The mycobacterial Mpa-proteasome unfolds and degrades pupylated substrates by engaging Pup's N-terminus

EMBO Journal

Volumn 29, Issue 7, 2010, Pages 1262-1271

  Striebel, Frank ^a   Hunkeler, Moritz ^a   Summer, Heike ^a   Weber Ban, Eilika ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

ARC; Degradation; Mpa; Proteasome; Pupylation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GENOMIC DNA; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEASOME; UBIQUITIN;

ARTICLE; ENZYME ACTIVITY; MOLECULAR CLONING; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; UBIQUITINATION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; MYCOBACTERIUM TUBERCULOSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; UBIQUITINS;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTA;

EID: 77950524360     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.23     Document Type: Article

References (60)

1. Burns KE, Liu WT, Boshoff HI, Dorrestein PC, Barry III CE (2009) Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein. J Biol Chem 284: 3069-3075
2. Chaudhuri BN, Sawaya MR, Kim CY, Waldo GS, Park MS, Terwilliger TC, Yeates TO (2003) The crystal structure of the first enzyme in the pantothenate biosynthetic pathway, keto-pantoate hydroxymethyltransferase, from M tuberculosis. Structure 11: 753-764
3. Chen X, Solomon WC, Kang Y, Cerda-Maira F, Darwin KH, Walters KJ (2009) Prokaryotic ubiquitin-like protein pup is intrinsically disordered. J Mol Biol 392: 208-217
4. Crosas B, Hanna J, Kirkpatrick DS, Zhang DP, Tone Y, Hathaway NA, Buecker C, Leggett DS, Schmidt M, King RW, Gygi SP, Finley D (2006) Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell 127: 1401-1413
5. Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302: 1963-1966
6. Darwin KH, Lin G, Chen Z, Li H, Nathan CF (2005) Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol Microbiol 55: 561-571
7. Deveraux Q, Ustrell V, Pickart C, Rechsteiner M (1994) A 26 S protease subunit that binds ubiquitin conjugates. J Biol Chem 269: 7059-7061
8. Djuranovic S, Hartmann MD, Habeck M, Ursinus A, Zwickl P, Martin J, Lupas AN, Zeth K (2009) Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol Cell 34: 580-590
9. Erbse A, Schmidt R, Bornemann T, Schneider-Mergener J, Mogk A, Zahn R, Dougan DA, Bukau B (2006) ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439: 753-756
10. Fenton WA, Kashi Y, Furtak K, Horwich AL (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371: 614-619
11. Forster A, Masters EI, Whitby FG, Robinson H, Hill CP (2005) The 1.9 A structure of a proteasome-11S activator complex and implications for proteasome-PAN/PA700 interactions. Mol Cell 18: 589-599
12. Forster A, Whitby FG, Hill CP (2003) The pore of activated 20S proteasomes has an ordered 7-fold symmetric conformation. EMBO J 22: 4356-4364 (Pubitemid 37087190)
13. Gandotra S, Schnappinger D, Monteleone M, Hillen W, Ehrt S (2007) In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 13: 1515-1520 (Pubitemid 350224249)
14. Gillette TG, Kumar B, Thompson D, Slaughter CA, DeMartino GN (2008) Differential roles of the COOH termini of AAA subunits of PA700 (19 S regulator) in asymmetric assembly and activation of the 26 S proteasome. J Biol Chem 283: 31813-31822
15. Goldberg AL (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899
16. Hanson PI, Whiteheart SW (2005) AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 6: 519-529
17. Hennecke F, Krebber C, Pluckthun A (1998) Non-repetitive single-chain Fv linkers selected by selectively infective phage (SIP) technology. Protein Eng 11: 405-410 (Pubitemid 28279665)
