Different types of secondary information in the genetic code

RNA

Volumn 20, Issue 7, 2014, Pages 977-984

  Maraia, Richard J ^a   Iben, James R ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Anticodon; Codons; Silent mutation; tRNA modification

Indexed keywords

ANTICODON; BIOINFORMATICS; GENETIC CODE; HUMAN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS;

ANTICODON; CODONS; SILENT MUTATION; TRNA MODIFICATION;

ANIMALS; BASE SEQUENCE; CODON; GENETIC CODE; GENOME; HUMANS; PENETRANCE; RNA, MESSENGER; RNA, TRANSFER;

EID: 84902662079     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.044115.113     Document Type: Review

References (105)

1. Agris PF. 2004. Decoding the genome: a modified view. Nucleic Acids Res 32: 223-238. (Pubitemid 38228621)
2. Agris PF. 2008. Bringing order to translation: the contributions of transfer RNA anticodon-domain modifications. EMBO Rep 9: 629-635. (Pubitemid 351927683)
3. Agris PF, Vendeix FA, Graham WD. 2007. tRNA's wobble decoding of the genome: 40 years of modification. J Mol Biol 366: 1-13. (Pubitemid 46123342)
4. Akashi H. 1995. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics 139: 1067-1076.
5. Barski A, Chepelev I, Liko D, Cuddapah S, Fleming AB, Birch J, Cui K, White RJ, Zhao K. 2010. Pol II and its associated epigenetic marks are present at Pol III-transcribed noncoding RNA genes. Nat Struct Mol Biol 17: 629-634.
6. Bauer F, Matsuyama A, Candiracci J, Dieu M, Scheliga J, Wolf DA, Yoshida M, Hermand D. 2012. Translational control of cell division by elongator. Cell Rep 1: 424-433.
7. Begley U, Dyavaiah M, Patil A, Rooney JP, Direnzo D, Young CM, Conklin DS, Zitomer RS, Begley TJ. 2007. Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 28: 860-870. (Pubitemid 350217051)
8. Bennetzen JL, Hall BD. 1982. Codon selection in yeast. J Biol Chem 257: 3026-3031. (Pubitemid 12118818)
9. Berg OG, Kurland CG. 1997. Growth rate-optimised tRNA abundance and codon usage. J Mol Biol 270: 544-550. (Pubitemid 27313794)
10. Bloom-Ackermann Z, Navon S, Gingold H, Towers R, Pilpel Y, Dahan O. 2014. A comprehensive tRNA deletion library unravels the genetic architecture of the tRNA pool. PLoS Genet 10: e1004084.
11. Bollenbach T, Vetsigian K, Kishony R. 2007. Evolution and multilevel optimization of the genetic code. Genome Res 17: 401-404. (Pubitemid 46556443)
12. Brambillasca S, Altkrueger A, Colombo SF, Friederich A, Eickelmann P, Mark M, Borgese N, Solimena M. 2012. CDK5 regulatory subunit-associated protein 1-like 1 (CDKAL1) is a tail-anchored protein in the endoplasmic reticulum (ER) of insulinoma cells. J Biol Chem 287: 41808-41819.
13. Brest P, Lapaquette P, Souidi M, Lebrigand K, Cesaro A, Vouret-Craviari V, Mari B, Barbry P, Mosnier JF, Hebuterne X, et al. 2011. A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease. Nat Genet 43: 242-245.
14. Bulmer M. 1987. Coevolution of codon usage and transfer RNA abundance. Nature 325: 728-730. (Pubitemid 17054044)
15. Bulmer M. 1991. The selection-mutation-drift theory of synonymous codon usage. Genetics 129: 897-907.
16. Canella D, Praz V, Reina JH, Cousin P, Hernandez N. 2010. Defining the RNA polymerase III transcriptome: genome-wide localization of the RNA polymerase III transcription machinery in human cells. Genome Res 20: 710-721.
17. Canella D, Bernasconi D, Gilardi F, Lemartelot G, Migliavacca E, Praz V, Cousin P, Delorenzi M, Hernandez N. 2012. A multiplicity of factors contributes to selective RNA polymerase III occupancy of a subset of RNA polymerase III genes in mouse liver. Genome Res 22: 666-680.
