Prokaryotic proteasomes: Nanocompartments of degradation

Journal of Molecular Microbiology and Biotechnology

Volumn 23, Issue 4-5, 2013, Pages 321-334

  Humbard, Matthew A ^a   Maupin Furlow, Julie A ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Prokaryotic ubiquitin like protein; Pupylation; Sampylation; Small archaeal modifier proteins

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; OLIGONUCLEOTIDE; PROKARYOTIC PROTEASOME; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; MICROORGANISM PROTEIN; PROKARYOTIC UBIQUITIN LIKE PROTEIN; PROTEINASE; SMALL ARCHAEAL MODIFIER PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; EUKARYOTE; HEAT SHOCK; MOLECULAR WEIGHT; NONHUMAN; PROKARYOTE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TARGETING; PYROCOCCUS FURIOSUS; RHODOCOCCUS ERYTHROPOLIS; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; THERMOPLASMA ACIDOPHILUM; UBIQUITINATION; ACTINOBACTERIA; ADENYLATION; ARCHAEON; DEAMINATION; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTIC CELL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN UNFOLDING; STRUCTURE ANALYSIS;

ACTINOBACTERIA; ARCHAEA; EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTA;

EID: 84881484794     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000351348     Document Type: Article

References (119)

1. Akopian TN, Kisselev AF, Goldberg AL: Processive degradation of proteins and other catalytic properties of the proteasome from Thermoplasma acidophilum. J Biol Chem 1997; 272:1791-1798.
2. Asher G, Tsvetkov P, Kahana C, Shaul Y: A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73. Genes Dev 2005; 19:316-321.
3. Bader M, Steller H: Regulation of cell death by the ubiquitin-proteasome system. Curr Opin Cell Biol 2009; 21:878-884.
4. Bar-Nun S, Glickman MH: Proteasomal AAA-ATPases: structure and function. Biochim Biophys Acta 2012; 1823:67-82.
5. Barthelme D, Sauer RT: Identification of the Cdc48 * 20S proteasome as an ancient AAA+ proteolytic machine. Science 2012; 337:843-846.
6. Barthelme D, Sauer RT: Bipartite determinants mediate an evolutionarily conserved interaction between Cdc48 and the 20S peptidase. Proc Natl Acad Sci USA 2013; 110:3327-3332.
7. Baugh JM, Viktorova EG, Pilipenko EV: Protea-somes can degrade a significant proportion of cellular proteins independent of ubiquitina-tion. J Mol Biol 2009; 386:814-827.
8. Baumeister W, Walz J, Zuhl F, Seemuller E: The proteasome: paradigm of a self-compartmentalizing protease. Cell 1998; 92:367-380.
9. Beck F, Unverdorben P, Bohn S, Schweitzer A, Pfeifer G, Sakata E, Nickell S, Plitzko JM, Villa E, Baumeister W, Forster F: Near-atomic resolution structural model of the yeast 26S proteasome. Proc Natl Acad Sci USA 2012; 109:14870-14875.
10. Benaroudj N, Zwickl P, Seemuller E, Baumeister W, Goldberg AL: ATP hydrolysis by the pro-teasome regulatory complex PAN serves multiple functions in protein degradation. Mol Cell 2003; 11:69-78.
11. Bengtson MH, Joazeiro CA: Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 2010; 467:470-473.
12. Berko D, Tabachnick-Cherny S, Shental-Bechor D, Cascio P, Mioletti S, Levy Y, Admon A, Ziv T, Tirosh B, Goldberg AL, Navon A: The direction of protein entry into the proteasome determines the variety of products and depends on the force needed to unfold its two termini. Mol Cell 2012; 48:601-611.
13. Bochtler M, Ditzel L, Groll M, Hartmann C, Huber R: The proteasome. Annu Rev Biophys Biomol Struct 1999; 28:295-317.
14. Bohn S, Beck F, Sakata E, Walzthoeni T, Beck M, Aebersold R, Forster F, Baumeister W, Nick-ell S: Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc Natl Acad Sci USA 2010; 107: 20992-20997.
15. Brannigan JA, Dodson G, Duggleby HJ, Moody PC, Smith JL, Tomchick DR, Murzin AG: A protein catalytic framework with an N-termi-nal nucleophile is capable of self-activation. Nature 1995; 378:416-419.
