1932

Abstract

The pool of transfer RNA (tRNA) molecules in cells allows the ribosome to decode genetic information. This repertoire of molecular decoders is positioned in the crossroad of the genome, the transcriptome, and the proteome. Omics and systems biology now allow scientists to explore the entire repertoire of tRNAs of many organisms, revealing basic exciting biology. The tRNA gene set of hundreds of species is now characterized, in addition to the tRNA genes of organelles and viruses. Genes encoding tRNAs for certain anticodon types appear in dozens of copies in a genome, while others are universally absent from any genome. Transcriptome measurement of tRNAs is challenging, but in recent years new technologies have allowed researchers to determine the dynamic expression patterns of tRNAs. These advances reveal that availability of ready-to-translate tRNA molecules is highly controlled by several transcriptional and posttranscriptional regulatory processes. This regulation shapes the proteome according to the cellular state. The tRNA pool profoundly impacts many aspects of cellular and organismal life, including protein expression level, translation accuracy, adequacy of folding, and even mRNA stability. As a result, the shape of the tRNA pool affects organismal health and may participate in causing conditions such as cancer and neurological conditions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100617-062754
2018-10-06
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/34/1/annurev-cellbio-100617-062754.html?itemId=/content/journals/10.1146/annurev-cellbio-100617-062754&mimeType=html&fmt=ahah

Literature Cited

  1. Akashi H 1994. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136:3927–35
    [Google Scholar]
  2. 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 21:187–96
    [Google Scholar]
  3. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR et al. 1981. Sequence and organization of the human mitochondrial genome. Nature 290:5806457–65
    [Google Scholar]
  4. Azpurua J, Ke Z, Chen IX, Zhang Q, Ermolenko DN et al. 2013. Naked mole-rat has increased translational fidelity compared with the mouse, as well as a unique 28S ribosomal RNA cleavage. PNAS 110:4317350–55
    [Google Scholar]
  5. Bacher JM, de Crécy-Lagard V, Schimmel PR 2005. Inhibited cell growth and protein functional changes from an editing-defective tRNA synthetase. PNAS 102:51697–701
    [Google Scholar]
  6. Bailly-Bechet M, Vergassola M, Rocha E 2007. Causes for the intriguing presence of tRNAs in phages. Genome Res 17:101486–95
    [Google Scholar]
  7. Barski A, Chepelev I, Liko D, Cuddapah S, Fleming AB et al. 2010. Pol II and its associated epigenetic marks are present at Pol III–transcribed noncoding RNA genes. Nat. Struct. Mol. Biol. 17:5629–34
    [Google Scholar]
  8. Bazzini AA, Viso F, Moreno-Mateos MA, Johnstone TGT, Charles E et al. 2016. Codon identity regulates mRNA stability and translation efficiency during the maternal-to-zygotic transition. EMBO J 35:192087–103
    [Google Scholar]
  9. Bermudez-Santana C, Attolini CS-O, Kirsten T, Engelhardt J, Prohaska SJ et al. 2010. Genomic organization of eukaryotic tRNAs. BMC Genom 11:1270
    [Google Scholar]
  10. Bezerra AR, Simoes 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. PNAS 110:2711079–84
    [Google Scholar]
  11. Björk GR 1995. Biosynthesis and function of modified nucleosides. tRNA: Structure, Biosynthesis, and Function D Söll 165–205 Washington, DC: Am. Soc. Microbiol
    [Google Scholar]
  12. Blanco S, Dietmann S, Flores JV, Hussain S, Kutter C et al. 2014. Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders. EMBO J 33:182020–39
    [Google Scholar]
  13. 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 10:1e1004084
    [Google Scholar]
  14. Boël G, Letso R, Neely H, Price WN, Wong K-H et al. 2016. Codon influence on protein expression in E. coli correlates with mRNA levels. Nature 529:7586358–63
    [Google Scholar]
  15. Botzman M, Margalit H 2011. Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biol 12:10R109
