL MFNLQEPYFTWPLIAADGGYAFKYENGKYDIKDVGVDNAGAKAGLTFLVD LIKNKHMNADTDYSIAEAAFNKGETAMTINGPWAWSNIDTSKVNYGVTVL PTFKGQPSKPFVGVLSAGINAASPNKELAKEFLENYLLTDEGLEAVNKDK PLGAVALKSYEEELAKDPRIAATMENAQKGEIMPNIPQMSAFWYAVRTAV INAASGRQTVDEALKDAQTNGTGC (His.sub.10-ZZ-TEV-MBP) SEQIDNO:6 MHHHHHHHHHHGSNKFNKEQQNAFYEILHLPNLNEEQRNAFIQSLKDDPS QSANLLAEAKKLNDAQAPKVAMNKFNKEQQNAFYEILHLPNLNEEQRNAF IQSLKDDPSQSANLLAEAKKLNDAQAPKVAMSGENLYFQGTKTEEGKLVI WINGDKGYNGLAEVGKKFEKDTGIKVTVEHPDKLEEKFPQVAATGDGPDI IFWAHDRFGGYAQSGLLAEITPDKAFQDKLYPFTWDAVRYNGKLIAYPIA VEALSLIYNKDLLPNPPKTWEEIPALDKELKAKGKSALMFNLQEPYFTWP LIAADGGYAFKYENGKYDIKDVGVDNAGAKAGLTFLVDLIKNKHMNADTD YSIAEAAFNKGETAMTINGPWAWSNIDTSKVNYGVTVLPTFKGQPSKPFV GVLSAGINAASPNKELAKEFLENYLLTDEGLEAVNKDKPLGAVALKSYEE ELAKDPRIAATMENAQKGEIMPNIPQMSAFWYAVRTAVINAASGRQTVDE ALKDAQTNGTGC (His.sub.14-bdNEDD8-MBP) SEQIDNO:7 MSKHHHHSGHHHTGHHHHSGSHHHSGTMIKVKTLTGKEIEIDIEPTDTID RIKERVEEKEGIPPVQQRLIYAGKQLADDKTAKDYNIEGGSVLHLVLALR GGAGTKTEEGKLVIWINGDKGYNGLAEVGKKFEKDTGIKVTVEHPDKLEE KFPQVAATGDGPDIIFWAHDRFGGYAQSGLLAEITPDKAFQDKLYPFTWD AVRYNGKLIAYPIAVEALSLIYNKDLLPNPPKTVVEEIPALDKELKAKGK SALMFNLQEPYFTWPLIAADGGYAFKYENGKYDIKDVGVDNAGAKAGLTF LVDLIKNKHMNADTDYSIAEAAFNKGETAMTINGPWAWSNIDTSKVNYGV TVLPTFKGQPSKPFVGVLSAGINAASPNKELAKEFLENYLLTDEGLEAVN KDKPLGAVALKSYEEELAKDPRIAATMENAQKGEIMPNIPQMSAFWYAVR TAVINAASGRQTVDEALKDAQTNGTGC (His.sub.14-bdSUMO-MBP) SEQIDNO:8 MSKHHHHSGHHHTGHHHHSGSHHHSGSAAGGEEDKKPAGGEGGGAHINLK VKGQDGNEVFFRIKRSTQLKKLMNAYCDRQSVDMTAIAFLFDGRRLRAEQ TPDELEMEDGDEIDAMLHQTGGAGTKTEEGKLVIWINGDKGYNGLAEVGK KFEKDTGIKVTVEHPDKLEEKFPQVAATGDGPDIIFWAHDRFGGYAQSGL LAEITPDKAFQDKLYPFTWDAVRYNGKLIAYPIAVEALSLIYNKDLLPNP PKTWEEIPALDKELKAKGKSALMFNLQEPYFTWPLIAADGGYAFKYENGK YDIKDVGVDNAGAKAGLTFLVDLIKNKHMNADTDYSIAEAAFNKGETAMT INGPWAWSNIDTSKVNYGVTVLPTFKGQPSKPFVGVLSAGINAASPNKEL AKEFLENYLLTDEGLEAVNKDKPLGAVALKSYEEELAKDPRIAATMENAQ KGEIMPNIPQMSAFWYAVRTAVINAASGRQTVDEALKDAQTNGTGC (His.sub.14-xlUb-MBP) SEQIDNO:9 MSKHHHHSGHHHTGHHHHSGSHHHTGGSSGSESSMQIFVKTLTGKTITLE VEPSDTIENVKAKIQDKEGIPPDQQRLIFAGKQLEDGRTLSDYNIQKEST LHLVLRLRGGAGTKTEEGKLVIWINGDKGYNGLAEVGKKFEKDTGIKVTE HPDKLEEKFPQVAATGDGPDIIFWAHDRFGGYAQSGLLAEITPDKAFQDK LYPFTWDAVRYNGKLIAYPIAVEALSLIYNKDLLPNPPKTWEEIPALDKE LKAKGKSALMFNLQEPYFTWPLIAADGGYAFKYENGKYDIKDVGVDNAGA KAGLTFLVDLIKNKHMNADTDYSIAEAAFNKGETAMTINGPWAWSNIDTS KVNYGVTVLPTFKGQPSKPFVGVLSAGINAASPNKELAKEFLENYLLTDE GLEAVNKDKPLGAVALKSYEEELAKDPRIAATMENAQKGEIMPNIPQMSA FWYAVRTAVINAASGRQTVDEALKDAQTNGTGC (bdSUMOaminoacids21-97) SEQIDNO:10 HINLKVKGQDGNEVFFRIKRSTQLKKLMNAYCDRQSVDMTAIAFLFDGRR LRAEQTPDELEMEDGDEIDAMLHQTGG (bdSENP1aminoacids248-481) SEQIDNO:11 PFVPLTDEDEDNVRHALGGRKRSETLSVHEASNIVITREILQCLNDKEWL NDEVINLYLELLKERELREPNKFLKCHFFNTFFYKKLINGGYDYKSVRRW TTKRKLGYNLIDCDKIFVPIHKDVHWCLAVINIKEKKFQYLDSLGYMDMK ALRILAKYLVDEVKDKSGKQIDVHAWKQEGVQNLPLQENGWDCGMFMLKY IDFYSRDMELVFGQKHMSYFRRRTAKEILDLKAG (bdNEDD8;BrachypodiumdistachyonNEDD8) SEQIDNO:12 MIKVKTLTGKEIEIDIEPTDTIDRIKERVEEKEGIPPVQQRLIYAGKQLA DDKTAKDYNIEGGSVLHLVLALRGG (bdNEDP1;BrachypodiumdistachyonNEDP1) SEQIDNO:13 MDERVLSYGDVVLLRSDLAILRGPHFLNDRIIAFYLAHLSASFHGDGDLL LLPPSIPYLLSNLPDPESVAEPLCLASRRLVLLPVNDNPDASVANGGSHW TLLVLDAATTDPQAPRFVHHDSLRGSANAAAARRLARALTAGGAPLRFVE APTPTQRNGHDCGVYVLAVARAICGWWRSSRRRENQQGGGGDWFATMMEE VDAESVGAMRAELLQLIHRLIQDKEQEEEKKSKAGVEDTCGQ (TEVproteaserecognitionsite-spacerfusion(the spacerbeingunderlined);cf.FIG.10A) SEQIDNO:14 ENLYFQGT (TEVprotease;TobaccoetchvirusNlaprotease) SEQIDNO:15 GESLFKGPRDYNPISSTICHLTNESDGHTTSLYGIGFGPFIITNKHLFRR NNGTLLVQSLHGVFKVKNTTTLQQHLIDGRDMIIIRMPKDFPPFPQKLKF