Trm9-Catalyzed tRNA Modifications Regulate Global Protein Expression by Codon-Biased Translation

PLoS Genetics

Volumn 11, Issue 12, 2015, Pages

  Deng, Wenjun ^a,f   Babu, I Ramesh ^a   Su, Dan ^a,g   Yin, Shanye ^b   Begley, Thomas J ^c,d   Dedon, Peter C ^a,e  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c SUNY POLYTECHNIC INSTITUTE   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

^e SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g LifeTech   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CODON; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSFER RNA; TRANSFER RNA METHYLTRANSFERASE; TRM9 PROTEIN, S CEREVISIAE; URIDINE;

BIOSYNTHESIS; CODON; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN PROCESSING; PROTEOMICS; RIBOSOME; SACCHAROMYCES CEREVISIAE;

CODON; GENE EXPRESSION REGULATION, FUNGAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; RIBOSOMES; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRNA METHYLTRANSFERASES; URIDINE;

EID: 84953302322     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005706     Document Type: Article

References (50)

1. Maraia RJ, Blewett NH, Bayfield MA, (2008) It's a mod mod tRNA world. Nat Chem Biol 4: 162–164. doi: 10.1038/nchembio0308-162 18277975
2. Novoa EM, Pavon-Eternod M, Pan T, Ribas de Pouplana L, (2012) A role for tRNA modifications in genome structure and codon usage. Cell 149: 202–213. doi: 10.1016/j.cell.2012.01.050 22464330
3. Phizicky EM, Hopper AK, (2010) tRNA biology charges to the front. Genes Dev 24: 1832–1860. doi: 10.1101/gad.1956510 20810645
4. Johansson MJ, Esberg A, Huang B, Bjork GR, Bystrom AS, (2008) Eukaryotic wobble uridine modifications promote a functionally redundant decoding system. Mol Cell Biol 28: 3301–3312. doi: 10.1128/MCB.01542-07 18332122
5. Chechetkin VR, (2006) Genetic code from tRNA point of view. J Theor Biol 242: 922–934. 16808928
6. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, et al. (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21: 87–96. 16387656
7. Yarian C, Townsend H, Czestkowski W, Sochacka E, Malkiewicz AJ, et al. (2002) Accurate translation of the genetic code depends on tRNA modified nucleosides. J Biol Chem 277: 16391–16395. 11861649
8. Leipuviene R, Bjork GR, (2005) A reduced level of charged tRNAArgmnm5UCU triggers the wild-type peptidyl-tRNA to frameshift. RNA 11: 796–807. 15840821
9. Rezgui VA, Tyagi K, Ranjan N, Konevega AL, Mittelstaet J, et al. (2013) tRNA tKUUU, tQUUG, and tEUUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding. Proc Natl Acad Sci U S A 110: 12289–12294. doi: 10.1073/pnas.1300781110 23836657
10. Bauer F, Matsuyama A, Candiracci J, Dieu M, Scheliga J, et al. (2012) Translational control of cell division by Elongator. Cell Rep 1: 424–433. 22768388
11. Kalhor HR, Clarke S, (2003) Novel methyltransferase for modified uridine residues at the wobble position of tRNA. Mol Cell Biol 23: 9283–9292. 14645538
12. Noma A, Sakaguchi Y, Suzuki T, (2009) Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions. Nucleic Acids Res 37: 1335–1352. doi: 10.1093/nar/gkn1023 19151091
13. Mazauric MH, Dirick L, Purushothaman SK, Bjork GR, Lapeyre B, (2010) Trm112p is a 15-kDa zinc finger protein essential for the activity of two tRNA and one protein methyltransferases in yeast. J Biol Chem 285: 18505–18515. doi: 10.1074/jbc.M110.113100 20400505
