Analysis of genetic code ambiguity arising from nematode-specific misacylated tRNAs

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Hamashima, Kiyofumi ^a   Mori, Masaru ^a   Andachi, Yoshiki ^b,c   Tomita, Masaru ^a   Kohara, Yuji ^a   Kanai, Akio ^a  

^a KEIO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; TRANSFER RNA; ANTICODON; CODON;

AMINOACYLATION; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE EXPRESSION; GENE LOCATION; GENETIC CODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEOMICS; RNA PROCESSING; ANIMAL; ANTICODON; CODON; GENETICS; METABOLISM; NEMATODE;

CAENORHABDITIS ELEGANS;

ANIMALS; ANTICODON; CAENORHABDITIS ELEGANS; CODON; GENETIC CODE; NEMATODA; RNA, TRANSFER;

EID: 84928905710     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116981     Document Type: Article

References (45)

1. McClain WH (1993) Rules that govern tRNA identity in protein synthesis. J Mol Biol 234:257-280. doi: 10.1006/jmbi.1993.1582 PMID: 8230212
2. Drummond DA, Wilke CO (2009) The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet 10:715-724. doi: 10.1038/nrg2662 PMID: 19763154
3. Reynolds NM, Lazazzera BA, Ibba M (2010) Cellular mechanisms that control mistranslation. Nat Rev Microbiol 8:849-856. doi: 10.1038/nrmicro2472 PMID: 21079633
4. Harris RP, Kilby PM (2014) Amino acid misincorporation in recombinant biopharmaceutical products. CurrOpin Biotechnol 30 C: 45-50. doi: 10.1016/j.copbio.2014.05.003 PMID: 24922333
5. De Pouplana LR, Santos MAS, Zhu J-H, Farabaugh PJ, Javid B (2014) Protein mistranslation: friend or foe? Trends Biochem Sci 39:355-362. doi: 10.1016/j.tibs.2014.06.002
6. Moura GR, Carreto LC, Santos MAS (2009) Genetic code ambiguity: an unexpected source of proteome innovation and phenotypicdiversity. CurrOpin Microbiol 12:631-637. doi: 10.1016/j.mib.2009. 09.004 PMID: 19853500
7. Moura GR, Paredes JA, Santos MAS (2010) Development of the genetic code: insights from a fungal codon reassignment. FEBS Lett 584:334-341. doi: 10.1016/j.febslet.2009.11.066 PMID: 19941859
8. Hamashima K, Kanai A (2013) Alternative genetic code for amino acids and transfer RNA revisited. Biomol Concepts 4:309-318. doi: 10.1515/bmc-2013-0002 PMID: 25436582
9. Söll D (1988) Genetic code: enter a new amino acid. Nature 331:662-663. doi: 10.1038/331662a0 PMID: 2963962
10. Hao B, Gong W, Ferguson TK, James CM, Krzycki JA, et al. (2002) A new UAG-encoded residue in the structure of a methanogen methyltransferase. Science 296:1462-1466. doi: 10.1126/science. 1069556 PMID: 12029132
11. Srinivasan G, James CM, Krzycki JA (2002) Pyrrolysine encoded by UAG in Archaea: charging of a UAG-decoding specialized tRNA. Science 296:1459-1462. doi: 10.1126/science.1069588 PMID: 12029131
12. Sugita T, Nakase T (1999) Non-universal usage of the leucine CUG codon and the molecular phylogeny of the genus Candida. SystAppl Microbiol 22:79-86. doi: 10.1016/S0723-2020 (99) 80030-7 PMID: 10188281
13. Iben JR, Maraia RJ (2012) tRNAomics: tRNA gene copy number variation and codon use provide bioinformatic evidence of anew anticodon: codon wobble pair in aeukaryote. RNA 18:1358-1372. doi: 10. 1261/rna.032151.111 PMID: 22586155
14. 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. doi: 10.1017/S1355838202022021 PMID: 12403461
15. Sprinzl M, Horn C, Brown M, Ioudovitch A, Steinberg S (1998) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 26:148-153. doi: 10.1093/nar/26.1.148 PMID: 9399820
16. Hamashima K, Fujishima K, Masuda T, Sugahara J, Tomita M, et al. (2012) Nematode-specific tRNAs that decode an alternative genetic code for leucine. Nucleic Acids Res 40:3653-3662. doi: 10.1093/nar/gkr1226 PMID: 22187151
17. Breitschopf K, Achsel T, Busch K, Gross HJ (1995) Identity elements of human tRNA (Leu): structural requirements for converting human tRNA (Ser) into a leucine acceptor in vitro. Nucleic Acids Res 23:3633-3637. doi: 10.1093/nar/23.18.3633 PMID: 7478989
18. Soma A, Uchiyama K, Sakamoto T, Maeda M, Himeno H (1999) Unique recognition style of tRNA (Leu) by Haloferaxvolcanii leucyl-tRNAsynthetase. J Mol Biol 293:1029-1038. doi: 10.1006/jmbi.1999. 3219 PMID: 10547283
19. Fukunaga R, Yokoyama S (2005) Aminoacylation complex structures of leucyl-tRNA synthetase and tRNALeu reveal two modes of discriminator-base recognition. Nat Struct Mol Biol 12:915-922. doi: 10. 1038/nsmb985 PMID: 16155584
20. El Yacoubi B, Bailly M, De Crécy-Lagard V (2012) Biosynthesis and Function of Posttranscriptional Modifications of Transfer RNAs. Annu Rev Genet 46:69-95. doi: 10.1146/annurev-genet-110711-155641 PMID: 22905870
21. Lee YS, Shibata Y, Malhotra A, Dutta A (2009) A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 23:2639-2649. doi: 10.1101/gad.1837609 PMID: 19933153