16. Burns KE, Cerda-Maira FA, Wang T, Li H, Bishai WR, Darwin KH: 'Depupylation' of prokary-otic ubiquitin-like protein from mycobacte-rial proteasome substrates. Mol Cell 2010a;39: 821-827.
17. Burns KE, Liu WT, Boshoff HI, Dorrestein PC, Barry CE 3rd: Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein. J Biol Chem 2009; 284:3069-3075.
18. Burns KE, McAllister FE, Schwerdtfeger C, Mint-seris J, Cerda-Maira F, Noens EE, Wilmanns M, Hubbard SR, Melandri F, Ovaa H, Gygi SP, Darwin KH: Mycobacterium tuberculosis pro-karyotic ubiquitin-like protein-deconjugat-ing enzyme is an unusual aspartate amidase. J Biol Chem 2012; 287:37522-37529.
19. Burns KE, Pearce MJ, Darwin KH: Prokaryotic ubiquitin-like protein provides a two-part degron to Mycobacterium proteasome substrates. J Bacteriol 2010b;192: 2933-2935.
20. Burroughs AM, Balaji S, Iyer LM, Aravind L: Small but versatile: the extraordinary functional and structural diversity of the beta-grasp fold. Biol Direct 2007; 2:18.
21. Burroughs AM, Iyer LM, Aravind L: Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system. Mol Biosyst 2011; 7:2261-2277.
22. Cerda-Maira FA, McAllister F, Bode NJ, Burns KE, Gygi SP, Darwin KH: Reconstitution of the Mycobacterium tuberculosis pupylation pathway in Escherichia coli. EMBO Rep 2011; 12:863-870.
23. Chen X, Solomon WC, Kang Y, Cerda-Maira F, Darwin KH, Walters KJ: Prokaryotic ubiqui-tin-like protein pup is intrinsically disordered. J Mol Biol 2009; 392:208-217.
24. Dahlmann B, Kopp F, Kuehn L, Niedel B, Pfeifer G, Hegerl R, Baumeister W: The multicata-lytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria. FEBS Lett 1989; 251:125-131.
25. Dahlmann B, Kuehn L, Grziwa A, Zwickl P, Baumeister W: Biochemical properties of the pro-teasome from Thermoplasma acidophilum. Eur J Biochem 1992; 208:789-797.
26. Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF: The proteasome of Mycobac-terium tuberculosis is required for resistance to nitric oxide. Science 2003; 302:1963-1966.
27. Darwin KH, Lin G, Chen Z, Li H, Nathan CF: Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol Microbiol 2005; 55:561-571.
28. De Mot R, Nagy I, Walz J, Baumeister W: Protea-somes and other self-compartmentalizing proteases in prokaryotes. Trends Microbiol 1999; 7:88-92.
29. Delley CL, Striebel F, Heydenreich FM, Ozcelik D, Weber-Ban E: Activity of the mycobacte-rial proteasomal ATPase Mpa is reversibly regulated by pupylation. J Biol Chem 2012; 287:7907-7914.
30. Djuranovic S, Hartmann MD, Habeck M, Ursinus A, Zwickl P, Martin J, Lupas AN, Zeth K: Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol Cell 2009; 34:580-590.
31. Djuranovic S, Rockel B, Lupas AN, Martin J: Characterization of AMA, a new AAA protein from Archaeoglobus and methanogenic archaea. J Struct Biol 2006; 156:130-138.
32. Festa RA, McAllister F, Pearce MJ, Mintseris J, Burns KE, Gygi SP, Darwin KH: Prokaryotic ubiquitin-like protein (Pup) proteome of My-cobacterium tuberculosis. PLoS One 2010; 5:e8589.
33. Forouzan D, Ammelburg M, Hobel CF, Stroh LJ, Sessler N, Martin J, Lupas AN: The archaeal proteasome is regulated by a network of AAA ATPases. J Biol Chem 2012; 287:39254-39262.
34. Forster A, Hill CP: Proteasome degradation: enter the substrate. Trends Cell Biol 2003; 13:550-553.
35. Gandotra S, Schnappinger D, Monteleone M, Hil-len W, Ehrt S: In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 2007; 13:1515-1520.
36. Gillette TG, Kumar B, Thompson D, Slaughter CA, DeMartino GN: 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 2008; 283:31813-31822.