    [Google Scholar]
  16. Bouadloun F, Donner D, Kurland CG 1983. Codon-specific missense errors in vivo. EMBO J 2:81351–56
    [Google Scholar]
  17. Bratulic S, Toll-Riera M, Wagner A 2017. Mistranslation can enhance fitness through purging of deleterious mutations. Nat. Commun. 8:15410
    [Google Scholar]
  18. Burgess-Brown NA, Sharma S, Sobott F, Loenarz C, Oppermann U, Gileadi O 2008. Codon optimization can improve expression of human genes in Escherichia coli: a multi-gene study. Protein Expr. Purif. 59:194–102
    [Google Scholar]
  19. Burroughs AM, Ando Y, de Hoon MJL, Tomaru Y, Suzuki H et al. 2011. Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol 8:1158–77
    [Google Scholar]
  20. Cannarrozzi G, Schraudolph NN, Faty M, von Rohr P, Friberg MT et al. 2010. A role for codon order in translation dynamics. Cell 141:2355–67
    [Google Scholar]
  21. Caponigro G, Muhlrad D, Parker R 1993. A small segment of the MAT alpha 1 transcript promotes mRNA decay in Saccharomyces cerevisiae: a stimulatory role for rare codons. Mol. Cell. Biol. 13:95141–48
    [Google Scholar]
  22. Chan PP, Lowe TM 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37:database issueD93–97
    [Google Scholar]
  23. Chan PP, Lowe TM 2016. GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes. Nucleic Acids Res 44:database issueD184–89
    [Google Scholar]
  24. Chaney JL, Steele A, Carmichael R, Rodriguez A, Specht AT et al. 2017. Widespread position-specific conservation of synonymous rare codons within coding sequences. PLOS Comput. Biol. 13:5e1005531
    [Google Scholar]
  25. Chapman KB, Byström AS, Boeke JD 1992. Initiator methionine tRNA is essential for Ty1 transposition in yeast. PNAS 89:83236–40
    [Google Scholar]
  26. Chatterjee K, Nostramo RT, Wan Y, Hopper AK 2018. tRNA dynamics between the nucleus, cytoplasm and mitochondrial surface: location, location, location. Biochim. Biophys. Acta Gene Regul. Mech. 1861:4373–86
    [Google Scholar]
  27. Chen Q, Yan M, Cao Z, Li X, Zhang Y et al. 2016. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351:6271397–400
    [Google Scholar]
  28. Chernyakov I, Whipple JM, Kotelawala L, Grayhack EJ, Phizicky EM 2008. Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5′-3′ exonucleases Rat1 and Xrn1. Genes Dev 22:101369–80
    [Google Scholar]
  29. Close P, Bose D, Chariot A, Leidel SA 2018. Dynamic regulation of tRNA modifications in cancer. Cancer and Noncoding RNAs 1 J Chakrabarti, S Mitra 163–86 London: Academic
    [Google Scholar]
  30. Conn CS, Qian SB 2013. Nutrient signaling in protein homeostasis: an increase in quantity at the expense of quality. Sci. Signal. 6:271ra24
    [Google Scholar]
  31. Copela LA, Chakshusmathi G, Sherrer RL, Wolin SL 2006. The La protein functions redundantly with tRNA modification enzymes to ensure tRNA structural stability. RNA 12:4644–54
    [Google Scholar]
  32. Czech A, Wende S, Mörl M, Pan T, Ignatova Z 2013. Reversible and rapid transfer-RNA deactivation as a mechanism of translational repression in stress. PLOS Genet 9:8e1003767
    [Google Scholar]
  33. Damon JR, Pincus D, Ploegh HL 2015. tRNA thiolation links translation to stress responses in Saccharomyces cerevisiae. Mol. Biol. . Cell 26:2270–82
    [Google Scholar]
  34. Diodato D, Ghezzi D, Tiranti V 2014. The mitochondrial aminoacyl tRNA synthetases: genes and syndromes. Int. J. Cell Biol. 2014:787956
    [Google Scholar]
  35. Dittmar KA, Goodenbour JM, Pan T 2006. Tissue-specific differences in human transfer RNA expression. PLOS Genet 2:12e221
    [Google Scholar]
  36. Dittmar KA, Sørensen MA, Elf J, Ehrenberg M, Pan T 2005. Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep 6:2151–57
    [Google Scholar]
  37. Dix DB, Thompson RC 1989. Codon choice and gene expression: Synonymous codons differ in translational accuracy. PNAS 86:186888–92
    [Google Scholar]
  38. 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. 260:649–63
    [Google Scholar]
