The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like β-grasp domains

Genome Biology

Volumn 7, Issue 7, 2006, Pages

  Iyer, Lakshminarayan M ^a   Burroughs, A Maxwell ^a,b   Aravind, L ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GRASP FOLD PROTEIN; E2 RELATED PROTEIN; EI LIKE PROTEIN; JAB PEPTIDASE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEASOME; PROTEIN UBC; RIBONUCLEASE; RNA BINDING PROTEIN; SIDEROPHORE; TRANSFER RNA; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE; CAMPYLOBACTER JEJUNI; CONSENSUS SEQUENCE; CONTROLLED STUDY; EUKARYOTE; EVOLUTION; GENE CLUSTER; GENETIC CODE; MESORHIZOBIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RALSTONIA SOLANACEARUM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; THERMOTOGA MARITIMA; BACTERIUM; CHEMISTRY; METABOLISM; MOLECULAR EVOLUTION;

EUKARYOTA; PROKARYOTA;

BACTERIA; BACTERIOPHAGES; EVOLUTION, MOLECULAR; SIGNAL TRANSDUCTION; UBIQUITIN;

EID: 33747219426     PISSN: 1474760X     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2006-7-7-r60     Document Type: Article

References (98)

1. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P: Molecular Biology of the Cell, (book and CD-ROM) 4th edition. New York, NY: Garland Science Publishing; 2002.
2. Hershko A, Ciechanover A: The ubiquitin system. Annu Rev Biochem 1998, 67:425-479.
3. Ciechanover A, Orian A, Schwartz AL: Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays 2000, 22:442-451.
4. Ardley HC, Robinson PA: E3 ubiquitin ligases. Essays Biochem 2005, 41:15-30.
5. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, et al: De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004, 430:694-699.
6. Pickart CM: Mechanisms underlying ubiquitination. Annu Rev Biochem 2001, 70:503-533.
7. Weissman AM: Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2001, 2:169-178.
8. Schwartz DC, Hochstrasser M: A superfamily of protein tags: ubiquitin, SUMO and related modifiers. Trends Biochem Sci 2003, 28:321-328.
9. Hochstrasser M: Biochemistry. All in the ubiquitin family. Science 2000, 289:563-564.
10. Iyer LM, Koonin EV, Aravind L: Novel predicted peptidases with a potential role in the ubiquitin signaling pathway. Cell Cycle 2004, 3:1440-1450.
11. Aravind L, Ponting CP: Homologues of 26S proteasome subunits are regulators of transcription and translation. Protein Sci 1998, 7:1250-1254.
12. Hofmann K, Bucher P: The PCI domain: a common theme in three multiprotein complexes. Trends Biochem Sci 1998, 23:204-205.
13. Anantharaman V, Aravind L: Evolutionary history, structural features and biochemical diversity of the NIpC/P60 superfamily of enzymes. Genome Biol 2003, 4:R11.
14. Anantharaman V, Koonin EV, Aravind L: Peptide-N-glycanases and DNA repair proteins, Xp-C/Rad4, are, respectively, active and inactivated enzymes sharing a common transglutaminase fold. Hum Mol Genet 2001, 10:1627-1630.
15. Makarova KS, Aravind L, Koonin EV: A superfamily of archaeal, bacterial, and eukaryotic proteins homologous to animal transglutaminases. Protein Sci 1999, 8:1714-1719.
16. Makarova KS, Aravind L, Koonin EV: A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem Sci 2000, 25:50-52.
17. Guterman A, Glickman MH: Deubiquitinating enzymes are IN/ (trinsic to proteasome function). Curr Protein Pept Sci 2004, 5:201-211.
18. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R: A genomic and functional inventory of deubiquitinating enzymes. Cell 2005, 123:773-786.
19. Soboleva TA, Baker RT: Deubiquitinating enzymes: their functions and substrate specificity. Curr Protein Pept Sci 2004, 5:191-200.
20. Wing SS: Deubiquitinating enzymes: the importance of driving in reverse along the ubiquitin-proteasome pathway. Int J Biochem Cell Biol 2003, 35:590-605.
21. Cope GA, Suh GS, Aravind L, Schwarz SE, Zipursky SL, Koonin EV, Deshaies RJ: Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cull. Science 2002, 298:608-611.