18. Cannarozzi G, Schraudolph NN, Faty M, von Rohr P, Friberg MT, Roth AC, Gonnet P, Gonnet G, Barral Y. 2010. A role for codon order in translation dynamics. Cell 141: 355-367.
19. Chamary JV, Hurst LD. 2005. Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol 6: R75.
20. Chamary JV, Parmley JL, Hurst LD. 2006. Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat Rev Genet 7: 98-108. (Pubitemid 43128905)
21. Chan PP, Lowe TM. 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37: D93-D97.
22. Chan CT, Dyavaiah M, DeMott MS, Taghizadeh K, Dedon PC, Begley TJ. 2010. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet 6: e1001247.
23. Chan CT, Pang YL, Deng W, Babu IR, Dyavaiah M, Begley TJ, Dedon PC. 2012. Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 3: 937.
24. Claverie JM. 2001. Gene number. What if there are only 30,000 human genes? Science 291: 1255-1257.
25. Comeron JM. 2004. Selective and mutational patterns associated with gene expression in humans: influences on synonymous composition and intron presence. Genetics 167: 1293-1304. (Pubitemid 39045637)
26. Cortazzo P, Cerveñansky C, Marín M, Reiss C, Ehrlich R, Deana A. 2002. Silent mutations affect in vivo protein folding in Escherichia coli. Biochem Biophys Res Commun 293: 537-541. (Pubitemid 34694241)
27. Dedon PC, Begley TJ. 2014. A system of RNA modifications and biased codon use controls cellular stress response at the level of translation. Chem Res Toxicol 27: 330-337.
28. Dhanvantari S, Shen FS, Adams T, Snell CR, Zhang C, Mackin RB, Morris SJ, Loh YP. 2003. Disruption of a receptor-mediated mechanism for intracellular sorting of proinsulin in familial hyperproinsulinemia. Mol Endocrinol 17: 1856-1867. (Pubitemid 37072300)
29. Diabetes Genetics Initiative of Broad Institute of Harvard and MIT, Lund University, and Novartis Institutes of BioMedical Research. 2007. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316: 1331-1336.
30. Dittmar KA, Goodenbour JM, Pan T. 2006. Tissue-specific differences in human transfer RNA expression. PLoS Genet 2: e221.
31. Dong H, Nilsson L, Kurland CG. 1996. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J Mol Biol 260: 649-663. (Pubitemid 26270960)
32. dos Reis M, Savva R, Wernisch L. 2004. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res 32: 5036-5044. (Pubitemid 39445490)
33. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. 2005. Why highly expressed proteins evolve slowly. Proc Natl Acad Sci 102: 14338-14343. (Pubitemid 41429699)
34. Duret L. 2000. tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet 16: 287-289. (Pubitemid 30389593)
35. Duret L. 2002. Evolution of synonymous codon usage in metazoans. Curr Opin Genet Dev 12: 640-649. (Pubitemid 35335981)
36. Elhaik E, Landan G, Graur D. 2009. Can GC content at third-codon positions be used as a proxy for isochore composition? Mol Biol Evol 26: 1829-1833.
37. Fernández-Vázquez J, Vargas-Pérez I, Sansó M, Buhne K, Carmona M, Paulo E, Hermand D, Rodríguez-Gabriel M, Ayté J, Leidel S, et al. 2013. Modification of tRNALys UUU by elongator is essential for efficient translation of stress mRNAs. PLoS Genet 9: e1003647.
38. Forsburg SL. 1994. Codon usage table for Schizosaccharomyces pombe. Yeast 10: 1045-1047. (Pubitemid 24261809)
39. Fredrick K, Ibba M. 2010. How the sequence of a gene can tune its translation. Cell 141: 227-229.
