Tissue- and Time-Specific Expression of Otherwise Identical tRNA Genes

PLoS Genetics

Volumn 12, Issue 8, 2016, Pages

  Sagi, Dror ^a   Rak, Roni ^a   Gingold, Hila ^b   Adir, Idan ^a   Maayan, Gadi ^a   Dahan, Orna ^b   Broday, Limor ^a   Pilpel, Yitzhak ^b   Rechavi, Oded ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II; CAENORHABDITIS ELEGANS PROTEIN; CODON; TRANSFER RNA;

ADULT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENETIC ASSOCIATION; IN VITRO STUDY; INTRON; LIFESPAN; NONHUMAN; POLII GENE; PROMOTER REGION; SUP21 GENE; SUP24 GENE; SUP28 GENE; SUP29 GENE; SUP33 GENE; SUP34 GENE; SUP5 GENE; SUP7 GENE; YOUNG ADULT; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; CODON; GENE EXPRESSION REGULATION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; LONGEVITY; PROTEIN SYNTHESIS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CODON; GENE EXPRESSION REGULATION; GENOME; INTRONS; LONGEVITY; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; RNA, TRANSFER;

EID: 84984887314     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006264     Document Type: Article

References (81)

1. Crombie T, Swaffield JC, Brown AJ, Protein folding within the cell is influenced by controlled rates of polypeptide elongation. J Mol Biol. 1992;228: 7–12. Available: http://www.ncbi.nlm.nih.gov/pubmed/14477951447795
2. Pedersen S, Escherichia coli ribosomes translate in vivo with variable rate. EMBO J. 1984;3: 2895–8. Available: http://www.ncbi.nlm.nih.gov/pubmed/63960826396082
3. Stoletzki N, Eyre-Walker A, Synonymous Codon Usage in Escherichia coli: Selection for Translational Accuracy. Mol Biol Evol. 2006;24: 374–381. doi: 10.1093/molbev/msl16617101719
4. Kudla G, Murray AW, Tollervey D, Plotkin JB, Coding-sequence determinants of gene expression in Escherichia coli. Science. 2009;324: 255–8. doi: 10.1126/science.117016019359587
5. Varenne S, Buc J, Lloubes R, Lazdunski C, Translation is a non-uniform process. J Mol Biol. 1984;180: 549–576. doi: 10.1016/0022-2836(84)90027-56084718
6. Nedialkova DD, Leidel SA, Optimization of Codon Translation Rates via tRNA Modifications Maintains Proteome Integrity. Cell. Elsevier; 2015; doi: 10.1016/j.cell.2015.05.022
7. Kimchi-Sarfaty C, Oh JM, Kim I-W, Sauna ZE, Calcagno AM, Ambudkar S V, et al. A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science. 2007;315: 525–8. doi: 10.1126/science.113530817185560
8. Komar AA, A pause for thought along the co-translational folding pathway. Trends Biochem Sci. 2009;34: 16–24. doi: 10.1016/j.tibs.2008.10.00218996013
9. Goodarzi H, Nguyen HCB, Zhang S, Dill BD, Molina H, Tavazoie SF, Modulated Expression of Specific tRNAs Drives Gene Expression and Cancer Progression. Cell. 2016;165: 1416–27. doi: 10.1016/j.cell.2016.05.04627259150
10. Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, Pan T, tRNA over-expression in breast cancer and functional consequences. Nucleic Acids Res. 2009;37: 7268–80. doi: 10.1093/nar/gkp78719783824
11. Gingold H, Tehler D, Christoffersen NR, Nielsen MM, Asmar F, Kooistra SM, et al. A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation. Cell. 2014;158: 1281–1292. doi: 10.1016/j.cell.2014.08.01125215487
12. Kirchner S, Ignatova Z, Emerging roles of tRNA in adaptive translation, signalling dynamics and disease. Nat Rev Genet. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2014;16: 98–112. doi: 10.1038/nrg386125534324
