Decoding mechanism of non-universal genetic codes in Loligo bleekeri mitochondria

Journal of Biological Chemistry

Volumn 288, Issue 11, 2013, Pages 7645-7652

  Ohira, Takayuki ^a   Suzuki, Takeo ^a   Miyauchi, Kenjyo ^a   Suzuki, Tsutomu ^a   Yokobori, Shin Ichi ^b   Yamagishi, Akihiko ^b   Watanabe, Kimitsuna ^b,c,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d RIKEN SPring 8 Center   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICODONS; CYTIDINE; DECODING SYSTEM; GENETIC CODE; MOLECULAR BASIS; POST-TRANSCRIPTIONAL MODIFICATION; PRIMARY STRUCTURES;

DECODING; MASS SPECTROMETRY; MOLLUSCS; SHELLFISH;

MITOCHONDRIA;

MITOCHONDRIAL RNA; TRANSFER RNA;

ANTICODON; ARTICLE; CONTROLLED STUDY; GENETIC CODE; LOLIGO BLEEKERI; MASS SPECTROMETRY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA ISOLATION; RNA TRANSCRIPTION; SQUID;

AMINO ACIDS; ANIMALS; ANTICODON; CODON; CYTIDINE; GENETIC CODE; LOLIGO; MASS SPECTROMETRY; MITOCHONDRIA; MODELS, GENETIC; NUCLEIC ACID CONFORMATION; NUCLEOSIDES; PROTEIN STRUCTURE, SECONDARY; RNA; RNA, TRANSFER;

EID: 84875144455     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.439554     Document Type: Article

References (39)

