Translation in mammalian mitochondria: Order and disorder linked to tRNAs and aminoacyl-tRNA synthetases

Translation in Mitochondria and Other Organelles

Volumn 9783642392801, Issue , 2013, Pages 55-83

  Florentz, Catherine ^a   Putz, Joern ^a   Juhling, Frank ^a,b   Schwenzer, Hagen ^a   Stadler, Peter F ^b   Lorber, Bernard ^a   Sauter, Claude ^a   Sissler, Marie ^a  

^a INST DE BIOL MOLEC ET CELLULAIRE   (France)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Mammalian mitochondria; Mitochondrial aminoacyl tRNA synthetase; Mitochondrial disorders; Mitochondrial tRNA; Plasticity; Structure function; Translation

Indexed keywords

AMINO ACIDS; BIOSYNTHESIS; CHAINS; GENES; LEAD COMPOUNDS; MACROMOLECULES; MAMMALS; PROTEINS;

AMINOACYL; AMINOACYL TRANSFER; MAMMALIAN MITOCHONDRIA; MITOCHONDRIAL AMINOACYL-TRANSFER RNA SYNTHETASE; MITOCHONDRIAL DISORDERS; MITOCHONDRIAL TRANSFER RNA; MITOCHONDRIAS; RNA SYNTHETASES; STRUCTURE FUNCTIONS; TRANSLATION;

MITOCHONDRIA;

EID: 84923603497     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-39426-3_3     Document Type: Chapter

References (116)

