Unusual domain architecture of aminoacyl tRNA synthetases and their paralogs from Leishmania major

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Gowri, V S ^a   Ghosh, Indira ^a   Sharma, Amit ^b   Madhubala, Rentala ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Aminoacyl tRNA synthetases; Editing domains; Paralog

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; ASPARTATE AMMONIA LIGASE; SELENOCYSTEINE;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; GENE DUPLICATION; LEISHMANIA MAJOR; MITOCHONDRION; NONHUMAN; OLIGOMERIZATION; PARASITE IDENTIFICATION; PHYLOGENY; PROTEIN SYNTHESIS; RNA BINDING; RNA EDITING;

AMINO ACID SEQUENCE; AMINO ACYL-TRNA SYNTHETASES; ARCHAEAL PROTEINS; ASPARAGINE; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; CYTOKINES; EVOLUTION, MOLECULAR; LEISHMANIA MAJOR; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; PHYLOGENY; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); KINETOPLASTIDA; LEISHMANIA MAJOR; PROKARYOTA; PROTOZOA;

EID: 84868713203     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-621     Document Type: Article

References (80)

1. Ibba M, Söll D. Aminoacyl-tRNA synthesis. Annu Rev Biochem 2000, 69:617-650. 10.1146/annurev.biochem.69.1.617, 10966471.
2. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, et al. The genome of the African trypanosome Trypanosoma brucei. Science 2005, 309:416-422. 10.1126/science.1112642, 16020726.
3. Charrière F, Helgadóttir S, Horn EK, Söll D, Schneider A. Dual targeting of a single tRNA(Trp) requires two different tryptophanyl-tRNA synthetases in Trypanosoma brucei. Proc Natl Acad Sci USA 2006, 103:6847-6852. 10.1073/pnas.0602362103, 1458982, 16636268.
4. Merritt EA, Arakaki TL, Gillespie JR, Larson ET, Kelley A, et al. Crystal structures of trypanosomal histidyl-tRNA synthetase illuminate differences between eukaryotic and prokaryotic homologs. J Mol Biol 2010, 397:481-494. 10.1016/j.jmb.2010.01.051, 2834879, 20132829.
5. Kwon NH, Kang T, Lee JY, Kim HH, Kim HR, et al. Dual role of methionyl-tRNA synthetase in the regulation of translation and tumor suppressor activity of aminoacyl-tRNA synthetase-interacting multifunctional protein-3. Proc Natl Acad Sci USA 2011, 108:19635-19640. 10.1073/pnas.1103922108, 3241768, 22106287.
6. Park SG, Choi EC, Kim S. Aminoacyl-tRNA synthetase-interacting multifunctional proteins (AIMPs): a triad for cellular homeostasis. IUBMB Life 2010, 62:296-302.
7. Bhatt TK, Khan S, Dwivedi VP, Banday MM, Sharma A, et al. Malaria parasite tyrosyl-tRNA synthetase secretion triggers pro-inflammatory responses. Nat Commun 2011, 2:530.
8. Hurdle JG, O'Neill AJ, Ingham E, Fishwick C, Chopra I. Analysis of mupirocin resistance and fitness in Staphylococcus aureus by molecular genetic and structural modeling techniques. Antimicrob Agents Chemother 2004, 48:4366-4376. 10.1128/AAC.48.11.4366-4376.2004, 525403, 15504866.
9. Hurdle JG, O'Neill AJ, Chopra I. Prospects for aminoacyl-tRNA synthetase inhibitors as new antimicrobial agents. Antimicrob Agents Chemother 2005, 49:4821-4833. 10.1128/AAC.49.12.4821-4833.2005, 1315952, 16304142.
10. Olmedo-Verd E, Santamaría-Gómez J, Ochoa De Alda JA, Ribas De Pouplana L, Luque I. Membrane Anchoring of Aminoacyl-tRNA Synthetases by Convergent Acquisition of a Novel Protein Domain. J Biol Chem 2011, 286:41057-41068. 10.1074/jbc.M111.242461, 3220467, 21965654.
11. Bhatt TK, Kapil C, Khan S, Jairajpuri MA, Sharma V, et al. A genomic glimpse of aminoacyl-tRNA synthetases in malaria parasite Plasmodium falciparum. BMC Genomics 2009, 10:644-657. 10.1186/1471-2164-10-644, 2813244, 20042123.
