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Biosynthesis and function of tRNA wobble modifications

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Fine-Tuning of RNA Functions by Modification and Editing

Part of the book series: Topics in Current Genetics ((TCG,volume 12))

Abstract

Post-transcriptional modifications at the first (wobble) position of the tRNA anticodon participate in the precise decoding of the genetic code that is mediated by the codon-anticodon interaction. However, the biosynthesis and functions of many wobble modifications remain unknown. We describe, here, a reverse genetic approach that we used to explore the uncharacterized genes of Escherichia coli and yeast that are responsible for the wobble modifications (the Ribonucleome analysis). By combining this method with a comparative genomics approach, we identified an essential gene (tilS) that is responsible for the biosynthesis of lysidine at the wobble position of the bacterial tRNAIle that is specific for the AUA codon. Lysidine is an essential wobble modification that is required for the identity of the tRNA and its AUA codon specificity. In vitro reconstitution of the wobble modification revealed the detailed mechanism by which lysidine is synthesized.

Accurate maintenance of wobble modifications is, thus, required for various biological functions. We also show that the subcellular localization of tRNAs in Leishmania tarentolae is controlled by different wobble modifications. Moreover, we describe our recent studies that have revealed that the lack of wobble modification of mitochondrial tRNAs leads to translational defects that are associated with mitochondrial diseases, which suggests that disordered RNA modification may be a causative factor of human diseases.

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References

  • 1. Agris PF, Soll D, Seno T (1973) Biological function of 2-thiouridine in Escherichia coli glutamic acid transfer ribonucleic acid. Biochemistry 12:4331-4337

    Google Scholar 

  • 2. Akerley BJ, Rubin EJ, Novick VL, Amaya K, Judson N, Mekalanos JJ (2002) A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc Natl Acad Sci USA 99:966-971

    Article  Google Scholar 

  • 3. Andachi Y, Yamao F, Iwami M, Muto A, Osawa S (1987) Occurrence of unmodified adenine and uracil at the first position of anticodon in threonine tRNAs in Mycoplasma capricolum. Proc Natl Acad Sci USA 84:7398-7402

    Google Scholar 

  • 4. Antonicka H, Floryk D, Klement P, Stratilova L, Hermanska J, Houstkova H, Kalous M, Drahota Z, Zeman J, Houstek J (1999) Defective kinetics of cytochrome c oxidase and alteration of mitochondrial membrane potential in fibroblasts and cytoplasmic hybrid cells with the mutation for myoclonus epilepsy with ragged-red fibres (‘MERRF’) at position 8344 nt. Biochem J 342:537-544

    Article  Google Scholar 

  • 5. Ashraf SS, Sochacka E, Cain R, Guenther R, Malkiewicz A, Agris PF (1999) Single atom modification (O $to$ S) of tRNA confers ribosome binding. Rna 5:188-194

    Article  Google Scholar 

  • 6. Auxilien S, Crain PF, Trewyn RW, Grosjean H (1996) Mechanism, specificity and general properties of the yeast enzyme catalysing the formation of inosine 34 in the anticodon of transfer RNA. J Mol Biol 262(4):437-458

    Article  Google Scholar 

  • 7. Barrell BG, Anderson S, Bankier AT, de Bruijn MH, Chen E, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1980) Different pattern of codon recognition by mammalian mitochondrial tRNAs. Proc Natl Acad Sci USA 77:3164-3166

    Google Scholar 

  • 8. Bjork GR (1995) Biosynthesis and function of modified nucleosides. In tRNA: Structure, Biosynthesis, and function, D.R. Soll and U.L. RajBhandary, eds. (Washington, DC: American Society for Microbiology), pp165-205

    Google Scholar 

  • 9. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474

    Article  CAS  PubMed  Google Scholar 

  • 10. Bonitz SG, Berlani R, Coruzzi G, Li M, Macino G, Nobrega FG, Nobrega MP, Thalenfeld BE, Tzagoloff A (1980) Codon recognition rules in yeast mitochondria. Proc Natl Acad Sci USA 77:3167-3170

    Google Scholar 

  • 11. Bork P, Koonin EV (1994) A P-loop-like motif in a widespread ATP pyrophosphatase domain: implications for the evolution of sequence motifs and enzyme activity. Proteins 20:347-355

    Google Scholar 

  • 12. Bregeon D, Colot V, Radman M, Taddei F (2001) Translational misreading: a tRNA modification counteracts a +2 ribosomal frameshift. Genes Dev 15:2295-2306

    Article  Google Scholar 

  • 13. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E, Emeson RB (1997) Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387:303-308

    Article  CAS  PubMed  Google Scholar 

  • 14. Caskey CT, Beaudet A, Nirenberg M (1968) RNA codons and protein synthesis. 15. Dissimilar responses of mammalian and bacterial transfer RNA fractions to messenger RNA codons. J Mol Biol 37:99-118

    Google Scholar 

  • 15. Cavaille J, Buiting K, Kiefmann M, Lalande M, Brannan CI, Horsthemke B, Bachellerie JP, Brosius J, Huttenhofer A (2000) Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. Proc Natl Acad Sci USA 97:14311-14316

