Bacterial proteasome and PafA, the Pup ligase, interact to form a modular protein tagging and degradation machine

Biochemistry

Volumn 52, Issue 50, 2013, Pages 9029-9035

  Forer, Nadav ^a   Korman, Maayan ^a   Elharar, Yifat ^a   Vishkautzan, Marina ^a   Gur, Eyal ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC PROTEINS; LYSINE SIDE CHAINS; MUTUALLY EXCLUSIVE EVENTS; OVERLAPPING REGIONS; PROTEASOMAL DEGRADATION; PROTEIN SUBSTRATE; REGULATORY SUBUNITS; UBIQUITIN-LIKE PROTEINS;

AMINO ACIDS;

PROTEINS;

BACTERIAL PROTEIN; CYTOPLASM PROTEIN; LIGASE; LYSINE; POLYHISTIDINE TAG; PROKARYOTIC UBIQUITIN LIKE PROTEIN; PROTEASOME; PROTEASOME ACCESSORY FACTOR A; PROTEIN TAG; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; BACTERIUM; BACTERIUM CONJUGATION; BINDING AFFINITY; BINDING ASSAY; COMPETITIVE INHIBITION; CRYSTAL STRUCTURE; HYDROLYSIS; HYPOTHESIS; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MYCOBACTERIUM SMEGMATIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SEQUENCE ALIGNMENT;

EID: 84890491578     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401017b     Document Type: Article

References (35)