13. Stoecklin G, Diederichs S, tRNAs: new tricks from old dogs. EMBO J. EMBO Press; 2014;33: 1981–3. doi: 10.15252/embj.20148963425216676
14. Schaffer AE, Eggens VRC, Caglayan AO, Reuter MS, Scott E, Coufal NG, et al. CLP1 founder mutation links tRNA splicing and maturation to cerebellar development and neurodegeneration. Cell. 2014;157: 651–63. doi: 10.1016/j.cell.2014.03.04924766810
15. Ishimura R, Nagy G, Dotu I, Zhou H, Yang X-L, Schimmel P, et al. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science (80-). 2014;345: 455–459. doi: 10.1126/science.1249749
16. Latour P, Thauvin-Robinet C, Baudelet-Méry C, Soichot P, Cusin V, Faivre L, et al. A major determinant for binding and aminoacylation of tRNA(Ala) in cytoplasmic Alanyl-tRNA synthetase is mutated in dominant axonal Charcot-Marie-Tooth disease. Am J Hum Genet. 2010;86: 77–82. doi: 10.1016/j.ajhg.2009.12.00520045102
17. Girstmair H, Saffert P, Rode S, Czech A, Holland G, Bannert N, et al. Depletion of Cognate Charged Transfer RNA Causes Translational Frameshifting within the Expanded CAG Stretch in Huntingtin. Cell Rep. 2013;3: 148–159. doi: 10.1016/j.celrep.2012.12.01923352662
18. Ishimura R, Nagy G, Dotu I, Zhou H, Yang X-L, Schimmel P, et al. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science (80-). 2014;345: 455–459. doi: 10.1126/science.1249749
19. Kutter C, Brown GD, Gonçalves A, Wilson MD, Watt S, Brazma A, et al. Pol III binding in six mammals shows conservation among amino acid isotypes despite divergence among tRNA genes. Nat Genet. 2011;43: 948–55. doi: 10.1038/ng.90621873999
20. Dittmar K a, Goodenbour JM, Pan T, Tissue-specific differences in human transfer RNA expression. PLoS Genet. 2006;2: e221. doi: 10.1371/journal.pgen.002022117194224
21. Pavon-Eternod M, Gomes S, Rosner MR, Pan T, Overexpression of initiator methionine tRNA leads to global reprogramming of tRNA expression and increased proliferation in human epithelial cells. RNA. 2013;19: 461–6. doi: 10.1261/rna.037507.11223431330
22. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, Zaborske J, et al. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell. 2010;141: 344–54. doi: 10.1016/j.cell.2010.03.03120403328
23. Novoa EM, Ribas de Pouplana L, Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet. 2012;28: 574–81. doi: 10.1016/j.tig.2012.07.00622921354
24. Crick FHC, Codon—anticodon pairing: The wobble hypothesis. J Mol Biol. Academic Press; 1966;19: 548–555. doi: 10.1016/S0022-2836(66)80022-05969078
25. Yu C-H, Dang Y, Zhou Z, Wu C, Zhao F, Sachs MS, et al. Codon Usage Influences the Local Rate of Translation Elongation to Regulate Co-translational Protein Folding. Mol Cell. 2015;59: 744–754. doi: 10.1016/j.molcel.2015.07.01826321254
26. Bartoszewski RA, Jablonsky M, Bartoszewska S, Stevenson L, Dai Q, Kappes J, et al. A synonymous single nucleotide polymorphism in DeltaF508 CFTR alters the secondary structure of the mRNA and the expression of the mutant protein. J Biol Chem. 2010;285: 28741–8. doi: 10.1074/jbc.M110.15457520628052
27. Sauna ZE, Kimchi-Sarfaty C, Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2011;12: 683–91. doi: 10.1038/nrg305121878961
28. Hunt RC, Simhadri VL, Iandoli M, Sauna ZE, Kimchi-Sarfaty C, Exposing synonymous mutations. Trends Genet. 2014;30: 308–21. doi: 10.1016/j.tig.2014.04.00624954581
29. Gingold H, Pilpel Y, Determinants of translation efficiency and accuracy. Mol Syst Biol. 2011;7: 481. doi: 10.1038/msb.2011.1421487400