22. Zisoulis DG, Kai ZS, Chang RK, Pasquinelli AE (2012) Autoregulation of microRNA biogenesis by let-7 and Argonaute. Nature 486:541-544. doi: 10.1038/nature11134 PMID: 22722835
23. Yu XC, Borisov OV, Alvarez M, Michels DA, Wang YJ, et al. (2009) Identification of codon-specific serine to asparagine mistranslation in recombinant monoclonal antibodies by high-resolution mass spectrometry. Anal Chem 81:9282-9290. doi: 10.1021/ac901541h PMID: 19852494
24. Zhang Z, Shah B, Bondarenko PV (2013) G/U and certain wobble position mismatches as possible main causes of amino acid misincorporations. Biochemistry 52:8165-8176. doi: 10.1021/bi401002c PMID: 24128183
25. Creasy DM, Cottrell JS (2002) Error tolerant searching of uninterpreted tandem mass spectrometry data. Proteomics 2:1426-1434. doi: 10.1002/1615-9861 (200210) 2:10%3C1426::AID-PROT1426% 3E3.0. CO;2-5 PMID: 12422359
26. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, et al. (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462:522-526. doi: 10.1038/nature08576 PMID: 19940929
27. Jones TE, Alexander RW, Pan T (2011) Misacylation of specific nonmethionyl tRNAs by abacterial methionyl-tRNA synthetase. Proc Natl Acad Sci U S A 108:6933-6938. doi: 10.1073/pnas. 1019033108 PMID: 21482813
28. Wiltrout E, Goodenbour JM, Fréchin M, Pan T (2012) Misacylation of tRNA with methionine in Saccharomyces cerevisiae. Nucleic Acids Res 40:10494-10506. doi: 10.1093/nar/gks805 PMID: 22941646
29. Pan T (2013) Adaptive translation as a mechanism of stress response and adaptation. Annu Rev Genet 47:121-137. doi: 10.1146/annurev-genet-111212-133522 PMID: 23988117
30. La Riviere FJ, Wolfson AD, Uhlenbeck OC (2001) Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 294:165-168. doi: 10.1126/science.1064242 PMID: 11588263
31. Fahlman RP, Dale T, Uhlenbeck OC (2004) Uniform binding of aminoacylated transfer RNAs to the ribosomal A and P sites. Mol Cell 16:799-805. doi: 10.1016/j.molcel.2004.10.030 PMID: 15574334
32. Ishimura R, Nagy G, Dotu I, Zhou H, Yang X-L, et al. (2014) Ribosome stalling induced by mutation of a CNS-specifictRNAcauses neurodegeneration. Science 345:455-459. doi: 10.1126/science.1249749 PMID: 25061210
33. Abe T, Ikemura T, Sugahara J, Kanai A, Ohara Y, et al. (2011) tRNADB-CE 2011: tRNA gene database curated manually by experts. Nucleic Acids Res 39:D210-213. doi: 10.1093/nar/gkq1007 PMID: 21071414
34. Levine RL, Mosoni L, Berlett BS, Stadtman ER (1996) Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci U S A 93:15036-15040. doi: 10.1073/pnas.93.26.15036 PMID: 8986759
35. Santos MA, Cheesman C, Costa V, Moradas-Ferreira P, Tuite MF (1999) Selective advantages created by codon ambiguity allowed for the evolution of an alternative genetic code in Candida spp. Mol Microbiol 31:937-947. doi: 10.1046/j.1365-2958.1999.01233.x PMID: 10048036
36. Dunn JG, Foo CK, Belletier NG, Gavis ER, Weissman JS (2013) Ribosome profiling reveals pervasive and regulated stop codon readthroughin Drosophila melanogaster. Elife 2:e01179. doi: 10.7554/eLife.01179 PMID: 24302569
37. Javid B, Sorrentino F, Toosky M, Zheng W, Pinkham JT, et al. (2014) Mycobacterial mistranslation is necessary and sufficient for rifampicin phenotypic resistance. Proc Natl Acad Sci U S A 111:1132-1137. doi: 10.1073/pnas.1317580111 PMID: 24395793
38. Bezerra AR, Simões J, Lee W, Rung J, Weil T, et al. (2013) Reversion of a fungal genetic code alteration links proteome instability with genomic and phenotypic diversification. Proc Natl Acad Sci U S A 110:11079-11084. doi: 10.1073/pnas.1302094110 PMID: 23776239
39. Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, et al. (2006) Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443:50-55. doi: 10.1038/nature05096 PMID: 16906134
40. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94. PMID: 4366476
41. Mitani S (1995) Genetic regulation of mec-3 gene expression implicated in the specification of the mechanosensory neuron cell types in Caenorhabditis elegans. Dev Growth Differ 37:551-557. doi: 10.1046/j.1440-169X.1995.t01-4-00010.x
42. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. doi: 10.1038/nmeth.2089 PMID: 22930834
43. Rappsilber J, Ishihama Y, Mann M (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 75:663-670. doi: 10.1021/ac026117i PMID: 12585499
44. Ishihama Y, Rappsilber J, Andersen JS, Mann M (2002) Microcolumns with self-assembled particle frits for proteomics. J Chromatogr A 979:233-239. doi: 10.1016/S0021-9673 (02) 01402-4 PMID: 12498253
45. Olsen J V, Ong S-E, Mann M (2004) Trypsin cleaves exclusively C-terminal to arginine and lysine residues. MolCell Proteomics 3:608-614. doi: 10.1074/mcp. T400003-MCP200 PMID: 15034119