12. Khan S, Sharma A, Jamwal A, Sharma V, Pole AK, et al. Uneven spread of cis- and trans-editing aminoacyl-tRNA synthetase domains within translational compartments of P. falciparum. Nature Scientific reports 2011, 1:1-11.
13. Shibata S, Gillespie JR, Kelley AM, Napuli AJ, Zhang Z, et al. Selective inhibitors of methionyl-tRNA synthetase have potent activity against Trypanosoma brucei Infection in Mice. Antimicrob Agents Chemother 2011, 55:1982-1989. 10.1128/AAC.01796-10, 3088252, 21282428.
14. Larson ET, Kim JE, Zucker FH, Kelley A, Mueller N, et al. Structure of Leishmania major methionyl-tRNA synthetase in complex with intermediate products methionyladenylate and pyrophosphate. Biochimie 2011, 93:570-582. 10.1016/j.biochi.2010.11.015, 3039092, 21144880.
15. Larson ET, Kim JE, Castaneda LJ, Napuli AJ, Zhang Z, et al. The double-length tyrosyl-tRNA synthetase from the eukaryote Leishmania major forms an intrinsically asymmetric pseudo-dimer. J Mol Biol 2011, 409:159-176. 10.1016/j.jmb.2011.03.026, 3095712, 21420975.
16. Wakasugi K, Schimmel P. Highly differentiated motifs responsible for two cytokine activities of a split human tRNA synthetase. J Biol Chem 1999, 274:23155-23159. 10.1074/jbc.274.33.23155, 10438485.
17. Ibba M, Söll D. The renaissance of aminoacyl-tRNA synthesis. EMBO Rep 2001, 2:382-387. 1083889, 11375928.
18. Geslain R, Aeby E, Guitart T, Jones TE, Castro De Moura M, et al. Trypanosoma seryl-tRNA synthetase is a metazoan-like enzyme with high affinity for tRNASec. J Biol Chem 2006, 281:38217-38225. 10.1074/jbc.M607862200, 17040903.
19. Cassago A, Rodrigues EM, Prieto EL, Gaston KW, Alfonzo JD, et al. Identification of Leishmania selenoproteins and SECIS element. Mol Biochem Parasitol 2006, 149:128-134. 10.1016/j.molbiopara.2006.05.002, 16766053.
20. Gurvitz A. Identification of the Leishmania major proteins LmjF07.0430, LmjF07.0440, and LmjF27.2440 as components of fatty acid synthase I. J Biomed Biotechnol 2009, 2009:950864-950872. 2817374, 20145708.
21. Nabholz C, Hauser R, Schneider A. Leishmania tarentolae contains distinct cytosolic and mitochondrial glutaminyltRNA synthetase activities. Proc Natl Acad Sci USA 1997, 94:7903-7908. 10.1073/pnas.94.15.7903, 21527, 9223285.
22. Rinehart J, Horn EK, Wei D, Soll D, Schneider A. Non-canonical eukaryotic glutaminyl- and glutamyl-tRNA synthetases form mitochondrial aminoacyl-tRNA in Trypanosoma brucei. J Biol Chem 2004, 279:1161-1166.
23. Nilsson D, Gunasekera K, Mani J, Osteras M, Farinelli L, et al. Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog 2010, 6:e1001037. 10.1371/journal.ppat.1001037, 2916883, 20700444.
24. Depledge DP, Evans KJ, Ivens AC, Naveed A, Asher M, Kaye PM, et al. Comparative expression profiling of leishmania: modulation in gene expression between species and in different host genetic backgrounds. PLoS Negl Trop Dis 2009, 3:e476. 10.1371/journal.pntd.0000476, 2701600, 19582145.
25. Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, et al. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 2006, 443:50-55. 10.1038/nature05096, 16906134.
26. Sankaranarayanan R, Dock-Bregeon AC, Romby P, Caillet J, Springer M, et al. 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. 10.1016/S0092-8674(00)80746-1, 10319817.
27. 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.
28. Guo M, Chong YE, Beebe K, Shapiro R, Yang XL, Schimmel P. The C-Ala domain brings together editing and aminoacylation functions on one tRNA. Science 2009, 325:744-747. 10.1126/science.1174343, 19661429.
