1932

Abstract

Interest in bacterial proteasomes was sparked by the discovery that proteasomal degradation is required for the pathogenesis of , one of the world's deadliest pathogens. Although bacterial proteasomes are structurally similar to their eukaryotic and archaeal homologs, there are key differences in their mechanisms of assembly, activation, and substrate targeting for degradation. In this article, we compare and contrast bacterial proteasomes with their archaeal and eukaryotic counterparts, and we discuss recent advances in our understanding of how bacterial proteasomes function to influence microbial physiology.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-091014-104201
2015-10-15
2024-05-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/69/1/annurev-micro-091014-104201.html?itemId=/content/journals/10.1146/annurev-micro-091014-104201&mimeType=html&fmt=ahah

Literature Cited

  1. Babula P, Masarik M, Adam V, Eckschlager T, Stiborova M. 1.  et al. 2012. Mammalian metallothioneins: properties and functions. Metallomics 4:739–50 [Google Scholar]
  2. Barandun J, Delley CL, Ban N, Weber-Ban E. 2.  2013. Crystal structure of the complex between prokaryotic ubiquitin-like protein and its ligase PafA. J. Am. Chem. Soc. 135:6794–97 [Google Scholar]
  3. Bowman LA, McLean S, Poole RK, Fukuto JM. 3.  2011. The diversity of microbial responses to nitric oxide and agents of nitrosative stress close cousins but not identical twins. Adv. Microb. Physiol. 59:135–219 [Google Scholar]
  4. Braun BC, Glickman M, Kraft R, Dahlmann B, Kloetzel PM. 4.  et al. 1999. The base of the proteasome regulatory particle exhibits chaperone-like activity. Nat. Cell Biol. 1:221–26 [Google Scholar]
  5. Burns KE, Cerda-Maira FA, Wang T, Li H, Bishai WR, Darwin KH. 5.  2010. “Depupylation” of prokaryotic ubiquitin-like protein from mycobacterial proteasome substrates. Mol. Cell 39:821–27 [Google Scholar]
  6. Burns KE, McAllister FE, Schwerdtfeger C, Mintseris J, Cerda-Maira F. 6.  et al. 2012. Mycobacterium tuberculosis prokaryotic ubiquitin-like protein-deconjugating enzyme is an unusual aspartate amidase. J. Biol. Chem. 287:37522–29 [Google Scholar]
  7. Burns KE, Pearce MJ, Darwin KH. 7.  2010. Prokaryotic ubiquitin-like protein provides a two-part degron to Mycobacterium proteasome substrates. J. Bacteriol. 192:2933–35 [Google Scholar]
  8. Cerda-Maira FA, McAllister F, Bode NJ, Burns KE, Gygi SP, Darwin KH. 8.  2011. Reconstitution of the Mycobacterium tuberculosis pupylation pathway in Escherichia coli. EMBO Rep. 12:863–70 [Google Scholar]
  9. Cerda-Maira FA, Pearce MJ, Fuortes M, Bishai WR, Hubbard SR, Darwin KH. 9.  2010. Molecular analysis of the prokaryotic ubiquitin-like protein (Pup) conjugation pathway in Mycobacterium tuberculosis. Mol. Microbiol. 77:1123–35 [Google Scholar]
  10. Chau V, Tobias JW, Bachmair A, Marriott D, Ecker DJ. 10.  et al. 1989. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243:1576–83 [Google Scholar]
  11. Chen X, Solomon WC, Kang Y, Cerda-Maira F, Darwin KH, Walters KJ. 11.  2009. Prokaryotic ubiquitin-like protein Pup is intrinsically disordered. J. Mol. Biol. 392:208–17 [Google Scholar]
  12. Dahlmann B, Kopp F, Kuehn L, Hegerl R, Pfeifer G, Baumeister W. 12.  1991. The multicatalytic proteinase (prosome, proteasome): comparison of the eukaryotic and archaebacterial enzyme. Biomed. Biochim. Acta 50:465–69 [Google Scholar]
  13. Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF. 13.  2003. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302:1963–66 [Google Scholar]
  14. Darwin KH, Lin G, Chen Z, Li H, Nathan CF. 14.  2005. Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol. Microbiol. 55:561–71 [Google Scholar]
  15. Delley CL, Laederach J, Ziemski M, Bolten M, Boehringer D, Weber-Ban E. 15.  2014. Bacterial proteasome activator Bpa (Rv3780) is a novel ring-shaped interactor of the mycobacterial proteasome. PLOS ONE 9:e114348 [Google Scholar]
  16. Djuranovic S, Hartmann MD, Habeck M, Ursinus A, Zwickl P. 16.  et al. 2009. Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol. Cell 34:580–90 [Google Scholar]