18. Hinnerwisch J, Fenton WA, Furtak KJ, Farr GW, Horwich AL (2005) Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121: 1029-1041 (Pubitemid 40894633)
19. Hu G, Lin G, Wang M, Dick L, Xu RM, Nathan C, Li H (2006) Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate. Mol Microbiol 59: 1417-1428
20. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453: 481-488 (Pubitemid 351733317)
21. Imkamp F, Rosenberger T, Striebel F, Keller PM, Amstutz B, Sander P, Weber-Ban E (2010) Deletion of dop in Mycobacterium smegmatis abolishes pupylation of protein substrates in vivo. Mol Microbiol 75: 744-754
22. Janse DM, Crosas B, Finley D, Church GM (2004) Localization to the proteasome is sufficient for degradation. J Biol Chem 279: 21415-21420 (Pubitemid 38656551)
23. Knipfer N, Shrader TE (1997) Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol Microbiol 25: 375-383 (Pubitemid 27351588)
24. Kress W, Maglica Z, Weber-Ban E (2009) Clp chaperone-proteases: structure and function. Res Microbiol 160: 618-628
25. Lam YA, Xu W, DeMartino GN, Cohen RE (1997) Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385: 737-740 (Pubitemid 27098096)
26. Lee C, Schwartz MP, Prakash S, Iwakura M, Matouschek A (2001) ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol Cell 7: 627-637 (Pubitemid 32706354)
27. Liao S, Shang Q, Zhang X, Zhang J, Xu C, Tu X (2009) Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem J 422: 207-215
28. Lin G, Hu G, Tsu C, Kunes YZ, Li H, Dick L, Parsons T, Li P, Chen Z, Zwickl P, Weich N, Nathan C (2006) Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol Microbiol 59: 1405-1416
29. Lin G, Li D, de Carvalho LP, Deng H, Tao H, Vogt G, Wu K, Schneider J, Chidawanyika T, Warren JD, Li H, Nathan C (2009) Inhibitors selective for mycobacterial versus human pro-teasomes. Nature 461: 621-626
30. Martin A, Baker TA, Sauer RT (2008) Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat Struct Mol Biol 15: 1147-1151
31. Maupin-Furlow JA, Gil MA, Humbard MA, Kirkland PA, Li W, Reuter CJ, Wright AJ (2005) Archaeal proteasomes and other regulatory proteases. Curr Opin Microbiol 8: 720-728 (Pubitemid 41643041)
32. Moore SD, Sauer RT (2007) The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 76: 101-124
33. Pearce MJ, Arora P, Festa RA, Butler-Wu SM, Gokhale RS, Darwin KH (2006) Identification of substrates of the Mycobacterium tuberculosis proteasome. EMBO J 25: 5423-5432 (Pubitemid 44764151)
34. Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322: 1104-1107
35. Petroski MD, Deshaies RJ (2003) Context of multiubiquitin chain attachment influences the rate of Sic1 degradation. Mol Cell 11: 1435-1444
36. Pickart CM, Cohen RE (2004) Proteasomes and their kin: proteases in the machine age. Nat Rev Mol Cell Biol 5: 177-187
37. Piwko W, Jentsch S (2006) Proteasome-mediated protein processing by bidirectional degradation initiated from an internal site. Nat Struct Mol Biol 13: 691-697 (Pubitemid 44175161)
38. Prakash S, Inobe T, Hatch AJ, Matouschek A (2009) Substrate selection by the proteasome during degradation of protein complexes. Nat Chem Biol 5: 29-36
39. Prakash S, Tian L, Ratliff KS, Lehotzky RE, Matouschek A (2004) An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat Struct Mol Biol 11: 830-837 (Pubitemid 39128798)
40. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y (2008) Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol Cell 30: 360-368 (Pubitemid 351615314)