1. Alfonzo JD, Söll D (2009) Mitochondrial tRNA import-the challenge to understand has just begun. Biol Chem 390:717-722
2. Anderson S, Bankier AT, Barrel BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon JC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457-465
3. Arcari P, Brownlee GG (1980) The nucleotide sequence of a small (3S) seryl-tRNA (anticodon GCU) from beef heart mitochondria. Nucleic Acids Res 8:5207-5212
4. Bayat V, Thiffault I, Jaiswal M, Tétreault M, Donti T, Sasarman F, Bernard G, Demers-Lamarche J, Dicaire MJ, Mathieu J, Vanasse M, Bouchard JP, Rioux MF, Lourenco CM, Li Z, Haueter C, Shoubridge EA, Graham BH, Brais B, Bellen HJ (2012) Mutations in the mitochondrial methionyl-tRNA synthetase cause a neurodegenerative phenotype in flies and a recessive ataxia (ARSAL) in humans. PLoS Biol 10:e1001288
5. Belostotsky R, Ben-Shalom E, Rinat C, Becker-Cohen R, Feinstein S, Zeligson S, Segel R, Elpeleg O, Nassar S, Frishberg Y (2011) Mutations in the mitochondrial seryl-tRNA synthetase cause hyperuricemia, pulmonary hypertension, renal failure in infancy and alkalosis, HUPRA syndrome. Am J Hum Genet 88:193-200
6. Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2012) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol [Epub ahead of print]
7. Bonnefond L, Fender A, Rudinger-Thirion J, Giegé R, Florentz C, Sissler M (2005a) Toward the full set of human mitochondrial aminoacyl-tRNA synthetases: characterization of AspRS and TyrRS. Biochemistry 44:4805-4816
8. Bonnefond L, Frugier M, Giegé R, Rudinger-Thirion J (2005b) Human mitochondrial TyrRS disobeys the tyrosine idenity rules. RNA 11:558-562
9. Bonnefond L, Frugier M, Touzé E, Lorber B, Florentz C, Giegé R, Sauter C, Rudinger-Thirion J (2007) Crystal structure of human mitochondrial tyrosyl-tRNA synthetase reveals common and idiosyncratic features. Structure 15:1505-1516
10. Braband A, Cameron SL, Podsiadlowski L, Daniels SR, Mayer G (2010) The mitochondrial genome of the onychophoran Opisthopatus cinctipes (Peripatopsidae) reflects the ancestral mitochondrial gene arrangement of Panarthropoda and Ecdysozoa. Mol Phylogenet Evol 57:285-292
11. Brindefalk B, Viklund J, Larsson D, Thollesson M, Andersson SG (2007) Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases. Mol Biol Evol 24:743-756
12. Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967-1971
13. Bullard J, Cai Y-C, Spremulli L (2000) Expression and characterization of the human mitochondrial leucyl-tRNA synthetase. Biochem Biophys Acta 1490:245-258
14. Cader MZ, Ren J, James PA, Bird LE, Talbot K, Stammers DK (2007) Crystal structure of human wildtype and S581L-mutant glycyl-tRNA synthetase, an enzyme underlying distal spinal muscular atrophy. FEBS Lett 581:2959-2964
15. Castellana S, Vicario S, Saccone C (2011) Evolutionary patterns of the mitochondrial genome in Metazoa: exploring the role of mutation and selection in mitochondrial protein coding genes. Genome Biol Evol 3:1067-1079
16. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 1387:628-644
17. Chimnaronk S, Gravers Jeppesen M, Suzuki T, Nyborg J, Watanabe K (2005) Dual-mode recognition of noncanonical tRNAs(Ser) by seryl-tRNA synthetase in mammalian mitochondria. EMBO J 24:3369-3379
18. de Bruijn MH, Schreier PH, Eperon IC, Barrell BG, Chen EY, Armstrong PW, Wong JF, Roe BA (1980) A mammalian mitochondrial serine transfer RNA lacking the "dihydrouridine" loop and stem. Nucleic Acids Res 8:5213-5222
19. Dörner M, Altmann M, Pääbo S, Mörl M (2001) Evidence for import of a lysyl-tRNA into marsupial mitochondria. Mol Biol Cell 12:2688-2698
20. Duchêne AM, Pujol C, Maréchal-Drouard L (2009) Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet 55:1-18
21. Edvardson S, Shaag A, Kolesnikova O, Gomori JM, Tarassov I, Einbinder T, Saada A, Elpeleg O (2007) Deleterious mutation in the mitochondrial arginyl-transfer RNA synthetase gene is associated with pontocerebellar hypoplasia. Am J Hum Genet 81:857-862
22. Elo JM, Yadavalli SS, Euro L, Isohanni P, Götz A, Carroll CJ, Valanne L, Alkuraya FS, Uusimaa J, Paetau A, Caruso EM, Pihko H, Ibba M, Tyynismaa H, Suomalainen A (2012) Mitochondrial phenylalanyl-tRNA synthetase mutations underlie fatal infantile Alpers encephalopathy. Hum Mol Genet 21:4521-4529