  17. Elharar Y, Roth Z, Hermelin I, Moon A, Peretz G. 17.  et al. 2014. Survival of mycobacteria depends on proteasome-mediated amino acid recycling under nutrient limitation. EMBO J. 33:1802–14 [Google Scholar]
  18. Eytan E, Ganoth D, Armon T, Hershko A. 18.  1989. ATP-dependent incorporation of 20S protease into the 26S complex that degrades proteins conjugated to ubiquitin. PNAS 86:7751–55 [Google Scholar]
  19. Festa RA, Jones MB, Butler-Wu S, Sinsimer D, Gerads R. 19.  et al. 2011. A novel copper-responsive regulon in Mycobacterium tuberculosis. Mol. Microbiol. 79:133–48 [Google Scholar]
  20. Festa RA, McAllister F, Pearce MJ, Mintseris J, Burns KE. 20.  et al. 2010. Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis. PLOS ONE 5:e8589 [Google Scholar]
  21. Festa RA, Pearce MJ, Darwin KH. 21.  2007. Characterization of the proteasome accessory factor (paf) operon in Mycobacterium tuberculosis. J. Bacteriol. 189:3044–50 [Google Scholar]
  22. Finley D. 22.  2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78:477–513 [Google Scholar]
  23. Gandotra S, Lebron MB, Ehrt S. 23.  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 [Google Scholar]
  24. Gandotra S, Schnappinger D, Monteleone M, Hillen W, Ehrt S. 24.  2007. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat. Med. 13:1515–20 [Google Scholar]
  25. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G. 25.  et al. 1998. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94:615–23 [Google Scholar]
  26. Gold B, Deng H, Bryk R, Vargas D, Eliezer D. 26.  et al. 2008. Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat. Chem. Biol. 4:609–16 [Google Scholar]
  27. Groll M, Ditzel L, Lowe J, Stock D, Bochtler M. 27.  et al. 1997. Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386:463–71 [Google Scholar]
  28. Guth E, Thommen M, Weber-Ban E. 28.  2011. Mycobacterial ubiquitin-like protein ligase PafA follows a two-step reaction pathway with a phosphorylated Pup intermediate. J. Biol. Chem. 286:4412–19 [Google Scholar]
  29. Hammond-Martel I, Yu H, Affar el B. 29.  2012. Roles of ubiquitin signaling in transcription regulation. Cell. Signal. 24:410–21 [Google Scholar]
  30. Heinemeyer W, Fischer M, Krimmer T, Stachon U, Wolf DH. 30.  1997. The active sites of the eukaryotic 20 S proteasome and their involvement in subunit precursor processing. J. Biol. Chem. 272:25200–9 [Google Scholar]
  31. Hong B, Wang L, Lammertyn E, Geukens N, Van Mellaert L. 31.  et al. 2005. Inactivation of the 20S proteasome in Streptomyces lividans and its influence on the production of heterologous proteins. Microbiology 151:3137–45 [Google Scholar]
  32. Hu G, Lin G, Wang M, Dick L, Xu RM. 32.  et al. 2006. Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate. Mol. Microbiol. 59:1417–28 [Google Scholar]
  33. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L. 33.  et al. 2008. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481–88 [Google Scholar]
  34. Imkamp F, Rosenberger T, Striebel F, Keller PM, Amstutz B. 34.  et al. 2010. Deletion of dop in Mycobacterium smegmatis abolishes pupylation of protein substrates in vivo. Mol. Microbiol. 75:744–54 [Google Scholar]
  35. Imkamp F, Striebel F, Sutter M, Ozcelik D, Zimmermann N. 35.  et al. 2010. Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway. EMBO Rep. 11:791–97 [Google Scholar]
  36. Iyer LM, Burroughs AM, Aravind L. 36.  2008. Unraveling the biochemistry and provenance of pupylation: a prokaryotic analog of ubiquitination. Biol. Direct 3:45 [Google Scholar]
  37. Jastrab JB, Wang T, Murphy JP, Bai L, Hu K. 37.  et al. 2015. An adenosine triphosphate-independent proteasome activator contributes to the virulence of Mycobacterium tuberculosis. PNAS 112:E1763–72 [Google Scholar]
  38. Knipfer N, Shrader TE. 38.  1997. Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol. Microbiol. 25:375–83 [Google Scholar]
  39. Kuberl A, Franzel B, Eggeling L, Polen T, Wolters DA, Bott M. 39.  2014. Pupylated proteins in Corynebacterium glutamicum revealed by MudPIT analysis. Proteomics 14:1531–42 [Google Scholar]
  40. Kunjappu MJ, Hochstrasser M. 40.  2014. Assembly of the 20S proteasome. Biochim. Biophys. Acta 1843:2–12 [Google Scholar]
  41. Kwon YD, Nagy I, Adams PD, Baumeister W, Jap BK. 41.  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. 335:233–45 [Google Scholar]