30. Plotkin JB, Kudla G, Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet. 2011;12: 32–42. doi: 10.1038/nrg289921102527
31. Goodenbour JM, Pan T, Diversity of tRNA genes in eukaryotes. Nucleic Acids Res. 2006;34: 6137–6146. doi: 10.1093/nar/gkl72517088292
32. Bermudez-Santana C, Attolini CS-O, Kirsten T, Engelhardt J, Prohaska SJ, Steigele S, et al. Genomic organization of eukaryotic tRNAs. BMC Genomics. 2010;11: 270. doi: 10.1186/1471-2164-11-27020426822
33. RajBhandary UL, Köhrer C, Early days of tRNA research: discovery, function, purification and sequence analysis. J Biosci. 2006;31: 439–51. Available: http://www.ncbi.nlm.nih.gov/pubmed/1720606417206064
34. Schramm L, Hernandez N, Recruitment of RNA polymerase III to its target promoters. Genes Dev. 2002;16: 2593–620. doi: 10.1101/gad.101890212381659
35. Ciliberto G, Traboni C, Cortese R, Relationship between the two components of the split promoter of eukaryotic tRNA genes. Proc Natl Acad Sci U S A. 1982;79: 1921–5. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=346093&tool=pmcentrez&rendertype=abstract6952243
36. Sharp S, Dingermann T, Söll D, The minimum intragenic sequences required for promotion of eukaryotic tRNA gene transcription. Nucleic Acids Res. 1982;10: 5393–5406. doi: 10.1093/nar/10.18.53936924209
37. Bloom-Ackermann Z, Navon S, Gingold H, Towers R, Pilpel Y, Dahan O, A comprehensive tRNA deletion library unravels the genetic architecture of the tRNA pool. PLoS Genet. 2014;10: e1004084. doi: 10.1371/journal.pgen.100408424453985
38. Geslain R, Pan T, Functional analysis of human tRNA isodecoders. J Mol Biol. 2010;396: 821–31. doi: 10.1016/j.jmb.2009.12.01820026070
39. Sharp SJ, Schaack J, Cooley L, Burke DJ, Söll D, Structure and transcription of eukaryotic tRNA genes. CRC Crit Rev Biochem. 1985;19: 107–44. Available: http://www.ncbi.nlm.nih.gov/pubmed/39052543905254
40. Ishimura R, Nagy G, Dotu I, Zhou H, Yang X-L, Schimmel P, et al. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science. 2014;345: 455–9. doi: 10.1126/science.124974925061210
41. Kondo K, Makovec B, Waterston RH, Hodgkin J, Genetic and molecular analysis of eight tRNA(Trp) amber suppressors in Caenorhabditis elegans. J Mol Biol. 1990;215: 7–19. doi: 10.1016/S0022-2836(05)80090-72398498
42. Kutter C, Brown GD, Gonçalves A, Wilson MD, Watt S, Brazma A, et al. Pol III binding in six mammals shows conservation among amino acid isotypes despite divergence among tRNA genes. Nat Genet. 2011;43: 948–55. doi: 10.1038/ng.90621873999
43. Zheng G, Qin Y, Clark WC, Dai Q, Yi C, He C, et al. Efficient and quantitative high-throughput tRNA sequencing. Nat Methods. 2015;12: 835–7. doi: 10.1038/nmeth.347826214130
44. Cozen AE, Quartley E, Holmes AD, Hrabeta-Robinson E, Phizicky EM, Lowe TM, ARM-seq: AlkB-facilitated RNA methylation sequencing reveals a complex landscape of modified tRNA fragments. Nat Methods. 2015;12: 879–84. doi: 10.1038/nmeth.350826237225
45. Pang YLJ, Abo R, Levine SS, Dedon PC, Diverse cell stresses induce unique patterns of tRNA up- and down-regulation: tRNA-seq for quantifying changes in tRNA copy number. Nucleic Acids Res. 2014;42: e170. doi: 10.1093/nar/gku94525348403
46. Kondo K, Hodgkin J, Waterston RH, Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans. Mol Cell Biol. 1988;8: 3627–35. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=365418&tool=pmcentrez&rendertype=abstract3221861