22. Verma R, Aravind L, Oania R, McDonald WH, Yates JR III, Koonin EV, Deshaies RJ: Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 2002, 298:611-615.
23. Furukawa K, Mizushima N, Noda T, Ohsumi Y: A protein conjugation system in yeast with homology to biosynthetic enzyme reaction of prokaryotes. J Biol Chem 2000, 275:7462-7465.
24. Goehring AS, Rivers DM, Sprague GF Jr: Attachment of the ubiquitin-related protein Urm1p to the antioxidant protein Ahp1p. Eukaryot Cell 2003, 2:930-936.
25. Duda DM, Walden H, Sfondouris J, Schulman BA: Structural analysis of Escherichia coli ThiF. J Mol Biol 2005, 349:774-786.
26. Lehmann C, Begley TP, Ealick SE: Structure of the Escherichia coli ThiS-ThiF complex, a key component of the sulfur transfer system in thiamin biosynthesis. Biochemistry 2006, 45:11-19.
27. Xi J, Ge Y, Kinsland C, McLafferty FW, Begley TP: 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 2001, 98:8513-8518.
28. Lake MW, Wuebbens MM, Rajagopalan KV, Schindelin H: Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB-MoaD complex. Nature 2001, 414:325-329.
29. Rudolph MJ, Wuebbens MM, Rajagopalan KV, Schindelin H: Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation. Nat Struct Biol 2001, 8:42-46.
30. Leimkuhler S, Wuebbens MM, Rajagopalan KV: Characterization of Escherichia coli MoeB and its involvement in the activation of molybdopterin synthase for the biosynthesis of the molybdenum cofactor. J Biol Chem 2001, 276:34695-34701.
31. Singh S, Tonelli M, Tyler RC, Bahrami A, Lee MS, Markley JL: Three-dimensional structure of the AAH26994.1 protein from Mus musculus, a putative eukaryotic Urm1. Protein Sci 2005, 14:2095-2102.
32. Hofmann K, Bucher P: The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem Sci 1996, 21:172-173.
33. Hofmann K, Falquet L: A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem Sci 2001, 26:347-350.
34. Makarova KS, Aravind L, Galperin MY, Grishin NV, Tatusov RL, Wolf YI, Koonin EV: Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell. Genome Res 1999, 9:608-628.
35. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q, et al.: Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 1998, 282:754-759.
36. Andreeva A, Howorth D, Brenner SE, Hubbard TJ, Chothia C, Murzin AG: SCOP database in 2004: refinements integrate structure and sequence family data. Nucleic Acids Res 2004, 32(Database):D226-D229.
37. Wolf YI, Aravind L, Grishin NV, Koonin EV: Evolution of aminoacyl-tRNA synthetases: analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res 1999, 9:689-710.
38. Vriend G, Sander C: Detection of common three-dimensional substructures in proteins. Proteins 1991, 11:52-58.
39. Sazinsky MH, Bard J, Di Donato A, Lippard SJ: Crystal structure of the toluene/o-xylene monooxygenase hydroxylase from Pseudomonas stutzeri OXI. Insight into the substrate specificity, substrate channeling, and active site tuning of multicomponent monooxygenases. J Biol Chem 2004, 279:30600-30610.
40. van den Ent F, Lowe J: Crystal structure of the ubiquitin-like protein YukD from Bacillus subtilis. FEBS Lett 2005, 579:3837-3841.
41. Huynen M, Snel B, Lathe W III, Bork P: Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome Res 2000, 10:1204-1210.
42. Wolf YI, Rogozin IB, Kondrashov AS, Koonin EV: Genome alignment, evolution of prokaryotic genome organization and prediction of gene function using genomic context. Genome Res 2001, 11:356-372.
43. Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P: SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 2006, 34(Database):D257-D260.
44. Maltsev N, Glass E, Sulakhe D, Rodriguez A, Syed MH, Bompada T, Zhang Y, D'Souza M: PUMA2: grid-based high-throughput analysis of genomes and metabolic pathways. Nucleic Acids Res 2006, 34(Database):D369-D372.