  42. Li D, Li H, Wang T, Pan H, Lin G, Li H. 42.  2010. Structural basis for the assembly and gate closure mechanisms of the Mycobacterium tuberculosis 20S proteasome. EMBO J. 29:2037–47 [Google Scholar]
  43. Liao S, Shang Q, Zhang X, Zhang J, Xu C, Tu X. 43.  2009. Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem. J. 422:207–15 [Google Scholar]
  44. Lin G, Hu G, Tsu C, Kunes YZ, Li H. 44.  et al. 2006. Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol. Microbiol. 59:1405–16 [Google Scholar]
  45. Liu CW, Millen L, Roman TB, Xiong H, Gilbert HF. 45.  et al. 2002. Conformational remodeling of proteasomal substrates by PA700, the 19 S regulatory complex of the 26 S proteasome. J. Biol. Chem. 277:26815–20 [Google Scholar]
  46. Lowe J, Stock D, Jap B, Zwickl P, Baumeister W, Huber R. 46.  1995. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268:533–39 [Google Scholar]
  47. MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, Nathan CF. 47.  1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. PNAS 94:5243–48 [Google Scholar]
  48. Martin A, Baker TA, Sauer RT. 48.  2008. Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat. Struct. Mol. Biol. 15:1147–51 [Google Scholar]
  49. Maupin-Furlow JA. 49.  2014. Prokaryotic ubiquitin-like protein modification. Annu. Rev. Microbiol. 68:155–75 [Google Scholar]
  50. Mc Cormack T, Baumeister W, Grenier L, Moomaw C, Plamondon L. 50.  et al. 1997. Active site-directed inhibitors of Rhodococcus 20 S proteasome. Kinetics and mechanism. J. Biol. Chem. 272:26103–9 [Google Scholar]
  51. Merkx R, Burns KE, Slobbe P, El Oualid F, El Atmioui D. 51.  et al. 2012. Synthesis and evaluation of a selective fluorogenic Pup derived assay reagent for Dop, a potential drug target in Mycobacterium tuberculosis. ChemBioChem 13:2056–60 [Google Scholar]
  52. Nussbaum AK, Dick TP, Keilholz W, Schirle M, Stevanovic S. 52.  et al. 1998. Cleavage motifs of the yeast 20S proteasome beta subunits deduced from digests of enolase 1. PNAS 95:12504–9 [Google Scholar]
  53. Ozcelik D, Barandun J, Schmitz N, Sutter M, Guth E. 53.  et al. 2012. Structures of Pup ligase PafA and depupylase Dop from the prokaryotic ubiquitin-like modification pathway. Nat. Commun. 3:1014 [Google Scholar]
  54. Pearce MJ, Arora P, Festa RA, Butler-Wu SM, Gokhale RS, Darwin KH. 54.  2006. Identification of substrates of the Mycobacterium tuberculosis proteasome. EMBO J. 25:5423–32 [Google Scholar]
  55. Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH. 55.  2008. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322:1104–7 [Google Scholar]
  56. Poulsen C, Akhter Y, Jeon AH, Schmitt-Ulms G, Meyer HE. 56.  et al. 2010. Proteome-wide identification of mycobacterial pupylation targets. Mol. Syst. Biol. 6:386 [Google Scholar]
  57. Prakash S, Tian L, Ratliff KS, Lehotzky RE, Matouschek A. 57.  2004. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 11:830–37 [Google Scholar]
  58. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y. 58.  2008. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30:360–68 [Google Scholar]
  59. Raule M, Cerruti F, Benaroudj N, Migotti R, Kikuchi J. 59.  et al. 2014. PA28αβ reduces size and increases hydrophilicity of 20S immunoproteasome peptide products. Chem. Biol. 21:470–80 [Google Scholar]
  60. Ravid T, Hochstrasser M. 60.  2008. Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 9:679–90 [Google Scholar]
  61. Rowland JL, Niederweis M. 61.  2013. A multicopper oxidase is required for copper resistance in Mycobacterium tuberculosis. J. Bacteriol. 195:3724–33 [Google Scholar]
  62. Russell DG. 62.  2011. Mycobacterium tuberculosis and the intimate discourse of a chronic infection. Immunol. Rev. 240:252–68 [Google Scholar]
  63. Samanovic MI, Tu S, Novak O, Lakshminarayan I, McAllister F. 63.  et al. 2015. Proteasomal control of cytokinin synthesis protects Mycobacterium tuberculosis against nitric oxide. Mol. Cell 57:984–94 [Google Scholar]
  64. Schreiner P, Chen X, Husnjak K, Randles L, Zhang N. 64.  et al. 2008. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 453:548–52 [Google Scholar]