47. Hodgkin J, Novel nematode amber suppressors. Genetics. 1985;111: 287–310. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1202644&tool=pmcentrez&rendertype=abstract17246299
48. Li L, Linning RM, Kondo K, Honda BM, Differential Expression of Individual Suppressor tRNATrp Gene Family Members In Vitro and In Vivo in the Nematode Caenorhabditis elegans. Mol Cell Biol. 1998;18: 703–709. Available: http://mcb.asm.org/content/18/2/703.full9447966
49. Waterston RH, A second informational suppressor, SUP-7 X, in Caenorhabditis elegans. Genetics. 1981;97: 307–25. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1214395&tool=pmcentrez&rendertype=abstract7274656
50. Greiss S, Chin JW, Expanding the genetic code of an animal. J Am Chem Soc. 2011;133: 14196–9. doi: 10.1021/ja205403421819153
51. Longman D, Plasterk RHA, Johnstone IL, Cáceres JF, Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes Dev. 2007;21: 1075–85. doi: 10.1101/gad.41770717437990
52. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science. 2010;330: 1775–87. doi: 10.1126/science.119691421177976
53. Araya CL, Kawli T, Kundaje A, Jiang L, Wu B, Vafeados D, et al. Regulatory analysis of the C. elegans genome with spatiotemporal resolution. Nature. Nature Publishing Group; 2014;512: 400–5. doi: 10.1038/nature1349725164749
54. Barski A, Chepelev I, Liko D, Cuddapah S, Fleming AB, Birch J, et al. Pol II and its associated epigenetic marks are present at Pol III-transcribed noncoding RNA genes. Nat Struct Mol Biol. 2010;17: 629–34. doi: 10.1038/nsmb.180620418881
55. Hodgkin Jonathan. Genetic suppression. WormBook, ed The C elegans Research Community. 2005. Available: http://www.wormbook.org/chapters/www_geneticsuppression/geneticsuppression.html#d0e73
56. Sánchez-Blanco A, Kim SK, Variable pathogenicity determines individual lifespan in Caenorhabditis elegans. PLoS Genet. Public Library of Science; 2011;7: e1002047. doi: 10.1371/journal.pgen.100204721533182
57. Gami MS, Wolkow CA, Studies of Caenorhabditis elegans DAF-2/insulin signaling reveal targets for pharmacological manipulation of lifespan. Aging Cell. 2006;5: 31–7. doi: 10.1111/j.1474-9726.2006.00188.x16441841
58. Fire A, Integrative transformation of Caenorhabditis elegans. EMBO J. 1986;5: 2673–80. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1167168&tool=pmcentrez&rendertype=abstract16453714
59. Dixon DK, Jones D, Candido EP, The differentially expressed 16-kD heat shock genes of Caenorhabditis elegans exhibit differential changes in chromatin structure during heat shock. DNA Cell Biol. 1990;9: 177–91. Available: http://www.ncbi.nlm.nih.gov/pubmed/21602462160246
60. Dittmar K a, Mobley EM, Radek AJ, Pan T, Exploring the regulation of tRNA distribution on the genomic scale. J Mol Biol. 2004;337: 31–47. doi: 10.1016/j.jmb.2004.01.02415001350
61. Braglia P, Percudani R, Dieci G, Sequence context effects on oligo(dT) termination signal recognition by Saccharomyces cerevisiae RNA polymerase III. J Biol Chem. 2005;280: 19551–62. doi: 10.1074/jbc.M41223820015788403
62. Hernandez N, Small Nuclear RNA Genes: a Model System to Study Fundamental Mechanisms of Transcription. J Biol Chem. 2001;276: 26733–26736. doi: 10.1074/jbc.R10003220011390411
63. Giuliodori S, Percudani R, Braglia P, Ferrari R, Guffanti E, Ottonello S, et al. A composite upstream sequence motif potentiates tRNA gene transcription in yeast. J Mol Biol. 2003;333: 1–20. Available: http://www.ncbi.nlm.nih.gov/pubmed/1451673914516739