40. Fu D, Brophy JA, Chan CT, Atmore KA, Begley U, Paules RS, Dedon PC, Begley TJ, Samson LD. 2010. Human AlkB homolog ABH8 is a tRNA methyltransferase required for wobble uridine modification and DNA damage survival. Mol Cell Biol 30: 2449-2459.
41. Fung KL, Pan J, Ohnuma S, Lund PE, Pixley JN, Kimchi-Sarfaty C, Ambudkar SV, Gottesman MM. 2014. MDR1 synonymous polymorphisms alter transporter specificity and protein stability in a stable epithelial monolayer. Cancer Res 74: 598-608.
42. Goodman DB, Church GM, Kosuri S. 2013. Causes and effects of N-terminal codon bias in bacterial genes. Science 342: 475-479.
43. Gouy M, Gautier C. 1982. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10: 7055-7074.
44. Grantham R, Gautier C, Gouy M, Mercier R, Pave A. 1980. Codon catalog usage and the genome hypothesis. Nucleic Acids Res 8: r49-r62. (Pubitemid 10154683)
45. Gu W, Zhou T, Wilke CO. 2010. A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes. PLoS Comput Biol 6: e1000664.
46. Hunt R, Sauna ZE, Ambudkar SV, Gottesman MM, Kimchi-Sarfaty C. 2009. Silent (synonymous) SNPs: Should we care about them? Methods Mol Biol 578: 23-39.
47. Hurst LD. 2011. Molecular genetics: the sound of silence. Nature 471: 582-583.
48. Iben JR, Maraia RJ. 2012. Yeast tRNAomics: tRNA gene copy number variation and codon use provide bioinformatics evidence of a new wobble pair in a eukaryote. RNA 18: 1358-1372.
49. Iben JR, Maraia RJ. 2013. tRNA gene copy number variation in humans. Gene 536: 376-384.
50. Iben JR, Epstein JA, Bayfield MA, Bruinsma MW, Hasson S, Bacikova D, Ahmad D, Rockwell D, Kittler EL, Zapp ML, et al. 2011. Comparative whole genome sequencing reveals phenotypic tRNA gene duplication in spontaneous Schizosaccharomyces pombe La mutants. Nucleic Acids Res 39: 4728-4742.
51. Ikemura T. 1981. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol 151: 389-409. (Pubitemid 12252691)
52. Ikemura T. 1985. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2: 13-34. (Pubitemid 15152046)
53. Itzkovitz S, Alon U. 2007. The genetic code is nearly optimal for allowing additional information within protein-coding sequences. Genome Res 17: 405-412. (Pubitemid 46556444)
54. Jühling F, Mörl M, Hartmann RK, Sprinzl M, Stadler PF, Pütz J. 2009. tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 37: D159-D162.
55. Kanaya S, Yamada Y, Kinouchi M, Kudo Y, Ikemura T. 2001. Codon usage and tRNA genes in eukaryotes: correlation of codon usage diversity with translation efficiency and with CG-dinucleotide usage as assessed by multivariate analysis. J Mol Evol 53: 290-298. (Pubitemid 32889537)
56. Kimchi-Sarfaty C, Oh JM, Kim IW, Sauna ZE, Calcagno AM, Ambudkar SV, Gottesman MM. 2007. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 315: 525-528. (Pubitemid 46175758)
57. Kramer EB, Farabaugh PJ. 2007. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13: 87-96. (Pubitemid 46026183)
58. Kramer G, Boehringer D, Ban N, Bukau B. 2009. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat Struct Mol Biol 16: 589-597.
59. Kramer EB, Vallabhaneni H, Mayer LM, Farabaugh PJ. 2010. A comprehensive analysis of translational missense errors in the yeast Saccharomyces cerevisiae. RNA 16: 1797-1808.
60. Kudla G, Murray AW, Tollervey D, Plotkin JB. 2009. Coding-sequence determinants of gene expression in Escherichia coli. Science 324: 255-258.
61. Lamichhane TN, Blewett NH, Maraia RJ. 2011. Plasticity and diversity of tRNA anticodon determinants of substrate recognition by eukaryotic A37 isopentenyltransferases. RNA 17: 1846-1857.