  39. dos Reis M, Savva R, Wernisch L 2004. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res 32:175036–44
    [Google Scholar]
  40. Drummond DA, Wilke CO 2008. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:2341–52
    [Google Scholar]
  41. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ et al. 2010. A three-dimensional model of the yeast genome. Nature 465:7296363–67
    [Google Scholar]
  42. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA et al. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:741457–74
    [Google Scholar]
  43. Elf J, Nilsson D, Tenson T, Ehrenberg M 2003. Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 300:56261718–22
    [Google Scholar]
  44. Endres L, Dedon PC, Begley TJ 2015. Codon-biased translation can be regulated by wobble-base tRNA modification systems during cellular stress responses. RNA Biol 12:6603–14
    [Google Scholar]
  45. Evans ME, Clark WC, Zheng G, Pan T 2017. Determination of tRNA aminoacylation levels by high-throughput sequencing. Nucleic Acids Res 108:14E794–802
    [Google Scholar]
  46. Francklyn C, Schimmel P 1990. Enzymatic aminoacylation of an eight-base-pair microhelix with histidine. PNAS 87:218655–59
    [Google Scholar]
  47. Frumkin I, Lajoie MJ, Gregg CJ, Hornung G, Church GM, Pilpel Y 2018. Codon usage of highly expressed genes affects proteome-wide translation efficiency. PNAS 115:21E4940–49
    [Google Scholar]
  48. Fu H, Feng J, Liu Q, Sun F, Tie Y et al. 2009. Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett 583:2437–42
    [Google Scholar]
  49. Galili T, Gingold H, Shaul S, Benjamini Y 2016. Identifying the ligated amino acid of archaeal tRNAs based on positions outside the anticodon. RNA 22:101477–91
    [Google Scholar]
  50. Gardin J, Yeasmin R, Yurovsky A, Cai Y, Skiena S, Futcher B 2014. Measurement of average decoding rates of the 61 sense codons in vivo. eLife 3:e03735
    [Google Scholar]
  51. Giegé R, Sissler M, Florentz C 1998. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 26:225017–35
    [Google Scholar]
  52. Gingold H, Dahan O, Pilpel Y 2012. Dynamic changes in translational efficiency are deduced from codon usage of the transcriptome. Nucleic Acids Res 40:2010053–63
    [Google Scholar]
  53. Gingold H, Pilpel Y 2011. Determinants of translation efficiency and accuracy. Mol. Syst. Biol. 7:481
    [Google Scholar]
  54. Gingold H, Tehler D, Christoffersen NR, Nielsen MM, Asmar F et al. 2014. A dual program for translation regulation in cellular proliferation and differentiation. Cell 158:61281–92
    [Google Scholar]
  55. Giuliodori S, Percudani R, Braglia P, Ferrari R, Guffanti E et al. 2003. A composite upstream sequence motif potentiates tRNA gene transcription in yeast. J. Mol. Biol. 333:11–20
    [Google Scholar]
  56. Godinic-Mikulcic V, Jaric J, Greber BJ, Franke V, Hodnik V et al. 2014. Archaeal aminoacyl-tRNA synthetases interact with the ribosome to recycle tRNAs. Nucleic Acids Res 42:85191–201
    [Google Scholar]
  57. Gomes AC, Miranda I, Silva RM, Moura GR, Thomas B et al. 2007. A genetic code alteration generates a proteome of high diversity in the human pathogen Candida albicans. . Genome Biol 8:10R206
    [Google Scholar]
  58. Goodarzi H, Liu X, Nguyen HCB, Zhang S, Fish L, Tavazoie SF 2015. Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement. Cell 161:4790–802
    [Google Scholar]
  59. Goodarzi H, Nguyen HCB, Zhang S, Dill BD, Molina H, Tavazoie SF 2016. Modulated expression of specific tRNAs drives gene expression and cancer progression. Cell 165:61416–27
    [Google Scholar]
  60. Goodenbour JM, Pan T 2006. Diversity of tRNA genes in eukaryotes. Nucleic Acids Res 34:216137–46
    [Google Scholar]
  61. Gorochowski TE, Ignatova Z, Bovenberg RAL, Roubos JA 2015. Trade-offs between tRNA abundance and mRNA secondary structure support smoothing of translation elongation rate. Nucleic Acids Res 43:63022–32
    [Google Scholar]
  62. Gromadski KB, Rodnina MV 2004. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell 13:2191–200
