Combination of the Loss of cmnm5U34 with the Lack of s2U34 Modifications of tRNALys, tRNAGlu, and tRNAGln Altered Mitochondrial Biogenesis and Respiration

Journal of Molecular Biology

Volumn 395, Issue 5, 2010, Pages 1038-1048

  Wang, Xinjian ^a   Yan, Qingfeng ^a,b   Guan, Min Xin ^a,c  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

biogenesis; metabolism; mitochondrial tRNA; nucleotide modification; respiration

Indexed keywords

CARBOXYMETHYLAMINOMETHYL URIDINE; GLUTAMIC ACID TRANSFER RNA; GLUTAMINE TRANSFER RNA; LYSINE TRANSFER RNA; MITOCHONDRIAL RNA; NUCLEOSIDE; UNCLASSIFIED DRUG; URIDINE; FUNGAL RNA; GUANINE NUCLEOTIDE BINDING PROTEIN; MITOCHONDRIAL PROTEIN; MSS1 PROTEIN, S CEREVISIAE; MTO1 PROTEIN, S CEREVISIAE; RNA; RNA BINDING PROTEIN; RNA, MITOCHONDRIAL; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; FUNGAL GENE; GENE DELETION; GENE INTERACTION; GENE MUTATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; RNA DEGRADATION; RNA METABOLISM; SACCHAROMYCES CEREVISIAE; ALLELE; AMINOACYLATION; CHEMISTRY; GENETICS; METABOLISM; MITOCHONDRIAL GENOME; MUTATION; OXYGEN CONSUMPTION; PHENOTYPE;

SACCHAROMYCES CEREVISIAE;

ALLELES; BASE SEQUENCE; GENES, FUNGAL; GENOME, MITOCHONDRIAL; GTP-BINDING PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; OXYGEN CONSUMPTION; PHENOTYPE; RNA; RNA, FUNGAL; RNA, TRANSFER, GLN; RNA, TRANSFER, GLU; RNA, TRANSFER, LYS; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSFER RNA AMINOACYLATION;

EID: 73649147996     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.12.002     Document Type: Article

References (53)

