Prokaryotic ubiquitin-like protein modification

Annual Review of Microbiology

Volumn 68, Issue , 2014, Pages 155-175

  Maupin Furlow, Julie A ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Molybdopterin; Pupylation; Sampylation; Sulfur; TRNA thiolation; TtuB

Indexed keywords

AMIDASE; BACTERIAL PROTEIN; LIGASE; MOLYBDOPTERIN; PROTEASOME; PROTEIN DOP; PROTEIN PAFA; PROTEIN SAMP; PROTEIN TTUB; TRANSFER RNA; UBIQUITIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN;

ACTINOBACTERIA; AMINO ACID SEQUENCE; BIOSYNTHESIS; COMPLEX FORMATION; COVALENT BOND; ENZYME ACTIVITY; NITROSPIRAE; NONHUMAN; NUCLEOPHILICITY; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; THERMUS; UBIQUITINATION; ARCHAEON; BACTERIUM; CHEMISTRY; GENETICS; METABOLISM;

ARCHAEA; ARCHAEAL PROTEINS; BACTERIA; BACTERIAL PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; UBIQUITIN;

EID: 84907506806     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-091313-103447     Document Type: Review

References (137)

1. Agren D, Schnell R, Oehlmann W, SinghM, Schneider G. 2008. Cysteine synthase (CysM) of Mycobacterium tuberculosis is an O-phosphoserine sulfhydrylase: evidence for an alternative cysteine biosynthesis pathway in mycobacteria. J. Biol. Chem. 283:31567-74
2. Ambroggio XI, Rees DC, Deshaies RJ. 2004. JAMM: a metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol. 2:E2
3. Amerik AY, Hochstrasser M. 2004. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695:189-207
4. Barandun J, Delley CL, Ban N,Weber-Ban E. 2013. Crystal structure of the complex between prokaryotic ubiquitin-like protein and its ligase PafA. J. Am. Chem. Soc. 135:6794-97
5. Barandun J, Delley CL, Weber-Ban E. 2012. The pupylation pathway and its role in mycobacteria. BMC Biol. 10:95
6. Burns KE, Cerda-Maira FA, Wang T, Li H, Bishai WR, Darwin KH. 2010. "Depupylation" of prokaryotic ubiquitin-like protein from mycobacterial proteasome substrates. Mol. Cell 39:821-27
7. Burns KE, Darwin KH. 2010. Pupylation: a signal for proteasomal degradation in Mycobacterium tuberculosis. Subcell. Biochem. 54:149-57
8. Burns KE, Darwin KH. 2010. Pupylation versus ubiquitylation: tagging for proteasome-dependent degradation. Cell. Microbiol. 12:424-31
9. Burns KE, Darwin KH. 2012. Pupylation: proteasomal targeting by a protein modifier in bacteria. Methods Mol. Biol. 832:151-60
10. Burns KE, Liu WT, Boshoff HI, Dorrestein PC, Barry CE. 2009. Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein. J. Biol. Chem. 284:3069-75
11. Burns KE, McAllister FE, Schwerdtfeger C, Mintseris J, Cerda-Maira F, et al. 2012. Mycobacterium tuberculosis prokaryotic ubiquitin-like protein-deconjugating enzyme is an unusual aspartate amidase. J. Biol. Chem. 287:37522-29
12. Burns KE, Pearce MJ, Darwin KH. 2010. Prokaryotic ubiquitin-like protein provides a two-part degron to Mycobacterium proteasome substrates. J. Bacteriol. 192:2933-35
13. Burroughs AM, Balaji S, Iyer LM, Aravind L. 2007. A novel superfamily containing the β-grasp fold involved in binding diverse soluble ligands. Biol. Direct 2:4
14. Burroughs AM, Balaji S, Iyer LM, Aravind L. 2007. Small but versatile: the extraordinary functional and structural diversity of the β-grasp fold. Biol. Direct 2:18
15. Burroughs AM, Iyer LM, Aravind L. 2012. Structure and evolution of ubiquitin and ubiquitin-related domains. Methods Mol. Biol. 832:15-63
16. Burroughs AM, Iyer LM, Aravind L. 2012. The natural history of ubiquitin and ubiquitin-related domains. Front. Biosci. 17:1433-60
17. Cerda-Maira FA, McAllister F, Bode NJ, Burns KE, Gygi SP, Darwin KH. 2011. Reconstitution of the Mycobacterium tuberculosis pupylation pathway in Escherichia coli. EMBO Rep. 12:863-70