29. Francin M, Kaminska M, Kerjan P, Mirande M. The N-terminal domain of mammalian Lysyl-tRNA synthetase is a functional tRNA-binding domain. J Biol Chem 2002, 277:1762-1769. 10.1074/jbc.M109759200, 11706011.
30. Bilokapic S, Maier T, Ahel D, Gruic-Sovulj I, Söll D, et al. Structure of the unusual seryl-tRNA synthetase reveals a distinct zinc-dependent mode of substrate recognition. EMBO J 2006, 25:2498-2509. 10.1038/sj.emboj.7601129, 1478180, 16675947.
31. Liu RJ, Tan M, Du DH, Xu BS, Eriani G, et al. Peripheral insertion modulates editing activity of the isolated CP1 domain of leucyl-tRNA synthetase. Biochem J 2011, 440:217-227. 10.1042/BJ20111177, 21819379.
32. Seiradake E, Mao W, Hernandez V, Baker SJ, Plattner JJ, et al. Crystal structures of the human and fungal cytosolic Leucyl-tRNA synthetase editing domains: a structural basis for the rational design of antifungal benzoxaboroles. J Mol Biol 2009, 390:196-207. 10.1016/j.jmb.2009.04.073, 19426743.
33. Zhao MW, Zhu B, Hao R, Xu MG, Eriani G, et al. Leucyl-tRNA synthetase from the ancestral bacterium Aquifex aeolicus contains relics of synthetase evolution. EMBO J 2005, 24:1430-1439. 10.1038/sj.emboj.7600618, 1142543, 15775966.
34. Sokabe M, Okada A, Yao M, Nakashima T, Tanaka I. Molecular basis of alanine discrimination in editing site. Proc Natl Acad Sci USA 2005, 102:11669-11674. 10.1073/pnas.0502119102, 1187966, 16087889.
35. Fukunaga R, Yokoyama S. Structure of the AlaX-M trans-editing enzyme from Pyrococcus horikoshii. Acta Crystallogr D Biol Crystallogr 2007, 63:390-400. 10.1107/S090744490605640X, 17327676.
36. Ahel I, Korencic D, Ibba M, Söll D. Trans-editing of mischarged tRNAs. Proc Natl Acad Sci USA 2003, 100:15422-15427. 10.1073/pnas.2136934100, 307583, 14663147.
37. Ruan B, Söll D. The bacterial YbaK protein is a Cys-tRNAPro and Cys-tRNACys deacylase. J Biol Chem 2005, 280:25887-25891. 10.1074/jbc.M502174200, 15886196.
38. An S, Musier-Forsyth K. Trans-editing of Cys-tRNAPro by Haemophilus influenzae YbaK protein. J Biol Chem 2004, 279:42359-42362. 10.1074/jbc.C400304200, 15322138.
39. Zhang H, Huang K, Li Z, Banerjei L, Fisher KE, et al. Crystal structure of YbaK protein from Haemophilus influenzae (HI1434) at 1.8 A resolution: functional implications. Proteins 2000, 40:86-97. 10.1002/(SICI)1097-0134(20000701)40:1<86::AID-PROT100>3.0.CO;2-Y, 10813833.
40. Wong FC, Beuning PJ, Silvers C, Musier-Forsyth K. An isolated class II aminoacyl-tRNA synthetase insertion domain is functional in amino acid editing. J Biol Chem 2003, 278:52857-52864. 10.1074/jbc.M309627200, 14530268.
41. Lam H, Oh DC, Cava F, Takacs CN, Clardy J, et al. D-aminoacids govern stationary phase cell wall remodeling in bacteria. Science 2009, 325:1552-1555. 10.1126/science.1178123, 2759711, 19762646.
42. Miyoshi Y, Hamase K, Tojo Y, Mita M, Konno R, Zaitsu K. Determination of D-serine and D-alanine in the tissues and physiological fluids of mice with various D-amino-acid oxidase activities using two-dimensional high-performance liquid chromatography with fluorescence detection. J Chromatogr B Analyt Technol Biomed Life Sci 2009, 877:2506-2512. 10.1016/j.jchromb.2009.06.028, 19586804.