    Google Scholar 

  • 16. Chheda GB, Hong CI, Piskorz CF, Harmon GA (1972) Biosynthesis of N-(purin-6-ylcarbamoyl)-L-threonine riboside. Incorporation of L-threonine in vivo into modified nucleoside of transfer ribonucleic acid. Biochem J 127:515-519

    Google Scholar 

  • 17. Chomyn A, Martinuzzi A, Yoneda M, Daga A, Hurko O, Johns D, Lai ST, Nonaka I, Angelini C, Attardi G (1992) MELAS mutation in mtDNA binding site for transcription termination factor causes defects in protein synthesis and in respiration but no change in levels of upstream and downstream mature transcripts. Proc Natl Acad Sci USA 89:4221-4225

    Google Scholar 

  • 18. Chomyn A, Meola G, Bresolin N, Lai ST, Scarlato G, Attardi G (1991) In vitro genetic transfer of protein synthesis and respiration defects to mitochondrial DNA-less cells with myopathy-patient mitochondria. Mol Cell Biol 11:2236-2244

    Google Scholar 

  • 19. Cougot N, van Dijk E, Babajko S, Seraphin B (2004) ‘Cap-tabolism’. Trends Biochem Sci 29(8):436-444

    Article  Google Scholar 

  • 20. Crick FH (1966) Codon–anticodon pairing: the wobble hypothesis. J Mol Biol 19:548-555

    Google Scholar 

  • 21. Curran JF (1998) Modified nucleosides in translation. In Modification and Editing of RNA, H. Grosjean, and R. Benne, eds. (Washington, D.C.: ASM Press), pp463-516

    Google Scholar 

  • 22. Dietrich A, Small I, Cosset A, Weil JH, Marechal-Drouard L (1996) Editing and import: strategies for providing plant mitochondria with a complete set of functional transfer RNAs. Biochimie 78:518-529

    Article  Google Scholar 

  • 23. Dubois DY, Blaise M, Becker HD, Campanacci V, Keith G, Giege R, Cambillau C, Lapointe J, Kern D (2004) An aminoacyl-tRNA synthetase-like protein encoded by the Escherichia coli yadB gene glutamylates specifically tRNAAsp. Proc Natl Acad Sci USA 101:7530-7535. Epub 2004 Apr 7519

    Article  Google Scholar 

  • 24. Dunbar DR, Moonie PA, Zeviani M, Holt IJ (1996) Complex I deficiency is associated with 3243G:C mitochondrial DNA in osteosarcoma cell cybrids. Hum Mol Genet 5:123-129

    Article  Google Scholar 

  • 25. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498

    Article  CAS  PubMed  Google Scholar 

  • 26. Elseviers D, Petrullo LA, Gallagher PJ (1984) Novel E. coli mutants deficient in biosynthesis of 5-methylaminomethyl-2-thiouridine. Nucleic Acids Res 12:3521-3534

    Google Scholar 

  • 27. Enriquez JA, Chomyn A, Attardi G (1995) MtDNA mutation in MERRF syndrome causes defective aminoacylation of tRNA(Lys) and premature translation termination. Nat Genet 10:47-55

    Article  Google Scholar 

  • 28. Geggel HS, Ament ME, Heckenlively JR, Martin DA, Kopple JD (1985) Nutritional requirement for taurine in patients receiving long-term parenteral nutrition. N Engl J Med 312:142-146

    Google Scholar 

  • 29. Gerber AP, Keller W (1999) An adenosine deaminase that generates inosine at the wobble position of tRNAs. Science 286:1146-1149

    Article  Google Scholar 

  • 30. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274:546, 563-547

    Article  CAS  PubMed  Google Scholar 

  • 31. Goto Y, Nonaka I, Horai S (1990) A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 348:651-653

    Google Scholar 

  • 32. Goto Y, Nonaka I, Horai S (1991) A new mtDNA mutation associated with mitochondrial myopathy, encephalopathy, lactic acidosis and stroke-like episodes (MELAS). Biochim Biophys Acta 1097:238-240

    Google Scholar 

  • 33. Goto Y, Tojo M, Tohyama J, Horai S, Nonaka I (1992) A novel point mutation in the mitochondrial tRNA(Leu)(UUR) gene in a family with mitochondrial myopathy. Ann Neurol 31:672-675

    Article  Google Scholar 

  • 34. Grosjean H, Sankoff D, Jou WM, Fiers W, Cedergren RJ (1978) Bacteriophage MS2 RNA: a correlation between the stability of the codon: anticodon interaction and the choice of code words. J Mol Evol 12:113-119

    Google Scholar 

  • 35. Hagervall TG, Pomerantz SC, McCloskey JA (1998) Reduced misreading of asparagine codons by Escherichia coli tRNALys with hypomodified derivatives of 5-methylaminomethyl-2-thiouridine in the wobble position. J Mol Biol 284:33-42

