Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity

Molecular Microbiology

Volumn 59, Issue 5, 2006, Pages 1405-1416

  Lin, Gang ^a   Hu, Guiqing ^b   Tsu, Christopher ^c   Kunes, Yune Z ^c   Li, Huilin ^b   Dick, Lawrence ^c   Parsons, Thomas ^c   Li, Ping ^c   Chen, Zhiqiang ^b   Zwickl, Peter ^d   Weich, Nadine ^c   Nathan, Carl ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c MILLENNIUM PHARMACEUTICALS INC   (United States)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGOPEPTIDE; PROTEASOME;

ACTINOBACTERIA; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BETA CHAIN; CONTROLLED STUDY; ELECTRON MICROSCOPY; ESCHERICHIA COLI; GENE DELETION; GENE FUNCTION; GENETIC CODE; HYDROPHOBICITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; RHODOCOCCUS ERYTHROPOLIS;

BACTERIAL PROTEINS; BINDING SITES; GENE EXPRESSION REGULATION, BACTERIAL; ION CHANNEL GATING; MICROSCOPY, ELECTRON; MUTATION; MYCOBACTERIUM TUBERCULOSIS; OLIGOPEPTIDES; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; SUBSTRATE SPECIFICITY; SUBTILISINS; TITRIMETRY;

ACTINOBACTERIA; ACTINOBACTERIA (CLASS); ARCHAEA; BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS; RHODOCOCCUS; RHODOCOCCUS ERYTHROPOLIS;

EID: 33645073409     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.05035.x     Document Type: Article

References (48)