REPQREERICLVTINFQTKSMSSMVSDTSCTFPSSDGIFWKHWIQTKDGQ CGSPLVSTRDGFIVGIHSASNFTNTNNYFTSVPKNFMELLTNQEAQQWVS GWRLNADSVLWGGHKVFMSKPEEPFQPVKEATQLMNELVYSQ (TEV(SH)C6) SEQIDNO:16 ESLFKGPRDYNPISSSICHLTNESDGHTTSLYGIGFGPFIITNKHLFRRN NGTLLVQSLHGVFKVKDTTTLQQHLVDGRDMIIIRMPKDFPPFPQKLKFR EPQREERICLVTTNFQTKSMSSMVSDTSCTFPSSDGIFWKHWIQTKDGQC GSPLVSTRDGFIVGIHSASNFTNTNNYFTSVPKNFMELLTNQEAQQWVSG WRLNADSVLWGGHKVFMNKPEEPFQPVKEATQLMN (xlUb;Xenopuslaevisubiquitin) SEQIDNO:17 MQIFVKILTGKTITLEVEPSDTIENVKAKIQDKEGIPPDQQRLIFAGKQL EDGRTLSDYNIQKESTLHLVLRLRGG (xIUsp2;Xenopuslaevisubiquitin-specificpro- cessingprotease2) SEQIDNO:18 MRSHTLRIHGMGAGREHQIPGTVILSSIMDFILHRAKSSKHVQGLVGLRN LGNTCFMNSILQCLSNTKDLRDYCQQNSYRRDLSSKKCNTAIMEEFARLL QAIWTSSANEVVSPSEFKTQIQRYAPRFMGYNQQDAQEFLRFLLDGLHNE VNRVTVKPRPSSQDLDHMPDSEKGKKMWKRYLEREDSRIVELFVGQLKSS LTCTDCGYCSTVFDPFWDLSLPIAKKSASEVSLVDCMRLFTKEDVLDGDE KPTCCRCKARRRCTKKFTIQRFPKILVLHLKRFSEGRIRSGKLSTFVNFP LKDLDLREFSSESNPHATYNLYAVSNHSGTTMGGHYTAYCKNPSNGEWYT FNDSRVTAMSSSQVKSSDAYVLFYELSGPSSRM (HomosapiensAtg4B(hsAtg4B)) SEQIDNO:19 MDAATLTYDTLRFAEFEDFPETSEPVWILGRKYSIFTEKDEILSDVASRL WFTYRKNFPAIGGTGPTSDTGWGCMLRCGQMIFAQALVCRHLGRDWRWTQ RKRQPDSYFSVLNAFIDRKDSYYSIHQIAQMGVGEGKSIGQWYGPNTVAQ VLKKLAVFDTWSSLAVHIAMDNTVVMEEIRRLCRTSVPCAGATAFPADSD RHCNGFPAGAEVTNRPSPWRPLVLLIPLRLGLTDINEAYVETLKHCFMMP QSLGVIGGKPNSAHYFIGYVGEELIYLDPHTTQPAVEPTDGCFIPDESFH CQHPPCRMSIAELDPSIAVGFFCKTEDDFNDWCQQVKKLSLLGGALPMFE LVELQPSHLACPDVLNLSLDSSDVERLERFFDSEDEDFEILSL (HomosapiensLC3B(hsLC3B)) SEQIDNO:20 MPSEKTFKQRRSFEQRVEDVRLIREQHPTKIPVIIERYKGEKQLPVLDKT KFLVPDHVNMSELIKIIRRRLQLNANQAFFLLVNGHSMVSVSTPISEVYE SERDEDGFLYMVYASQETFG (HomosapiensGATE16(hsGATE16)) SEQIDNO:21 MKWMFKEDHSLEHRCVESAKIRAKYPDRVPVIVEKVSGSQIVDIDKRKYL VPSDITVAQFMWIIRKRIQLPSEKAIFLFVDKTVPQSSLTMGQLYEKEKD EDGFLYVAYSGENTFG (His.sub.14-SUMOstar-MBP) SEQIDNO:22 MSKHHHHSGHHHTGHHHHSGSHHHTGSDSEVNQEAKPEVKPEVKPETHIN LKVSDGSSEIFFKIKKTTPLRRLMEAFAKRQGKEMDSLTFLYDGIEIQAD QTPEDLDMEDNDIIEAHREQIGGAGTKTEEGKLVIWINGDKGYNGLAEVG KKFEKDTGIKVTVEHPDKLEEKFPQVAATGDGPDIIFWAHDRFGGYAQSG LLAEITPDKAFQDKLYPFTINDAVRYNGKLIAYPIAVEALSLIYNKDLLP NPPKTWEEIPALDKELKAKGKSALMENLQEPYFTWPLIAADGGYAFKYEN GKYDIKDVGVDNAGAKAGLTFLVDLIKNKHMNADTDYSIAEAAFNKGETA MTINGPWAWSNIDTSKVNYGVTVLPTFKGQPSKPFVGVLSAGINAASPNK ELAKEFLENYLLTDEGLEAVNKDKPLGAVALKSYEEELAKDPRIAATMEN AQKGEIMPNIPQMSAFWYAVRTAVINAASGRQTVDEALKDAQTNGTGC (SUMOstar) SEQIDNO:23 MSDSEVNQEAKPEVKPEVKPETHINLKVSDGSSEIFFKIKKTTPLRRLME AFAKRQGKEMDSLTFLYDGIEIQADQTPEDLDMEDNDIIEAHREQIGG (SUMOstarprotease) SEQIDNO:24 LVPELNEKDDDQVQKALASRENTQLMNRDNIEITVRDFKTLAPRRWLNDT IIEFFMKYIEKSTPNTVAFNSFFYTNLSERGYQGVRRWMKRKKTQIDKLD KIFTPINLNQSHWALGIIDLKKKTIGYVDSLSNGPNAMSFAILTDLQKYV MEESKHTIGEDFDLIHLDCPQQPNGYDCGIYVCMNTLYGSADAPLDFDYK DAIRMRRFIAHLILTDALK (His.sub.14-IF2d1-xlLC3B-MBP) SEQIDNO:25 MSKHHHHSGHHHTGHHHHSGSHHHTGGSSGTDVTIKTLAAERQTSVERLV QQFADAGIRKSADDSVSAQEKQTLIDHLNQKNSGPDKLTLQRKTRSTLNI PGTGGKSKSVQIEVRKKRTFVKRDPQEAERLAAEEQAQREAEEQARREAE ESAKREAQQKAEREAAEQAKREAAEQAKREAAEKDKVTSSEKTFKQRRSL EQRVEDVRLIREQHPTKIPVIIERYKGEKQLPVLDKTKFLVPDHVNMSEL IKIIRRRLQLNSNQAFFLLVNGHSMVSVSTPISEVYEREKDEDGFLYMVY ASQETFGAGTKTEEGKLVIWINGDKGYNGLAEVGKKFEKDTGIKVIVEHP DKLEEKFPQVAATGDGPDIIFWAHDRFGGYAQSGLLAEITPDKAFQDKLY PFTWDAVRYNGKLIAYPIAVEALSLIYNKDLLPNPPKTWEEIPALDKELK AKGKSALMFNLQEPYFTINPLIAADGGYAFKYENGKYDIKDVGVDNAGAK AGLTFLVDLIKNKHMNADTDYSIAEAAFNKGETAMTINGPWAWSNIDTSK VNYGVTVLPTFKGQPSKPFVGVLSAGINAASPNKELAKEFLENYLLTDEG LEAVNKDKPLGAVALKSYEEELAKDPRIAATMENAQKGEIMPNIPQMSAF WYAVRTAVINAASGRQTVDEALKDAQTNGTGC