    Article  Google Scholar 

  • 36. Hanada T, Suzuki T, Yokogawa T, Takemoto-Hori C, Sprinzl M, Watanabe K (2001) Translation ability of mitochondrial tRNAsSer with unusual secondary structures in an in vivo translation system of bovine mitochondria. Genes Cells 6:1019-1030

    Article  Google Scholar 

  • 37. Hancock K, Hajduk SL (1990) The mitochondrial tRNAs of Trypanosoma brucei are nuclear encoded. J Biol Chem 265:19208-19215

    Google Scholar 

  • 38. Harada F, Nishimura S (1972) Possible anticodon sequences of tRNA His, tRNA Asm , and tRNA Asp from Escherichia coli B. Universal presence of nucleoside Q in the first postion of the anticondons of these transfer ribonucleic acids. Biochemistry 11:301-308

    Google Scholar 

  • 39. Harada F, Nishimura S (1974) Purification and characterization of AUA specific isoleucine transfer ribonucleic acid from Escherichia coli B. Biochemistry 13:300-307

    Google Scholar 

  • 40. Harris RS, Petersen-Mahrt SK, Neuberger MS (2002) RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol Cell 10:1247-1253

    Article  Google Scholar 

  • 41. Hayashi J, Ohta S, Kikuchi A, Takemitsu M, Goto Y, Nonaka I (1991) Introduction of disease-related mitochondrial DNA deletions into HeLa cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc Natl Acad Sci USA 88:10614-10618

    Google Scholar 

  • 42. Hayashi J, Ohta S, Takai D, Miyabayashi S, Sakuta R, Goto Y, Nonaka I (1993) Accumulation of mtDNA with a mutation at position 3271 in tRNA(Leu)(UUR) gene introduced from a MELAS patient to HeLa cells lacking mtDNA results in progressive inhibition of mitochondrial respiratory function. Biochem Biophys Res Commun 197:1049-1055

    Article  Google Scholar 

  • 43. Hayes KC (1985) Taurine requirement in primates. Nutr Rev 43:65-70

    Google Scholar 

  • 44. Hayes KC, Carey RE, Schmidt SY (1975) Retinal degeneration associated with taurine deficiency in the cat. Science 188:949-951

    Google Scholar 

  • 45. Honjo T, Muramatsu M, Fagarasan S (2004) AID: how does it aid antibody diversity? Immunity 20:659-668

    Article  Google Scholar 

  • 46. Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101-163

    CAS  PubMed  Google Scholar 

  • 47. Igloi GL (1988) Interaction of tRNAs and of phosphorothioate-substituted nucleic acids with an organomercurial. Probing the chemical environment of thiolated residues by affinity electrophoresis. Biochemistry 27:3842-3849

    Google Scholar 

  • 48. Ikeuchi Y, Shigi N, Kato J, Nishimura A, Suzuki T (submitted-a) Identification and characterization of four genes responsible for 2-thiouridine formation of tRNA wobble modification.

    Google Scholar 

  • 49. Ikeuchi Y, Soma A, Kanemasa S, Ote T, Kato J, Sekine M, Suzuki T (submitted-b) Molecular mechanism of lysidine synthesis and substrate discrimination of tRNA-Ile lysidine synthetase.

    Google Scholar 

  • 50. Inagaki Y, Kojima A, Bessho Y, Hori H, Ohama T, Osawa S (1995) Translation of synonymous codons in family boxes by Mycoplasma capricolum tRNAs with unmodified uridine or adenosine at the first anticodon position. J Mol Biol 251:486-492

    Article  Google Scholar 

  • 51. Jacobs HT (2003) Disorders of mitochondrial protein synthesis. Hum Mol Genet 12:293-301

    Article  Google Scholar 

  • 52. Jager G, Leipuviene R, Pollard MG, Qian Q, Bjork GR (2004) The conserved Cys-X1-X2-Cys motif present in the TtcA protein is required for the thiolation of cytidine in position 32 of tRNA from Salmonella enterica serovar typhimurium. J Bacteriol 186:750-757

    Article  Google Scholar 

  • 53. James AM, Wei YH, Pang CY, Murphy MP (1996) Altered mitochondrial function in fibroblasts containing MELAS or MERRF mitochondrial DNA mutations. Biochem J 318:401-407

    Google Scholar 

  • 54. Johns DR, Hurko O (1991) Mitochondrial leucine tRNA mutation in neurological diseases. Lancet 337:927-928

    Article  Google Scholar 

  • 55. Kambampati R, Lauhon CT (2003) MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli. Biochemistry 42:1109-1117

    Article  Google Scholar 

  • 56. Kaneko T, Suzuki T, Kapushoc ST, Rubio MA, Ghazvini J, Watanabe K, Simpson L (2003) Wobble modification differences and subcellular localization of tRNAs in Leishmania tarentolae: implication for tRNA sorting mechanism. Embo J 22:657-667

    Article  Google Scholar 

  • 57. Kapushoc ST, Alfonzo JD, Rubio MA, Simpson L (2000) End processing precedes mitochondrial importation and editing of tRNAs in Leishmania tarentolae. J Biol Chem 275:37907-37914