14. Huang B, Lu J, Bystrom AS, (2008) A genome-wide screen identifies genes required for formation of the wobble nucleoside 5-methoxycarbonylmethyl-2-thiouridine in Saccharomyces cerevisiae. RNA 14: 2183–2194. doi: 10.1261/rna.1184108 18755837
15. Begley U, Sosa MS, Avivar-Valderas A, Patil A, Endres L, et al. (2013) A human tRNA methyltransferase 9-like protein prevents tumour growth by regulating LIN9 and HIF1-alpha. EMBO Mol Med. 5: 366–383. doi: 10.1002/emmm.201201161 23381944
16. Chan CT, Dyavaiah M, DeMott MS, Taghizadeh K, Dedon PC, et al. (2010) A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet 6: e1001247. doi: 10.1371/journal.pgen.1001247 21187895
17. Chan CTY, Pang YLJ, Deng W, Babu IR, Dyavaiah M, et al. (2012) Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 3: 937. doi: 10.1038/ncomms1938 22760636
18. Fu D, Brophy JA, Chan CT, Atmore KA, Begley U, et al. (2010) Human AlkB homolog ABH8 Is a tRNA methyltransferase required for wobble uridine modification and DNA damage survival. Mol Cell Biol 30: 2449–2459. doi: 10.1128/MCB.01604-09 20308323
19. Patil A, Chan CT, Dyavaiah M, Rooney JP, Dedon PC, et al. (2012) Translational infidelity-induced protein stress results from a deficiency in Trm9-catalyzed tRNA modifications. RNA Biol 9: 990–1001. doi: 10.4161/rna.20531 22832247
20. Begley U, Dyavaiah M, Patil A, Rooney JP, DiRenzo D, et al. (2007) Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 28: 860–870. 18082610
21. Begley TJ, Rosenbach AS, Ideker T, Samson LD, (2004) Hot spots for modulating toxicity identified by genomic phenotyping and localization mapping. Mol Cell 16: 117–125. 15469827
22. Begley TJ, Rosenbach AS, Ideker T, Samson LD, (2002) Recovery Pathways in S. cerevisiae Revealed by Genomic Phenotyping and Interactome Mapping. Mol Canc Res 1.
23. Chan CT, Deng W, Li F, DeMott MS, Babu IR, et al. (2015) Highly Predictive Reprogramming of tRNA Modifications Is Linked to Selective Expression of Codon-Biased Genes. Chem Res Toxicol 28: 978–988. doi: 10.1021/acs.chemrestox.5b00004 25772370
24. Zinshteyn B, Gilbert WV, (2013) Loss of a conserved tRNA anticodon modification perturbs cellular signaling. PLoS Genet 9: e1003675. doi: 10.1371/journal.pgen.1003675 23935536
25. Romero IG, Ruvinsky I, Gilad Y, (2012) Comparative studies of gene expression and the evolution of gene regulation. Nat Rev Genet 13: 505–516. doi: 10.1038/nrg3229 22705669
26. Warnecke T, Hurst LD, (2011) Error prevention and mitigation as forces in the evolution of genes and genomes. Nat Rev Genet 12: 875–881. doi: 10.1038/nrg3092 22094950
27. Deng WJ, Nie S, Dai J, Wu JR, Zeng R, (2010) Proteome, phosphoproteome, and hydroxyproteome of liver mitochondria in diabetic rats at early pathogenic stages. Mol Cell Proteomics 9: 100–116. doi: 10.1074/mcp.M900020-MCP200 19700791
28. Parmley JL, Urrutia AO, Potrzebowski L, Kaessmann H, Hurst LD, (2007) Splicing and the evolution of proteins in mammals. PLoS Biol 5: e14. 17298171
29. Schwartz S, Ast G, (2010) Chromatin density and splicing destiny: on the cross-talk between chromatin structure and splicing. EMBO J 29: 1629–1636. doi: 10.1038/emboj.2010.71 20407423
30. Lei H, Zhai B, Yin S, Gygi S, Reed R, (2013) Evidence that a consensus element found in naturally intronless mRNAs promotes mRNA export. Nucleic Acids Res 41: 2517–2525. doi: 10.1093/nar/gks1314 23275560
31. Wang P, Yin S, Zhang Z, Xin D, Hu L, et al. (2008) Evidence for common short natural trans sense-antisense pairing between transcripts from protein coding genes. Genome Biol 9: R169. doi: 10.1186/gb-2008-9-12-r169 19055728