EXAMPLES

[0208] Methods

[0209] Protein sequence alignments were performed using the ClustalW algorithm implemented in Protean version 11.2.1. (DNAStar, Inc.).

[0210] Substrate proteins and proteases were over-expressed in E. coli strain NEB Express from appropriate low copy expression vectors harboring an ColE1 origin of replication and conferring Kanamycin resistance as described before (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105). Further sequences are provided on request. Briefly, to produce protease substrates containing MBP as a target protein, E. coli cultures containing the appropriate expression vectors were grown with vigorous shaking over night at 30 C. in 50 ml TB medium containing 50 g/ml Kanamycin (TB-Kan). Cultures were diluted by addition of 300 ml fresh TB-Kan medium and further shaken at 30 C. After 30 min, expression of substrate proteins was induced by addition of IPTG to a final concentration of 200 M. After 3-4 h, 5 mM EDTA and 1 mM PMSF were added directly to the culture and cells were harvested by centrifugation for 7 min at 5000 g. The cell pellet was resuspended in ice-cold LS buffer (280 mM NaCl, 45 mM Tris/HCl pH 7.5, 4.5 mM MgCl.sub.2, 10 mM DTT) containing 15 mM imidazole at a final density of 100 OD.sub.600. After cell-lysis by sonication, cell debris were removed by centrifugation for 1 h at 200 000g. The supernatant was incubated with 2 ml of an EDTA- and DTT-resistant Ni.sup.2+-chelate resin (e.g. Roche cOmplete His-Tag Purification Resin) pre-equilibrated with LS buffer containing 15 mM imidazole for 1 h at 4 C. After washing off unbound proteins with LS buffer containing 15 mM imidazole, polyHis-tagged substrate proteins were eluted with LS buffer containing 300 mM imidazole. After exchanging the buffer to LS buffer using a PD-10 column (GE Healthcare), the substrate protein was mixed with 1/9 volume 2.5 M sucrose. Aliquots were snap-frozen in liquid nitrogen and stored at 80 C. until used.

[0211] Protease substrates with fluorescent target proteins (GFP or mCherry), and proteases were produced analogously after expression for 14-16 h at 18 C.

[0212] To obtain tag-free protease preparations, imidazole eluates were cleaved to completion with a polyHis-tagged protease appropriate for removal of the polyHis tag. After gel filtration on a SD200 16/60 column (GE Healthcare) pre-equilibrated with LS buffer, remaining traces of cleaved polyHis-tag and polyHis-tagged protease were removed by reverse Ni.sup.2+ chelate chromatography. This guaranteed the final enzyme preparation to be free of any contaminating proteolytic activity. Final protease preparations were diluted with 1/9 volume 2.5 M sucrose. Aliquots ere snap-frozen in liquid nitrogen and stored at 80 C. until used. All proteins were quantified via their absorption at 280 nm and computed extinction coefficients. Accuracy of quantification and purity of the proteins were validated by SDS-PAGE followed by Coomassie-staining.

[0213] Cleavage assays in solution and on column were performed as described before (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105; Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 106-115): If not stated otherwise, cleavage reactions were performed in LS-S buffer (250 mM NaCl, 40 mM Tris/HCl pH 7.5, 2 mM MgCl.sub.2, 250 mM sucrose, 2 mM DTT). Generally, substrates and proteases were pre-diluted in LS-S buffer to twice the aspired end-concentration. Cleavage was initiated by mixing identical volumes (generally 5 l) of substrate and protease pre-dilutions and stopped by mixing with 9 volumes of hot SDS sample buffer. A fraction corresponding to 2.5 pg of substrate was separated by SDS-PAGE on 7-15% gradient gels. Gels were stained with Coomassie G250 and scanned.

[0214] On-column cleavage assays were done on EDTA- and DTT-resistant silica- or Sepharose-based Ni.sup.2+ chelate resins with high porosity.

[0215] Dynamic light scattering (DLS): Proteases diluted to 10 M in LS-S buffer were ultracentrifuged (200 000 g, 30 min), and assayed in a closed cuvette using a DynaPro NanoStar DLS instrument (Wyatt Technology). To acquire heat denaturation curves, the temperature was automatically raised by 1 C. every 10 min. DLS signals were acquired just before each temperature step.

[0216] In vitro binding assays: An EDTA- and DTT-resistant Ni.sup.2+ chelate resin was loaded with 40 M His.sub.14-Spacer-xlLC3B-GFP or His.sub.14-Spacer-xlGATE16-GFP. An empty resin served as a control. 20 l aliquots were incubated with 100 l of an equimolar mixture of full-length protease and a protease fragment (10 M each) for 1 h at 25 C. in LS-S buffer. After washing (330 sec) with the same buffer, bound proteins were eluted with SDS sample buffer containing 500 mM imidazole and analyzed by SDS-PAGE.

[0217] Example purifications from E. coli: Relevant fusion proteins were over-expressed from appropriate expression vectors in E. coli (ColE1 origin, Kanamycin resistance). Cleared lysates in LS buffer containing 15 mM imidazole were incubated with an EDTA- and DTT-resistant Ni.sup.2+ chelate resin. After washing with the same buffer, the target proteins were eluted with 500 nM xlAtg4B.sup.14-384 in LS buffer at 4 C. After 1 h, proteins remaining on the resin were eluted with LS buffer containing 0.5 M imidazole. Relevant fractions were analyzed by SDS-PAGE.

[0218] Samples taken during elution were in addition quantified by measuring the OD.sub.280. Substrate stability in eukaryotic extracts:

[0219] Rabbit reticulocyte lysate was purchased from Promega, wheat germ extract was prepared according to (Cathrin Enke, Doktorarbeit 2010, Cuvillier Verlag Gottingen, ISBN 978-3-86955-483-9), low-speed Xenopus egg extract was prepared according to (Blow, J. J., Laskey, R. A. (1986) Cell 47, 577-587). 1.25 l of 10 M protease substrates containing MBP as a target protein in LS-S buffer were incubated with 10 l of indicated lysates in the presence or absence of a protease mix containing scUlp1, SUMOstar protease, xlAtg4B.sup.14-384 and trAtg4B (0.1 M each final concentration, supplied in 1.25 l LS-S buffer) for 2 h at 25 C. in 12.5 l total volume. Reaction products were analyzed by Western blot with an antibody recognizing E. coli MBP (Sigma-Aldrich # M1321).