    Article  Google Scholar 

  • 58. Kapushoc ST, Alfonzo JD, Simpson L (2002) Differential localization of nuclear-encoded tRNAs between the cytosol and mitochondrion in Leishmania tarentolae. Rna 8:57-68

    Article  Google Scholar 

  • 59. Kasai H, Nakanishi K, Macfarlane RD, Torgerson DF, Ohashi Z, McCloskey JA, Gross HJ, Nishimura S (1976) Letter: The structure of Q* nucleoside isolated from rabbit liver transfer ribonucleic acid. J Am Chem Soc 98:5044-5046

    Google Scholar 

  • 60. Katoh T, Susa M, Suzuki T, Umeda N, Watanabe K, Suzuki T (2003) Simple and rapid synthesis of siRNA derived from in vivo transcribed shRNA. Nucleic Acids Res Suppl:249-250

    Google Scholar 

  • 61. Katoh T, Suzuki T (submitted) Specific residues at every third position of siRNAs involve efficient RNAi activity.

    Google Scholar 

  • 62. Kawahara Y, Ito K, Sun H, Aizawa H, Kanazawa I, Kwak S (2004) Glutamate receptors: RNA editing and death of motor neurons. Nature 427:801

    Article  CAS  PubMed  Google Scholar 

  • 63. Kawai G, Yamamoto Y, Kamimura T, Masegi T, Sekine M, Hata T, Iimori T, Watanabe T, Miyazawa T, Yokoyama S (1992) Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction between the base and the 2’-hydroxyl group. Biochemistry 31:1040-1046

    Google Scholar 

  • 64. King MP, Attardi G (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246:500-503

    Google Scholar 

  • 65. Kirino Y, Yasukawa T, Ohta S, Akira S, Ishihara K, Watanabe K, Suzuki T (2004) Codon-specific translational defect caused by a wobble modification deficiency in mutant tRNA from a human mitochondrial disease. Proc Natl Acad Sci USA: in press

    Google Scholar 

  • 66. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, Arnaud M, Asai K, Ashikaga S, Aymerich S, Bessieres P, Boland F, Brignell SC, Bron S, Bunai K, Chapuis J, Christiansen LC, Danchin A, Debarbouille M, Dervyn E, Deuerling E, Devine K, Devine SK, Dreesen O, Errington J, Fillinger S, Foster SJ, Fujita Y, Galizzi A, Gardan R, Eschevins C, Fukushima T, Haga K, Harwood CR, Hecker M, Hosoya D, Hullo MF, Kakeshita H, Karamata D, Kasahara Y, Kawamura F, Koga K, Koski P, Kuwana R, Imamura D, Ishimaru M, Ishikawa S, Ishio I, Le Coq D, Masson A, Mauel C, Meima R, Mellado RP, Moir A, Moriya S, Nagakawa E, Nanamiya H, Nakai S, Nygaard P, Ogura M, Ohanan T, O’Reilly M, O’Rourke M, Pragai Z, Pooley HM, Rapoport G, Rawlins JP, Rivas LA, Rivolta C, Sadaie A, Sadaie Y, Sarvas M, Sato T, Saxild HH, Scanlan E, Schumann W, Seegers JF, Sekiguchi J, Sekowska A, Seror SJ, Simon M, Stragier P, Studer R, Takamatsu H, Tanaka T, Takeuchi M, Thomaides HB, Vagner V, van Dijl JM, Watabe K, Wipat A, Yamamoto H, Yamamoto M, Yamamoto Y, Yamane K, Yata K, Yoshida K, Yoshikawa H, Zuber U, Ogasawara N (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 100:4678-4683

    Article  CAS  PubMed  Google Scholar 

  • 67. Kobayashi Y, Momoi MY, Tominaga K, Momoi T, Nihei K, Yanagisawa M, Kagawa Y, Ohta S (1990) A point mutation in the mitochondrial tRNA(Leu)(UUR) gene in MELAS (mitochondrial myopathy, encephalopathy, lactic acidosis and stroke-like episodes). Biochem Biophys Res Commun 173:816-822

    Google Scholar 

  • 68. Kobayashi Y, Momoi MY, Tominaga K, Shimoizumi H, Nihei K, Yanagisawa M, Kagawa Y, Ohta S (1991) Respiration-deficient cells are caused by a single point mutation in the mitochondrial tRNA-Leu (UUR) gene in mitochondrial myopathy, encephalopathy, lactic acidosis, and strokelike episodes (MELAS). Am J Hum Genet 49:590-599

    Google Scholar 

  • 69. Koga Y, Nonaka I, Kobayashi M, Tojyo M, Nihei K (1988) Findings in muscle in complex I (NADH coenzyme Q reductase) deficiency. Ann Neurol 24:749-756

    Article  Google Scholar 

  • 70. Kuchino Y, Borek E, Grunberger D, Mushinski JF, Nishimura S (1982) Changes of post-transcriptional modification of wye base in tumor-specific tRNAPhe. Nucleic Acids Res 10:6421-6432