41. Reid BG, Fenton WA, Horwich AL, Weber-Ban EU (2001) ClpA mediates directional translocation of substrate proteins into the ClpP protease. Proc Natl Acad Sci USA 98: 3768-3772
42. Rieger CE, Lee J, Turnbull JL (1997) A continuous spectrophoto-metric assay for aspartate transcarbamylase and ATPases. Anal Biochem 246: 86-95 (Pubitemid 27100511)
43. Sauer RT, Bolon DN, Burton BM, Burton RE, Flynn JM, Grant RA, Hersch GL, Joshi SA, Kenniston JA, Levchenko I, Neher SB, Oakes ES, Siddiqui SM, Wah DA, Baker TA (2004) Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 11 9: 9-18 (Pubitemid 39349316)
44. Schlieker C, Weibezahn J, Patzelt H, Tessarz P, Strub C, Zeth K, Erbse A, Schneider-Mergener J, Chin JW, Schultz PG, Bukau B, Mogk A (2004) Substrate recognition by the AAA+ chaperone ClpB. Nat Struct Mol Biol 11: 607-615 (Pubitemid 38823526)
45. Schrader EK, Harstad KG, Matouschek A (2009) Targeting proteins for degradation. Nat Chem Biol 5: 815-822
46. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL (2007) Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol Cell 27: 731-744 (Pubitemid 47333222)
47. Striebel F, Imkamp F, Sutter M, Steiner M, Mamedov A, Weber-Ban E (2009a) Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat Struct Mol Biol 16: 647-651
48. Striebel F, Kress W, Weber-Ban E (2009b) Controlled destruction: AAA+ ATPases in protein degradation from bacteria to eukar-yotes. Curr Opin Struct Biol 19: 209-217
49. Sutter M, Striebel F, Damberger FF, Allain FH, 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
50. Takeuchi J, Chen H, Coffino P (2007) Proteasome substrate degradation requires association plus extended peptide. EMBO J 26: 123-131 (Pubitemid 46094705)
51. Tamura T, Nagy I, Lupas A, Lottspeich F, Cejka Z, Schoofs G, Tanaka K, De Mot R, Baumeister W (1995) The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr Biol 5: 766-774
52. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19: 94-102 (Pubitemid 30009229)
53. Verma R, Aravind L, Oania R, McDonald WH, Yates III JR, Koonin EV, Deshaies RJ (2002) Role of Rpn11 metalloprotease in deubi-quitination and degradation by the 26S proteasome. Science 298: 611-615 (Pubitemid 35215317)
54. Wang J, Song JJ, Franklin MC, Kamtekar S, Im YJ, Rho SH, Seong IS, Lee CS, Chung CH, Eom SH (2001) Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent pro-teolysis mechanism. Structure 9: 177-184 (Pubitemid 32209191)
55. Wang T, Li H, Lin G, Tang C, Li D, Nathan C, Darwin KH, Li H (2009) Structural insights on the Mycobacterium tuberculosis proteasomal ATPase Mpa. Structure 17: 1377-1385
56. Weber-Ban EU, Reid BG, Miranker AD, Horwich AL (1999) Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 401: 90-93 (Pubitemid 29418449)
57. Wolf S, Nagy I, Lupas A, Pfeifer G, Cejka Z, Muller SA, Engel A, De Mot R, Baumeister W (1998) Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropo-lis. J Mol Biol 277: 13-25 (Pubitemid 28151880)
58. Yao T, Cohen RE (2002) A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419: 403-407
59. Yu Y, Smith DM, Kim HM, Rodriguez V, Goldberg AL, Cheng Y (2010) Interactions of PAN's C-termini with archaeal 20S proteasome and implications for the eukaryotic proteasome-ATPase interactions. EMBO J 29: 692-702
60. Zhang X, Stoffels K, Wurzbacher S, Schoofs G, Pfeifer G, Banerjee T, Parret AH, Baumeister W, De Mot R, Zwickl P (2004) The N-terminal coiled coil of the Rhodococcus erythropolis ARC AAA ATPase is neither necessary for oligomerization nor nucleotide hydrolysis. J Struct Biol 146: 155-165 (Pubitemid 38369028)