[0220] Yeast expression: S. cerevisiae strain SFY122 (S288C, Mata, H2B-CFP::TRP1, his3200, leu20, lys20, met150, ura30) was transformed with 2 expression plasmids encoding N-terminally ZZ-UBL-tagged Citrine (Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A. and Tsien, R. Y. (2001) J Biol Chem 276, 29188-29194; Heikal, A. A., Hess, S. T., Baird, G. S., Tsien, R. Y. and Webb, W. W. (2000) Proc Natl Acad Sci U S A 97, 11996-12001) under the control of the GAL1 promoter (Sequences are provided on request). Single colonies were grown over night in CSM-Ura containing 2% glucose and 2% raffinose. Cells were washed three times in CSM-Ura +2% raffinose, diluted to OD.sub.600=0.2 and shaken over night at 30 C. Protein expression was induced by addition of 2% galactose for 5 h. Total lysates were prepared by the NaOH/TCA method (modified from (Riezman, H., Hase, T., van Loon, A. P., Grivell, L. A., Suda, K. and Schatz, G. (1983) EMBO J 2, 2161-2168)) and analyzed by Western blot using an antibody recognizing Citrine and CFP. The ZZ-tag was detected using a fluorescently labeled anti-mouse-IgG antibody.

[0221] For protein purifications from yeast, cells extracts were prepared by glass bead lysis (modified from (Conzelmann, A., Riezman, H., Desponds, C. and Bron, C. (1988) EMBO J 7, 2233-2240)) in LS-S buffer with protease protection. After centrifugation for 1 h at 200 000 g, cleared lysates were incubated with an anti-ZZ affinity resin. Non-bound material was washed off with LS-S buffer and target proteins were eluted with the appropriate protease in the same buffer within 1 h at 4 C. Material remaining on the resin was analyzed after elution with SDS sample buffer.

Example 1

Expression of xlLC3B-Fusions in E. coli

[0222] Initially, the primary aim was to analyze the suitability of xlAtg4B for tag removal from recombinant proteins fused to Xenopus laevis Atg8 orthologs. As the inventors had observed before that fusions to S. cerevisiae Atg8 only show suboptimal expression levels (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105), the inventors first compared the impact of various UBLs including xlLC3B on expression and solubility of GFP (FIG. 2). Indeed, xlLC3B-GFP could be highly over-expressed in E. coli and produced nearly 3-times higher levels of soluble GFP as compared to the corresponding scAtg8 fusion. Remarkably, with regard to the expression level, both xlLC3B and bdNEDD8 clearly outperformed scSUMO, which is well known for its expression- and solubility-enhancing effects.

Example 2

Identification and Characterization of xlAtg4B Protease and xlAtg4B Protease Fragments

[0223] As a next step, the inventors wanted to find well-expressible and well-soluble xlAtg4B fragments displaying optimal stability and catalytic properties. Based on known structures of the human Atg4B homolog (Kumanomidou, T., Mizushima, T., Komatsu, M., Suzuki, A., Tanida, I., Sou, Y. S., Ueno, T., Kominami, E., Tanaka, K. and Yamane, T. (2006) J Mol Biol 355, 612-618; Sugawara, K., Suzuki, N. N., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2005) J Biol Chem 280, 40058-40065; Satoo, K., Noda, N. N., Kumeta, H., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2009) EMBO J 28, 1341-1350), full-length xlAtg4B (residues 1-384) and five shorter xlAtg4B fragments harboring N- and/or C-terminal truncations (xlAtg4B.sup.14-384, xlAtg4B.sup.25-384 xlAtg4B.sup.1-345, xlAtg4B.sup.14-345 and xlAtg4B.sup.25-345) were cloned and expressed. All proteases fragments could be over-expressed in E. coli and obtained in high yield and purity (FIG. 3). Typical yields of the pure proteases were >120 mg per liter culture, i.e. 10-20 times more than obtained for the yeast ortholog scAtg4 (typically 5-10 mg).

[0224] To compare their catalytic properties efficiencies, a subset of these protease fragments was assayed in various in vitro cleavage assay (Frey, S. and GOrlich, D. (2014) J Chromatogr A 1337, 95-105) using two analogous substrate proteins with different xlAtg4B protease recognition sites (xlLC3B or xlGATE16, respectively; FIG. 4A). For a direct comparison, all reactions of a given experimental setups were performed in parallel for all analyzed protease fragments and substrates. In a first setup, the inventors titrated the protease concentration and assayed the cleavage of substrate proteins at 0 C. and 25 C., respectively (FIG. 4B and D). At 0 C., all four proteases cleaved the xlLC3B substrate with similar efficiency: 1 M of each protease fragment was sufficient to cleave 100 M of substrate within 1 h (FIG. 4B, left panel). At closer inspection, however, it became apparent that the C-terminal truncation within xlAtg4B.sup.25-345 slightly impaired xlLC3B processing while the two N-terminally shortened protease fragments were similarly active as the full-length enzyme. These subtle differences were more obvious when analyzing the cleavage kinetics using a fixed protease concentration (FIG. 4C): Here, efficient cleavage (i.e. >95% cleavage) of the xlLC3B substrate required twice as long when using xlAtg4B.sup.25-345 instead of the full-length or just N-terminally truncated xlAtg4B enzymes. At 25 C., about 10-fold less full-length or N-terminally truncated protease was required for efficient xlLC3B cleavage (FIG. 4B, right panel). Thus, the C-terminal deletion caused at 25 C. a more drastic loss in activity than at 0 C. Compared to the xlLC3B substrate, processing of the xlGATE16 substrate was generally more efficient and required 2- to 3-fold less full-length or N-terminally truncated proteases at either temperature (FIG. 4D). xlGATE16 processing was, however, strikingly more sensitive towards the C-terminal protease truncations: 10-fold and 30-fold more xlAtg4B.sup.25-345 was required for xlGATE16 processing as compared to the other protease fragments at 0 C. and 25 C., respectively. Consistently, 500 nM of xlAtg4B.sup.25-345 were insufficient to cleave 100 M of xlGATE16 substrate within 2 h at 0 C. (FIG. 4E). As with the xlLC3B substrate, no significant differences in activity could be observed between full-length and N-terminally truncated xlAtg4B fragments.

[0225] Salt Sensitivity

[0226] To learn more about the nature of the possible interaction between xlAtg4B and its substrates xlLC3B and xlGATE16, the inventors next tested the salt sensitivity of substrate processing. To this end, each substrate was incubated with 500 nM of each protease for 1 h at 0 C. at defined salt concentrations (FIG. 5A). Strikingly, xlLC3B processing by full-length xlAtg4B or its N-terminally truncated fragments was remarkably insensitive towards NaCl concentrations up to 1.5 M. Deletion of the protease's C-terminus, however, rendered the reaction salt sensitive at NaCl concentrations 0.5 M (FIG. 5A, left). In contrast to the xlLC3B substrate, xlGATE16 processing was generally more salt sensitive (FIG. 5A, right): Here, also full-length or N-terminally truncated xlAtg4B fragments showed a reduced cleavage activity at 1 M NaCl. The weak activity of xlAtg4B.sup.25-345 on xlGATE16 was further reduced at salt concentrations 0.5 M.

[0227] Temperature Dependence

[0228] Next, the temperature dependence of substrate processing by the xlAtg4B fragments was analyzed (FIG. 5B). As expected, the efficiency of xlLC3B cleavage increased with increasing temperature for all protease fragments (FIG. 5B, left). The full-length enzyme showed a remarkable activity boost between 16 and 37 C. A similar boost could be observed already between 0 C. and 25 C. for the two N-terminally truncated protease fragments. Within 1 h at 37 C., all three enzymes were able to cleave a >3000-fold excess of the xlLC3B substrate to near completion. At 0 C., also the protease fragment lacking the C-terminal extension was similarly active as the other three fragments tested. The boost of xlLC3B substrate processing at higher temperatures, however, was much weaker for this protease fragment. A similar general trend was observed also for the xlGATE16 substrate (FIG. 5B, right). Here, however, near-complete cleavage of a 6600-fold substrate excess was reached for the two N-terminally shortened protease fragments already at 25 C., while the full-length enzyme required 37 C. for a similarly efficient cleavage. The C-terminally shortened xlAtg4B.sup.25-345 fragment could only cleave 30-4 0% of a 6600-fold substrate excess even at 37 C.