23. Enriquez JA, Attardi G (1996) Analysis of aminoacylation of human mitochondrial tRNAs. Methods Enzymol 264:183-196
24. Fender A, Gaudry A, Jühling F, Sissler M, Florentz C (2012) Adaptation of aminoacylation rules to mammalian mitochondria. Biochimie 94:1090-1097
25. Fender A, Sauter C, Messmer M, Pütz J, Giegé R, Florentz C, Sissler M (2006) Loss of a primordial identity element for a mammalian mitochondrial aminoacylation system. J Biol Chem 281:15980-15986
26. Florentz C, Sissler M (2001) Disease-related versus polymorphic mutations in human mitochondrial tRNAs: where is the difference? EMBO Rep 2(6):481-486
27. Florentz C, Sissler M (2003) Mitochondrial tRNA aminoacylation and human diseases. In: Lapointe J, Brakier-Gingras L (eds) Translation mechanisms. Landes Bioscience, Georgetown, pp 129-143
28. Florentz C, Sohm B, Tryoen-Tóth P, Pütz J, Sissler M (2003) Human mitochondrial tRNAs in health and disease. Cell Mol Life Sci 60:1356-1375
29. Frechin M, Duchêne A-M, Becker HD (2009a) Translating organellar glutamine codons: A case by case scenario? RNA Biol 6:31-34
30. Frechin M, Senger B, Brayé M, Kern D, Martin RP, Becker HD (2009b) Yeast mitochondrial Gln-tRNA(Gln) is generated by a GatFAB-mediated transamidation pathway involving Arc1p-controlled subcellular sorting of cytosolic GluRS. Genes Dev 23:1119-1130
31. Friederich MW, Hagerman PJ (1997) The angle between the anticodon and aminoacyl acceptor stems of yeast tRNA(Phe) is strongly modulated by magnesium ions. Biochemistry 36:6090-6099
32. Gaudry A, Lorber B, Messmer M, Neuenfeldt A, Sauter C, Florentz C, Sissler M (2012) Redesigned N-terminus enhances expression, solubility, and crystallisability of mitochondrial enzyme. Protein Eng Des Sel 25:473-481
33. Giegé R (2008) Toward a more complete view of tRNA biology. Nat Struct Mol Biol 15:1007-1014
34. Giegé R, Florentz C, Kern D, Gangloff J, Eriani G, Moras D (1996) Aspartate identity of transfer RNAs. Biochimie 78:605-623
35. Giegé R, Jühling F, Pütz J, Stadler P, Sauter C, Florentz C (2012) Structure of transfer RNAs: similarity and variability. Wiley Interdiscip Rev RNA 3:37-61
36. Giegé R, Sissler M, Florentz C (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 26:5017-5035
37. Goto Y, Nonaka I, Horai S (1990) A mutation in the tRNALeu(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 348:651-653
38. Götz A, Tyynismaa H, Euro L, Ellonen P, Hyötyläinen T, Ojala T, Hämäläinen RH, Tommiska J, Raivio T, Oresic M, Karikoski R, Tammela O, Simola KO, Paetau A, Tyni T, Suomalainen A (2011) Exome sequencing identifies mitochondrial alanyl-tRNA synthetase mutations in infantile mitochondrial cardiomyopathy. Am J Hum Genet 88:635-642
39. Guo M, Ignatov M, Musier-Forsyth K, Schimmel P, Yang XL (2008) Crystal structure of tetrameric form of human lysyl-tRNA synthetase: Implications for multisynthetase complex formation. Proc Natl Acad Sci USA 105:2331-2336
40. Guo M, Schimmel P (2013) Essential nontranslational functions of tRNA synthetases. Nat Chem Biol 9:145-153
41. Guo M, Schimmel P, Yang X-L (2010a) Functional expansion of human tRNA synthetases achieved by structural inventions. FEBS Lett 584:434-442
42. Guo M, Yang XL, Schimmel P (2010b) New functions of aminoacyl-tRNA synthetases beyond translation. Nat Rev Mol Cell Biol 11:668-674
43. Haen KM, Pett W, Lavrov DV (2010) Parallel loss of nuclear-encoded mitochondrial aminoacyltRNA synthetases and mtDNA-encoded tRNAs in Cnidaria. Mol Biol Evol 27:2216-2219
44. Helm M, Attardi G (2004) Nuclear control of cloverleaf structure of human mitochondrial tRNA(Lys). J Mol Biol 337:545-560
45. Helm M, Brulé H, Degoul F, Cepanec C, Leroux J-P, Giegé R, Florentz C (1998) The presence of modified nucleotides is required for cloverleaf folding of a human mitochondrial tRNA. Nucleic Acids Res 26:1636-1643
46. Helm M, Brulé H, Friede D, Giegé R, Pütz J, Florentz C (2000) Search for characteristic structural features of mammalian mitochondrial tRNAs. RNA 6:1356-1379
47. Helm M, Florentz C, Chomyn A, Attardi G (1999) Search for differences in post-transcriptional modification patterns of mitochondrial DNA-encoded wild-type and mutant human tRNALys and tRNALeu(UUR). Nucleic Acids Res 27:756-763