    [Google Scholar]
  63. Grosjean H, de Crécy-Lagard V, Marck C 2010. Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett 584:2252–64
    [Google Scholar]
  64. Gu C, Begley TJ, Dedon PC 2014. tRNA modifications regulate translation during cellular stress. FEBS Lett 588:234287–96
    [Google Scholar]
  65. Gustafsson C, Govindarajan S, Minshull J 2004. Codon bias and heterologous protein expression. Trends Biotechnol 22:7346–53
    [Google Scholar]
  66. Haas J, Park EC, Seed B 1996. Codon usage limitation in the expression of HIV-1 envelope glycoprotein. Curr. Biol. 6:3315–24
    [Google Scholar]
  67. Hanson G, Coller J 2017. Codon optimality, bias and usage in translation and mRNA decay. Nat. Rev. Mol. Cell Biol. 19:120–30
    [Google Scholar]
  68. Harigaya Y, Parker R 2016. Analysis of the association between codon optimality and mRNA stability in Schizosaccharomyces pombe. . BMC Genom 17:1895
    [Google Scholar]
  69. Hess A-K, Saffert P, Liebeton K, Ignatova Z 2015. Optimization of translation profiles enhances protein expression and solubility. PLOS ONE 10:5e0127039
    [Google Scholar]
  70. Hoekema A, Kastelein RA, Vasser M, de Boer HA 1987. Codon replacement in the PGK1 gene of Saccharomyces cerevisiae: experimental approach to study the role of biased codon usage in gene expression. Mol. Cell. Biol. 7:82914–24
    [Google Scholar]
  71. Hoffman KS, Berg MD, Shilton BH, Brandl CJ, O'Donoghue P 2016. Genetic selection for mistranslation rescues a defective co-chaperone in yeast. Nucleic Acids Res 45:63407–21
    [Google Scholar]
  72. Hopfield JJ, Yamane T, Yue V, Coutts SM 1976. Direct experimental evidence for kinetic proofreading in amino acylation of tRNAIle (stoichiometry of energy coupling/amino acyl tRNA synthetase/error rate in biosynthesis). PNAS 73:41164–68
    [Google Scholar]
  73. Hopper AK, Pai DA, Engelke DR 2010. Cellular dynamics of tRNAs and their genes. FEBS Lett 584:2310–17
    [Google Scholar]
  74. Horton R, Wilming L, Rand V, Lovering RC, Bruford EA et al. 2004. Gene map of the extended human MHC. Nat. Rev. Genet. 5:12889–99
    [Google Scholar]
  75. Hussmann JA, Press WH 2014. Local correlations in codon preferences do not support a model of tRNA recycling. Cell Rep 8:61624–29
    [Google Scholar]
  76. Iben JR, Maraia RJ 2012. tRNAomics: tRNA gene copy number variation and codon use provide bioinformatic evidence of a new anticodon:codon wobble pair in a eukaryote. RNA 18:71358–72
    [Google Scholar]
  77. Iben JR, Maraia RJ 2014. tRNA gene copy number variation in humans. Gene 536:2376–84
    [Google Scholar]
  78. Ishimura R, Nagy G, Dotu I, Zhou H, Yang X-L et al. 2014. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science 345:6195455–59
    [Google Scholar]
  79. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P 2011. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell 43:4613–23
    [Google Scholar]
  80. Jiang H, Zhang Y, Sun J, Wang W, Gu Z 2008. Differential selection on gene translation efficiency between the filamentous fungus Ashbya gossypii and yeasts. BMC Evol. Biol. 8:1343
    [Google Scholar]
  81. Johansson M, Zhang J, Ehrenberg M 2012. Genetic code translation displays a linear trade-off between efficiency and accuracy of tRNA selection. PNAS 109:1131–36
    [Google Scholar]
  82. Jones TE, Alexander RW, Pan T 2011. Misacylation of specific nonmethionyl tRNAs by a bacterial methionyl-tRNA synthetase. PNAS 108:176933–38
    [Google Scholar]
  83. Kadaba S, Krueger A, Trice T, Krecic AM, Hinnebusch AG, Anderson J 2004. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. . Genes Dev 18:111227–40
    [Google Scholar]
  84. Kaminska M, Havrylenko S, Decottignies P, Le Maréchal P, Negrutskii B, Mirande M 2009. Dynamic organization of aminoacyl-tRNA synthetase complexes in the cytoplasm of human cells. J. Biol. Chem. 284:2013746–54
    [Google Scholar]
  85. Kanaya S, Yamada Y, Kudo Y, Ikemura T 1999. Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 238:1143–55
    [Google Scholar]