[0229] xlAtg4B C-terminus

[0230] The results herein thus far show that deletion of the C-terminal xlAtg4B extension significantly impairs substrate processing, especially when using the xlGATE16 substrate at higher temperatures or elevated NaCl concentrations. Three possible explanations could possibly account for these effects: (i) The C-terminus of xlAtg4B might be required for enzymatic turnover, (ii) it could contribute to substrate recognition or (iii) be required for xlAtg4B stability. In the following, these scenarios were tested individually.

[0231] First, the cleavage efficiency of the xlAtg4B fragments at different dilutions was analyzed (FIG. 6A). Within one set of reactions, the concentrations of both, substrate and protease were varied proportionally while keeping the initial substrate/protease ratio constant. Strikingly, at 300 M concentration of xlLC3B substrate, all protease fragments were similarly active, clearly showing that the C-terminus of xlAtg4B is dispensable for general enzymatic turnover (FIG. 6A, left). At higher dilutions, however, clear differences became apparent: While full-length xlAtg4B and both N-terminally shortened fragments could cleave the xlLC3B substrate rather efficiently even at substrate concentrations as low as 3-10 M, the C-terminally truncated protease showed significantly reduced cleavage already at 100-30 M substrate concentration (FIG. 6A, left lower panel).

[0232] At high concentrations, also the xlGATE16 substrate was efficiently cleaved by the full-length protease or both N-terminally truncated fragments (FIG. 6A, right). xlGATE16 processing, however, significantly dropped already at substrate concentrations lower than 30 M. Even more drastic effects were observed when cleaving xlGATE16-MBP with xlAtg4B.sup.25-345 (FIG. 6A, right lower panel). Here, processing was poor even at 300 M substrate concentration. These results clearly indicate that a deletion of the C-terminal protease extension does not impair the enzymatic turnover but rather prevents efficient substrate recognition at high dilutions. In general, the xlGATE16 substrate is more sensitive to dilution indicating that the Michaelis-Menten constant (K.sub.M) of the reaction is higher for xlGATE16 than for xlLC3B substrates.

[0233] To directly compare binding of N- and/or C-terminally shortened protease fragments with the full-length enzyme, competitive pull-down assays using equimolar binary protease mixtures as a prey were performed (FIG. 6B). In this setup, even small differences in affinity should affect the relative protease stoichiometries between the input and the bound fractions. xlLC3B pulled down a 1:1 mixture of full-length xlAtg4B and the N-terminally shortened fragments. The N-terminal protease truncations hence did not influence binding. Interaction of all protease fragments lacking the C-terminal extension was, however, reduced to background levels in the presence of full-length protease. Interestingly, also degradation products lacking less than 39 residues from the C-terminus (unintentionally present in the enzyme preparations) bound xlLC3B far less efficiently than the respective enzymes with full-length C-termini, showing that even the extreme C-terminus is required for full substrate binding. Similar results were obtained when using xlGATE16 as a bait. The interaction of all proteases with xlGATE16 was, however, significantly weaker than with xlLC3B.

[0234] Together, the experiments so far clearly show that xlAtg4B's C-terminal extension substantially contributes to recognition of both xlLC3B and xlGATE16 and is therefore required for robust substrate cleavage.

[0235] Thermal Stability

[0236] The inventors next asked if the N- and C-terminal extensions influence the (thermal) stability of xlAtg4B. To this end, all xlAtg4B fragments were pre-incubated for 16 h at different temperatures before analyzing their remaining activity in a standard xlLC3B cleavage assay (FIG. 7A, left). In this assay, the full-length enzyme retained full activity after over-night incubation at 37 C., but lost activity at higher temperatures. xlAtg4B.sup.14-384 was more temperature stable and survived at least 42 C. for 16 h. A drastic loss in activity was, however, observed already at 37 C. for both enzyme fragments lacking the N-terminal 24 residues. Identical effects were obtained when using the xlGATE16 substrate (FIG. 7A, right).

[0237] In a second assay, dynamic light scattering (DLS) was used to analyze the thermal denaturation of the xlAtg4B fragments (FIG. 7B). The full-length enzyme started to unfold at 47-48 C. Fragments lacking the N-terminal 13 residues were slightly stabilized while an N-terminal deletion of 24 residues reduced the temperature stability by 7-8 C. All tested enzymes with an intact C-terminus showed biphasic denaturation curves, pointing to distinct steps of initial unfolding and subsequent aggregation (FIG. 7B). A deletion of the C-terminal extension did not significantly change the onset of denaturation (FIG. 7B, compare solid with dashed lines), but promoted subsequent aggregate formation. The strongly negatively charged C-terminus might thus act as a solubility enhancer that prevents immediate aggregation.

[0238] Interestingly, the temperatures required to observe an initial decline of enzymatic activity (FIG. 7A) were generally 5 C. lower than the onset of thermal denaturation observed by DLS (FIG. 7B). This discrepancy could be resolved by long-term DLS experiment with xlAtg4B.sup.25-384 at 37 C. (FIG. 7C): Here, during the initial two hours of incubation, the protease appeared rather stable. At longer incubation, however, xlAtg4B.sup.25-384 started to unfold and aggregate. The discrepancy between the activity assay (after 16 h of thermal denaturation) and the DLS experiment (temperature increase 1 C. per 10 min) can thus most likely be explained by the different experimental time-scales.

[0239] Promiscuity for Residues in the P.sub.1 Position

[0240] The experiments herein show that xlAtg4B.sup.14-384 combines optimal enzyme stability with efficient and robust substrate cleavage. The inventors further analyzed the properties of this protease fragment with respect to in-vitro cleavage of recombinant proteins. If target proteins with a defined (e.g. the authentic) N-terminus are to be produced, the enzyme's sensitivity to the residue in the P.sub.1 position (i.e. the residue following the scissile bond; FIG. 8A) is an important parameter. An optimal enzyme will offer a maximal freedom to choose any desired residue in the P.sub.1 position. Therefore, the protease concentration required for cleavage of several analogous substrates with altered residues in the P.sub.1 position was analyzed. Surprisingly, the enzyme showed remarkable promiscuity and required only slightly more protease for efficient cleavage of substrates harboring Met, Tyr, Arg or Glu in the P.sub.1 position as compared to the original P.sub.1.sub.Ala substrate. The enzyme, however, was unable to process a P.sub.1.sub.Pro substrate.