1. Hopper A.K., and Phizicky E.M. tRNA transfers to the limelight. Genes Dev. 17 (2003) 162-180
2. Agris P.F., Vendeix F.A., and Graham W.D. tRNA's wobble decoding of the genome: 40 years of modification. J. Mol. Biol. 366 (2007) 1-13
3. Czerwoniec A., Dunin-Horkawicz S., Purta E., Kaminska K.H., Kasprzak J.M., Bujnicki J.M., et al. MODOMICS: a database of RNA modification pathways. 2008 update. Nucleic Acids Res. 37 (2008) D118-D121
4. Björk G.R. Stable RNA modification. In: Neidhardt F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low B.K., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., and Umbarger H.E. (Eds). Escherichia coli and Salmonella: Cellular and Molecular Biology (1996), American Society for Microbiology, Washington, DC 861-886
5. Yan Q., and Guan M.X. Identification and characterization of mouse TRMU gene encoding the mitochondrial 5-methylaminomethyl-2-thiouridylate-methyltransferase. Biochim. Biophys. Acta 1676 (2004) 119-126
6. Ishitani R., Yokoyama S., and Nureki O. Structure, dynamics, and function of RNA modification enzymes. Curr. Opin. Struct. Biol. 18 (2008) 330-339
7. Brégeon D., Colot V., Miroslav M., Radman M., and Taddei F. Translational misreading: a tRNA modification counteracts a + 2 ribosomal frameshift. Genes Dev. 15 (2001) 2295-2306
8. Moukadiri I., Prado S., Piera J., Velazquez-Campoy A., Bjork G.R., and Armengod M.-E. Evolutionarily conserved proteins MnmE and GidA catalyze the formation of two methyluridine derivatives at tRNA wobble positions. Nucleic Acids Res. 37 (2009) 7177-7193
9. Li X., and Guan M.X. A human mitochondrial GTP binding protein related to tRNA modification may modulate the phenotypic expression of the deafness-associated mitochondrial 12S rRNA mutation. Mol. Cell. Biol. 22 (2002) 7701-7711
10. Li R., Li X., Yan Q., Mo J.Q., and Guan M.X. Isolation and characterization of mouse MTO1 related to mitochondrial tRNA modification. Biochim. Biophys. Acta 1629 (2003) 53-59
11. Kambampati R., and Lauhon C.T. MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli. Biochemistry 42 (2003) 1109-1117
12. Yan Q., Li X., Faye G., and Guan M.X. Mutations in MTO2 related to tRNA modification impair mitochondrial gene expression and protein synthesis in the presence of a paromomycin resistance mutation in mitochondrial 15S rRNA. J. Biol. Chem. 280 (2005) 29151-29157
13. Elseviers D., Petrullo L.A., and Gallagher P. Novel E. coli mutants deficient in biosynthesis of 5-methylaminomethyl-2-thiouridine. Nucleic Acids Res. 12 (1984) 3521-3534
14. Meyer S., Scrima A., Versées W., and Wittinghofer A. Crystal structures of the conserved tRNA-modifying enzyme GidA: implications for its interaction with MnmE and substrate. J. Mol. Biol. 380 (2008) 532-547
15. Scrima A., Vetter I.R., Armengod M.F., and Wittinghofer A. The structure of the TrmE GTP-binding protein and its implications for tRNA modification. EMBO J. 24 (2005) 23-33
16. Ikeuchi Y., Shigi N., Kato J., Nishimura A., and Suzuki T. Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol. Cell 21 (2006) 97-108
17. Numata T., Ikeuchi Y., Fukai S., Suzuki T., and Nureki O. Snapshots of tRNA sulphuration via an adenylated intermediate. Nature 442 (2006) 419-424
18. Colby G., Wu M., and Tzagoloff A. MTO1 codes for a mitochondrial protein required for respiration in paromomycin-resistant mutants of Saccharomyces cerevisiae. J. Biol. Chem. 273 (1998) 27945-27952
19. Decoster E., Vassal A., and Faye G. MSS1, a nuclear-encoded mitochondrial GTPase involved in the expression of COX1 subunit of cytochrome c oxidase. J. Mol. Biol. 232 (1993) 79-88
20. Umeda N., Suzuki T., Yukawa M., Ohya Y., Shindo H., Watanabe K., and Suzuki T. 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. 280 (2004) 1613-1624
21. Wang X., Yan Q., and Guan M.X. Deletion of the MTO2 gene related to tRNA modification causes a failure in mitochondrial RNA metabolism in the yeast Saccharomyces cerevisiae. FEBS Lett. 581 (2007) 4228-4234
22. Wang X., Yan Q., and Guan M.X. Mutation in MTO1 involved in tRNA modification impairs mitochondrial RNA metabolism in the yeast Saccharomyces cerevisiae. Mitochondrion 9 (2009) 180-185
23. Qian Y., and Guan M.X. Interaction of aminoglycosides with human mitochondrial 12S ribosomal RNA carrying the deafness-associated mutation. Antimicrob. Agents Chemother. 53 (2009) 4612-4618
24. Guan M.X., Yan Q., Li X., Bykhovskaya Y., Gallo-Teran J., Hajek P., et al. Mutation in TRMU related to transfer RNA modification modulates the phenotypic expression of the deafness-associated mitochondrial 12S ribosomal RNA mutations. Am. J. Hum. Genet. 79 (2006) 291-302
25. Clark-Walker G.D., and Miklos G.L.G. Complementation in cytoplasmic petite mutants of yeast to form respiratory competent cells. Proc. Natl Acad. Sci. USA 72 (1975) 372-375
