Allosteric transitions direct protein tagging by PafA, the prokaryotic ubiquitin-like protein (Pup) ligase

Journal of Biological Chemistry

Volumn 288, Issue 16, 2013, Pages 11287-11293

  Ofer, Naomi ^a   Forer, Nadav ^a   Korman, Maayan ^a   Vishkautzan, Marina ^a   Khalaila, Isam ^a   Gur, Eyal ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC TRANSITION; ENGINEERED-SUBSTRATE; ENZYMATIC MECHANISMS; PROTEIN SUBSTRATE; PROTEIN TAGGING; SUBSTRATE BINDING; TARGET-SUBSTRATE; UBIQUITIN-LIKE PROTEINS;

PROTEINS;

SUBSTRATES;

ADENOSINE TRIPHOSPHATE; LYSINE; PAFA PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; BACTERIAL VIRULENCE; CONJUGATION; CONTROLLED STUDY; ENZYME BINDING; ENZYME SUBSTRATE; HYDROLYSIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN TARGETING;

ADENOSINE TRIPHOSPHATE; ALKALINE PHOSPHATASE; ALLOSTERIC REGULATION; BACTERIAL PROTEINS; MYCOBACTERIUM SMEGMATIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

PROKARYOTA;

EID: 84876592311     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.435842     Document Type: Article

References (27)

1. Burns, K. E., and Darwin, K. H. (2010) Pupylation versus ubiquitylation: tagging for proteasome-dependent degradation. Cell Microbiol. 12, 424-431.
2. 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.
3. Nagy, I., Tamura, T., Vanderleyden, J., Baumeister, W., and De Mot, R. (1998) The 20S proteasome of Streptomyces coelicolor. J. Bacteriol. 180, 5448-5453.
4. Knipfer, N., Seth, A., Roudiak, S. G., and Shrader, T. E. (1999) Species variation in ATP-dependent protein degradation: protease profiles differ between mycobacteria and protease functions differ between Mycobacterium smegmatis and Escherichia coli. Gene 231, 95-104.
5. 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.
6. Sutter, M., Striebel, F., Damberger, F. F., Allain, F. H., and Weber-Ban, E. (2009) A distinct structural region of the prokaryotic ubiquitin-like protein (Pup) is recognized by the N-terminal domain of the proteasomal ATPase Mpa. FEBS Lett. 583, 3151-3157.
7. 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.
8. Burns, K. E., Pearce, M. J., and Darwin, K. H. (2010) Prokaryotic ubiquitinlike protein provides a two-part degron to Mycobacterium proteasome substrates. J. Bacteriol. 192, 2933-2935.
9. 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.
10. 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. 17, 1352-1357.
11. 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.
12. 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 ubiquitinlike protein (Pup) conjugation pathway in Mycobacterium tuberculosis. Mol. Microbiol. 77, 1123-1135.
13. Lupas, A., Zwickl, P., and Baumeister, W. (1994) Proteasome sequences in eubacteria. Trends Biochem. Sci. 19, 533-534.
14. Iyer, L. M., Burroughs, A. M., and Aravind, L. (2008) Unraveling the biochemistry and provenance of pupylation: a prokaryotic analog of ubiquitination. Biol. Direct 3, 45.
15. Liao, S., Shang, Q., Zhang, X., Zhang, J., Xu, C., and Tu, X. (2009) Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem. J. 422, 207-215.
16. Chen, X., Solomon, W. C., Kang, Y., Cerda-Maira, F., Darwin, K. H., and Walters, K. J. (2009) Prokaryotic ubiquitin-like protein pup is intrinsically disordered. J. Mol. Biol. 392, 208-217.
17. 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.
18. Imkamp, F., Rosenberger, T., Striebel, F., Keller, P. M., Amstutz, B., Sander, P., and Weber-Ban, E. (2010) Deletion of dop in Mycobacterium smegmatis abolishes pupylation of protein substrates in vivo. Mol. Microbiol. 75, 744-754.
19. 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.
20. Maupin-Furlow, J. (2012) Proteasomes and protein conjugation across domains of life. Nat. Rev. Microbiol. 10, 100-111.
21. 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.
22. Chaudhuri, B. N., Sawaya, M. R., Kim, C. Y., Waldo, G. S., Park, M. S., Terwilliger, T. C., and Yeates, T. O. (2003) The crystal structure of the first enzyme in the pantothenate biosynthetic pathway, ketopantoate hydroxymethyltransferase, from M. tuberculosis. Structure 11, 753-764.
23. Monod, J., Wyman, J., and Changeux, J. P. (1965) On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118.
24. + Lon proteolytic machine. Proc. Natl. Acad. Sci. U.S.A. 106, 18503-18508.
25. Özcelik, D., Barandun, J., Schmitz, N., Sutter, M., Guth, E., Damberger, F. F., Allain, F. H., Ban, N., and Weber-Ban, E. (2012) Structures of Pup ligase PafA and depupylase Dop from the prokaryotic ubiquitin-like modification pathway. Nat. Commun. 3, 1014.
26. + degradation machine. Cell 114, 511-520.
27. Segel, IH (1975) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, pp. 421-461, John Wiley & Sons, New York.