[0241] Discussion

[0242] Based on the known structure of the human Atg4B ortholog (hsAtg4B) (Kumanomidou, T., Mizushima, T., Komatsu, M., Suzuki, A., Tanida, I., Sou, Y. S., Ueno, T., Kominami, E., Tanaka, K. and Yamane, T. (2006) J Mol Blot 355, 612-618; Sugawara, K., Suzuki, N. N., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2005) J Biol Chem 280, 40058-40065; Satoo, K., Noda, N. N., Kumeta, H., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2009) EMBO J 28, 1341-1350), a series xlAtg4B fragments with N-terminal and C-terminal truncations was designed. At low temperature, the analyzed N-terminally truncated xlAtg4B fragments (xlAtg4B.sup.14-384 and xlAtg4B.sup.25-384) showed a catalytic activity comparable to the full-length enzyme. While these results seem to be in contrast to earlier studies on the human Atg4B ortholog that suggested an auto-inhibitory function of the N-terminal extension (Li, M., Hou, Y., Wang, J., Chen, X., Shao, Z. M. and Yin, X. M. (2011) J Biol Chem 286, 7327-7338; Satoo, K., Noda, N. N., Kumeta, H., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2009) EMBO J 28, 1341-1350), the inventors observed that at temperatures 16 C., indeed the two shorter fragments were slightly more active than the full-length enzyme. Without being bound by theory, this temperature effect could potentially be a result of several hydrophobic interactions that are observed between the N-terminal extension of the human enzyme and the protease surface near the catalytic center. Importantly, deletion of only 13 N-terminal residues was sufficient to is efficiently prevent auto-inhibition and in addition created an enzyme fragment (xlAtg4B.sup.14-384) with superior temperature stability compared to xlAtg4B.sup.25-384.

[0243] The contribution of the flexible C-terminal protease extension (residues 346-384) to substrate recognition and processing was also analyzed. While the significance of this region so far had not been directly addressed, it was now found compelling evidence that it is required for an efficient interaction with two dedicated xlAtg4B substrate proteins, xlLC3B and xlGATE16. This finding was surprising for two reasons. First, the available structures of the substrate-free human Atg4B (hsAtg4B) suggest that the protease's C-terminus partially occupies the substrate-binding site (Kumanomidou, T., Mizushima, T., Komatsu, M., Suzuki, A., Tanida, I., Sou, Y. S., Ueno, T., Kominami, E., Tanaka, K. and Yamane, T. (2006) J Mol Biol 355, 612-618; Sugawara, K., Suzuki, N. N., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2005) J Biol Chem 280, 40058-40065). It therefore has to be displaced before substrate binding can occur, which may thus hamper formation of the proteasesubstrate complex. Second, crystals of LC3B-bound hsAtg4B could be obtained only after removal of the C-terminal extension (Satoo, K., Noda, N. N., Kumeta, H., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2009) EMBO J 28, 1341-1350), which (i) shows that the C-terminus of xlAtg4B is not strictly required for substrate interaction and (ii) could indeed suggest an inhibitory effect on complex formation. In contrast, the results herein clearly show that the C-terminal extension is an integral part of the protease's substrate interaction surface.

[0244] While the C-terminal protease truncation affects processing of xlLC3B mainly under stringent conditions (high salt, elevated temperature or low substrate concentration), the effect is pronounced already under standard conditions (0 C., 250 mM NaCl, 100 M initial substrate concentration) when using the xlGATE16 substrate. This striking difference might be attributed to the overall lower affinity of xlGATE16 to xlAtg4B as compared to xlLC3B (see FIG. 6). In addition the data herein indicates that the interaction between xlGATE16 and xlAtg4B is strongly dependent on protease's C-terminus while xlLC3B significantly interacts also with the folded protease domain. Although the C-terminally truncated protease fragment shows similar temperature stability as the corresponding full-length variant, impairment of substrate cleavage is stronger at higher temperatures. This suggests that the interaction of substrates with the protease core is mainly ionic (and thus weakened at higher temperatures) while interaction with the C-terminal extension involves a strong hydrophobic component. This conclusion is also in line with the observation that all protease fragments with intact C-termini robustly cleave the xlLC3B substrate at both high salt conditions and low temperature, suggesting that hydrophobic as well as ionic interactions participate in the proteasesubstrate interaction.

[0245] In combination, the folded core and the C-terminal extension of xlAtg4B mediate a strong interaction with the xlLC3B substrate, which is beneficial for efficient substrate processing at high dilution and complete processing of substrates. Strikingly, however, the turnover rate at high substrate concentrations is clearly lower for xlLC3B as compared to the xlGATE16 substrate, which has a lower affinity to the protease. Without being bound by theory, this seemingly paradoxical finding suggests that the rate-limiting step in xlAtg4B-mediated substrate cleavage is the substrate release. As a consequence, cleavage of xlLC3B substrates is slower but more robust.

Example 3

Application of the xlAtg4B Protease System for Tag Removal and On-Column Cleavage

[0246] An important application of tag-cleaving proteases is on-column cleavage of recombinant proteins. The inventors directly addressed the suitability of xlAtg4B.sup.14-384 for this purpose using polyHis-tagged substrate proteins bound to a Silica-based Ni.sup.2+ chelate resin of high porosity (FIG. 9). More specifically, 100 M of His.sub.14-IF2d1-xlLC3B-GFP or His.sub.14-IF2d1-xlGATE16-GFP were immobilized on the respective matrices along with the control protein His.sub.14-bdNEDD8-mCherry (FIG. 9A) before incubation with defined concentrations of xlAtg4B.sup.14-384 or bdNEDP1 for 1 h at 4 C. Under these conditions, 250-500 nM of xlAtg4B.sup.14-384 was sufficient for near-quantitative elution of GFP from the Silica-based resin (FIG. 9B, C). The cleavage was specific as even at much higher concentrations of xlAtg4B.sup.14-384 no elution of the bdNEDD8-tagged mCherry control protein could be detected. Vice versa, after treatment with a high concentration of the bdNEDD8-specific protease bdNEDP1, only mCherry but no GFP could be detected in the eluates. When using a Sepharose-based resin with high porosity, only slightly higher protease concentrations were required for efficient elution (not shown). The elution efficiency was, however, significantly reduced when matrices with low porosity or substrate proteins without flexible linker between the polyHis tag and the protease recognition site were used (data not shown). to The xlAtg4B/xlLC3B protease/substrate pair was exploited to purify the model target protein maltose binding protein (MBP) by on-column cleavage of either His.sub.14-IF2d1-xlLC3B-MBP or His.sub.14-IF2d1-xlGATE16-MBP (FIG. 9 D, E). Even at moderate induction strength, both proteins were highly over-expressed in E. coli and displayed excellent solubility (FIG. 9E). Stronger induction led to massive over-expression of fusion proteins without compromising their solubility (not shown). About 160-200 M of each fusion protein was immobilized on a Ni.sup.2+ chelate resin and treated in batch with 500 nM xlAtg4B.sup.14-384 at 4 C. Strikingly, the initial cleavage rate was very high when using the xlGATE16 fusion protein (FIG. 9D). Here, >80% and >90% of the MBP target protein was released already after 15 min and 30 min, respectively. At the corresponding time points, the xlLC3B fusion protein was processed to only P-50% and 75%. In both cases, however, efficient release of highly pure MBP was reached within one hour (FIG. 9D and E).