45. Overbeek R, Fonstein M, D'Souza M, Pusch GD, Maltsev N: The use of gene clusters to infer functional coupling. Proc Natl Acad Sci USA 1999, 96:2896-2901.
46. Overbeek R, Larsen N, Pusch GD, D'Souza M, Selkov E Jr, Kyrpides N, Fonstein M, Maltsev N, Selkov E: WIT: integrated system for high-throughput genome sequence analysis and metabolic reconstruction. Nucleic Acids Res 2000, 28:123-125.
47. Aravind L, Koonin EV: A natural classification of ribonucleases. Methods Enzymol 2001, 341:3-28.
48. Anantharaman V, Aravind L: The NYN domains: Novel predicted RNAses with a PIN Domain-like fold. RNA Biology 2006 in press.
49. Anantharaman V, Koonin EV, Aravind L: Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. J Mol Biol 2001, 307:1271-1292.
50. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS: Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J Biol Chem 2002, 277:48949-48959.
51. Settembre EC, Dorrestein PC, Zhai H, Chatterjee A, McLafferty FW, Begley TP, Ealick SE: Thiamin biosynthesis in Bacillus subtilis: structure of the thiazole synthase/sulfur carrier protein complex. Biochemistry 2004, 43:11647-11657.
52. Schwarz G, Mendel RR: Molybdenum cofactor biosynthesis and molybdenum enzymes. Annu Rev Plant Biol 2006, 57:623-647.
53. Schwarz G: Molybdenum cofactor biosynthesis and deficiency. Cell Mol Life Sci 2005, 62:2792-2810.
54. Anantharaman V, Aravind L: MOSC domains: ancient, predicted sulfur-carrier domains, present in diverse metal-sulfur cluster biosynthesis proteins including Molybdenum cofactor sulfurases. FEMS Microbiol Lett 2002, 207:55-61.
55. Rajagopalan KV: Biosynthesis and processing of the molybdenum cofactors. Biochem Soc Trans 1997, 25:757-761.
56. Johnson JL, Rajagopalan KV, Mukund S, Adams MW: Identification of molybdopterin as the organic component of the tungsten cofactor in four enzymes from hyperthermophilic Archaea. J Biol Chem 1993, 268:4848-4852.
57. Matthijs S, Baysse C, Koedam N, Tehrani KA, Verheyden L, Budzikiewicz H, Schafer M, Hoorelbeke B, Meyer JM, De Greve H, et al.: The Pseudomonas siderophore quinolobactin is synthesized from xanthurenic acid, an intermediate of the kynurenine pathway. Mol Microbiol 2004, 52:371-384.
58. Cornelis P, Matthijs S: Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol 2002, 4:787-798.
59. Koonin EV, Aravind L, Galperin MY: A comparative-genomic view of the microbial stress response. In Bacterial Stress Response Edited by: Storz G, Hengge-Aronis R. Washington, DC: ASM Press; 2000:417-444.
60. Wietzorrek A, Schwarz H, Herrmann C, Braun V: The genome of the novel phage Rtp, with a rosette-like tail tip, is homologous to the genome of phage TI. J Bacteriol 2006, 188:1419-1436.
61. Nameki N, Yoneyama M, Koshiba S, Tochio N, Inoue M, Seki E, Matsuda T, Tomo Y, Harada T, Saito K, et al.: Solution structure of the RWD domain of the mouse GCN2 protein. Protein Sci 2004, 13:2089-2100.
62. Schubert S, Dufke S, Sorsa J, Heesemann J: A novel integrative and conjugative element (ICE) of Escherichia coli: the putative progenitor of the Yersinia high-pathogenicity island. Mol Microbiol 2004, 51:837-848.
63. Aravind L, Koonin EV: DNA polymerase beta-like nucleotidyl-transferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res 1999, 27:1609-1618.
64. Doerks T, Copley RR, Schultz J, Ponting CP, Bork P: Systematic identification of novel protein domain families associated with nuclear functions. Genome Res 2002, 12:47-56.
65. Karzai AW, Roche ED, Sauer RT: The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat Struct Biol 2000, 7:449-455.
66. Jouanneau Y, Jeong HS, Hugo N, Meyer C, Willison JC: Overexpression in Escherichia coli of the rnf genes from Rhodobacter capsulatus: characterization of two membrane-bound iron-sulfur proteins. Eur J Biochem 1998, 251:54-64.
67. Pallen MJ: The ESAT-6/WXG100 superfamily: and a new Gram-positive secretion system? Trends Microbiol 2002, 10:209-212.