32. Yin S, Deng W, Zheng H, Zhang Z, Hu L, et al. (2009) Evidence that the nonsense-mediated mRNA decay pathway participates in X chromosome dosage compensation in mammals. Biochem Biophys Res Commun 383: 378–382. doi: 10.1016/j.bbrc.2009.04.021 19364502
33. Yin S, Wang P, Deng W, Zheng H, Hu L, et al. (2009) Dosage compensation on the active X chromosome minimizes transcriptional noise of X-linked genes in mammals. Genome Biol 10: R74. doi: 10.1186/gb-2009-10-7-r74 19594925
34. Warnecke T, Hurst LD, (2007) Evidence for a trade-off between translational efficiency and splicing regulation in determining synonymous codon usage in Drosophila melanogaster. Mol Biol Evol 24: 2755–2762. 17905999
35. Nedialkova DD, Leidel SA, (2015) Optimization of Codon Translation Rates via tRNA Modifications Maintains Proteome Integrity. Cell 161: 1606–1618. doi: 10.1016/j.cell.2015.05.022 26052047
36. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57. doi: 10.1038/nprot.2008.211 19131956
37. Ishihama Y, Sato T, Tabata T, Miyamoto N, Sagane K, et al. (2005) Quantitative mouse brain proteomics using culture-derived isotope tags as internal standards. Nat Biotechnol 23: 617–621. 15834404
38. Kristiansson MH, Bhat VB, Babu IR, Wishnok JS, Tannenbaum SR, (2007) Comparative time-dependent analysis of potential inflammation biomarkers in lymphoma-bearing SJL mice. J Proteome Res 6: 1735–1744. 17388619
39. Bjork GR, Huang B, Persson OP, Bystrom AS, (2007) A conserved modified wobble nucleoside (mcm5s2U) in lysyl-tRNA is required for viability in yeast. RNA 13: 1245–1255. 17592039
40. Parmley JL, Huynen MA, (2009) Clustering of codons with rare cognate tRNAs in human genes suggests an extra level of expression regulation. PLoS Genet 5: e1000548. doi: 10.1371/journal.pgen.1000548 19578405
41. Warnecke T, Hurst LD, (2010) GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution. Mol Syst Biol 6: 340. doi: 10.1038/msb.2009.94 20087338
42. Cannarozzi G, Schraudolph NN, Faty M, von Rohr P, Friberg MT, et al. (2010) A role for codon order in translation dynamics. Cell 141: 355–367. doi: 10.1016/j.cell.2010.02.036 20403329
43. Clarke TFt, Clark PL, (2008) Rare codons cluster. PLoS One 3: e3412. doi: 10.1371/journal.pone.0003412 18923675
44. Chen C, Tuck S, Bystrom AS, (2009) Defects in tRNA modification associated with neurological and developmental dysfunctions in Caenorhabditis elegans elongator mutants. PLoS Genet 5: e1000561. doi: 10.1371/journal.pgen.1000561 19593383
45. Jackson R, Standart N, (2015) The awesome power of ribosome profiling. RNA 21: 652–654. doi: 10.1261/rna.049908.115 25780177
46. Charneski CA, Hurst LD, (2013) Positively charged residues are the major determinants of ribosomal velocity. PLoS Biol 11: e1001508. doi: 10.1371/journal.pbio.1001508 23554576
47. Komili S, Farny NG, Roth FP, Silver PA, (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131: 557–571. 17981122
48. de Hoon MJ, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453–1454. 14871861
49. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, et al. (2010) An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141: 344–354. doi: 10.1016/j.cell.2010.03.031 20403328
50. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS, (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218–223. doi: 10.1126/science.1168978 19213877