    Google Scholar 

  • 71. Kurata S, Ohtsuki T, Wada T, Kirino Y, Takai K, Saigo K, Watanabe K, Suzuki T (2003) Decoding property of C5 uridine modification at the wobble position of tRNA anticodon. Nucleic Acids Res Suppl:245-246 Kutay U, Lipowsky G, Izaurralde E, Bischoff FR, Schwarzmaier P, Hartmann E, Gorlich D (1998) Identification of a tRNA-specific nuclear export receptor. Mol Cell 1:359-369

    Google Scholar 

  • 72. Lauhon CT (2002) Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli. J Bacteriol 184:6820-6829

    Article  Google Scholar 

  • 73. Li R, Li X, Yan Q, Qin Mo J, Guan MX (2003) Identification and characterization of mouse MTO1 gene related to mitochondrial tRNA modification. Biochim Biophys Acta 1629:53-59

    Google Scholar 

  • 74. Li X, Guan MX (2002) A human mitochondrial GTP binding protein related to tRNA modification may modulate phenotypic expression of the deafness-associated mitochondrial 12S rRNA mutation. Mol Cell Biol 22:7701-7711

    Article  Google Scholar 

  • 75. Li X, Li R, Lin X, Guan MX (2002) Isolation and characterization of the putative nuclear modifier gene MTO1 involved in the pathogenesis of deafness-associated mitochondrial 12 S rRNA A1555G mutation. J Biol Chem 277:27256-27264

    Article  Google Scholar 

  • 76. Lustig F, Boren T, Claesson C, Simonsson C, Barciszewska M, Lagerkvist U (1993) The nucleotide in position 32 of the tRNA anticodon loop determines ability of anticodon UCC to discriminate among glycine codons. Proc Natl Acad Sci USA 90:3343-3347

    Google Scholar 

  • 77. Maas S, Patt S, Schrey M, Rich A (2001) Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc Natl Acad Sci USA 98:14687-14692

    Article  Google Scholar 

  • 78. Mahapatra S, Adhya S (1996) Import of RNA into Leishmania mitochondria occurs through direct interaction with membrane-bound receptors. J Biol Chem 271:20432-20437

    Article  Google Scholar 

  • 79. Mahapatra S, Ghosh S, Bera SK, Ghosh T, Das A, Adhya S (1998) The D arm of tRNATyr is necessary and sufficient for import into Leishmania mitochondria in vitro. Nucleic Acids Res 26:2037-2041

    Article  Google Scholar 

  • 80. Mahapatra S, Ghosh T, Adhya S (1994) Import of small RNAs into Leishmania mitochondria in vitro. Nucleic Acids Res 22:3381-3386

    Google Scholar 

  • 81. Marck C, Grosjean H (2002) tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. Rna 8:1189-1232

    Article  Google Scholar 

  • 82. Matsugi J, Murao K, Ishikura H (1996) Characterization of a B. subtilis minor isoleucine tRNA deduced from tDNA having a methionine anticodon CAT. J Biochem (Tokyo) 119:811-816

    Google Scholar 

  • 83. Matsuyama S, Ueda T, Crain PF, McCloskey JA, Watanabe K (1998) A novel wobble rule found in starfish mitochondria. Presence of 7-methylguanosine at the anticodon wobble position expands decoding capability of tRNA. J Biol Chem 273:3363-3368

    Article  Google Scholar 

  • 84. Mattaj IW, Englmeier L (1998) Nucleocytoplasmic transport: the soluble phase. Annu Rev Biochem 67:265-306

    Article  Google Scholar 

  • 85. McCloskey JA, Graham DE, Zhou S, Crain PF, Ibba M, Konisky J, Soll D, Olsen GJ (2001) Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res 29:4699-4706

    Article  Google Scholar 

  • 86. Meier F, Suter B, Grosjean H, Keith G, Kubli E (1985) Queuosine modification of the wobble base in tRNAHis influences in vivo decoding properties. EMBO J 4(3):823-827

    Google Scholar 

  • 87. Mihara H, Kato S, Lacourciere GM, Stadtman TC, Kennedy RA, Kurihara T, Tokumoto U, Takahashi Y, Esaki N (2002) The iscS gene is essential for the biosynthesis of 2-selenouridine in tRNA and the selenocysteine-containing formate dehydrogenase H. Proc Natl Acad Sci USA 99:6679-6683

    Article  Google Scholar 

  • 88. Mitchell JR, Wood E, Collins K (1999) A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402:551-555

    Article  CAS  PubMed  Google Scholar 

  • 89. Moise NS, Pacioretty LM, Kallfelz FA, Stipanuk MH, King JM, Gilmour RF Jr (1991) Dietary taurine deficiency and dilated cardiomyopathy in the fox. Am Heart J 121:541-547

    Article  Google Scholar 

  • 90. Moraes CT, Ciacci F, Silvestri G, Shanske S, Sciacco M, Hirano M, Schon EA, Bonilla E, DiMauro S (1993) Atypical clinical presentations associated with the MELAS mutation at position 3243 of human mitochondrial DNA. Neuromuscul Disord 3:43-50