26. Moriya J., Yokogawa T., Wakita K., Ueda T., Nishikawa K., Crain P.F., et al. A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 33 (1994) 2234-2239
27. Shigi N., Suzuki T., Tamakoshi M., Oshima T., and Watanabe K. Conserved bases in the TΨC Loop of tRNA are determinants for thermophile-specific 2-thiouridylation at position 54. J. Biol. Chem. 277 (2002) 39128-39135
28. Suzuki T., Suzuki T., Wada T., Saigo K., and Watanabe K. Taurine as a constituent of mitochondrial tRNA: new insights into the functions of taurine and human mitochondrial diseases. EMBO J. 21 (2002) 6581-6589
29. Glu in vivo. J. Mol. Biol. 284 (1998) 609-620
30. Glu is a positive determinant for aminoacylation by Escherichia coli glutamyl-tRNA synthetase. Biochemistry 32 (1993) 3836-3841
31. Foury F., Roganti T., Lecrenier N., and Purnelle B. The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 440 (1998) 325-331
32. Villarroya M., Prado S., Esteve J.M., Soriano M.A., Aguado C., Pérez-Martínez D., et al. Characterization of human GTPBP3, a GTP-binding protein involved in mitochondrial tRNA modification. Mol. Cell. Biol. 28 (2008) 7514-7531
33. (Lys) stabilize a canonical U-turn structure. Biochemistry 39 (2000) 12575-12584
34. Lys with hypomodified derivatives of 5-methylaminomethyl-2-thiouridine in the wobble position. J. Mol. Biol. 284 (1998) 33-42
35. Alexandrov A., Chernyakov I., Gu W., Hiley S.L., Hughes T.R., Grayhack E.J., and Phizicky E.M. Rapid tRNA decay can result from lack of nonessential modifications. Mol. Cell 21 (2006) 87-96
36. Chernyakov I., Whipple J.M., Kotelawala L., Grayhack E.J., and Phizicky E.M. Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5′-3′ exonucleases Rat1 and Xrn1. Genes Dev. 22 (2008) 1369-1380
37. Ashraf S.S., Sochacka E., Cain R., Guenther R., Malkiewicz A., and Agris P.F. Single atom modification (O → S) of tRNA confers ribosome binding. RNA 5 (1999) 188-194
38. Hagervall T.G., and Björk G.R. Undermodification in the first position of the anticodon of supG-tRNA reduces translational efficiency. Mol. Gen. Genet. 196 (1984) 194-200
39. Urbonavicius U., Qian Q., Durand J.M., Hagervall T.G., and Björk G.R. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J. 20 (2001) 4863-4873
40. UUU species. Biochemistry 39 (2000) 13390-13395
41. Yasukawa T., Suzuki T., Ishii N., Ohta S., and Watanabe K. Wobble modification defect in tRNA disturbs codon-anticodon interaction in a mitochondrial disease. EMBO J. 20 (2001) 4794-4802
42. Costanzo M.C., and Fox T.D. Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu. Rev. Genet. 24 (1990) 91-108
43. Islas-Osuna M.A., Ellis T.P., Marnell L.L., Mittelmeier T.M., and Dieckmann C.L. Cbp1 is required for translation of the mitochondrial cytochrome b mRNA of Saccharomyces cerevisiae. J. Biol. Chem. 277 (2002) 37987-37990
44. Myers A.M., Pape L.K., and Tzagoloff A. Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J. 4 (1985) 2087-2092
45. Barrientos A., Korr D., Barwell K.J., Sjulsen C., Gajewski C.D., Manfredi G., et al. MTG1 codes for a conserved protein required for mitochondrial translation. Mol. Biol. Cell 14 (2003) 2292-2302
46. Williams E.H., Butler C.A., Bonnefoy N., and Fox T.D. Translation initiation in Saccharomyces cerevisiae mitochondria: functional interactions among mitochondrial ribosomal protein Rsm28p, initiation factor 2, methionyl-tRNA-formyltransferase and novel protein Rmd9p. Genetics 175 (2007) 1117-1126
47. Hensgens L.A., Bonen L., de Haan M., van der Horst G., and Grivell L.A. Two intron sequences in yeast mitochondrial COX1 gene: homology among URF-containing introns and strain-dependent variation in flanking exons. Cell 32 (1983) 379-389
48. Van Dyck E., and Clayton D.A. Transcription-dependent DNA transactions in the mitochondrial genome of a yeast hypersuppressive petite mutant. Mol. Cell. Biol. 18 (1998) 2976-2985
49. Burnett K.G., and Scheffler I.E. Integrity of mitochondria in a mammalian cell mutant defective in mitochondrial protein synthesis. J. Cell Biol. 90 (1981) 108-115
50. Guan M.X. Cytoplasmic tyrosyl-tRNA synthetase rescues the defect in mitochondrial genome maintenance caused by the nuclear mutation mgm104-1 in the yeast Saccharomyces cerevisiae. Mol. Gen. Genet. 255 (1997) 525-532
51. Sherman F., Fink G.R., and Hicks J.B. Methods in Yeast Genetics (1983), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
52. Enríquez J.A., and Attardi G. Analysis of aminoacylation of human mitochondrial tRNAs. Methods Enzymol. 264 (1996) 183-196
53. Barrientos A., Korr D., and Tzagoloff A. Shy1p is necessary for full expression of mitochondrial COX1 in the yeast model of Leigh's syndrome. EMBO J. 21 (2002) 43-52