18. Chen X, Qiu JD, Shi SP, Suo SB, Liang RP. 2013. Systematic analysis and prediction of pupylation sites in prokaryotic proteins. PLoS ONE 8:e74002
19. Chen X, SolomonWC, Kang Y, Cerda-Maira F, Darwin KH, Walters KJ. 2009. Prokaryotic ubiquitinlike protein Pup is intrinsically disordered. J. Mol. Biol. 392:208-17
20. Ciechanover A. 2005. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol. 6:79-87
21. Ciechanover A, Elias S, Heller H, Hershko A. 1982. "Covalent affinity" purification of ubiquitinactivating enzyme. J. Biol. Chem. 257:2537-42
22. Ciechanover A, Heller H, Katz-Etzion R, Hershko A. 1981. Activation of the heat-stable polypeptide of the ATP-dependent proteolytic system. Proc. Natl. Acad. Sci. USA 78:761-65
23. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-44
24. Dahl JU, Urban A, Bolte A, Sriyabhaya P, Donahue JL, et al. 2011. The identification of a novel protein involved in molybdenum cofactor biosynthesis in Escherichia coli. J. Biol. Chem. 286:35801-12
25. Darwin KH. 2009. Prokaryotic ubiquitin-like protein (Pup), proteasomes and pathogenesis. Nat. Rev. Microbiol. 7:485-91
26. DarwinKH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF. 2003. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302:1963-66
27. Darwin KH, Hofmann K. 2010. SAMPyling proteins in archaea. Trends Biochem. Sci. 35:348-51
28. Delley CL, Striebel F, Heydenreich FM, Ozcelik D,Weber-Ban E. 2012. Activity of the mycobacterial proteasomal ATPase Mpa is reversibly regulated by pupylation. J. Biol. Chem. 287:7907-14
29. Festa RA, McAllister F, PearceMJ, Mintseris J, Burns KE, et al. 2010. Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis [corrected]. PLoS ONE 5:e8589
30. Festa RA, Pearce MJ, Darwin KH. 2007. Characterization of the proteasome accessory factor ( paf ) operon in Mycobacterium tuberculosis. J. Bacteriol. 189:3044-50
31. Finley D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78:477-513
32. Forer N, Korman M, Elharar Y, Vishkautzan M, Gur E. 2013. Bacterial proteasome and PafA, the Pup ligase, interact to form a modular protein tagging and degradation machine. Biochemistry 52:9029-35
33. Gandotra S, Lebron MB, Ehrt S. 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
34. Gandotra S, Schnappinger D, Monteleone M, HillenW, Ehrt S. 2007. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat. Med. 13:1515-20
35. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, 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
36. Godert AM, Jin M, McLaffertyFW,Begley TP. 2007. Biosynthesis of the thioquinolobactin siderophore: an interesting variation on sulfur transfer. J. Bacteriol. 189:2941-44
37. Goldstein G, Scheid M, Hammerling U, Schlesinger DH, Niall HD, Boyse EA. 1975. Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells. Proc. Natl. Acad. Sci. USA 72:11-15
38. Guth E, Thommen M,Weber-Ban E. 2011. Mycobacterial ubiquitin-like protein ligase PafA follows a two-step reaction pathway with a phosphorylated Pup intermediate. J. Biol. Chem. 286:4412-19
39. Hartman A, Norais C, Badger J, Delmas S, Haldenby S, et al. 2010. The complete genome sequence of Haloferax volcanii DS2, a model archaeon. PLoS ONE 5:e9605
40. Hepowit NL, Uthandi S, Miranda HV, Toniutti M, Prunetti L, et al. 2012. Archaeal JAB1/MPN/ MOV34 metalloenzyme (HvJAMM1) cleaves ubiquitin-like small archaeal modifier proteins (SAMPs) from protein-conjugates. Mol. Microbiol. 86:971-87
41. Hershko A, Heller H, Elias S, Ciechanover A. 1983. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258:8206-14
42. Hochstrasser M. 2009. Origin and function of ubiquitin-like proteins. Nature 458:422-29
43. Hoeller D, Hecker CM, Wagner S, Rogov V, Dotsch V, Dikic I. 2007. E3-independent monoubiquitination of ubiquitin-binding proteins. Mol. Cell 26:891-98