37. Groll M, Brandstetter H, Bartunik H, Bourenkow G, Huber R: Investigations on the maturation and regulation of archaebacterial protea-somes. J Mol Biol 2003; 327:75-83.
38. Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber R: Structure of 20S pro-teasome from yeast at 2.4 Å resolution. Nature 1997; 386:463-471.
39. Grziwa A, Baumeister W, Dahlmann B, Kopp F: Localization of subunits in proteasomes from Thermoplasma acidophilum by immunoelec-tron microscopy. FEBS Lett 1991; 290:186-190.
40. Hegerl R, Pfeifer G, Puhler G, Dahlmann B, Baumeister W: The three-dimensional structure of proteasomes from Thermoplasma acido-philum as determined by electron microscopy using random conical tilting. FEBS Lett 1991; 283:117-121.
41. Hepowit NL, Uthandi S, Miranda HV, Toniutti M, Prunetti L, Olivarez O, De Vera IM, Fa-nucci GE, Chen S, Maupin-Furlow JA: Ar-chaeal JAB1/MPN/MOV34 metalloenzyme (HvJAMM1) cleaves ubiquitin-like small ar-chaeal modifier proteins (SAMPs) from protein-conjugates. Mol Microbiol 2012;86:971-987.
42. Hochstrasser M: Origin and function of ubiqui-tin-like proteins. Nature 2009; 458:422-429.
43. Hu G, Lin G, Wang M, Dick L, Xu RM, Nathan C, Li H: Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate. Mol Microbiol 2006; 59:1417-1428.
44. Humbard MA, Miranda HV, Lim JM, Krause DJ, Pritz JR, Zhou G, Chen S, Wells L, Maupin-Furlow JA: Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax vol-canii. Nature 2010a;463: 54-60.
45. Humbard MA, Reuter CJ, Zuobi-Hasona K, Zhou G, Maupin-Furlow JA: Phosphorylation and methylation of proteasomal proteins of the haloarcheon Haloferax volcanii. Archaea 2010b;2010: 481725.
46. α acetylation and protein levels as well as growth rate and stress responses of Haloferax volcanii. J Bacteriol 2009; 191:3794-3803.
47. Imkamp F, Rosenberger T, Striebel F, Keller PM, Amstutz B, Sander P, Weber-Ban E: Deletion of dop in Mycobacterium smegmatis abolishes pupylation of protein substrates in vivo. Mol Microbiol 2010a;75: 744-754.
48. Imkamp F, Striebel F, Sutter M, Ozcelik D, Zimmermann N, Sander P, Weber-Ban E: Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway. EMBO Rep 2010b;11: 791-797.
49. Jeong YJ, Jeong BC, Song HK: Crystal structure of ubiquitin-like small archaeal modifier protein 1 (SAMP1) from Haloferax volcanii. Biochem Biophys Res Commun 2011; 405:112-117.
50. Kaczowka SJ, Maupin-Furlow JA: Subunit topology of two 20S proteasomes from Haloferax volcanii. J Bacteriol 2003; 185:165-174.
51. Karadzic I, Maupin-Furlow J, Humbard M, Pru-netti L, Singh P, Goodlett DR: Chemical cross-linking, mass spectrometry, and in sili-co modeling of proteasomal 20S core particles of the haloarchaeon Haloferax volcanii. Pro-teomics 2012; 12:1806-1814.
52. Kerscher O, Felberbaum R, Hochstrasser M: Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 2006; 22:159-180.
53. α-acetylation and proteolytic activity of the yeast 20 S proteasome. J Biol Chem 2000; 275: 4635-4639.
54. Kirkland PA, Gil MA, Karadzic IM, Maupin-Fur-low JA: Genetic and proteomic analyses of a proteasome-activating nucleotidase A mutant of the haloarchaeon Haloferax volcanii. J Bacteriol 2008; 190:193-205.
55. Kirkland PA, Maupin-Furlow JA: Stabilization of an archaeal DNA-sliding clamp protein, PCNA, by proteasome-activating nucleotid-ase gene knockout in Haloferax volcanii. FEMS Microbiol Lett 2009; 294:32-36.
56. Kirkland PA, Reuter CJ, Maupin-Furlow JA: Effect of proteasome inhibitor clasto-lactacystin-β-lactone on the proteome of the haloarchaeon Haloferax volcanii. Microbiology 2007; 153:2271-2280.