[0247] An important parameter for the practical application of tag-cleaving proteases is their substrate specificity. This parameter is especially important when mutually exclusive specificity (orthogonality) to other proteases is strictly required, e.g. for purification of protein complexes with controlled subunit stoichiometry (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 106-115). Also, it is important to know which host proteases could potentially cleave a given protease recognition site during expression. For practical applications, the inventors were especially interested in the cross-reactivity of xlAtg4B with the well-established TEV protease (Kapust, R. B., et al. (2001) Protein Engineering 14(12), 993-1000; van den Berg, S., et al. (2006) Journal of Biotechnology 121, 291-298), scUlp1 (Malakhov, M. P., et al. (2004) J Struct Funct Genomics 5, 75-86), SUMOstar protease (Liu, L., et al. (2008) Protein Expr Purif 62, 21-28; Peroutka, R. J., et al. (2008) Protein Sci 17, 1586-1595) and the recently described proteases bdSENP1, bdNEDP1, and xlUsp2 (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105; Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 106-115). In addition, the wheat (Triticum) Atg4 ortholog (trAtg4) was also included. To analyze the specificity profiles of these proteases, a high concentration (20 M) of each protease was incubated with 100 M of each substrate protein (see FIG. 10A) for 3 h at 25 C. in all possible binary combinations (FIG. 10B). For all proteases but TEV protease, these conditions correspond to a significant (>200- to 30 000-fold) over-digestion. Under these conditions, both xlAtg4B.sup.14-384 and trAtg4 only cleaved substrates containing Atg8-like UBLs (xlLC3B, xlGATE16 or trAtg8), but none of the substrates dedicated to other proteases. Vice versa, substrates containing Atg8-like UBLs were exclusively cleaved by Atg4 proteases. Atg4 proteases and Atg8-type substrate proteins are therefore truly orthogonal to all other protease/substrate pairs analyzed. Within the Atg8-type substrates, interesting differences became apparent: While xlLC3B was nearly exclusively recognized by xlAtg4B.sup.14-384, both xlGATE16 and trAtg8-containing substrates were in addition also cleaved by trAtg4.

[0248] These inter- and intra-species substrate preferences of Atg4-like enzymes were analyzed further using detailed protease titration assays (FIG. 10C). Here, the S. cerevisiae Atg4 ortholog (scAtg4) was also included along with its cognate substrate scAtg8 that have been described recently (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105). In this assay, xlAtg4B showed the broadest substrate promiscuity and cleaved a 1000-fold excess of all four substrate proteins (containing xlLC3B, xlGATE16, trAtg8 or scAtg8) within 1 h at 25 C. irrespective of their origin (FIG. 10C, left column). The yeast scAtg4 protease could efficiently process xlGATE16, trAtg8 and scAtg8, but was completely unable to cleave the xlLC3B substrate (FIG. 10C, middle column). The Triticum protease trAtg4 cleaved only its cognate substrate trAtg8 and the yeast substrate with decent efficiency (FIG. 10C, right column). In comparison, the Xenopus xlGATE16 substrate required drastically (>100-fold) higher trAtg4 concentrations for significant cleavage; xlLC3B cleavage by trAtg4 was only barely detectable.

[0249] The best performing xlAtg4B fragment, xlAtg4B.sup.14-384, has great potential as a new tag-cleaving protease. This protease fragment is highly active and routinely cleaves a 100- to 200-fold substrate excess within 1 h at 0 C. For comparison, TEV protease, which is probably still the most common tag-cleaving protease, requires 30- to 50-fold higher protease concentrations under these conditions (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105). In addition, xlAtg4B.sup.14-384 is highly temperature stable (42 C. for 16 h) and can therefore also be used at higher temperatures. At 25 C., e.g., xlAtg4B.sup.14-384 can cleave a 2 000-fold substrate excess within one hour; at 37 C. even less protease is required for efficient cleavage. When used for in-vitro tag removal from recombinant proteins, this high specific activity reduces contamination of the final protein preparation by the protease. Compared to other tag-cleaving proteases like yeast Ulp1p (Malakhov, M. P., Mattern, M. R., Malakhova, O. A., Drinker, M., Weeks, S. D. and Butt, T. R. (2004) J Struct Funct Genomics 5, 75-86; Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105) or SUMOstar protease (Liu, L., Spurrier, J., Butt, T. R. and Strickler, J. E. (2008) Protein Expr Purif 62, 21-28), xlAtg4B displays a superior salt tolerance (tested up to 1.5 M NaCl) and a broad P.sub.1 promiscuity, parameters that are important for robust cleavage of recombinant substrate proteins in various buffer conditions and sequence contexts.

[0250] When analyzing cross-reactivity with other tag-cleaving proteases, the inventors found out that xlAtg4B displays orthogonal specificity to the recently introduced bdSENP1 and bdNEDP1 proteases (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105). Together, these highly efficient proteases thus ideally complement each other and can be combined to purify protein complexes with is controlled subunit stoichiometry by successive affinity capture and proteolytic release steps (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 106-115).

Example 4

Application of the xlAtg4B Protease System for Purification of Proteins from Eukaryotic Hosts

[0251] The unexpectedly high resistance of xlLC3B towards cleavage by Atg4-like proteases originating from other species encouraged to address the stability of xlLC3B- and xlGATE16 fusions in various eukaryotic cell extracts (FIG. 11A, B). As controls, analogous fusions to trAtg8, scSUMO and the cleavage-resistant scSUMO variant SUMOstar (Liu, L., Spurrier, J., Butt, T. R. and Strickler, J. E. (2008) Protein Expr Purif 62, 21-28; Peroutka, R. J., Elshourbagy, N., Piech, T. and Butt, T. R. (2008) Protein Sci 17, 1586-1595) were also included. Indeed, in wheat germ extract 1 M of xlLC3B and xlGATE16 substrates were not significantly processed within 2 h at 25 C., while the corresponding trAtg8 fusion was completely cleaved. In comparison, all substrate proteins harboring Atg8 homologs were completely cleaved both in Xenopus egg extract and rabbit reticulocyte lysate. Interestingly, the scSUMO fusion was only partially cleaved in wheat germ extract and remained stable in rabbit reticulocyte lysate. Control incubations containing a protease mix (1 M each of scUlp1, SUMOstar protease, xlAtg4B.sup.14-384 and trAtg4) confirmed that the extracts did not contain any substances inhibiting specific proteolytic substrate processing.

[0252] Next, it was desired to find out if some of the analyzed ubiquitin-like protease recognition sites would also be compatible with production of intact full-length recombinant fusion proteins in a living eukaryotic host. Therefore different ZZ-UBL-Citrine substrate proteins (FIG. 11C) were over-expressed in S. cerevisiae under the control of the GAL1 promoter. In line with the in-vitro cleavage experiments presented before (FIG. 10C) even after 5 h induction the xlLC3B substrate was completely intact. In contrast, the scSUMO-, xlGATE16-, trAtg8- and bdSUMO-fusions were largely cleaved by endogenous yeast proteases. Surprisingly, also the cleavage-resistant SUMOstar variant (Liu, L., Spurrier, J., Butt, T. R. and Strickler, J. E. (2008) Protein Expr Purif 62, 21-28; Peroutka, R. J., Elshourbagy, N., Piech, T. and Butt, T. R. (2008) Protein Sci 17, 1586-1595) was not completely inert in vivo as both, N-terminal and C-terminal cleavage products could be detected with specific antibodies (FIG. 11D). Unexpectedly it was found that a fusion protein containing bdNEDD8 was even more resistant towards in vivo cleavage than the SUMOstar substrate. These findings suggest that xlLC3B and the previously introduced bdNEDD8 (Frey, S. and GOrlich, D. (2014) J Chromatogr A 1337, 95-105) could potentially be used as protease recognition sites for the recombinant expression of intact full-length fusion proteins in S. cerevisiae.

[0253] To show that the xlLC3B/xlAtg4B and bdNEDD8/bdNEDP1 systems are indeed suited for purification of recombinant proteins from a eukaryotic host, recombinant Citrine was purified as a model target protein from S. cerevisiae. To this end, the ZZ-UBL-Citrine fusions were over-expressed in yeast for 5 h as before. After cell lysis in a native buffer, the full-length fusion protein was found in the soluble fraction from which highly pure recombinant Citrine could be obtained by an efficient one-step capture and on-column cleavage procedure (FIG. 12).