  86. Kapur M, Monaghan CE, Ackerman SL 2017. Regulation of mRNA translation in neurons—a matter of life and death. Neuron 96:616–37
    [Google Scholar]
  87. Ke Z, Mallik P, Johnson AB, Luna F, Nevo E et al. 2017. Translation fidelity coevolves with longevity. Aging Cell 16:5988–93
    [Google Scholar]
  88. Kimchi-Sarfaty C, Oh JM, Kim I-W, Sauna ZE, Calcagno AM et al. 2007. A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315:5811525–28
    [Google Scholar]
  89. Kirchner S, Cai Z, Rauscher R, Kastelic N, Anding M et al. 2017. Alteration of protein function by a silent polymorphism linked to tRNA abundance. PLOS Biol 15:5e2000779
    [Google Scholar]
  90. Kleiman L 2002. tRNALys3: the primer tRNA for reverse transcription in HIV-1. IUBMB Life 53:2107–14
    [Google Scholar]
  91. Komar AA 2009. A pause for thought along the co-translational folding pathway. Trends Biochem. Sci. 34:116–24
    [Google Scholar]
  92. Kramer EB, Farabaugh PJ 2006. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13:187–96
    [Google Scholar]
  93. Krisko A, Copic T, Gabaldón T, Lehner B, Supek F 2014. Inferring gene function from evolutionary change in signatures of translation efficiency. Genome Biol 15:3R44
    [Google Scholar]
  94. Kumar P, Anaya J, Mudunuri SB, Dutta A 2014. Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets. BMC Biol 12:178
    [Google Scholar]
  95. Kumar P, Mudunuri SB, Anaya J, Dutta A 2015. tRFdb: a database for transfer RNA fragments. Nucleic Acids Res 43:database issueD141–45
    [Google Scholar]
  96. Kurland CG, Ehrenberg M 1987. Growth-optimizing accuracy of gene expression. Annu. Rev. Biophys. Biophys. Chem. 16:1291–317
    [Google Scholar]
  97. Kutter C, Brown GD, Gonçalves A, Wilson MD, Watt S et al. 2011. Pol III binding in six mammals shows conservation among amino acid isotypes despite divergence among tRNA genes. Nat. Genet. 43:10948–55
    [Google Scholar]
  98. Lee SR, Collins K 2005. Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J. Biol. . Chem 280:5242744–49
    [Google Scholar]
  99. Li C, Qian W, Maclean CJ, Zhang J 2016. The fitness landscape of a tRNA gene. Science 352:6287837–40
    [Google Scholar]
  100. Li M, Kao E, Gao X, Sandig H, Limmer K et al. 2012. Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11. Nature 491:7422125–28
    [Google Scholar]
  101. Limor-Waisberg K, Carmi A, Scherz A, Pilpel Y, Furman I 2011. Specialization versus adaptation: two strategies employed by cyanophages to enhance their translation efficiencies. Nucleic Acids Res 39:146016–28
    [Google Scholar]
  102. Lithwick G, Margalit H 2003. Hierarchy of sequence-dependent features associated with prokaryotic translation. Genome Res 13:122665–73
    [Google Scholar]
  103. Loss-Morais G, Waterhouse PM, Margis R 2013. Description of plant tRNA–derived RNA fragments (tRFs) associated with argonaute and identification of their putative targets. Biol. Direct. 8:16
    [Google Scholar]
  104. Lowe TM, Eddy SR 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:5955–64
    [Google Scholar]
  105. Luo S, Levine RL 2009. Methionine in proteins defends against oxidative stress. FASEB J 23:2464–72
    [Google Scholar]
  106. Machnicka MA, Milanowska K, Oglou OO, Purta E, Kurkowska M et al. 2013. MODOMICS: a database of RNA modification pathways—2013 update. Nucleic Acids Res 41:database issueD262–67
    [Google Scholar]
  107. Man O, Pilpel Y 2007. Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nat. Genet. 39:3415–21
    [Google Scholar]
  108. Maraia RJ, Arimbasseri AG 2017. Factors that shape eukaryotic tRNAomes: processing, modification and anticodon-codon use. Biomolecules 7:126
    [Google Scholar]
  109. Maréchal-Drouard L, Guillemaut P, Pfitzingzer H, Weil JH 1991. Chloroplast tRNAs and tRNA genes: structure and function. The Translational Apparatus of Photosynthetic Organelles R Mache, E Stutz, AR Subramanian 45–57 Berlin/Heidelberg: Springer
    [Google Scholar]
  110. Martinez G 2017. tRNA-derived small RNAs: new players in genome protection against retrotransposons. RNA Biol 15:2170–75