57. Kisselev AF, Akopian TN, Goldberg AL: Range of sizes of peptide products generated during degradation of different proteins by archaeal pro-teasomes. J Biol Chem 1998; 273: 1982-1989.
58. Kisselev AF, Akopian TN, Woo KM, Goldberg AL: The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes: implications for understanding the degrada-tive mechanism and antigen presentation. J Biol Chem 1999; 274:3363-3371.
59. Kwon YD, Nagy I, Adams PD, Baumeister W, Jap BK: Crystal structures of the Rhodococcus proteasome with and without its pro-pep-tides: implications for the role of the pro-pep-tide in proteasome assembly. J Mol Biol 2004; 335:233-245.
60. Lamichhane G, Raghunand TR, Morrison NE, Woolwine SC, Tyagi S, Kandavelou K, Bishai WR: Deletion of a Mycobacterium tubercu losis proteasomal ATPase homologue gene produces a slow-growing strain that persists in host tissues. J Infect Dis 2006; 194:1233-1240.
61. Leidel S, Pedrioli PG, Bucher T, Brost R, Costanzo M, Schmidt A, Aebersold R, Boone C, Hofmann K, Peter M: Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA. Nature 2009; 458: 228-232.
62. Le Tallec B, Barrault MB, Courbeyrette R, Guerois R, Marsolier-Kergoat MC, Pey-roche A: 20S proteasome assembly is orchestrated by two distinct pairs of chaperones in yeast and in mammals. Mol Cell 2007; 27: 660-674.
63. Li D, Li H, Wang T, Pan H, Lin G: Structural basis for the assembly and gate closure mechanisms of the Mycobacterium tuberculosis 20S prote-asome. Embo J 2010; 29:2037-2047.
64. Liao S, Shang Q, Zhang X, Zhang J, Xu C, Tu X: Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem J 2009; 422:207-215.
65. Lin G, Hu G, Tsu C, Kunes YZ, Li H, Dick L, Parsons T, Li P, Chen Z, Zwickl P, Weich N, Nathan C: Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol Microbiol 2006; 59:1405-1416.
66. Löwe J, Stock D, Jap B, Zwickl P, Baumeister W, Huber R: Crystal structure of the 20S protea-some from the archaeon T. acidophilum at 3.4 Å resolution. Science 1995; 268:533-539.
67. Lupas A, Koster AJ, Walz J, Baumeister W: Predicted secondary structure of the 20 S protea-some and model structure of the putative peptide channel. FEBS Lett 1994; 354:45-49.
68. Madding LS, Michel JK, Shockley KR, Conners SB, Epting KL, Johnson MR, Kelly RM: Role of the β1 subunit in the function and stability of the 20S proteasome in the hyperthermo-philic archaeon Pyrococcus furiosus. J Bacte-riol 2007; 189:583-590.
69. Makarova KS, Koonin EV: Archaeal ubiquitin-like proteins: functional versatility and putative ancestral involvement in tRNA modification revealed by comparative genomic analysis. Archaea 2010; 2010:710303.
70. Maupin-Furlow JA, Aldrich HC, Ferry JG: Biochemical characterization of the 20S protea-some from the methanoarchaeon Methano-sarcina thermophila. J Bacteriol 1998; 180: 1480-1487.
71. Maupin-Furlow JA, Wilson HL, Kaczowka SJ, Ou MS: Proteasomes in the Archaea: from structure to function. Front Biosci 2000; 5:D837-D865.
72. Medalia N, Beer A, Zwickl P, Mihalache O, Beck M, Medalia O, Navon A: Architecture and molecular mechanism of PAN, the archaeal proteasome regulatory ATPase. J Biol Chem 2009; 284:22952-22960.
73. Mehnert M, Sommer T, Jarosch E: ERAD ubiqui-tin ligases: multifunctional tools for protein quality control and waste disposal in the en-doplasmic reticulum. Bioessays 2010; 32:905-913.
74. Meyer H, Bug M, Bremer S: Emerging functions of the VCP/p97 AAA-ATPase in the ubiqui-tin system. Nat Cell Biol 2012; 14:117-123.
75. Miranda HV, Nembhard N, Su D, Hepowit N, Krause DJ, Pritz JR, Phillips C, Soll D, Mau-pin-Furlow JA: E1-and ubiquitin-like proteins provide a direct link between protein conjugation and sulfur transfer in Archaea. Proc Natl Acad Sci USA 2011; 108:4417-4422.