    Article  Google Scholar 

  • 91. Moriya J, Yokogawa T, Wakita K, Ueda T, Nishikawa K, Crain PF, Hashizume T, Pomerantz SC, McCloskey JA, Kawai G, Hayashi N, Yokoyama S, Watanabe K (1994) A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 33:2234-2239

    Google Scholar 

  • 92. Munz P, Leupold U, Agris P, Kohli J (1981) In vivo decoding rules in Schizosaccharomyces pombe are at variance with in vitro data. Nature 294:187-188

    Google Scholar 

  • 93. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553-563

    Article  Google Scholar 

  • 94. Muramatsu T, Nishikawa K, Nemoto F, Kuchino Y, Nishimura S, Miyazawa T, Yokoyama S (1988a) Codon and amino-acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature 336:179-181

    Google Scholar 

  • 95. Muramatsu T, Yokoyama S, Horie N, Matsuda A, Ueda T, Yamaizumi Z, Kuchino Y, Nishimura S, Miyazawa T (1988b) A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA from Escherichia coli. J Biol Chem 263:9261-9267

    Google Scholar 

  • 96. Nakai Y, Umeda N, Suzuki T, Nakai M, Hayashi H, Watanabe K, Kagamiyama H (2004) Yeast Nfs1p is involved in thio-modification of both mitochondrial and cytoplasmic tRNAs. J Biol Chem 279:12363-12368

    Article  Google Scholar 

  • 97. Nakayashiki T, Inokuchi H (1998) Novel temperature-sensitive mutants of Escherichia coli that are unable to grow in the absence of wild-type tRNA6Leu. J Bacteriol 180:2931-2935

    Google Scholar 

  • 98. Nilsson K, Lundgren HK, Hagervall TG, Bjork GR (2002) The cysteine desulfurase IscS is required for synthesis of all five thiolated nucleosides present in tRNA from Salmonella enterica serovar typhimurium. J Bacteriol 184:6830-6835

    Article  Google Scholar 

  • 99. Nishimura S (1983) Structure, biosynthesis, and function of queuosine in transfer RNA. Prog Nucleic Acid Res Mol Biol 28:49-73

    Google Scholar 

  • 100. Ogle JM, Murphy FV, Tarry MJ, Ramakrishnan V (2002) Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111:721-732

    Article  Google Scholar 

  • 101. Osawa S (1995) Evolution of the genetic code. Oxford Univ. Press

    Google Scholar 

  • 102. Osawa S, Jukes TH (1989) Codon reassignment (codon capture) in evolution. J Mol Evol 28(4):271-278

    Google Scholar 

  • 103. Petersen-Mahrt SK, Harris RS, Neuberger MS (2002) AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418:99-103

    Google Scholar 

  • 104. Pion PD, Kittleson MD, Rogers QR, Morris JG (1987) Myocardial failure in cats associated with low plasma taurine: a reversible cardiomyopathy. Science 237:764-768

    Google Scholar 

  • 105. Powers DM, Peterkofsky A (1972) The presence of N-(purin-6-ylcarbamoyl)threonine in transfer ribonucleic acid species whose codons begin with adenine. J Biol Chem 247:6394-6401

    Google Scholar 

  • 106. Ravn K, Wibrand F, Hansen FJ, Horn N, Rosenberg T, Schwartz M (2001) An mtDNA mutation, 14453G$to$A, in the NADH dehydrogenase subunit 6 associated with severe MELAS syndrome. Eur J Hum Genet 9:805-809

    Article  Google Scholar 

  • 107. Revy P, Muto T, Levy Y, Geissmann F, Plebani A, Sanal O, Catalan N, Forveille M, Dufourcq-Labelouse R, Gennery A, Tezcan I, Ersoy F, Kayserili H, Ugazio AG, Brousse N, Muramatsu M, Notarangelo LD, Kinoshita K, Honjo T, Fischer A, Durandy A (2000) Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102:565-575

    Article  CAS  PubMed  Google Scholar 

  • 108. Rubio MA, Liu X, Yuzawa H, Alfonzo JD, Simpson L (2000) Selective importation of RNA into isolated mitochondria from Leishmania tarentolae. Rna 6:988-1003

    Article  Google Scholar 

  • 109. Ruggero D, Grisendi S, Piazza F, Rego E, Mari F, Rao PH, Cordon-Cardo C, Pandolfi PP (2003) Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 299:259-262

    Article  CAS  PubMed  Google Scholar 

  • 110. Rusconi CP, Cech TR (1996) The anticodon is the signal sequence for mitochondrial import of glutamine tRNA in Tetrahymena. Genes Dev 10:2870-2880

    Google Scholar 

  • 111. Sakurai M, Ohtsuki T, Suzuki T, Watanabe K (submitted) Characteristic modification at wobble uridine in mitochondrial tRNAs of the nematode Ascaris suum.