1. Cerda-Maira, F. and Darwin, K. H. (2009) The Mycobacterium tuberculosis proteasome: more than just a barrel-shaped protease Microbes Infect. 11, 1150-1155
2. Barandun, J., Delley, C. L., and Weber-Ban, E. (2013) The pupylation pathway and its role in mycobacteria BMC Biol. 10, 95
3. Darwin, K. H., Ehrt, S., Gutierrez-Ramos, J. C., Weich, N., and Nathan, C. F. (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide Science 302, 1963-1966 (Pubitemid 37523503)
4. Cerda-Maira, F. A., Pearce, M. J., Fuortes, M., Bishai, W. R., Hubbard, S. R., and Darwin, K. H. (2010) Molecular analysis of the prokaryotic ubiquitin-like protein (Pup) conjugation pathway in Mycobacterium tuberculosis Mol. Microbiol. 77, 1123-1135
5. Gandotra, S., Lebron, M. B., and Ehrt, S. (2010) The Mycobacterium tuberculosis proteasome active site threonine is essential for persistence yet dispensable for replication and resistance to nitric oxide PLoS Pathog. 6, e1001040
6. Groll, M., Ditzel, L., Lowe, J., Stock, D., Bochtler, M., Bartunik, H. D., and Huber, R. (1997) Structure of 20S proteasome from yeast at 2.4 A resolution Nature 386, 463-471 (Pubitemid 27164066)
7. Hu, G., Lin, G., Wang, M., Dick, L., Xu, R. M., Nathan, C., and Li, H. (2006) Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate Mol. Microbiol. 59, 1417-1428
8. Darwin, K. H., Lin, G., Chen, Z., Li, H., and Nathan, C. F. (2005) Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue Mol. Microbiol. 55, 561-571 (Pubitemid 40179387)
9. Wang, T., Li, H., Lin, G., Tang, C., Li, D., Nathan, C., Darwin, K. H., and Li, H. (2009) Structural insights on the Mycobacterium tuberculosis proteasomal ATPase Mpa Structure 17, 1377-13785
10. Wolf, S., Nagy, I., Lupas, A., Pfeifer, G., Cejka, Z., Müller, S. A., Engel, A., De Mot, R., and Baumeister, W. (1998) Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropolis J. Mol. Biol. 277, 13-25 (Pubitemid 28151880)
11. Pearce, M. J., Mintseris, J., Ferreyra, J., Gygi, S. P., and Darwin, K. H. (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis Science 322, 1104-1107
12. Burns, K. E., Liu, W. T., Boshoff, H. I., Dorrestein, P. C., and Barry, C. E., 3rd (2009) Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein J. Biol. Chem. 284, 3069-3075
13. Sutter, M., Damberger, F. F., Imkamp, F., Allain, F. H., and Weber-Ban, E. (2010) Prokaryotic ubiquitin-like protein (Pup) is coupled to substrates via the side chain of its C-terminal glutamate J. Am. Chem. Soc. 132, 5610-5612
14. Striebel, F., Imkamp, F., Sutter, M., Steiner, M., Mamedov, A., and Weber-Ban, E. (2009) Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes Nat. Struct. Mol. Biol. 16, 647-651
15. Burns, K. E., Cerda-Maira, F. A., Wang, T., Li, H., Bishai, W. R., and Darwin, K. H. (2010) "Depupylation" of prokaryotic ubiquitin-like protein from mycobacterial proteasome substrates Mol. Cell 39, 821-827
16. Imkamp, F., Striebel, F., Sutter, M., Ozcelik, D., Zimmermann, N., Sander, P., and Weber-Ban, E. (2010) Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway EMBO J. 11, 791-797
17. Striebel, F., Hunkeler, M., Summer, H., and Weber-Ban, E. (2010) The mycobacterial Mpa-proteasome unfolds and degrades pupylated substrates by engaging Pup's N-terminus EMBO J. 29, 1262-1271
18. Wang, T., Darwin, K. H., and Li, H. (2010) Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation Nat. Struct. Mol. Biol. 7, 1352-1357
19. Barandun, J., Delley, C. L., Ban, N., and Weber-Ban, E. (2013) Crystal structure of the complex between prokaryotic ubiquitin-like protein and its ligase PafA J. Am. Chem. 135, 6794-6797
20. Ofer, N., Forer, N., Korman, M., Vishkautzan, M., Khalaila, I., and Gur, E. (2013) Allosteric transitions direct protein tagging by PafA, the prokaryotic ubiquitin-like protein (pup) ligase J. Biol. Chem. 288, 11287-11293
21. Norby, J. G. (1988) Coupled assay of Na+,K+-ATPase activity Methods Enzymol. 156, 116-119
22. Lindsley, J. E. (2001) Use of a real-time, coupled assay to measure the ATPase activity of DNA topoisomerase II Methods Mol. Biol. 95, 57-64
23. Van Kessel, J. C., Marinelli, L. J., and Hatfull, G. F. (2008) Recombineering mycobacteria and their phages Nat. Rev. Microbiol. 6, 851-857
24. Festa, R. A., McAllister, F., Pearce, M. J., Mintseris, J., Burns, K. E., Gygi, S. P., and Darwin, K. H. (2010) Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis PLoS One 5, e8589
25. Poulsen, C., Akhter, Y., Jeon, A. H., Schmitt-Ulms, G., Meyer, H. E., Stefanski, A., Stühler, K., Wilmanns, M., and Song, Y. H. (2010) Proteome-wide identification of mycobacterial pupylation targets Mol. Syst. Biol. 6, 386
26. Watrous, J., Burns, K., Liu, W. T., Patel, A., Hook, V., Bafna, V., Barry, C. E., 3rd, Bark, S., and Dorrestein, P. C. (2010) Expansion of the mycobacterial ″PUPylome″ Mol. Biosyst. 6, 376-385
27. Delley, C. L., Striebel, F., Heydenreich, F. M., Özcelik, D., and Weber-Ban, E. (2012) Activity of the mycobacterial proteasomal ATPase Mpa is reversibly regulated by pupylation J. Biol. Chem. 287, 7907-7914
28. Burns, K. E., Pearce, M. J., and Darwin, K. H. (2010) Prokaryotic ubiquitin-like protein provides a two-part degron to Mycobacterium proteasome substrates J. Bacteriol. 192, 2933-2935
29. Cerda-Maira, F. A., McAllister, F., Bode, N. J., Burns, K. E., Gygi, S. P., and Darwin, K. H. (2011) Reconstitution of the Mycobacterium tuberculosis pupylation pathway in Escherichia coli EMBO Rep. 12, 863-870
30. Guth, E., Thommen, M., and Weber-Ban, E. (2011) Mycobacterial ubiquitin-like protein ligase PafA follows a two-step reaction pathway with a phosphorylated pup intermediate J. Biol. Chem. 286, 4412-4419
31. Barandun, J., Delley, C. L., and Weber-Ban, E. (2012) The pupylation pathway and its role in mycobacteria BMC Biol. 10, 95
32. Levchenko, I., Seidel, M., Sauer, R. T., and Baker, T. A. (2000) A specificity-enhancing factor for the ClpXP degradation machine Science 289, 2354-2356
33. Baker, T. A. and Sauer, R. T. (2012) ClpXP, an ATP-powered unfolding and protein-degradation machine Biochim. Biophys. Acta 1823, 15-28
34. Darwin, K. H., Ehrt, S., Gutierrez-Ramos, J. C., Weich, N., and Nathan, C. F. (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide Science 302, 1963-1966 (Pubitemid 37523503)
35. Segel, I. H. (1975) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, pp 421-461, John Wiley & Sons, Inc., New York.