76. Murzin AG: OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. Embo J 1993; 12:861-867.
77. Nagy I, Tamura T, Vanderleyden J, Baumeister W, De Mot R: The 20S proteasome of Strepto-myces coelicolor. J Bacteriol 1998; 180:5448-5453.
78. Navon A, Goldberg AL: Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol Cell 2001; 8: 1339-1349.
79. Nunoura T, Takaki Y, Kakuta J, Nishi S, Sugahara J, Kazama H, Chee GJ, Hattori M, Kanai A, Atomi H, Takai K, Takami H: Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res 2011; 39:3204-3223.
80. Park S, Isaacson R, Kim HT, Silver PA, Wagner G: Ufd1 exhibits the AAA-ATPase fold with two distinct ubiquitin interaction sites. Structure 2005; 13:995-1005.
81. Pearce MJ, Arora P, Festa RA, Butler-Wu SM, Gokhale RS, Darwin KH: Identification of substrates of the Mycobacterium tuberculosis proteasome. Embo J 2006; 25:5423-5432.
82. Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH: Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 2008; 322:1104-1107.
83. Poulsen C, Akhter Y, Jeon AH, Schmitt-Ulms G, Meyer HE, Stefanski A, Stuhler K, Wilmanns M, Song YH: Proteome-wide identification of mycobacterial pupylation targets. Mol Syst Biol 2010; 6:386.
84. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y: Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol Cell 2008; 30:360-368.
85. Ranjan N, Damberger FF, Sutter M, Allain FH, Weber-Ban E: Solution structure and activation mechanism of ubiquitin-like small ar-chaeal modifier proteins. J Mol Biol 2011; 405: 1040-1055.
86. Religa TL, Sprangers R, Kay LE: Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR. Science 2010; 328: 98-102.
87. Reuter CJ, Kaczowka SJ, Maupin-Furlow JA: Differential regulation of the PanA and PanB proteasome-activating nucleotidase and 20S proteasomal proteins of the haloarchaeon Haloferax volcanii. J Bacteriol 2004; 186: 7763-7772.
88. Ruepp A, Rockel B, Gutsche I, Baumeister W, Lu-pas AN: The chaperones of the archaeon Thermoplasma acidophilum. J Struct Biol 2001; 135:126-138.
89. Ruschak AM, Religa TL, Breuer S, Witt S, Kay LE: The proteasome antechamber maintains substrates in an unfolded state. Nature 2010; 467: 868-871.
90. Sauer RT, Baker TA: AAA+ proteases: ATP-fu-eled machines of protein destruction. Annu Rev Biochem 2011; 80:587-612.
91. Seemuller E, Lupas A, Stock D, Lowe J, Huber R, Baumeister W: Proteasome from Thermoplasma acidophilum: a threonine protease. Science 1995; 268:579-582.
92. Sharon M, Witt S, Felderer K, Rockel B, Baumeister W, Robinson CV: 20S proteasomes have the potential to keep substrates in store for continual degradation. J Biol Chem 2006; 281: 9569-9575.
93. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL: Docking of the proteasomal ATPases' carboxyl termini in the 20S protea-some's α ring opens the gate for substrate entry. Mol Cell 2007; 27:731-744.
94. Smith DM, Fraga H, Reis C, Kafri G, Goldberg AL: ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 2011; 144:526-538.
95. Smith DM, Kafri G, Cheng Y, Ng D, Walz T, Goldberg AL: ATP binding to PAN or the 26S ATPases causes association with the 20S pro-teasome, gate opening, and translocation of unfolded proteins. Mol Cell 2005; 20:687-698.
96. Snider J, Thibault G, Houry WA: The AAA+ su-perfamily of functionally diverse proteins. Genome Biol 2008; 9:216.
97. Stadtmueller BM, Hill CP: Proteasome activators. Mol Cell 2011; 41:8-19.
98. 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 2010; 29: 1262-1271.
99. Striebel F, Imkamp F, Sutter M, Steiner M, Mam-edov A, Weber-Ban E: Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat Struct Mol Biol 2009; 16:647-651.
100. Summer H, Bruderer R, Weber-Ban E: Characterization of a new AAA+ protein from Archaea. J Struct Biol 2006; 156:120-129.