1. Akopian TN. Kisselev AF. Goldberg AL. 1997 Processive degradation of proteins and other catalytic properties of the proteasome from Thermoplasma acidophilum J Biol Chem 272 1791 1798
2. Arendt CS. Hochstrasser M. 1999 Eukaryotic 20S proteasome catalytic subunit propeptides prevent active site inactivation by N-terminal acetylation and promote particle assembly EMBO J 18 3575 3585
3. Baumeister W. Walz J. Zuhl F. Seemuller E. 1998 The proteasome: paradigm of a self-compartmentalizing protease Cell 92 367 380
4. Benaroudj N. Zwickl P. Seemuller E. Baumeister W. Goldberg AL. 2003 ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation Mol Cell 11 69 78
5. Chen P. Hochstrasser M. 1996 Autocatalytic subunit processing couples active site formation in the 20S proteasome to completion of assembly Cell 86 961 972
6. Cole ST. Brosch R. Parkhill J. Garnier T. Churcher C. Harris D. et al. 1998 Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence Nature 393 537 544
7. Dahlmann B. Kopp F. Kuehn L. Niedel B. Pfeifer G. Hegerl R. Baumeister W. 1989 The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria FEBS Lett 251 125 131
8. 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
9. Darwin KH. Lin G. Chen Z. Li H. Nathan CF. 2005 Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue Mol Microbiol 55 561 571
10. De Mot R. Nagy I. Baumeister W. 1998 A self-compartmentalizing protease in Rhodococcus: the 20S proteasome Antonie Van Leeuwenhoek 74 83 87
11. De Mot R. Nagy I. Walz J. Baumeister W. 1999 Proteasomes and other self-compartmentalizing proteases in prokaryotes Trends Microbiol 7 88 92
12. Dick LR. Moomaw CR. Pramanik BC. DeMartino GN. Slaughter CA. 1992 Identification and localization of a cysteinyl residue critical for the trypsin-like catalytic activity of the proteasome Biochemistry 31 7347 7355
13. Ferrell K. Wilkinson CR. Dubiel W. Gordon C. 2000 Regulatory subunit interactions of the 26S proteasome, a complex problem Trends Biochem Sci 25 83 88
14. 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
15. Frank J. Radermacher M. Penczek P. Zhu J. Li Y. Ladjadj M. Leith A. 1996 SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J Struct Biol 116 190 199
16. Glickman MH. 2000 Getting in and out of the proteasome Semin Cell Dev Biol 11 149 158
17. Groll M. Ditzel L. Lowe J. Stock D. Bochtler M. Bartunik HD. Huber R. 1997 Structure of 20S proteasome from yeast at 2.4 A resolution Nature 386 463 471
18. Groll M. Bajorek M. Kohler A. Moroder L. Rubin DM. Huber R. et al. 2000 A gated channel into the proteasome core particle Nat Struct Biol 7 1062 1067
19. Hu G. Lin G. Wang M. Dick L. Xu R-M. Nathan C. Li H. 2006 Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate Mol Microbiol doi:10.1111/j.1365-2958.2005. 05036.x
20. Kisselev AF. Goldberg AL. 2001 Proteasome inhibitors: from research tools to drug candidates Chem Biol 8 739 758
21. Knipfer N. Shrader TE. 1997 Inactivation of the 20S proteasome in Mycobacterium smegmatis Mol Microbiol 25 375 383
22. Kohler A. Cascio P. Leggett DS. Woo KM. Goldberg AL. Finley D. 2001 The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release Mol Cell 7 1143 1152
23. Kwon YD. Nagy I. Adams PD. Baumeister W. Jap BK. 2004 Crystal structures of the Rhodococcus proteasome with and without its pro-peptides: implications for the role of the pro-peptide in proteasome assembly J Mol Biol 335 233 245
24. Lowe J. Stock D. Jap B. Zwickl P. Baumeister W. Huber R. 1995 Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution Science 268 533 539
25. Ludtke SJ. Baldwin PR. Chiu W. 1999 EMAN: semiautomated software for high-resolution single-particle reconstructions J Struct Biol 128 82 97
26. McCormack T. Baumeister W. Grenier L. Moomaw C. Plamondon L. Pramanik B. et al. 1997 Active site-directed inhibitors of Rhodococcus 20S proteasome. Kinetics and mechanism J Biol Chem 272 26103 26109
27. MacMicking JD. North RJ. LaCourse R. Mudgett JS. Shah SK. Nathan CF. 1997 Identification of nitric oxide synthase as a protective locus against tuberculosis Proc Natl Acad Sci USA 94 5243 5248
28. MacMicking JD. Taylor GA. McKinney JD. 2003 Immune control of tuberculosis by IFN-gamma-inducible LRG-47 Science 302 654 659
29. Mollenkopf HJ. Jungblut PR. Raupach B. Mattow J. Lamer S. Zimny-Arndt U. et al. 1999 A dynamic two-dimensional polyacrylamide gel electrophoresis database: the mycobacterial proteome via Internet Electrophoresis 20 2172 2180
30. Momose I. Sekizawa R. Hashizume H. Kinoshita N. Homma Y. Hamada M. et al. 2001 Tyropeptins A and B, new proteasome inhibitors produced by Kitasatospora sp. MK993-dF2. I. Taxonomy, isolation, physico-chemical properties and biological activities J Antibiot (Tokyo) 54 997 1003
31. Momose I. Umezawa Y. Hirosawa S. Iinuma H. Ikeda D. 2005 Structure-based design of derivatives of tyropeptin A as the potent and selective inhibitors of mammalian 20S proteasome Bioorg Med Chem Lett 15 1867 1871
32. Ortega J. Bernard Heymann J. Kajava AV. Ustrell V. Rechsteiner M. Steven AC. 2005 The axial channel of the 20S proteasome opens upon binding of the PA200 activator J Mol Biol 346 1221 1227
33. Pouch MN. Cournoyer B. Baumeister W. 2000 Characterization of the 20S proteasome from the actinomycete Frankia Mol Microbiol 35 368 377
34. Sassetti CM. Boyd DH. Rubin EJ. 2001 Comprehensive identification of conditionally essential genes in mycobacteria Proc Natl Acad Sci USA 98 12712 12717
35. Savory PJ. Rivett AJ. 1993 Leupeptin-binding site(s) in the mammalian multicatalytic proteinase complex Biochem J 289 45 48
36. Schmidt M. Haas W. Crosas B. Santamaria PG. Gygi SP. Walz T. Finley D. 2005 The HEAT repeat protein Blm10 regulates the yeast proteasome by capping the core particle Nat Struct Mol Biol 12 294 303
37. Seemuller E. Lupas A. Baumeister W. 1996 Autocatalytic processing of the 20S proteasome Nature 382 468 471
38. Stein RL. Melandri F. Dick L. 1996 Kinetic characterization of the chymotryptic activity of the 20S proteasome Biochemistry 35 3899 3908
39. Tamura T. Nagy I. Lupas A. Lottspeich F. Cejka Z. Schoofs G. et al. 1995 The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus Curr Biol 5 766 774
40. Venkatraman P. Wetzel R. Tanaka M. Nukina N. Goldberg AL. 2004 Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins Mol Cell 14 95 104
41. Voges D. Zwickl P. Baumeister W. 1999 The 26S proteasome: a molecular machine designed for controlled proteolysis Annu Rev Biochem 68 1015 1068
42. Wenzel T. Eckerskorn C. Lottspeich F. Baumeister W. 1994 Existence of a molecular ruler in proteasomes suggested by analysis of degradation products FEBS Lett 349 205 209
43. Whitby FG. Masters EI. Kramer L. Knowlton JR. Yao Y. Wang CC. Hill CP. 2000 Structural basis for the activation of 20S proteasomes by 11S regulators Nature 408 115 120
44. Zhang X. Stoffels K. Wurzbacher S. Schoofs G. Pfeifer G. Banerjee T. et al. 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
45. Zühl F. Seemuller E. Golbik R. Baumeister W. 1997a Dissecting the assembly pathway of the 20S proteasome FEBS Lett 418 189 194
46. Zühl F. Tamura T. Dolenc I. Cejka Z. Nagy I. De Mot R. Baumeister W. 1997b Subunit topology of the Rhodococcus proteasome FEBS Lett 400 83 90
47. Zwickl P. 2002 The 20S proteasome Curr Top Microbiol Immunol 268 23 41
48. Zwickl P. Kleinz J. Baumeister W. 1994 Critical elements in proteasome assembly Nat Struct Biol 1 765 770