44. Horiuchi KY, Harpel MR, Shen L, Luo Y, Rogers KC, Copeland RA. 2001. Mechanistic studies of reaction coupling in Glu-tRNAGln amidotransferase. Biochemistry 40:6450-57
45. Huang B, Lu J, Byström AS. 2008. A genome-wide screen identifies genes required for formation of the wobble nucleoside 5-methoxycarbonylmethyl-2-thiouridine in Saccharomyces cerevisiae. RNA 14:2183-94
46. Humbard M, Miranda H, Lim J, Krause D, Pritz J, et al. 2010. Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463:54-60
47. Imkamp F,Rosenberger T, Striebel F, Keller PM, Amstutz B, et al. 2010. Deletion of dop in Mycobacterium smegmatis abolishes pupylation of protein substrates in vivo. Mol. Microbiol. 75:744-54
48. Imkamp F, Striebel F, SutterM, Ozcelik D, Zimmermann N, et al. 2010. Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway. EMBO Rep. 11:791-97
49. Iyer LM,BurroughsAM, AravindL. 2006. The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like β-grasp domains. Genome Biol. 7:R60
50. Iyer LM, Burroughs AM, Aravind L. 2008. Unraveling the biochemistry and provenance of pupylation: a prokaryotic analog of ubiquitination. Biol. Direct 3:45
51. Jackson SP, Durocher D. 2013. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49:795-807
52. Kanda F, Sykes DE, Yasuda H, Sandberg AA, Matsui S. 1986. Substrate recognition of isopeptidase: specific cleavage of the epsilon-(alpha-glycyl)lysine linkage in ubiquitin-protein conjugates. Biochim. Biophys. Acta 870:64-75
53. Katz EJ, Isasa M, Crosas B. 2010. A new map to understand deubiquitination. Biochem. Soc. Trans. 38:21-28
54. Kerscher O, Felberbaum R, HochstrasserM. 2006. Modification of proteins by ubiquitin and ubiquitinlike proteins. Annu. Rev. Cell Dev. Biol. 22:159-80
55. Kessler D. 2006. Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30:825-40
56. Knipfer N, Shrader TE. 1997. Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol. Microbiol. 25:375-83
57. Koonin EV. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11:209
58. Krishnamoorthy K, Begley TP. 2011. Protein thiocarboxylate-dependent methionine biosynthesis in Wolinella succinogenes. J. Am. Chem. Soc. 133:379-86
59. Krishnaswamy PR, Pamiljans V, Meister A. 1960. Activated glutamate intermediate in the enzymatic synthesis of glutamine. J. Biol. Chem. 235:PC39-40
60. Lake MW, Wuebbens MM, Rajagopalan KV, Schindelin H. 2001. Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB-MoaD complex. Nature 414:325-29
61. Lamichhane G, Raghunand TR, Morrison NE, Woolwine SC, Tyagi S, et al. 2006. Deletion of a Mycobacterium tuberculosis proteasomal ATPase homologue gene produces a slow-growing strain that persists in host tissues. J. Infect. Dis. 194:1233-40
62. Leidel S, Pedrioli PG, Bucher T, Brost R, Costanzo M, et al. 2009. Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA. Nature 458:228-32
63. Leigh JA, Albers SV, Atomi H, Allers T. 2011. Model organisms for genetics in the domain Archaea: methanogens, halophiles, Thermococcales and Sulfolobales. FEMS Microbiol. Rev. 35:577-608
64. Leimkuhler S, Freuer A, Araujo JA, Rajagopalan KV, Mendel RR. 2003. Mechanistic studies of human molybdopterin synthase reaction and characterization of mutants identified in group B patients of molybdenum cofactor deficiency. J. Biol. Chem. 278:26127-34
65. Leimkuhler S, Wuebbens MM, Rajagopalan KV. 2001. Characterization of Escherichia coli MoeB and its involvement in the activation of molybdopterin synthase for the biosynthesis of the molybdenum cofactor. J. Biol. Chem. 276:34695-701
66. 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. 422:207-15
67. Liaw SH, Eisenberg D. 1994. Structural model for the reaction mechanism of glutamine synthetase, based on five crystal structures of enzyme-substrate complexes. Biochemistry 33:675-81