43. Bhatt TK, Yogavel M, Wydau S, Berwal R, Sharma A. Ligand-bound structures provide atomic snapshots for the catalytic mechanism of D-amino acid deacylase. J Biol Chem 2010, 285:5917-5930. 10.1074/jbc.M109.038562, 2820817, 20007323.
44. Feng L, Tumbula-Hansen D, Toogood H, Söll D. Expanding tRNA recognition of a tRNA synthetase by a single amino acid change. Proc Natl Acad Sci USA 2003, 100:5676-5681. 10.1073/pnas.0631525100, 156260, 12730374.
45. Charron C, Roy H, Blaise M, Giegé R, Kern D. Non-discriminating and discriminating aspartyl-tRNA synthetases differ in the anticodon-binding domain. EMBO J 2003, 22:1632-1643. 10.1093/emboj/cdg148, 152893, 12660169.
46. Frechin M, Senger B, Brayé M, Kern D, Martin RP, Becker HD. Yeast mitochondrial Gln-tRNA(Gln) is generated by a GatFAB-mediated transamidation pathway involving Arc1p-controlled subcellular sorting of cytosolic GluRS. Genes Dev 2009, 23:1119-1130. 10.1101/gad.518109, 2682957, 19417106.
47. Liao CC, Lin CH, Chen SJ. Trans-kingdom rescue of Gln-tRNAGln synthesis in yeast cytoplasm and mitochondria 2012, Wang CC: Nucleic Acids Res, [Epub ahead of print].
48. Roy H, Ibba M. Bridging the gap between ribosomal and nonribosomal protein synthesis. Proc Natl Acad Sci USA 2010, 107:14517-14518. 10.1073/pnas.1009939107, 2930406, 20696925.
49. Sissler M, Delorme C, Bond J, Ehrlich SD, Renault P, et al. An aminoacyl-tRNA synthetase paralog with a catalytic role in histidine biosynthesis. Proc Natl Acad Sci USA 1999, 96:8985-8990. 10.1073/pnas.96.16.8985, 17719, 10430882.
50. Francklyn C. tRNA synthetase paralogs: evolutionary links in the transition from tRNA-dependent amino acid biosynthesis to de novo biosynthesis. Proc Natl Acad Sci USA 2003, 100:9650-9652. 10.1073/pnas.1934245100, 187799, 12913115.
51. Roy H, Zou SB, Bullwinkle TJ, Wolfe BS, Gilreath MS, et al. The tRNA synthetase paralog PoxA modifies elongation factor-P with(R)-β-lysine. Nat Chem Biol 2011, 7:667-669. 3177975, 21841797.
52. Gilreath MS, Roy H, Bullwinkle TJ, Katz A, Navarre WW, et al. β-Lysine discrimination by lysyl-tRNA synthetase. FEBS Lett 2011, 585:3284-3288. 10.1016/j.febslet.2011.09.008, 3196068, 21925499.
53. Ambrogelly A, O'Donoghue P, Söll D, Moses S. A bacterial ortholog of class II lysyl-tRNA synthetase activates lysine. FEBS Lett 2010, 584:3055-3060. 10.1016/j.febslet.2010.05.036, 2900529, 20580719.
54. Yanagisawa T, Sumida T, Ishii R, Takemoto C, Yokoyama S. A paralog of lysyl-tRNA synthetase aminoacylates a conserved lysine residue in translation elongation factor P. Nat Struct Mol Biol 2010, 17:1136-1143. 10.1038/nsmb.1889, 20729861.
55. Nakatsu T, Kato H, Oda J. Crystal structure of asparagine synthetase reveals a close evolutionary relationship to class II aminoacyl-tRNA synthetase. Nat Struct Biol 1998, 5:15-19. 10.1038/nsb0198-15, 9437423.
56. Richards NG, Schuster SM. An alternative mechanism for the nitrogen transfer reaction in asparagine synthetase. FEBS Lett 1992, 313:98-102. 10.1016/0014-5793(92)81421-H, 1358677.
57. Boehlein SK, Richards NG, Schuster SM. Glutamine-dependent nitrogen transfer in Escherichia coli asparagine synthetase B. Searching for the catalytic triad. J Biol Chem 1994, 269:7450-7457.
58. Charron C, Roy H, Blaise M, Giegé R, Kern D. Crystallization and preliminary X-ray diffraction data of an archaeal asparagine synthetase related to asparaginyl-tRNA synthetase. Acta Crystallogr D Biol Crystallogr 2004, 60:767-769. 10.1107/S0907444904003117, 15039580.