1. 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, 11-39
2. Watanabe, K., and Yokobori, S. (2011) tRNA modification and genetic code variations in animal mitochondria. J. Nucleic Acids 2011, 623095
3. Moriya, J., Yokogawa, T., Wakita, K., Ueda, T., Nishikawa, K., Crain, P. F., Hashizume, T., Pomerantz, S. C., McCloskey, J. A., and Kawai, G. (1994) A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 33, 2234-2239
4. Suzuki, T., Nagao, A., and Suzuki, T. (2011) Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases. Annu. Rev. Genet. 45, 299-329
5. Watanabe, Y., Tsurui, H., Ueda, T., Furushima, R., Takamiya, S., Kita, K., Nishikawa, K., and Watanabe, K. (1994) Primary and higher order structures of nematode (Ascaris suum) mitochondrial tRNAs lacking either the T or D stem. J. Biol. Chem. 269, 22902-22906
6. Tomita, K., Ueda, T., Ishiwa, S., Crain, P. F., McCloskey, J. A., and Watanabe, K. (1999) Codon reading patterns in Drosophila melanogaster mitochondria based on their tRNA sequences: a unique wobble rule in animal mitochondria. Nucleic Acids Res. 27, 4291-4297
7. Suzuki, T., Suzuki, T., Wada, T., Saigo, K., and 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
8. Suzuki, T., Nagao, A., and Suzuki, T. (2011) Human mitochondrial diseases caused by lack of taurine modification in mitochondrial tRNAs. Wiley Interdiscip. Rev. RNA 2, 376-386
9. Suzuki, T. (2005) in Fine-Tuning of RNA Functions by Modification and Editing (Grosjean, H., ed) pp. 23-69, Springer Verlag, Berlin
10. Suzuki, T., Miyauchi, K., Suzuki, T., Yokobori, S., Shigi, N., Kondow, A., Takeuchi, N., Yamagishi, A., and Watanabe, K. (2011) Taurine-containing uridine modifications in tRNA anticodons are required to decipher nonuniversal genetic codes in ascidian mitochondria. J. Biol. Chem. 286, 35494-35498
11. Shimayama, T., Himeno, H., Sasuga, J., Yokobori, S., Ueda, T., and Watanabe, K. (1990) The genetic code of a squid mitochondrial gene. Nucleic Acids Symp. Ser. 22, 73-74
12. Tomita, K., Ueda, T., and Watanabe, K. (1998) 7-Methylguanosine at the anticodon wobble position of squid mitochondrial tRNA(Ser)GCU: molecular basis for assignment ofAGA/AGGcodons as serine in invertebrate mitochondria. Biochim. Biophys. Acta 1399, 78-82
13. Matsuyama, S., Ueda, T., Crain, P. F., McCloskey, J. A., and 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
14. Tomita, K., Ueda, T., and Watanabe, K. (1997) 5-formyl-cytidine (f5C) found in the wobble position of the anticodon of squid mitochondrial tRNAMet(CAU). Nucleic Acids Symp. Ser. 37, 197-198
15. Miyauchi, K., Ohara, T., and Suzuki, T. (2007) Automated parallel isolation of multiple species of non-coding RNAs by the reciprocal circulating chromatography method. Nucleic Acids Res. 35, e24
16. Suzuki, T., Ikeuchi, Y., Noma, A., Suzuki, T., and Sakaguchi, Y. (2007) Mass spectrometric identification and characterization of RNA-modifying enzymes. Methods Enzymol. 425, 211-229
17. Kiryu, H., Terai, G., Imamura, O., Yoneyama, H., Suzuki, K., and Asai, K. (2011) A detailed investigation of accessibilities around target sites of siRNAs and miRNAs. Bioinformatics 27, 1788-1797
18. Sasuga, J., Yokobori, S., Kaifu, M., Ueda, T., Nishikawa, K., and Watanabe, K. (1999) Gene contents and organization of a mitochondrial DNA segment of the squid Loligo bleekeri. J. Mol. Evol. 48, 692-702
19. Tomita, K., Yokobori, S., Oshima, T., Ueda, T., and Watanabe, K. (2002) The cephalopod Loligo bleekeri mitochondrial genome: multiplied noncoding regions and transposition of tRNA genes. J. Mol. Evol. 54, 486-500
20. Ikeuchi, Y., Shigi, N., Kato, J., Nishimura, A., and Suzuki, T. (2006) Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol. Cell 21, 97-108
21. Mcluckey, S. A., Vanberkel, G. J., and Glish, G. L. (1992) Tandem mass spectrometry of small, multiply charged oligonucleotides. J. Am. Soc. Mass Spectr. 3, 60-70
22. Grosjean, H., de Crécy-Lagard, V., and Marck, C. (2010) Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett. 584, 252-264
23. Miyauchi, K., Kimura, S., and Suzuki, T. (2012) A cyclic form of N6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification. Nat. Chem. Biol. 9, 105-111
24. Yarian, C., Townsend, H., Czestkowski, W., Sochacka, E., Malkiewicz, A. J., Guenther, R., Miskiewicz, A., and Agris, P. F. (2002) Accurate translation of the genetic code depends on tRNA modified nucleosides. J. Biol. Chem. 277, 16391-16395
25. Hirsh, D. (1970) Tryptophan RNA of Escherichia coli. Nature 228, 57
26. Schmeing, T. M., Voorhees, R. M., Kelley, A. C., and Ramakrishnan, V. (2011) How mutations in tRNA distant from the anticodon affect the fidelity of decoding. Nat. Struct. Mol. Biol. 18, 432-436
27. Canaday, J., Dirheimer, G., and Martin, R. P. (1980) Yeast mitochondrial methionine initiator tRNA: characterization and nucleotide sequence. Nucleic Acids Res. 8, 1445-1457
28. Sibler, A. P., Dirheimer, G., and Martin, R. P. (1985) Yeast mitochondrial tRNAIle and tRNAMetm: nucleotide sequence and codon recognition patterns. Nucleic Acids Res. 13, 1341-1345
29. Dubin, D. T., and HsuChen, C. C. (1984) Sequence and structure of a methionine transfer RNA from mosquito mitochondria. Nucleic Acids Res. 12, 4185-4189
30. Takemoto, C., Spremulli, L. L., Benkowski, L. A., Ueda, T., Yokogawa, T., and Watanabe, K. (2009) Unconventional decoding of the AUA codon as methionine by mitochondrial tRNAMet with the anticodon f5CAU as revealed with a mitochondrial in vitro translation system. Nucleic Acids Res. 37, 1616-1627
31. Lusic, H., Gustilo, E. M., Vendeix, F. A., Kaiser, R., Delaney, M. O., Graham, W. D., Moye, V. A., Cantara, W. A., Agris, P. F., and Deiters, A. (2008) Synthesis and investigation of the 5-formylcytidine modified, anticodon stem and loop of the human mitochondrial tRNAMet. Nucleic Acids Res. 36, 6548-6557
32. Martin, R. P., Sibler, A. P., Gehrke, C. W., Kuo, K., Edmonds, C. G., Mc-Closkey, J. A., and Dirheimer, G. (1990) 5-[[(carboxymethyl)amino]-methyl] uridine is found in the anticodon of yeast mitochondrial tRNAs recognizing two-codon families ending in a purine. Biochemistry 29, 956-959
33. Umeda, N., Suzuki, T., Yukawa, M., Ohya, Y., Shindo, H., Watanabe, K., and 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. 280, 1613-1624
34. Sakurai, M., Ohtsuki, T., Suzuki, T., and Watanabe, K. (2005) Unusual usage of wobble modifications in mitochondrial tRNAs of the nematode Ascaris suum. FEBS Lett. 579, 2767-2772
35. Numata, T., Ikeuchi, Y., Fukai, S., Suzuki, T., and Nureki, O. (2006) Snapshots of tRNA sulphuration via an adenylated intermediate. Nature 442, 419-424
36. Jühling, F., Mörl, M., Hartmann, R. K., Sprinzl, M., Stadler, P. F., and Pütz, J. (2009) tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res. 37, D159-162
37. 2+-dependent tRNA folding. Nucleic Acids Res. 30, 4751-4760
38. Alexandrov, A., Chernyakov, I., Gu, W., Hiley, S. L., Hughes, T. R., Grayhack, E. J., and Phizicky, E. M. (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol. Cell 21, 87-96
39. Motorin, Y., and Helm, M. (2010) tRNA stabilization by modified nucleotides. Biochemistry 49, 4934-4944