68. Lin G, Chidawanyika T, Tsu C, Warrier T, Vaubourgeix J, et al. 2013. N,C-Capped dipeptides with selectivity for mycobacterial proteasome over human proteasomes: role of S3 and S1 binding pockets. J. Am. Chem. Soc. 135:9968-71
69. Lin G, Li D, de Carvalho LP, Deng H, Tao H, et al. 2009. Inhibitors selective for mycobacterial versus human proteasomes. Nature 461:621-26
70. Liu Z, Ma Q, Cao J, Gao X, Ren J, Xue Y. 2011. GPS-PUP: computational prediction of pupylation sites in prokaryotic proteins. Mol. Biosyst. 7:2737-40
71. Lorenz S, Cantor AJ, Rape M, Kuriyan J. 2013. Macromolecular juggling by ubiquitylation enzymes. BMC Biol. 11:65
72. Lupas A, Zwickl P, Baumeister W. 1994. Proteasome sequences in eubacteria. Trends Biochem. Sci. 19:533-34
73. Makarova KS, Koonin EV. 2010. Archaeal ubiquitin-like proteins: functional versatility and putative ancestral involvement in tRNA modification revealed by comparative genomic analysis. Archaea 2010:710303
74. Maldonado AY, Burz DS, Reverdatto S, Shekhtman A. 2013. Fate of Pup inside the Mycobacterium proteasome studied by in-cell NMR. PLoS ONE 8:e74576
75. Marchese A, Trejo J. 2013. Ubiquitin-dependent regulation of G protein-coupled receptor trafficking and signaling. Cell. Signal. 25:707-16
76. Marelja Z, Mullick Chowdhury M, Dosche C, Hille C, Baumann O, et al. 2013. The L-cysteine desulfurase NFS1 is localized in the cytosol where it provides the sulfur for molybdenum cofactor biosynthesis in humans. PLoS ONE 8:e60869
77. Maupin-Furlow J. 2012. Proteasomes and protein conjugation across domains of life. Nat. Rev. Microbiol. 10:100-11
78. Maupin-Furlow JA. 2013. Archaeal proteasomes and sampylation. Subcell. Biochem. 66:297-327
79. Maupin-Furlow JA. 2013. Ubiquitin-like proteins and their roles in archaea. Trends Microbiol. 21:31-38
80. McGrath JP, Jentsch S, Varshavsky A. 1991. UBA1: an essential yeast gene encoding ubiquitin-activating enzyme. EMBO J. 10:227-36
81. Mendel RR, Kruse T. 2012. Cell biology of molybdenum in plants and humans. Biochim. Biophys. Acta 1823:1568-79
82. Midelfort CF, Rose IA. 1976. A stereochemical method for detection of ATP terminal phosphate transfer in enzymatic reactions. Glutamine synthetase. J. Biol. Chem. 251:5881-87
83. Min M, Mayor U, Lindon C. 2013. Ubiquitination site preferences in anaphase promoting complex/ cyclosome (APC/C) substrates. Open Biol. 3:130097
84. Miranda H, Nembhard N, Su D, Hepowit N, Krause D, et al. 2011. E1- and ubiquitin-like proteins provide a direct link between protein conjugation and sulfur transfer in archaea. Proc. Natl. Acad. Sci. USA 108:4417-22
85. Miranda HV, Antelmann H, Hepowit N, Chavarria NE, Krause DJ, et al. 2014. Archaeal ubiquitinlike SAMP3 is isopeptide-linked to proteins via a UbaA-dependent mechanism. Mol. Cell. Proteomics 13:220-39
86. Moffat JM, Mintern JD, Villadangos JA. 2013. Control of MHC II antigen presentation by ubiquitination. Curr. Opin. Immunol. 25:109-14
87. Nakagawa H, Kuratani M, Goto-Ito S, Ito T, Katsura K, et al. 2013. Crystallographic and mutational studies on the tRNA thiouridine synthetase TtuA. Proteins 81:1232-44
88. Nakai Y, Harada A, Hashiguchi Y, Nakai M, Hayashi H. 2012. Arabidopsis molybdopterin biosynthesis protein Cnx5 collaborates with the ubiquitin-like protein Urm11 in the thio-modification of tRNA. J. Biol. Chem. 287:30874-84
89. Nakai Y, Nakai M, Hayashi H. 2008. Thio-modification of yeast cytosolic tRNA requires a ubiquitinrelated system that resembles bacterial sulfur transfer systems. J. Biol. Chem. 283:27469-76
90. Nercessian D, de Castro RE, Conde RD. 2002. Ubiquitin-like proteins in halobacteria. J. BasicMicrobiol. 42:277-83
