Structures of Pup ligase PafA and depupylase Dop from the prokaryotic ubiquitin-like modification pathway

Nature Communications

Volumn 3, Issue , 2012, Pages

  Özcelik, Dennis ^a   Barandun, Jonas ^a   Schmitz, Nikolaus ^a   Sutter, Markus ^a   Guth, Ethan ^a   Damberger, Fred F ^a   Allain, Frédéric H T ^a   Ban, Nenad ^a   Weber Ban, Eilika ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; DOP PROTEIN; LIGASE; PAFA PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CATALYSIS; NUCLEAR MAGNETIC RESONANCE; PROTEIN MODIFICATION; PROTEIN STRUCTURE;

ACTINOBACTERIA; CORYNEBACTERINEAE; PROKARYOTA;

EID: 84866114528     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2009     Document Type: Article

References (30)

1. Burns, K. E., Liu, W. T., Boshoff, H. I., Dorrestein, P. C. & Barry, C. E. III. Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein. J. Biol. Chem. 284, 3069-3075 (2009).
2. Pearce, M. J., Mintseris, J., Ferreyra, J., Gygi, S. P. & Darwin, K. H. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322, 1104-1107 (2008).
3. Striebel, F. et al. Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat. Struct. Mol. Biol. 16, 647-651 (2009).
4. Darwin, K. H., Ehrt, S., Gutierrez-Ramos, J. C., Weich, N. & Nathan, C. F. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302, 1963-1966 (2003). (Pubitemid 37523503)
5. Gandotra, S., Schnappinger, D., Monteleone, M., Hillen, W. & Ehrt, S. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat. Med. 13, 1515-1520 (2007). (Pubitemid 350224249)
6. De Mot, R. Actinomycete-like proteasomes in a Gram-negative bacterium. Trends Microbiol. 15, 335-338 (2007). (Pubitemid 47126850)
7. Iyer, L. M., Burroughs, A. M. & Aravind, L. Unraveling the biochemistry and provenance of pupylation: a prokaryotic analog of ubiquitination. Biol. Direct 3, 45 (2008).
8. Chen, X. et al. Prokaryotic ubiquitin-like protein pup is intrinsically disordered. J. Mol. Biol. 392, 208-217 (2009).
9. Liao, S. et al. Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem. J. 422, 207-215 (2009).
10. Sutter, M., Striebel, F., Damberger, F. F., Allain, F. H. & Weber-Ban, E. 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 (2009).
11. Wang, T., Darwin, K. H. & Li, H. Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation. Nat. Struct. Mol. Biol. 17, 1352-1357 (2010).
12. Wang, T. et al. Structural insights on the Mycobacterium tuberculosis proteasomal ATPase Mpa. Structure 17, 1377-1385 (2009).
13. Striebel, F., Hunkeler, M., Summer, H. & Weber-Ban, E. The mycobacterial Mpa-proteasome unfolds and degrades pupylated substrates by engaging Pup's N-terminus. EMBO J. 29, 1262-1271 (2010).
14. Sutter, M., Damberger, F. F., Imkamp, F., Allain, F. H. & Weber-Ban, E. 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 (2010).
15. Burns, K. E. et al. 'Depupylation' of prokaryotic ubiquitin-like protein from mycobacterial proteasome substrates. Mol. Cell 39, 821-827 (2010).
16. Imkamp, F. et al. Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway. EMBO Rep. 11, 791-797 (2010).
17. Guth, E., Thommen, M. & Weber-Ban, E. Mycobacterial ubiquitin-like protein ligase PafA follows a two-step reaction pathway with a phosphorylated pup intermediate. J. Biol. Chem. 286, 4412-4419 (2011).
18. Pearce, M. J. et al. Identification of substrates of the Mycobacterium tuberculosis proteasome. EMBO J. 25, 5423-5432 (2006). (Pubitemid 44764151)
19. Eisenberg, D., Gill, H. S., Pfluegl, G. M. & Rotstein, S. H. Structure-function relationships of glutamine synthetases. Biochim. Biophys. Acta 1477, 122-145 (2000).
20. Gill, H. S. & Eisenberg, D. The crystal structure of phosphinothricin in the active site of glutamine synthetase illuminates the mechanism of enzymatic inhibition. Biochemistry 40, 1903-1912 (2001). (Pubitemid 32165658)
21. Lizak, C., Gerber, S., Numao, S., Aebi, M. & Locher, K. P. X-ray structure of a bacterial oligosaccharyltransferase. Nature 474, 350-355 (2011).
22. Festa, R. A. et al. Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis [corrected]. Plos One 5, e8589 (2010).
23. Watrous, J. et al. Expansion of the mycobacterial 'PUPylome'. Mol. Biosyst. 6, 376-385 (2010).
24. Imkamp, F. et al. Deletion of dop in Mycobacterium smegmatis abolishes pupylation of protein substrates in vivo. Mol. Microbiol. 75, 744-754 (2010).
25. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
26. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
27. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213-221 (2010).
28. Adams, P. D. et al. The Phenix software for automated determination of macromolecular structures. Methods 55, 94-106 (2011).
29. Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D. Biol. Crystallogr. 62, 1002-1011 (2006). (Pubitemid 44337374)
30. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).