62. Lamichhane TN, Blewett NH, Cherkasova VA, Crawford AK, Iben JR, Farabaugh PJ, Begley TJ, Maraia RJ. 2013a. Lack of tRNA modification isopentenyl-A37 alters mRNA decoding and causes metabolic deficiencies in fission yeast. Mol Cell Biol 33: 2918-2929.
63. Lamichhane TN, Mattijssen S, Maraia RJ. 2013b. Human cells have a limited set of tRNA anticodon loop substrates of the tRNA isopentenyltransferase TRIT1 tumor suppressor. Mol Cell Biol 33: 4900-4908.
64. Li GW, Oh E, Weissman JS. 2012. The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484: 538-541.
65. Maraia RJ, Blewett NH, Bayfield MA. 2008. It's a mod mod tRNA world. Nat Chem Biol 4: 162-164. (Pubitemid 351264137)
66. Marck C, Grosjean H. 2002. tRNomics: Analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodonsparing strategies and domain-specific features. RNA 8: 1189-1232.
67. Nackley AG, Shabalina SA, Tchivileva IE, Satterfield K, Korchynskyi O, Makarov SS, Maixner W, Diatchenko L. 2006. Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science 314: 1930-1933. (Pubitemid 46026115)
68. Netzer WJ, Hartl FU. 1997. Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature 388: 343-349. (Pubitemid 27334805)
69. 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.
70. Oresic M, Shalloway D. 1998. Specific correlations between relative synonymous codon usage and protein secondary structure. J Mol Biol 281: 31-48. (Pubitemid 28360669)
71. Oresic M, Dehn M, Korenblum D, Shalloway D. 2003. Tracing specific synonymous codon-secondary structure correlations through evolution. J Mol Evol 56: 473-484. (Pubitemid 36390778)
72. Paredes JA, Carreto L, Simões J, Bezerra AR, Gomes AC, Santamaria R, Kapushesky M, Moura GR, Santos MA. 2012. Low level genome mistranslations deregulate the transcriptome and translatome and generate proteotoxic stress in yeast. BMC Biol 10: 55.
73. Parisien M, Wang X, Pan T. 2013. Diversity of human tRNA genes from the 1000-genomes project. RNA Biol 10: 1853-1867.
74. 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.
75. Parmley JL, Urrutia AO, Potrzebowski L, Kaessmann H, Hurst LD. 2007. Splicing and the evolution of proteins in mammals. PLoS Biol 5: e14.
76. Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, Pan T. 2009. tRNA over-expression in breast cancer and functional consequences. Nucleic Acids Res 37: 7268-7280.
77. Pechmann S, Frydman J. 2013. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat Struct Mol Biol 20: 237-243.
78. Percudani R, Pavesi A, Ottonello S. 1997. Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. J Mol Biol 268: 322-330. (Pubitemid 27208057)
79. Plant EP, Nguyen P, Russ JR, Pittman YR, Nguyen T, Quesinberry JT, Kinzy TG, Dinman JD. 2007. Differentiating between near- and non-cognate codons in Saccharomyces cerevisiae. PLoS One 2: e517.
80. Plotkin JB, Kudla G. 2011. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12: 32-42.
81. Purvis IJ, Bettany AJ, Santiago TC, Coggins JR, Duncan K, Eason R, Brown AJ. 1987. The efficiency of folding of some proteins is increased by controlled rates of translation in vivo. A hypothesis. J Mol Biol 193: 413-417.
82. Reynolds NM, Lazazzera BA, Ibba M. 2010. Cellular mechanisms that control mistranslation. Nat Rev Microbiol 8: 849-856.
83. Rocha EP. 2004. Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14: 2279-2286. (Pubitemid 39517335)
84. Salari R, Kimchi-Sarfaty C, Gottesman MM, Przytycka TM. 2013. Sensitive measurement of single-nucleotide polymorphism-induced changes of RNA conformation: application to disease studies. Nucleic Acids Res 41: 44-53.