91. Nercessian D, Marino Buslje C, Ordonez MV, de Castro RE, Conde RD. 2009. Presence of structural homologs of ubiquitin in haloalkaliphilic Archaea. Int. Microbiol. 12:167-73
92. Noma A, Sakaguchi Y, Suzuki T. 2009. Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions. Nucleic Acids Res. 37:1335-52
93. Nunoura T, Takaki Y, Kakuta J, Nishi S, Sugahara J, et al. 2011. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39:3204-23
94. Ofer N, Forer N, Korman M, Vishkautzan M, Khalaila I, Gur E. 2013. Allosteric transitions direct protein tagging by PafA, the prokaryotic ubiquitin-like protein (Pup) ligase. J. Biol. Chem. 288:11287-93
95. OLeary SE, Jurgenson CT, Ealick SE, Begley TP. 2008. O-phospho-L-serine and the thiocarboxylated sulfur carrier protein CysO-COSH are substrates for CysM, a cysteine synthase from Mycobacterium tuberculosis. Biochemistry 47:11606-15
96. Orlowski M, Meister A. 1971. Partial reactions catalyzed by γ-glutamylcysteine synthetase and evidence for an activated glutamate intermediate. J. Biol. Chem. 246:7095-105
97. Ozcelik D, Barandun J, Schmitz N, Sutter M, Guth E, et al. 2012. Structures of Pup ligase PafA and depupylase Dop from the prokaryotic ubiquitin-like modification pathway. Nat. Commun. 3:1014
98. Pearce MJ, Arora P, Festa RA, Butler-Wu SM, Gokhale RS, Darwin KH. 2006. Identification of substrates of the Mycobacterium tuberculosis proteasome. EMBO J. 25:5423-32
99. Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH. 2008. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322:1104-7
100. Poulsen C, Akhter Y, Jeon AH, Schmitt-Ulms G, Meyer HE, et al. 2010. Proteome-wide identification of mycobacterial pupylation targets. Mol. Syst. Biol. 6:386
101. Prunetti L, Reuter CJ,Hepowit NL,WuY, BarruetoL, et al. 2014. Structural and biochemical properties of an extreme salt-loving proteasome activating nucleotidase from the archaeon Haloferax volcanii. Extremophiles 18:283-93
102. Ranjan N, Damberger FF, Sutter M, Allain FH,Weber-Ban E. 2011. Solution structure and activation mechanism of ubiquitin-like small archaeal modifier proteins. J. Mol. Biol. 405:1040-55
103. Reyes-Turcu FE, Ventii KH, Wilkinson KD. 2009. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78:363-97
104. Rodriguez MS, Dargemont C, Hay RT. 2001. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276:12654-59
105. Samanovic MI, Li H, Darwin KH. 2013. The Pup-proteasome system of Mycobacterium tuberculosis. Subcell. Biochem. 66:267-95
106. Sato Y, Yoshikawa A, Yamagata A, Mimura H, Yamashita M, et al. 2008. Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains. Nature 455:358-62
107. Schlieker CD, van der Veen AG, Damon JR, Spooner E, Ploegh HL. 2008. A functional proteomics approach links the ubiquitin-related modifier Urm1 to a tRNA modification pathway. Proc. Natl. Acad. Sci. USA 105:18255-60
108. Schmitz J, Chowdhury MM, Hänzelmann P, Nimtz M, Lee EY, et al. 2008. The sulfurtransferase activity of Uba4 presents a link between ubiquitin-like protein conjugation and activation of sulfur carrier proteins. Biochemistry 47:6479-89
109. Schulman BA, Harper JW. 2009. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 10:319-31
110. SeufertW, Jentsch S. 1991. Yeast ubiquitin-conjugating enzymes involved in selective protein degradation are essential for cell viability. Acta Biol. Hung. 42:27-37
111. Seufert W, McGrath JP, Jentsch S. 1990. UBC1 encodes a novel member of an essential subfamily of yeast ubiquitin-conjugating enzymes involved in protein degradation. EMBO J. 9:4535-41
112. Shigi N. 2012. Posttranslational modification of cellular proteins by a ubiquitin-like protein in bacteria. J. Biol. Chem. 287:17568-77
113. Shigi N, Sakaguchi Y, Asai S, Suzuki T, Watanabe K. 2008. Common thiolation mechanism in the biosynthesis of tRNA thiouridine and sulphur-containing cofactors. EMBO J. 27:3267-78