    [Google Scholar]
  111. Maute RL, Schneider C, Sumazin P, Holmes A, Califano A et al. 2013. tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. PNAS 110:41404–9
    [Google Scholar]
  112. McClain WH, Schneider J, Gabriel K 1994. Distinctive acceptor-end structure and other determinants of Escherichia coli tRNAPro identity. Nucleic Acids Res 22:3522–29
    [Google Scholar]
  113. McDonald MJ, Chou C-H, Swamy KB, Huang H-D, Leu J-Y 2015. The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli. BMC Evol. Biol 151163
    [Google Scholar]
  114. Meyerovich M, Mamou G, Ben-Yehuda S 2010. Visualizing high error levels during gene expression in living bacterial cells. PNAS 107:2511543–48
    [Google Scholar]
  115. Mishima Y, Tomari Y 2016. Codon usage and 3′ UTR length determine maternal mRNA stability in zebrafish. Mol. Cell 61:6874–85
    [Google Scholar]
  116. Mohler K, Ibba M 2017. Translational fidelity and mistranslation in the cellular response to stress. Nat. Microbiol. 24:217117
    [Google Scholar]
  117. Mordret E, Yehonadav A, Barnabas GD, Cox J, Dahan O et al. 2018. Systematic detection of amino acid substitutions in proteome reveals a mechanistic basis of ribosome errors. bioRxiv 255943
  118. Nangle LA, de Crécy Lagard V, Döring V, Schimmel P 2002. Genetic code ambiguity. J. Biol. Chem. 277:4845729–33
    [Google Scholar]
  119. Nedialkova DD, Leidel SA 2015. Optimization of codon translation rates via tRNA modifications maintains proteome integrity. Cell 161:71606–18
    [Google Scholar]
  120. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB et al. 2009. Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462:7272522–26
    [Google Scholar]
  121. Oler AJ, Alla RK, Roberts DN, Wong A, Hollenhorst PC et al. 2010. Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat. Struct. Mol. Biol. 17:5620–28
    [Google Scholar]
  122. Pang YLJ, Abo R, Levine SS, Dedon PC 2014. Diverse cell stresses induce unique patterns of tRNA up- and down-regulation: tRNA-seq for quantifying changes in tRNA copy number. Nucleic Acids Res 42:22e170
    [Google Scholar]
  123. Parker J 1989. Errors and alternatives in reading the universal genetic code. Microbiol. Rev. 53:3273–98
    [Google Scholar]
  124. Patil A, Chan C, Dyavaiah M, Rooney JP, Dedon PC, Begley TJ 2012. Translational infidelity-induced protein stress results from a deficiency in Trm9-catalyzed tRNA modifications. RNA Biol 9:7990–1001
    [Google Scholar]
  125. 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 37:217268–80
    [Google Scholar]
  126. Pechmann S, Frydman J 2013. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat. Struct. Mol. Biol. 20:2237–43
    [Google Scholar]
  127. Percudani R, Pavesi A, Ottonello S 1997. Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. J. Mol. Biol 268:2322–30
    [Google Scholar]
  128. Phizicky EM, Hopper AK 2010. tRNA biology charges to the front. Genes Dev 24:171832–60
    [Google Scholar]
  129. Pliatsika V, Loher P, Magee R, Telonis AG, Londin E et al. 2018. MINTbase v2.0: a comprehensive database for tRNA-derived fragments that includes nuclear and mitochondrial fragments from all The Cancer Genome Atlas projects. Nucleic Acids Res 46:database issueD152–59
    [Google Scholar]
  130. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP 2010. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465:73011033–38
    [Google Scholar]
  131. Presnyak V, Alhusaini N, Chen YH, Martin S, Morris N et al. 2015. Codon optimality is a major determinant of mRNA stability. Cell 160:61111–24
    [Google Scholar]
  132. Purvis IJ, Bettany AJ, Santiago TC, Coggins JR, Duncan K et al. 1987. The efficiency of folding of some proteins is increased by controlled rates of translation in vivo. A hypothesis. J. Mol. Biol 193:2413–17
    [Google Scholar]
  133. Radhakrishnan A, Chen YH, Martin S, Alhusaini N, Green R, Coller J 2016. The DEAD-box protein Dhh1p couples mRNA decay and translation by monitoring codon optimality. Cell 167:1122–32.e9