64. Zhang H, A C. elegans mediator protein confers regulatory selectivity on lineage-specific expression of a transcription factor gene. Genes Dev. 2000;14: 2161–2172. doi: 10.1101/gad.81470010970880
65. Thompson DM, Parker R, Stressing out over tRNA cleavage. Cell. 2009;138: 215–9. doi: 10.1016/j.cell.2009.07.00119632169
66. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P, Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell. 2011;43: 613–23. doi: 10.1016/j.molcel.2011.06.02221855800
67. Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science. 2015; science.aad7977–. doi: 10.1126/science.aad7977
68. Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science (80-). 2015; science.aad6780–. doi: 10.1126/science.aad6780
69. Maute RL, Schneider C, Sumazin P, Holmes A, Califano A, Basso K, et al. tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. Proc Natl Acad Sci U S A. 2013;110: 1404–9. doi: 10.1073/pnas.120676111023297232
70. Westholm JO, Lai EC, Mirtrons: microRNA biogenesis via splicing. Biochimie. 2011;93: 1897–904. doi: 10.1016/j.biochi.2011.06.01721712066
71. Gingold H, Dahan O, Pilpel Y, Dynamic changes in translational efficiency are deduced from codon usage of the transcriptome. Nucleic Acids Res. 2012;40: 10053–63. doi: 10.1093/nar/gks77222941644
72. Budovskaya Y V, Wu K, Southworth LK, Jiang M, Tedesco P, Johnson TE, et al. An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell. 2008;134: 291–303. doi: 10.1016/j.cell.2008.05.04418662544
73. Rechavi O, Kloog Y, Prion and anti-codon usage: does infectious PrP alter tRNA abundance to induce misfolding of PrP?Med Hypotheses. Elsevier Ltd; 2009;72: 193–5. doi: 10.1016/j.mehy.2008.07.05118809261
74. Brenner S, The genetics of Caenorhabditis elegans. Genetics. 1974;77: 71–94. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1213120&tool=pmcentrez&rendertype=abstract4366476
75. Kramer JM, French RP, Park EC, Johnson JJ, The Caenorhabditis elegans rol-6 gene, which interacts with the sqt-1 collagen gene to determine organismal morphology, encodes a collagen. Mol Cell Biol. 1990;10: 2081–9. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=360555&tool=pmcentrez&rendertype=abstract1970117
76. The Nematode Caenorhabditis elegans [Internet]. ed Wood WB (Cold Spring Harbor Lab Press, New York); 1988. Available: http://www.cshlpress.com/default.tpl?cart=1437563175311703908&fromlink=T&linkaction=full&linksortby=oop_title&—eqSKUdatarq=39
77. Volovik Y, Maman M, Dubnikov T, Bejerano-Sagie M, Joyce D, Kapernick EA, et al. Temporal requirements of heat shock factor-1 for longevity assurance. Aging Cell. 2012;11: 491–9. doi: 10.1111/j.1474-9726.2012.00811.x22360389
78. Davis MW, Morton JJ, Carroll D, Jorgensen EM, Gene activation using FLP recombinase in C. elegans. PLoS Genet. Public Library of Science; 2008;4: e1000028. doi: 10.1371/journal.pgen.100002818369447
79. Chan PP, Lowe TM, GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res. 2009;37: D93–7. doi: 10.1093/nar/gkn78718984615
80. Rozowsky J, Euskirchen G, Auerbach RK, Zhang ZD, Gibson T, Bjornson R, et al. PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat Biotechnol. Nature Publishing Group; 2009;27: 66–75. doi: 10.1038/nbt.151819122651
81. Liu T, Rechtsteiner A, Egelhofer TA, Vielle A, Latorre I, Cheung M-S, et al. Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res. Cold Spring Harbor Laboratory Press; 2011;21: 227–36. doi: 10.1101/gr.115519.11021177964