48. Hou YM, Yang X (2013) Regulation of cell death by transfer RNA. Antioxid Redox Signal [Epub ahead of print]
49. Ibba M, Francklyn C, Cusack S (2005) The aminoacyl-tRNA synthetases. Landes Biosciences, Georgetown
50. Jacobs HT, Holt IJ (2000) The np 3243 MELAS mutation: damned if you aminoacylate, damned if you don't. Hum Mol Genet 1:463-465
51. Jacobs HT (2003) Disorders of mitochondrial protein synthesis. Hum Mol Genet 12:R293-301
52. Jia J, Arif A, Ray PS, Fox PL (2008) WHEP domains direct noncanonical function of glutamyl- Prolyl-tRNA synthetase in translational control of gene expression. Mol Cell 29:679-690
53. Jühling F, Pütz J, Bernt M, Donath A, Middendorf M, Florentz C, Stadler PF (2012a) Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements. Nucleic Acids Res 40:2833-2845
54. Jühling F, Pütz J, Florentz C, Stadler PF (2012b) Armless mitochondrial tRNAs in Enoplea (Nematoda). RNA Biol 9:1161-1166
55. Kim DG, Choi JW, Lee JY, Kim H, Oh YS, Lee JW, Tak YK, Song JM, Razin E, Yun SH, Kim S (2012) Interaction of two translational components, lysyl-tRNA synthetase and p40/37LRP, in plasma membrane promotes laminin-dependent cell migration. FASEB J 26:4142-4159
56. Kirino Y, Goto Y, Campos Y, Arenas J, Suzuki T (2005) Specific correlation between the wobble modification deficiency in mutant tRNAs and the clinical features of a human mitochondrial disease. Proc Natl Acad Sci USA 102:7127-7132
57. Kleiman L, Cen S (2004) The tRNALys packaging complex in HIV-1. Int J Biochem Cell Biol 36:1776-1786
58. Klipcan L, Levin I, Kessler N, Moor N, Finarov I, Safro M (2008) The tRNA-induced conformational activation of human mitochondrial phenylalanyl-tRNA synthetase. Structure 16:1095-1104
59. Klipcan L, Moor N, Finarov I, Kessler N, Sukhanova M, Safro MG (2012) Crystal structure of human mitochondrial PheRS complexed with tRNA(Phe) in the active "open" state. J Mol Biol 415:527-537
60. Konovalova S, Tyynismaa H (2013) Mitochondrial aminoacyl-tRNA synthetases in human disease. Mol Genet Metab [Epub ahead of print]
61. Kumazawa Y, Himeno H, Miura K, Watanabe K (1991) Unilateral aminoacylation specificity between bovine mitochondria and eubacteria. J Biochem 109:421-427
62. LaRiviere FJ, Wolfson AD, Uhlenbeck OC (2001) Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 294:165-168
63. Laslett D, Canbäck B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24:172-175
64. Leontis NB, Stombaugh J, Westhof E (2002) The non-Watson-Crick base pairs and their associated isostericity matrices. Nucleic Acids Res 30:3497-3531
65. Levinger L, Mörl M, Florentz C (2004) Mitochondrial tRNA 3' end metabolism and human disease. Nucleic Acids Res 32:5430-5441
66. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955-964
67. Macey JR, Larson A, Ananjeva NB, Papenfuss TJ (1997) Replication slippage may cause parallel evolution in the secondary structures of mitochondrial transfer RNAs. Mol Biol Evol 14:30-39
68. McFarland R, Elson JL, Taylor RW, Howell N, Turnbull DM (2004) Assigning pathogenicity to mitochondrial tRNA mutations: when 'definitely maybe' is not good enough. Trends Genet 20:591-596
69. Mei Y, Yong J, Liu H, Shi Y, Meinkoth J, Dreyfuss G, Yang X (2010) tRNA binds to cytochrome c and inhibits caspase activation. Mol Cell 37:688-698
70. Messmer M, Pütz J, Suzuki T, Suzuki T, Sauter C, Sissler M, Florentz C (2009) Tertiary network in mammalian mitochondrial tRNAAsp revealed by solution probing and phylogeny. Nucleic Acids Res 37:6881-6895
71. Miyamoto H, Machida RJ, Nishida S (2010) Complete mitochondrial genome sequences of the three pelagic chaetognaths Sagitta nagae, Sagitta decipiens and Sagitta enflata. Comp Biochem Physiol Part D Genomics Proteomics 5:65-72
72. Motorin Y, Helm M (2010) tRNA stabilization by modified nucleotides. Biochemistry 49:4934-4944
73. Mudge SJ, Williams JH, Eyre HJ, Sutherland GR, Cowan PJ, Power DA (1998) Complex organisation of the 5'-end of the human glycine tRNA synthetase gene. Gene 209:45-50
74. Nagao A, Suzuki T, Katoh T, Sakaguchi Y, Suzuki T (2009) Biogenesis of glutaminyl-mt tRNAGln in human mitochondria. Proc Natl Acad Sci USA 106:16209-16214