59. Blaise M, Fréchin M, Oliéric V, Charron C, Sauter C, Lorber B, Roy H, Kern D. Crystal structure of the archaeal asparagine synthetase: interrelation with aspartyl-tRNA and asparaginyl-tRNA synthetases. J Mol Biol 2011, 412:437-452. 10.1016/j.jmb.2011.07.050, 21820443.
60. Nakamura M, Yamada M, Hirota Y, Sugimoto K, Oka A, et al. Nucleotide sequence of the asnA gene coding for asparagine synthetase of E. coli K-12. Nucleic Acids Res 1981, 9:4669-4676. 10.1093/nar/9.18.4669, 327466, 6117826.
61. Aurrecoechea C, Brestelli J, Brunk BP, Fischer S, Gajria B, et al. EuPathDB: a portal to eukaryotic pathogen databases. Nucleic Acids Res 2010, 38:D415-D419. 10.1093/nar/gkp941, 2808945, 19914931.
62. Cusack S, Härtlein M, Leberman R. Sequence, structural and evolutionary relationships between class 2 aminoacyl-tRNA synthetases. Nucleic Acids Res 1991, 19:3489-3498. 10.1093/nar/19.13.3489, 328370, 1852601.
63. Sauter C, Lorber B, Cavarelli J, Moras D, Giegé R. The free yeast aspartyl-tRNA synthetase differs from the tRNA(Asp)-complexed enzyme by structural changes in the catalytic site, hinge region, and anticodon-binding domain. J Mol Biol 2000, 299:1313-1324. 10.1006/jmbi.2000.3791, 10873455.
64. Laskowski RA. PDBsum new things. Nucleic Acids Res 2009, 37:D355-D359. 10.1093/nar/gkn860, 2686501, 18996896.
65. Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, et al. TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 2010, 38:D457-D462. 10.1093/nar/gkp851, 2808979, 19843604.
66. Krogh A, Brown M, Mian IS, Sjölander K, Haussler D. Hidden Markov models in computational biology. Applications to protein modeling. J Mol Biol 1994, 235:1501-1531. 10.1006/jmbi.1994.1104, 8107089.
67. Consortium UP. Ongoing and future developments at the Universal Protein Resource. Nucleic Acids Res 2011, 39:D214-D219. 3013648, 21051339.
68. Jain E, Bairoch A, Duvaud S, Phan I, Redaschi N, et al. Infrastructure for the life sciences: design and implementation of the UniProt website. BMC Bioinformatics 2009, 10:136-154. 10.1186/1471-2105-10-136, 2686714, 19426475.
69. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-3066. 10.1093/nar/gkf436, 135756, 12136088.
70. Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, et al. Protein database searches using compositionally adjusted substitution matrices. FEBS J 2005, 272:5101-5109. 10.1111/j.1742-4658.2005.04945.x, 1343503, 16218944.
71. Horton P, Nakai K. Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc Int Conf Intell Syst Mol Biol 1997, 5:147-152.
72. Buchan DW, Ward SM, Lobley AE, Nugent TC, Bryson K, et al. Protein annotation and modelling servers at University College London. Nucl Acids Res 2010, 38:W563-W568. 10.1093/nar/gkq427, 2896093, 20507913.
73. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. The Pfam protein families database. Nucleic Acids Res 2010, 38:D211-D222. 10.1093/nar/gkp985, 2808889, 19920124.
74. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 2011, 39:D225-D229. 10.1093/nar/gkq1189, 3013737, 21109532.
75. Gough J, Chothia C. SUPERFAMILY: HMMs representing all proteins of known structure. SCOP sequence searches, alignments and genome assignments. Nucleic Acids Res 2002, 30:268-272. 10.1093/nar/30.1.268, 99153, 11752312.
76. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
77. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992, 8:275-282.
78. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
79. Eswar N, Eramian D, Webb B, Shen MY, Sali A. Protein structure modeling with MODELLER. Methods Mol Biol 2008, 426:145-159. 10.1007/978-1-60327-058-8_8, 18542861.
80. DeLano WL. The PyMOL Molecular Graphics System San Carlos, CA, USA: DeLano Scientific LLC.