114. Smirnov D, Dhall A, Sivanesam K, Sharar RJ, Chatterjee C. 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
115. Striebel F, Hunkeler M, Summer H,Weber-Ban E. 2010. The mycobacterial Mpa-proteasome unfolds and degrades pupylated substrates by engaging Pups N-terminus. EMBO J. 29:1262-71
116. Striebel F, Imkamp F,OzcelikD,Weber-BanE. 2014. Pupylation as a signal for proteasomal degradation in bacteria. Biochim. Biophys. Acta 1843:103-13
117. Striebel F, Imkamp F, Sutter M, Steiner M, Mamedov A, Weber-Ban E. 2009. Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat. Struct. Mol. Biol. 16:647-51
118. SutterM,Damberger FF, Imkamp F, Allain FH,Weber-Ban E. 2010. Prokaryotic ubiquitin-like protein (Pup) is coupled to substrates via the side chain of its C-terminal glutamate. J. Am. Chem. Soc. 132:5610-12
119. 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. 583:3151-57
120. Tamura T, Nagy I, Lupas A, Lottspeich F, Cejka Z, et al. 1995. The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr. Biol. 5:766-74
121. Teixeira LK, Reed SI. 2013. Ubiquitin ligases and cell cycle control. Annu. Rev. Biochem. 82:387-414
122. Tran HJ, Allen MD, Löwe J, Bycroft M. 2003. Structure of the Jab1/MPN domain and its implications for proteasome function. Biochemistry 42:11460-65
123. Tung CW. 2012. PupDB: a database of pupylated proteins. BMC Bioinformatics 13:40
124. van der Veen AG, Ploegh HL. 2012. Ubiquitin-like proteins. Annu. Rev. Biochem. 81:323-57
125. VerlhacMH, TerretME, Pintard L. 2010. Control of the oocyte-to-embryo transition by the ubiquitinproteolytic system in mouse and C. elegans. Curr. Opin. Cell Biol. 22:758-63
126. Vierstra RD. 2012. The expanding universe of ubiquitin and ubiquitin-like modifiers. Plant Physiol. 160:2-14
127. Vijay-Kumar S, Bugg CE, Cook WJ. 1987. Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194:531-44
128. Wang T, Darwin KH, Li H. 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
129. WilcoxM. 1969. γ-Glutamyl phosphate attached to glutamine-specific tRNA.Aprecursor of glutaminyltRNA in Bacillus subtilis. Eur. J. Biochem. 11:405-12
130. Wilkinson KD, Audhya TK. 1981. Stimulation of ATP-dependent proteolysis requires ubiquitin with the COOH-terminal sequence Arg-Gly-Gly. J. Biol. Chem. 256:9235-41
131. WilliamsMJ, Kana BD,MizrahiV. 2011. Functional analysis ofmolybdopterin biosynthesis in mycobacteria identifies a fused molybdopterin synthase in Mycobacterium tuberculosis. J. Bacteriol. 193:98-106
132. Wilson HL, Ou MS, Aldrich HC, Maupin-Furlow J. 2000. Biochemical and physical properties of the Methanococcus jannaschii 20S proteasome and PAN, a homolog of the ATPase (Rpt) subunits of the eucaryal 26S proteasome. J. Bacteriol. 182:1680-92
133. Wolf S, Lottspeich F, Baumeister W. 1993. Ubiquitin found in the archaebacterium Thermoplasma acidophilum. FEBS Lett. 326:42-44
134. Wolf S, Nagy I, Lupas A, Pfeifer G, Cejka Z, et al. 1998. Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropolis. J. Mol. Biol. 277:13-25
135. Xi J, Ge Y, Kinsland C,McLafferty FW, Begley TP. 2001. Biosynthesis of the thiazole moiety of thiamin in Escherichia coli: identification of an acyldisulfide-linked protein-protein conjugate that is functionally analogous to the ubiquitin/E1 complex. Proc. Natl. Acad. Sci. USA 98:8513-18
136. Ye K, Liao S, Zhang W, Fan K, Zhang X, et al. 2013. Ionic strength-dependent conformations of a ubiquitin-like small archaeal modifier protein (SAMP1) from Haloferax volcanii. Protein Sci. 22:1174-82
137. Zwickl P, Ng D,Woo KM, Klenk HP, Goldberg AL. 1999. An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26 S proteasome, activates protein breakdown by 20 S proteasomes. J. Biol. Chem. 274:26008-14