    Google Scholar 

  • 112. Salazar JC, Ambrogelly A, Crain PF, McCloskey JA, Soll D (2004) A truncated aminoacyl-tRNA synthetase modifies RNA. Proc Natl Acad Sci USA 101:7536-7541, Epub 2004 Apr 7519

    Article  Google Scholar 

  • 113. Samuelsson T, Elias P, Lustig F, Axberg T, Folsch G, Akesson B, Lagerkvist U (1980) Aberrations of the classic codon reading scheme during protein synthesis in vitro. J Biol Chem 255:4583-4588

    Google Scholar 

  • 114. Schneider A, Marechal-Drouard L (2000) Mitochondrial tRNA import: are there distinct mechanisms? Trends Cell Biol 10:509-513

    Article  Google Scholar 

  • 115. Schon EA, Bonilla E, DiMauro S (1997) Mitochondrial DNA mutations and pathogenesis. J Bioenerg Biomembr 29:131-149

    Google Scholar 

  • 116. Shigi N, Suzuki T, Tamakoshi M, Oshima T, Watanabe K (2002) Conserved bases in the TPsi C loop of tRNA are determinants for thermophile-specific 2-thiouridylation at position 54. J Biol Chem 277:39128-39135

    Article  Google Scholar 

  • 117. Shoffner JM, Lott MT, Lezza AM, Seibel P, Ballinger SW, Wallace DC (1990) Myoclonic epilepsy and ragged-red fiber disease (MERRF) is associated with a mitochondrial DNA tRNA(Lys) mutation. Cell 61:931-937

    Article  Google Scholar 

  • 118. Sibler AP, Dirheimer G, Martin RP (1986) Codon reading patterns in Saccharomyces cerevisiae mitochondria based on sequences of mitochondrial tRNAs. FEBS Lett 194:131-138

    Article  Google Scholar 

  • 119. Simpson AM, Suyama Y, Dewes H, Campbell DA, Simpson L (1989) Kinetoplastid mitochondria contain functional tRNAs which are encoded in nuclear DNA and also contain small minicircle and maxicircle transcripts of unknown function. Nucleic Acids Res 17:5427-5445

    Google Scholar 

  • 120. Soll D, Jones DS, Ohtsuka E, Faulkner RD, Lohrmann R, Hayatsu H, Khorana HG (1966) Specificity of sRNA for recognition of codons as studied by the ribosomal binding technique. J Mol Biol 19:556-573

    Google Scholar 

  • 121. Soma A, Ikeuchi Y, Kanemasa S, Kobayashi K, Ogasawara N, Ote T, Kato J, Watanabe K, Sekine Y, Suzuki T (2003) An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA. Mol Cell 12:689-698

    Article  Google Scholar 

  • 122. Sommer B, Kohler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11-19

    Article  CAS  PubMed  Google Scholar 

  • 123. Sturman JA (1993) Taurine in development. Physiol Rev 73:119-147

    Google Scholar 

  • 124. Sullivan MA, Cannon JF, Webb FH, Bock RM (1985) Antisuppressor mutation in Escherichia coli defective in biosynthesis of 5-methylaminomethyl-2-thiouridine. J Bacteriol 161:368-376

    Google Scholar 

  • 125. Suzuki T, Suzuki T, Wada T, Saigo K, Watanabe K (2002) Taurine as a constituent of mitochondrial tRNAs: new insights into the functions of taurine and human mitochondrial diseases. Embo J 21:6581-6589

    Article  Google Scholar 

  • 126. Suzuki T, Ueda T, Watanabe K (1997) The ‘polysemous’ codon–a codon with multiple amino acid assignment caused by dual specificity of tRNA identity. Embo J 16:1122-1134

    Article  Google Scholar 

  • 127. Suzuki T, Ueda T, Yokogawa T, Nishikawa K, Watanabe K (1994) Characterization of serine and leucine tRNAs in an asporogenic yeast Candida cylindracea and evolutionary implications of genes for tRNA(Ser)CAG responsible for translation of a non-universal genetic code. Nucleic Acids Res 22:115-123

    Google Scholar 

  • 128. Tan TH, Pach R, Crausaz A, Ivens A, Schneider A (2002) tRNAs in Trypanosoma brucei: genomic organization, expression, and mitochondrial import. Mol Cell Biol 22:3707-3717

    Article  Google Scholar 

  • 129. Tarassov IA, Martin RP (1996) Mechanisms of tRNA import into yeast mitochondria: an overview. Biochimie 78:502-510

    Article  Google Scholar 

  • 130. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631-637

    Article  Google Scholar 

  • 131. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22-28

    Article  Google Scholar 

  • 132. Teng B, Burant CF, Davidson NO (1993) Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260:1816-1819

    Google Scholar 

  • 133. Tesmer JJ, Klem TJ, Deras ML, Davisson VJ, Smith JL (1996) The crystal structure of GMP synthetase reveals a novel catalytic triad and is a structural paradigm for two enzyme families. Nat Struct Biol 3:74-86

    Article  Google Scholar 

  • 134. Tomita K, Ueda T, Watanabe K (1998) 7-Methylguanosine at the anticodon wobble position of squid mitochondrial tRNA(Ser)GCU: molecular basis for assignment of AGA/AGG codons as serine in invertebrate mitochondria. Biochim Biophys Acta 1399:78-82