  65. Seemuller E, Lupas A, Stock D, Lowe J, Huber R, Baumeister W. 65.  1995. Proteasome from Thermoplasma acidophilum: a threonine protease. Science 268:579–82 [Google Scholar]
  66. Shi X, Festa RA, Ioerger TR, Butler-Wu S, Sacchettini JC. 66.  et al. 2014. The copper-responsive RicR regulon contributes to Mycobacterium tuberculosis virulence. mBio 5:e00876 [Google Scholar]
  67. Smirnov D, Dhall A, Sivanesam K, Sharar RJ, Chatterjee C. 67.  2013. Fluorescent probes reveal a minimal ligase recognition motif in the prokaryotic ubiquitin-like protein from Mycobacterium tuberculosis. J. Am. Chem. Soc. 135:2887–90 [Google Scholar]
  68. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL. 68.  2007. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol. Cell 27:731–44 [Google Scholar]
  69. Smith DM, Kafri G, Cheng Y, Ng D, Walz T, Goldberg AL. 69.  2005. ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol. Cell 20:687–98 [Google Scholar]
  70. Stadtmueller BM, Hill CP. 70.  2011. Proteasome activators. Mol. Cell 41:8–19 [Google Scholar]
  71. Streich FC Jr, Lima CD. 71.  2014. Structural and functional insights to ubiquitin-like protein conjugation. Annu. Rev. Biophys. 43:357–79 [Google Scholar]
  72. Striebel F, Hunkeler M, Summer H, Weber-Ban E. 72.  2010. The mycobacterial Mpa-proteasome unfolds and degrades pupylated substrates by engaging Pup's N-terminus. EMBO J. 29:1262–71 [Google Scholar]
  73. Striebel F, Imkamp F, Sutter M, Steiner M, Mamedov A, Weber-Ban E. 73.  2009. Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat. Struct. Mol. Biol. 16:647–51 [Google Scholar]
  74. Suraweera A, Munch C, Hanssum A, Bertolotti A. 74.  2012. Failure of amino acid homeostasis causes cell death following proteasome inhibition. Mol. Cell 48:242–53 [Google Scholar]
  75. Sutter M, Striebel F, Damberger FF, Allain FH, Weber-Ban E. 75.  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. 583:3151–57 [Google Scholar]
  76. Tamura T, Nagy I, Lupas A, Lottspeich F, Cejka Z. 76.  et al. 1995. The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr. Biol. 5:766–74 [Google Scholar]
  77. Tomko RJ Jr, Hochstrasser M. 77.  2013. Molecular architecture and assembly of the eukaryotic proteasome. Annu. Rev. Biochem. 82:415–45 [Google Scholar]
  78. Unno M, Mizushima T, Morimoto Y, Tomisugi Y, Tanaka K. 78.  et al. 2002. The structure of the mammalian 20S proteasome at 2.75 Å resolution. Structure 10:609–18 [Google Scholar]
  79. Verma R, Aravind L, Oania R, McDonald WH, Yates JR III. 79.  et al. 2002. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:611–15 [Google Scholar]
  80. Wang T, Darwin KH, Li H. 80.  2010. Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation. Nat. Struct. Mol. Biol. 17:1352–57 [Google Scholar]
  81. Wang T, Li H, Lin G, Tang C, Li D. 81.  et al. 2009. Structural insights on the Mycobacterium tuberculosis proteasomal ATPase Mpa. Structure 17:1377–85 [Google Scholar]
  82. Watrous J, Burns K, Liu WT, Patel A, Hook V. 82.  et al. 2010. Expansion of the mycobacterial “PUPylome.”. Mol. Biosyst. 6:376–85 [Google Scholar]
  83. Whitby FG, Masters EI, Kramer L, Knowlton JR, Yao Y. 83.  et al. 2000. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408:115–20 [Google Scholar]
  84. Witt S, Kwon YD, Sharon M, Felderer K, Beuttler M. 84.  et al. 2006. Proteasome assembly triggers a switch required for active-site maturation. Structure 14:1179–88 [Google Scholar]
  85. Wolf S, Nagy I, Lupas A, Pfeifer G, Cejka Z. 85.  et al. 1998. Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropolis. J. Mol. Biol. 277:13–25 [Google Scholar]
  86. Zhang X, Stoffels K, Wurzbacher S, Schoofs G, Pfeifer G. 86.  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. 146:155–65 [Google Scholar]
  87. Zuhl F, Seemuller E, Golbik R, Baumeister W. 87.  1997. Dissecting the assembly pathway of the 20S proteasome. FEBS Lett. 418:189–94 [Google Scholar]
  88. Zuhl F, Tamura T, Dolenc I, Cejka Z, Nagy I. 88.  et al. 1997. Subunit topology of the Rhodococcus proteasome. FEBS Lett. 400:83–90 [Google Scholar]
/content/journals/10.1146/annurev-micro-091014-104201
Loading
/content/journals/10.1146/annurev-micro-091014-104201
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error