68. Iyer LM, Makarova KS, Koonin EV, Aravind L: Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 2004, 32:5260-5279.
69. Brodin P, Rosenkrands I, Andersen P, Cole ST, Brosch R: ESAT-6 proteins: protective antigens and virulence factors? Trends Microbiol 2004, 12:500-508.
70. Rhee SG, Park SC, Koo JH: The role of adenylyltransferase and uridylyltransferase in the regulation of glutamine synthetase in Escherichia coli. Curr Top Cell Regul 1985, 27:221-232.
71. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV: A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 2006, 1:7.
72. Haft DH, Selengut J, Mongodin EF, Nelson KE: A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 2005, 1:e60.
73. Anantharaman V, Aravind L: New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system. Genome Biol 2003, 4:R81.
74. Roberts RJ, Vincze T, Posfai J, Macelis D: REBASE: restriction enzymes and DNA methyltransferases. Nucleic Acids Res 2005, 33(Database):D230-D232.
75. Lupas AN, Koretke KK: Bioinformatic analysis of ClpS, a protein module involved in prokaryotic and eukaryotic protein degradation. J Struct Biol 2003, 141:77-83.
76. Erbse A, Schmidt R, Bornemann T, Schneider-Mergener J, Mogk A, Zahn R, Dougan DA, Bukau B: ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 2006, 439:753-756.
77. Sankaranarayanan R, Dock-Bregeon AC, Romby P, Caillet J, Springer M, Rees B, Ehresmann C, Ehresmann B, Moras D: The structure of threonyl-tRNA synthetase-tRNA(Thr) complex enlightens its repressor activity and reveals an essential zinc ion in the active site. Cell 1999, 97:371-381.
78. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
79. Complete Microbial Genomes [http://www.ncbi.nlm.nih.gov/genomes/ lproks.cgi]
80. Draft assembly sequences database [http://www.ncbi.nlm.nih.gov/genomes/ static/eub_u.html]
81. Schaffer AA, Aravind L, Madden TL, Shavirin S, Spouge JL, Wolf YI, Koonin EV, Altschul SF: Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. Nucleic Acids Res 2001, 29:2994-3005.
82. Pfam Database [http://www.sanger.ac.uk/Software/Pfam/index.shtml]
83. Eddy SR: Profile hidden Markov models. Bioinformatics 1998, 14:755-763.
84. Notredame C, Higgins DG, Heringa J: T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000, 302:205-217.
85. Pei J, Sadreyev R, Grishin NV: PCMA: fast and accurate multiple sequence alignment based on profile consistency. Bioinformatics 2003, 19:427-428.
86. Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113.
87. Neuwald AF, Liu JS, Lawrence CE: Gibbs motif sampling: detection of bacterial outer membrane protein repeats. Protein Sci 1995, 4:1618-1632.
88. Schuler GD, Altschul SF, Lipman DJ: A workbench for multiple alignment construction and analysis. Proteins 1991, 9:180-190.
89. Guex N, Peitsch MC: SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 1997, 18:2714-2723.
90. Holm L, Sander C: The FSSP database: fold classification based on structure-structure alignment of proteins. Nucleic Acids Res 1996, 24:206-209.
91. Holm L, Sander C: Dali: a network tool for protein structure comparison. Trends Biochem Sci 1995, 20:478-480.
92. Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ: JPred: a consensus secondary structure prediction server. Bioinformatics 1998, 14:892-893.
93. BLASTCLUST program [ftp://ftp.ncbi.nih.gov/blast/documents/ blastclust.html]
94. Kelley LA, MacCallum RM, Sternberg MJ: Enhanced genome annotation using structural profiles in the program 3D-PSSM. J Mol Biol 2000, 299:499-520.
95. Felsenstein J: Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol 1996, 266:418-427.
96. Hasegawa M, Kishino H, Saitou N: On the maximum likelihood method in molecular phylogenetics. J Mol Evol 1991, 32:443-445.
97. Adachi J, Hasegawa M: MOLPHY: Programs for Molecular Phylogenetics Tokyo: Institute of Statistical Mathematics; 1992.
98. Additional date files [ftp://ftp.ncbi.nih.gov/pub/aravind/UB/]