    Google Scholar 

  • 135. Uchida S, Kwon HM, Yamauchi A, Preston AS, Marumo F, Handler JS (1992) Molecular cloning of the cDNA for an MDCK cell Na(+)- and Cl(-)-dependent taurine transporter that is regulated by hypertonicity. Proc Natl Acad Sci USA 89:8230-8234

    Google Scholar 

  • 136. Umeda N, Suzuki T, Yukawa M, Ohya Y, Shindo H, Watanabe K, Suzuki T (2005 Mitochondria-specific RNA-modifying enzymes responsible for the biosynthesis of the wobble base in mitochondrial tRNAs: implications for the molecular pathogenesis of human mitochondrial diseases. J Biol Chem, in press

    Google Scholar 

  • 137. van den Ouweland JM, Lemkes HH, Ruitenbeek W, Sandkuijl LA, de Vijlder MF, Struyvenberg PA, van de Kamp JJ, Maassen JA (1992) Mutation in mitochondrial tRNA(Leu)(UUR) gene in a large pedigree with maternally transmitted type II diabetes mellitus and deafness. Nat Genet 1:368-371

    Article  Google Scholar 

  • 138. Wallace DC (2000) Mitochondrial defects in cardiomyopathy and neuromuscular disease. Am Heart J 139:S70-85

    Article  CAS  PubMed  Google Scholar 

  • 139. Wallace DC, Lott MT (2003) MITOMAP: A Human Mitochondrial Genome Database” http://www.mitomap.org.

    Google Scholar 

  • 140. Watanabe K, Osawa S (1995) Evolution of the Genetic Code. ASM press, Washington, DC

    Google Scholar 

  • 141. Weber F, Dietrich A, Weil JH, Marechal-Drouard L (1990) A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucleic Acids Res 18:5027-5030

    CAS  PubMed  Google Scholar 

  • 142. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Davis RW, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906

    Article  CAS  PubMed  Google Scholar 

  • 143. Wolf J, Gerber AP, Keller W (2002) tadA, an essential tRNA-specific adenosine deaminase from Escherichia coli. Embo J 21:3841-3851

    Article  Google Scholar 

  • 144. Yarian C, Marszalek M, Sochacka E, Malkiewicz A, Guenther R, Miskiewicz A, Agris PF (2000) Modified nucleoside dependent Watson-Crick and wobble codon binding by tRNALysUUU species. Biochemistry 39:13390-13395

    Article  Google Scholar 

  • 145. Yasukawa T, Suzuki T, Ishii N, Ohta S, Watanabe K (2001) Wobble modification defect in tRNA disturbs codon-anticodon interaction in a mitochondrial disease. Embo J 20:4794-4802

    Article  Google Scholar 

  • 146. Yasukawa T, Suzuki T, Ishii N, Ueda T, Ohta S, Watanabe K (2000a) Defect in modification at the anticodon wobble nucleotide of mitochondrial tRNA(Lys) with the MERRF encephalomyopathy pathogenic mutation. FEBS Lett 467:175-178

    Article  Google Scholar 

  • 147. Yasukawa T, Suzuki T, Suzuki T, Ueda T, Ohta S, Watanabe K (2000b) Modification defect at anticodon wobble nucleotide of mitochondrial tRNAs(Leu)(UUR) with pathogenic mutations of mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes. J Biol Chem 275:4251-4257

    Article  Google Scholar 

  • 148. Yokobori S, Suzuki T, Watanabe K (2001) Genetic code variations in mitochondria: tRNA as a major determinant of genetic code plasticity. J Mol Evol 53(4-5):314-326

    Google Scholar 

  • 149. Yokoyama S, Nishimura S (1995) Modified nucleosides and codon recognition, Soll, D. and Rajbandary, U. L. edn. ASM press, Washington, DC

    Google Scholar 

  • 150. Yokoyama S, Watanabe T, Murao K, Ishikura H, Yamaizumi Z, Nishimura S, Miyazawa T (1985) Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon. Proc Natl Acad Sci USA 82:4905-4909

    Google Scholar 

  • 151. Yokoyama S, Yamaizumi Z, Nishimura S, Miyazawa T (1979) 1H NMR studies on the conformational characteristics of 2-thiopyrimidine nucleotides found in transfer RNAs. Nucleic Acids Res 6:2611-2626

    Google Scholar 

  • 152. Yoneda M, Miyatake T, Attardi G (1994) Complementation of mutant and wild-type human mitochondrial DNAs coexisting since the mutation event and lack of complementation of DNAs introduced separately into a cell within distinct organelles. Mol Cell Biol 14:2699-2712

    Google Scholar 

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Suzuki, T. Biosynthesis and function of tRNA wobble modifications. In: Grosjean, H. (eds) Fine-Tuning of RNA Functions by Modification and Editing. Topics in Current Genetics, vol 12. Springer, Berlin, Heidelberg. https://doi.org/10.1007/b106361

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