101. Tamura T, Nagy I, Lupas A, Lottspeich F, Cejka Z, Schoofs G, Tanaka K, De Mot R, Baumeister W: The first characterization of a eubacte-rial proteasome: the 20S complex of Rhodo-coccus. Curr Biol 1995; 5:766-774.
102. Tomko RJ Jr, Funakoshi M, Schneider K, Wang J, Hochstrasser M: Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: implications for proteasome structure and assembly. Mol Cell 2010; 38:393-403.
103. Tomko RJ Jr, Hochstrasser M: Order of the pro-teasomal ATPases and eukaryotic protea-some assembly. Cell Biochem Biophys 2011; 60:13-20.
104. Valafar H, Mayer KL, Bougault CM, LeBlond PD, Jenney FE Jr, Brereton PS, Adams MW, Pre-stegard JH: Backbone solution structures of proteins using residual dipolar couplings: application to a novel structural genomics target. J Struct Funct Genomics 2004; 5:241-254.
105. Van der Veen AG, Schorpp K, Schlieker C, Buti L, Damon JR, Spooner E, Ploegh HL, Jentsch S: Role of the ubiquitin-like protein Urm1 as a noncanonical lysine-directed protein modifier. Proc Natl Acad Sci USA 2011; 108:1763-1770.
106. Volker C, Lupas AN: Molecular evolution of proteasomes. Curr Top Microbiol Immunol 2002; 268:1-22.
107. Wang T, Darwin KH, Li H: Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation. Nat Struct Mol Biol 2010; 17:1352-1357.
108. Wang T, Li H, Lin G, Tang C, Li D, Nathan C, Darwin KH: Structural insights on the Myco-bacterium tuberculosis proteasomal ATPase Mpa. Structure 2009; 17:1377-1385.
109. Watrous J, Burns K, Liu WT, Patel A, Hook V, Bafna V, Barry CE 3rd, Bark S, Dorrestein PC: Expansion of the mycobacterial 'PUPylome'. Mol Biosyst 2010; 6:376-385.
110. Wenzel T, Eckerskorn C, Lottspeich F, Baumeister W: Existence of a molecular ruler in pro-teasomes suggested by analysis of degradation products. FEBS Lett 1994; 349:205-209.
111. Wilson HL, Aldrich HC, Maupin-Furlow J: Halo-philic 20S proteasomes of the archaeon Haloferax volcanii: purification, characterization, and gene sequence analysis. J Bacteriol 1999; 181:5814-5824.
112. Wilson HL, Ou MS, Aldrich HC, Maupin-Furlow J: Biochemical and physical properties of the Methanococcus jannaschii 20S proteasome and PAN, a homolog of the ATPase (Rpt) sub-units of the eucaryal 26S proteasome. J Bacte-riol 2000; 182:1680-1692.
113. Wolf S, Nagy I, Lupas A, Pfeifer G, Cejka Z, Muller SA, Engel A, De Mot R, Baumeister W: Characterization of ARC, a divergent member of the AAA ATPase family from Rhodo-coccus erythropolis. J Mol Biol 1998; 277:13-25.
114. Yu Y, Smith DM, Kim HM, Rodriguez V, Goldberg AL, Cheng Y: Interactions of PAN's C-termini with archaeal 20S proteasome and implications for the eukaryotic proteasome-ATPase interactions. Embo J 2010; 29:692-702.
115. Zhang F, Hu M, Tian G, Zhang P, Finley D, Jeffrey PD, Shi Y: Structural insights into the regulatory particle of the proteasome from Metha-nocaldococcus jannaschii. Mol Cell 2009a;34: 473-484.
116. Zhang F, Wu Z, Zhang P, Tian G, Finley D, Shi Y: Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jan-naschii. Mol Cell 2009b;34: 485-496.
117. Zhou G, Kowalczyk D, Humbard MA, Rohatgi S, Maupin-Furlow JA: Proteasomal components required for cell growth and stress responses in the haloarchaeon Haloferax volca-nii. J Bacteriol 2008; 190:8096-8105.
118. Zühl F, Seemuller E, Golbik R, Baumeister W: Dissecting the assembly pathway of the 20S proteasome. FEBS Lett 1997; 418:189-194.
119. Zwickl P, Ng D, Woo KM, Klenk HP, Goldberg AL: An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26 S proteasome, activates protein breakdown by 20 S protea-somes. J Biol Chem 1999; 274:26008-26014.