75. Nagao A, Suzuki T, Suzuki T (2007) Aminoacyl-tRNA surveillance by EF-Tu in mammalian mitochondria. Nucleic Acids Symp Ser (Oxf) 51:41-42
76. Nawroki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: Inference of RNA Alignments. Bioinformatics 25:1335-1337
77. Neuenfeldt A, Lorber B, Ennifar E, Gaudry A, Sauter C, Sissler M, Florentz C (2013) Thermodynamic properties distinguish human mitochondrial aspartyl-tRNA synthetase from bacterial homolog with same 3D architecture. Nucleic Acids Res 41:2698-2708
78. Ofir-Birin Y, Fang P, Bennett SP, Zhang HM, Wang J, Rachmin I, Shapiro R, Song J, Dagan A, Pozo J, Kim S, Marshall AG, Schimmel P, Yang XL, Nechushtan H, Razin E, Guo M (2013) Structural switch of lysyl-tRNA synthetase between translation and transcription. Mol Cell 49:30-42
79. Park MC, Kang T, Jin D, Han JM, Kim SB, Park YJ, Cho K, Park YW, Guo M, He W, Yang XL, Schimmel P, Kim S (2012) Secreted human glycyl-tRNA synthetase implicated in defense against ERK-activated tumorigenesis. Proc Natl Acad Sci USA 109:E640-E647
80. Park SG, Schimmel P, Kim S (2008) Aminoacyl tRNA synthetases and their connections to disease. Proc Natl Acad Sci USA 105:11043-11049
81. Pierce SB, Chisholm KM, Lynch ED, Lee MK, Walsh T, Opitz JM, Li W, Klevit RE, King MC (2011) Mutations in mitochondrial histidyl tRNA synthetase HARS2 cause ovarian dysgenesis and sensorineural hearing loss of Perrault syndrome. Proc Natl Acad Sci USA 108:6543-6548
82. Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated nonredundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 5(Database issue):D61-D65
83. Pütz J, Dupuis B, Sissler M, Florentz C (2007) Mamit-tRNA, a database of mammalian mitochondrial tRNA primary and secondary structures. RNA 13:1184-1190
84. Riley LG, Cooper S, Hickey P, Rudinger-Thirion J, McKenzie M, Compton A, Lim SC, Thorburn D, Ryan MT, Giegé R, Bahlo M, Christodoulou J (2010) Mutation of the mitochondrial tyrosyl-tRNA synthetase gene, YARS2, causes myopathy, lactic acidosis, and sideroblastic anemia-MLASA syndrome. Am J Hum Genet 87:52-59
85. Rinehart J, Krett B, Rubio M-AT, Alfonzo JD, Söll D (2005) Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondion. Genes Dev 19:583-592
86. Rötig A (2011) Human diseases with impaired mitochondrial protein synthesis. Biochim Biophys Acta 1807:1198-1205
87. Scheper GC, van der Klok T, van Andel RJ, van Berkel CG, Sissler M, Smet J, Muravina TI, Serkov SV, Uziel G, Bugiani M, Schiffmann R, Krageloh-Mann I, Smeitink JA, Florentz C, Coster RV, Pronk JC, van der Knaap MS (2007) Mitochondrial aspartyl-tRNA synthetase deficiency causes leukoencephalopathy with brain stem and spinal cord involvement and lactate elevation. Nat Genet 39:534-539
88. Schwenzer H, Zoll J, Florentz C, Sissler M (2013) Pathogenic implications of human mitochondrial aminoacyl-tRNA synthetases. In: KIM (ed) Topics in current chemistry-aminoacyltRNA synthetases: Applications in chemistry, Biology and Medicine. Springer (in press)
89. Segovia R, Pett W, Trewick S, Lavrov DV (2011) Extensive and evolutionarily persistent mitochondrial tRNA editing in Velvet Worms (phylum Onychophora). Mol Biol Evol 28:2873-2881
90. Seutin G, Lang BF, Mindell DP, Morais R (1994) Evolution of the WANCY region in amniote mitochondrial DNA. Mol Biol Evol 11:329-340
91. Shiba K, Schimmel P, Motegi H, Noda T (1994) Human glycyl-tRNA synthetase. Wide divergence of primary structure from bacterial counterpart and species-specific aminoacylation. J Biol Chem 269:30049-30055
92. Shoffner J, Lott M, Lezza AMS, Seibel P, Ballinger SW, Wallace DC (1990) Myoclonic epilepsy and ragged red fiber disease (MERRF) is associated with mitochondrial DNA tRNALys mutation. Cell 61:931-937
93. Sissler M, Pütz J, Fasiolo F, Florentz C (2005) Mitochondrial aminoacyl-tRNA synthetases. In: Ibba M, Francklyn C, Cusack S (eds), Aminoacyl-tRNA synthetases, chapter 24, pp 271- 284. Landes Biosciences, Georgetown
94. Sohm B, Frugier M, Brulé H, Olszak K, Przykorska A, Florentz C (2003) Towards understanding human mitochondrial leucine aminoacylation identity. J Mol Biol 328:995-1010