[0254] Discussion

[0255] Importantly, both analyzed xlAtg4B substrates, xlLC3B and xlGATE16, promote solubility and high-level expression of the respective fusion proteins in E. coli (see FIG. 2 and FIG. 9E). This is in striking contrast to their yeast homolog scAtg8, which in direct comparison consistently produces significantly lower levels of soluble fusion proteins (FIG. 2). All in all, both xlAtg4B substrates are thus promising fusion partners for expression of recombinant target proteins in E. coli and may at the same time serve as recognition sites for xlAtg4B. The right choice between the two possible protease recognition sites might depend on the specific application. While xlGATE16 is cleaved more efficiently under standard conditions, xlLC3B cleavage is slightly slower but extraordinary robust.

[0256] In addition, xlLC3B features additional remarkable advantages: It was found that xlLC3B fusions are stable in wheat germ extract and even under drastic conditions only marginally processed by wheat Atg4 (trAtg4) in vitro, suggesting that stable xlLC3B fusion proteins can be produced in plants. Even more, xlLC3B is not recognized by the S. cerevisiae Atg4 protease. Full-length xlLC3B fusions can thus be expressed in this eukaryotic host and purified by a simple one-step capture and proteolytic release strategy. Such eukaryotic expression might be exploited for the production of proteins that rely on the eukaryotic folding machinery or have to be modified by posttranslational modifications. Fully unexpectedly, it was found that also bdNEDD8 fusion proteins are only marginally processed in yeast. With xlLC3B, bdNEDD8 (Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105) and SUMOstar (Liu, L., Spurrier, J., Butt, T. R. and Strickler, J. E. (2008) Protein Expr Purif 62, 21-28; Peroutka, R. J., Elshourbagy, N., Piech, T. and Butt, T. R. (2008) Protein Sci 17, 1586-1595), there are now three orthogonal UBL-derived protease recognition sites that in principle allow for full-length protein production in S. cerevisiae (FIG. 11E and FIG. 12). Strikingly, amongst these UBLs xlLC3B is the only one that is strictly stable in vivo while traces of cleavage products originating from the bdNEDD8 substrate and low amounts of cleaved SUMOstar were clearly detected (FIG. 11D and FIG. 12B). In combination, these UBLs should allow for the in-vivo co-expression and purification of three-subunit complexes with defined subunit stoichiometry also in yeast (Frey, S. and GOrlich, D. (2014) J Chromatogr A 1337, 106-115).

LIST OF REFERENCES

[0257] WO 2015/049230

[0258] WO 2008/083271 A2

[0259] WO 2002/090495 A2

[0260] WO 2003/057174 A2

[0261] WO 2005/003313 A2

[0262] WO 2006/073976 A2

[0263] Hemelaar, J., Lelyveld, V. S., Kessler, B. M. and Ploegh, H. L. (2003) J Biol Chem 278, 51841-51850

[0264] Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y. and Yoshimori, T. (2004) J Cell Sci 117, 2805-2812

[0265] Marino, G., Uria, J. A., Puente, X. S., Quesada, V., Bordallo, J. and Lopez-Otin, C. (2003) J Biol Chem 278, 3671-3678

[0266] Tanida, I., Sou, Y. S., Ezaki, J., Minematsu-Ikeguchi, N., Ueno, T. and Kominami, E. (2004) J Biol Chem 279, 36268-36276

[0267] Li, M., Hou, Y., Wang, J., Chen, X., Shao, Z. M. and Yin, X. M. (2011) J Biol Chem 286, 7327-7338

[0268] Woo, J., Park, E. and Dinesh-Kumar, S. P. (2014) Proc Natl Acad Sci U S A 111, 863-868

[0269] Kumanomidou, T., Mizushima, T., Komatsu, M., Suzuki, A., Tanida, I., Sou, Y. S., Ueno, T., Kominami, E., Tanaka, K. and Yamane, T. (2006) J Mol Biol 355, 612-618

[0270] Sugawara, K., Suzuki, N. N., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2005) J Biol Chem 280, 40058-40065

[0271] Satoo, K., Noda, N. N., Kumeta, H., Fujioka, Y., Mizushima, N., Ohsumi, Y. and Inagaki, F. (2009) EMBO J 28, 1341-1350

[0272] van der Veen, A. G. and Ploegh, H. L. (2012) Annu Rev Biochem 81, 323-357

[0273] Yeh, E. T., Gong, L. and Kamitani, T. (2000) Gene 248, 1-14

[0274] Malakhov, M. P., Mattern, M. R., Malakhova, O. A., Drinker, M., Weeks, S. D. and Butt, T. R. (2004) J Struct Funct Genomics 5, 75-86

[0275] Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 95-105

[0276] Frey, S. and Grlich, D. (2014) J Chromatogr A 1337, 106-115

[0277] Liu, L., Spurrier, J., Butt, T. R. and Strickler, J. E. (2008) Protein Expr Purif 62, 21-28

[0278] Peroutka, R. J., Elshourbagy, N., Piech, T. and Butt, T. R. (2008) Protein Sci 17, 1586-1595

[0279] Taxis, C. and Knop, M. (2012) Methods Mol Biol 832, 611-626

[0280] Urabe, M., Kume, A., Takahashi, T., Serizawa, N., Tobita, K. and Ozawa, K. (1999) Biochem Biophys Res Commun 266, 92-96

[0281] Taxis, C., Stier, G., Spadaccini, R. and Knop, M. (2009) Mol Syst Biol 5, 267

[0282] Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A. and Tsien, R. Y. (2001) J Biol Chem 276, 29188-29194

[0283] Heikal, A. A., Hess, S. T., Baird, G. S., Tsien, R. Y. and Webb, W. W. (2000) Proc Natl Acad Sci U S A 97, 11996-12001

[0284] Riezman, H., Hase, T., van Loon, A. P., Grivell, L. A., Suda, K. and Schatz, G. (1983) EMBO J 2, 2161-2168

[0285] Conzelmann, A., Riezman, H., Desponds, C. and Bron, C. (1988) EMBO J 7, 2233-2240

[0286] Butt, T. R., Edavettal, S. C., Hall, J. P. and Mattern, M. R. (2005) Protein Expr Purif 43, 1-9

[0287] Arnau, J., Lauritzen, C., Petersen, G. E. and Pedersen, J. (2006) Protein Expr Purif 48, 1-13

[0288] Li, S. J. and Hochstrasser, M. (1999) Nature 398, 246-251

[0289] Nilsson, J., Stahl, S., Lundeberg, J., Uhlen, M. and Nygren, P. A. (1997) Protein Expr Purif 11, 1-16

[0290] Young, C. L., Britton, Z. T. and Robinson, A. S. (2012) Biotechnol J 7, 620-634

[0291] Renicke, C., Spadaccini, R. and Taxis, C. (2013) PLoS One 8, e67915 UniProt Q640G7

[0292] Kapust, R. B., Tozser, J., Fox, J. D., Anderson, D. E. (2001) Protein Engineering 14(12), 993-1000

[0293] van den Berg, S., Lofdahl, P.A., Hard, T., Berglund, H. (2006) Journal of Biotechnology 121, 291-298.

[0294] Cathrin Enke, Doktorarbeit 2010, Cuvillier Verlag Gottingen, ISBN 978-3-86955-483-9

[0295] Blow, J. J., Laskey, R. A. (1986) Cell 47, 577-587.