    [Google Scholar]
  134. Rapino F, Delaunay S, Zhou Z, Chariot A, Close P 2017. tRNA modification: Is cancer having a wobble?. Trends Cancer 3:4249–52
    [Google Scholar]
  135. Ribas de Pouplana L, Santos MAS, Zhu JH, Farabaugh PJ, Javid B 2014. Protein mistranslation: friend or foe?. Trends Biochem. Sci. 39:8355–62
    [Google Scholar]
  136. Rodnina MV, Wintermeyer W 2001. Ribosome fidelity: tRNA discrimination, proofreading and induced fit. Trends Biochem. Sci. 26:2124–30
    [Google Scholar]
  137. Rogers HH, Griffiths-Jones S 2014. tRNA anticodon shifts in eukaryotic genomes. RNA 20:3269–81
    [Google Scholar]
  138. Sagi D, Rak R, Gingold H, Adir I, Maayan G et al. 2016. Tissue- and time-specific expression of otherwise identical tRNA genes. PLOS Genet 12:8e1006264
    [Google Scholar]
  139. Santos MA, Tuite MF 1995. The CUG codon is decoded in vivo as serine and not leucine in Candida albicans. . Nucleic Acids Res 23:91481–86
    [Google Scholar]
  140. Saxena SK, Rybak SM, Davey RT, Youle RJ, Ackerman EJ 1992. Angiogenin is a cytotoxic, tRNA-specific ribonuclease in the RNase A superfamily. J. Biol. Chem. 267:3021982–86
    [Google Scholar]
  141. Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M et al. 2010. RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes Dev 24:151590–95
    [Google Scholar]
  142. Schaffrath R, Leidel SA 2017. Wobble uridine modifications—a reason to live, a reason to die?. ! RNA Biol 14:91209–22
    [Google Scholar]
  143. Schorn AJ, Gutbrod MJ, LeBlanc C, Martienssen R 2017. LTR-retrotransposon control by tRNA-derived small RNAs. Cell 170:161–71.e11
    [Google Scholar]
  144. Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG et al. 2016. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351:6271391–96
    [Google Scholar]
  145. Sharp PM, Li WH 1987. The codon Adaptation Index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:31281–95
    [Google Scholar]
  146. Shoemaker CJ, Green R 2012. Translation drives mRNA quality control. Nat. Struct. Mol. Biol. 19:6594–601
    [Google Scholar]
  147. Simões J, Bezerra AR, Moura GR, Araújo H, Gut I et al. 2016. The fungus Candida albicans tolerates ambiguity at multiple codons. Front. Microbiol. 7:401
    [Google Scholar]
  148. Sørensen MA, Kurland CG, Pedersen S 1989. Codon usage determines translation rate in Escherichia coli. J. Mol. Biol 207:2365–77
    [Google Scholar]
  149. Stefano JE 1984. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts. Cell 36:1145–54
    [Google Scholar]
  150. Stoletzki N, Eyre-Walker A 2007. Synonymous codon usage in Escherichia coli: selection for translational accuracy. Mol. Biol. Evol. 24:2374–81
    [Google Scholar]
  151. Su AAH, Randau L 2011. A-to-I and C-to-U editing within transfer RNAs. Biochemistry 76:8932–37
    [Google Scholar]
  152. Subramaniam AR, Pan T, Cluzel P 2013. Environmental perturbations lift the degeneracy of the genetic code to regulate protein levels in bacteria. PNAS 110:62419–24
    [Google Scholar]
  153. Telonis AG, Loher P, Kirino Y, Rigoutsos I 2016. Consequential considerations when mapping tRNA fragments. BMC Bioinform 17:124797–822
    [Google Scholar]
  154. Thanaraj TA, Argos P 1996. Ribosome-mediated translational pause and protein domain organization. Protein Sci 5:81594–612
    [Google Scholar]
  155. Thomas LK, Dix DB, Thompson RC 1988. Codon choice and gene expression: Synonymous codons differ in their ability to direct aminoacylated-transfer RNA binding to ribosomes in vitro. PNAS 85:124242–46
    [Google Scholar]
  156. Thompson DM, Parker R 2009. Stressing out over tRNA cleavage. Cell 138:2215–19
    [Google Scholar]
  157. Thompson M, Haeusler RA, Good PD, Engelke DR 2003. Nucleolar clustering of dispersed tRNA genes. Science 302:56491399–401
    [Google Scholar]
  158. Turowski TW, Karkusiewicz I, Kowal J, Boguta M 2012. Maf1-mediated repression of RNA polymerase III transcription inhibits tRNA degradation via RTD pathway. RNA 18:101823–32
    [Google Scholar]