95. Steenweg ME, Ghezzi D, Haack T, Abbink TE, Martinelli D, van Berkel CG, Bley A, Diogo L, Grillo E, Te Water Naudé J, Strom TM, Bertini E, Prokisch H, van der Knaap MS, Zeviani M (2012) Leukoencephalopathy with thalamus and brainstem involvement and high lactate 'LTBL' caused by EARS2 mutations. Brain 135:1387-1394
96. Suga K, Mark Welch DB, Tanaka Y, Sakakura Y, Hagiwara A (2008) Two circular chromosomes of unequal copy number make up the mitochondrial genome of the rotifer Brachionus plicatilis. Mol Biol Evol 25:1129-1137
97. Suzuki T, Nagao A, Suzuki T (2011) Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases. Annu Rev Genet 45:299-329
98. Taylor RW, Turnbull DM (2005) Mitochondrial DNA mutations in human disease. Nat Rev Genet 6:389-402
99. Tolkunova E, Park H, Xia J, King MP, Davidson E (2000) The human lysyl-tRNA synthetase gene encodes both the cytoplasmic and mitochondrial enzymes by means of an unusual splicing of the primary transcript. J Biol Chem 275:35063-35069
100. van Berge L, Dooves S, van Berkel CG, Polder E, van der Knaap MS, Scheper GC (2012) Leukoencephalopathy with brain stem and spinal cord involvement and lactate elevation is associated with cell-type-dependent splicing of mtAspRS mRNA. Biochem J 441:955-962
101. van der Knaap MS, van der Voorn P, Barkhof F, Van Coster R, Krägeloh-Mann I, Feigenbaum A, Blaser S, Vles JS, Rieckmann P, Pouwels PJ (2003) A new leukoencephalopathy with brainstem and spinal cord involvement and high lactate. Ann Neurol 53:252-258
102. Wakasugi K, Slike BM, Hood J, Ewalt KL, Cheresh DA, Schimmel P (2002a) Induction of angiogenesis by a fragment of human tyrosyl-tRNA synthetase. J Biol Chem 277:20124-20126
103. Wakasugi K, Slike BM, Hood J, Otani A, Ewalt KL, Friedlander M, Cheresh DA, Schimmel P (2002b) A human aminoacyl-tRNA synthetase as a regulator of angiogenesis. Proc Natl Acad Sci USA 99:173-177
104. Wakita K, Watanabe Y-I, Yokogawa T, Kumazawa Y, Nakamura S, Ueda T, Watanabe K, Nishikawa K (1994) Higher-order structure of bovine mitochondrial tRNAPhe lacking the 'conserved' GG and TYCG sequences as inferred by enzymatic and chemical probing. Nucleic Acids Res 22:347-353
105. Wang X, Lavrov DV (2008) Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS ONE 3:e2723
106. Watanabe K (2010) Unique features of animal mitochondrial translation systems. The non-universal genetic code, unusual features of the translational apparatus and their relevance to human mitochondrial diseases. Proc Jpn Acad Ser B Phys Biol Sci 86:11-36
107. Willkomm DK, Hartmann RK (2006) Intricacies and surprises of nuclear-mitochondrial co-evolution. Biochem J 399:e7-e9
108. Wittenhagen LM, Kelley SO (2003) Impact of disease-related mitochondrial mutations on tRNA structure and function. Trends Biochem Sci 28:605-611
109. Woese CR, Olsen GJ, Ibba M, Söll D (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol and Mol Biol Reviews 64:202-236
110. Wolstenholme DR, Okimoto R, Mcfarlane JL (1994) Nucleotide correlations that suggest tertiary interactions in the TV-replacement loop-containing mitochondrial tRNAs of the nematodes, Caenorhabditis elegans and Ascaris suum. Nucleic Acids Res 22:4300-4306
111. Xie W, Schimmel P, Yang XL (2006) Crystallization and preliminary X-ray analysis of a native human tRNA synthetase whose allelic variants are associated with Charcot-Marie-Tooth disease. Acta Crystallograph Sect F Struct Biol Cryst Commun 62:1243-1246
112. Yadavalli SS, Klipcan L, Zozulya A, Banerjee R, Svergun D, Safro M, Ibba M (2009) Largescale movement of functional domains facilitates aminoacylation by human mitochondrial phenylalanyl-tRNA synthetase. FEBS Lett 583:3204-3208
113. Yao YN, Wang L, Wu XF, Wang ED (2003) The processing of human mitochondrial leucyl-tRNA synthetase in the insect cells. FEBS Lett 534:139-142
114. Yarham JW, Al-Dosary M, Blakely EL, Alston CL, Taylor RW, Elson JL, McFarland R (2011) A comparative analysis approach to determining the pathogenicity of mitochondrial tRNA mutations. Hum Mutat 32:1319-1325
115. Yarham JW, Elson JL, Blakely EL, McFarland R, Taylor RW (2010) Mitochondrial tRNA mutations and disease. Wiley Interdiscip Rev RNA 1:304-324
116. Ylikallio E, Suomalainen A (2012) Mechanisms of mitochondrial diseases. Ann Med 44:41-59