85. Sauna ZE, Kimchi-Sarfaty C, Ambudkar SV, Gottesman MM. 2007. The sounds of silence: synonymous mutations affect function. Pharmacogenomics 8: 527-532. (Pubitemid 46939578)
86. Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE. 2005. Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res 33: 1141-1153. (Pubitemid 41439907)
87. Shimshek DR, Kim J, Hübner MR, Spergel DJ, Buchholz F, Casanova E, Stewart AF, Seeburg PH, Sprengel R. 2002. Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 32: 19-26. (Pubitemid 34117128)
88. Spencer PS, Siller E, Anderson JF, Barral JM. 2012. Silent substitutions predictably alter translation elongation rates and protein folding efficiencies. J Mol Biol 422: 328-335.
89. Stadler M, Fire A. 2011. Wobble base-pairing slows in vivo translation elongation in metazoans. RNA 17: 2063-2073.
90. Stergachis AB, Haugen E, Shafer A, Fu W, Vernot B, Reynolds A, Raubitschek A, Ziegler S, LeProust EM, Akey JM, et al. 2013. Exonic transcription factor binding directs codon choice and affects protein evolution. Science 342: 1367-1372.
91. Støy J, Steiner DF, Park SY, Ye H, Philipson LH, Bell GI. 2010. Clinical and molecular genetics of neonatal diabetes due to mutations in the insulin gene. Rev Endocr Metab Disord 11: 205-215.
92. Szathmary E, Jordan F, Pal C. 2001. Molecular biology and evolution. Can genes explain biological complexity? Science 292: 1315-1316. (Pubitemid 32476208)
93. Thompson KM, Gottesman S. 2014. The MiaA tRNA modification enzyme is necessary for robust RpoS expression in Escherichia coli. J Bacteriol 196: 754-761.
94. Tsai CJ, Sauna ZE, Kimchi-Sarfaty C, Ambudkar SV, Gottesman MM, Nussinov R. 2008. Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. J Mol Biol 383: 281-291.
95. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, Zaborske J, Pan T, Dahan O, Furman I, Pilpel Y. 2010. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141: 344-354.
96. Urrutia AO, Hurst LD. 2001. Codon usage bias covaries with expression breadth and the rate of synonymous evolution in humans, but this is not evidence for selection. Genetics 159: 1191-1199. (Pubitemid 34033460)
97. Wallace EW, Airoldi EM, Drummond DA. 2013. Estimating selection on synonymous codon usage from noisy experimental data. Mol Biol Evol 30: 1438-1453.
98. Weatheritt RJ, Babu MM. 2013. The hidden codes that shape protein evolution. Science 342: 1325-1326.
99. Wei FY, Tomizawa K. 2010. Functional loss of Cdkal1, a novel tRNA modification enzyme, causes the development of type 2 diabetes. Endocr J 58: 819-825.
100. Wei F, Suzuki T, Watanabe S, Kimura S, Kaitsuka T, Fujimura A, Matsui H, Atta M, Michiue H, Fontecave M, et al. 2011. Deficit of tRNALys modification by Cdkal1 causes the development of type 2 diabetes in mice. J Clin Invest 121: 3598-3608.
101. White RJ. 2011. Transcription by RNA polymerase III: more complex than we thought. Nat Rev Genet 12: 459-463.
102. Yarus M. 1982. Translational efficiency of transfer RNA's: uses of an extended anticodon. Science 218: 646-652. (Pubitemid 12005443)
103. Yona AH, Bloom-Ackermann Z, Frumkin I, Hanson-Smith V, Charpak-Amikam Y, Feng Q, Boeke JD, Dahan O, Pilpel Y. 2013. tRNA genes rapidly change in evolution to meet novel translational demands. Elife 2: e01339.
104. Zhou M, Guo J, Cha J, Chae M, Chen S, Barral JM, Sachs MS, Liu Y. 2013. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 495: 111-115.
105. Zolotukhin S, Potter M, Hauswirth WW, Guy J, Muzyczka N. 1996. A "humanized" green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J Virol 70: 4646-4654.