  159. Väre VYP, Eruysal ER, Narendran A, Sarachan KL, Agris PF 2017. Chemical and conformational diversity of modified nucleosides affects tRNA structure and function. Biomolecules 7:1E29
    [Google Scholar]
  160. Varenne S, Buc J, Lloubes R, Lazdunski C 1984. Translation is a non-uniform process: effect of tRNA availability on the rate of elongation of nascent polypeptide chains. J. Mol. Biol. 180:3549–76
    [Google Scholar]
  161. Wang X, Pan T 2015. Methionine mistranslation bypasses the restraint of the genetic code to generate mutant proteins with distinct activities. PLOS Genet 11:12e1005745
    [Google Scholar]
  162. Weinberg DE, Shah P, Eichhorn SW, Hussmann JA, Plotkin JB, Bartel DP 2016. Improved ribosome-footprint and mRNA measurements provide insights into dynamics and regulation of yeast translation. Cell Rep 14:71787–99
    [Google Scholar]
  163. Whipple JM, Lane EA, Chernyakov I, D'Silva S, Phizicky EM 2011. The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes Dev 25:111173–84
    [Google Scholar]
  164. Willis IM 1993. RNA polymerase III: genes, factors and transcriptional specificity. Eur. J. Biochem. 212:11–11
    [Google Scholar]
  165. Wiltrout E, Goodenbour JM, Frechin M, Pan T 2012. Misacylation of tRNA with methionine in Saccharomyces cerevisiae. . Nucleic Acids Res 40:2010494–506
    [Google Scholar]
  166. Wolf J, Gerber AP, Keller W 2002. TadA, an essential tRNA-specific adenosine deaminase from Escherichia coli. . EMBO J 21:143841–51
    [Google Scholar]
  167. Wong EH, Smith DK, Rabadan R, Peiris M, Poon LL 2010. Codon usage bias and the evolution of influenza A viruses. Codon usage biases of influenza virus. BMC Evol. Biol. 10:1253
    [Google Scholar]
  168. Yamane T, Hopfield JJ 1977. Experimental evidence for kinetic proofreading in the aminoacylation of tRNA by synthetase (stoichiometry of energy coupling/aminoacyl tRNA synthetase/error rate in biosynthesis). PNAS 74:62246–50
    [Google Scholar]
  169. Yamasaki S, Ivanov P, Hu G-F, Anderson P 2009. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol. 185:135–42
    [Google Scholar]
  170. Yokobori S, Kitamura A, Grosjean H, Bessho Y 2013. Life without tRNAArg-adenosine deaminase TadA: evolutionary consequences of decoding the four CGN codons as arginine in Mycoplasmas and other Mollicutes. Nucleic Acids Res 41:136531–43
    [Google Scholar]
  171. Yona AH, Bloom-Ackermann Z, Frumkin I, Hanson-Smith V, Charpak-Amikam Y et al. 2013. tRNA genes rapidly change in evolution to meet novel translational demands. eLife 2:e01339
    [Google Scholar]
  172. Zaborske JM, Bauer DuMont VL, Wallace EWJ, Pan T, Aquadro CF, Drummond DA 2014. A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. PLOS Biol 12:12e1002015
    [Google Scholar]
  173. Zaher HS, Green R 2009. Fidelity at the molecular level: lessons from protein synthesis. Cell 136:4746–62
    [Google Scholar]
  174. Zhang G, Hubalewska M, Ignatova Z 2009. Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat. Struct. Mol. Biol. 16:3274–80
    [Google Scholar]
  175. Zhang G, Lukoszek R, Mueller-Roeber B, Ignatova Z 2011. Different sequence signatures in the upstream regions of plant and animal tRNA genes shape distinct modes of regulation. Nucleic Acids Res 39:83331–39
    [Google Scholar]
  176. Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I 1999. Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J. Virol. 73:64972–82
    [Google Scholar]
  177. Zhou T, Weems M, Wilke CO 2009.a Translationally optimal codons associate with structurally sensitive sites in proteins. Mol. Biol. Evol. 26:Oct.1571–80
    [Google Scholar]
  178. Zhou Y, Goodenbour JM, Godley LA, Wickrema A, Pan T 2009.b High levels of tRNA abundance and alteration of tRNA charging by bortezomib in multiple myeloma. Biochem. Biophys. Res. Commun. 385:2160–64
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100617-062754
Loading
/content/journals/10.1146/annurev-cellbio-100617-062754
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error