Genomic evidence for elevated mutation rates in highly expressed genes

EMBO Reports

Volumn 13, Issue 12, 2012, Pages 1123-1129

  Park, Chungoo ^a   Qian, Wenfeng ^a   Zhang, Jianzhi ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

gene expression; human; Mutation rate; transcription; yeast

Indexed keywords

ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA STRAND; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; GENOME; GERM LINE; HUMAN; HUMAN TISSUE; MUTAGENESIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; REPORTER GENE; TRANSCRIPTION ASSOCIATED MUTAGENESIS;

GENE EXPRESSION REGULATION; GENOME, FUNGAL; GERM-LINE MUTATION; HUMANS; MUTAGENESIS; MUTATION RATE; POINT MUTATION; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC;

EID: 84870627323     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2012.165     Document Type: Article

References (56)

1. Hodgkinson A, Eyre-Walker A (2011) Variation in the mutation rate across mammalian genomes. Nat Rev Genet 12: 756-766
2. Lang GI, Murray AW (2011) Mutation rates across budding yeast chromosome VI are correlated with replication timing. Genome Biol Evol 3: 799-811
3. Stamatoyannopoulos JA, Adzhubei I, Thurman RE, Kryukov GV, Mirkin SM, Sunyaev SR (2009) Human mutation rate associated with DNA replication timing. Nat Genet 41: 393-395
4. Chen X, Chen Z, Chen H, Su Z, Yang J, Lin F, Shi S, He X (2012) Nucleosomes suppress spontaneous mutations base-specifically in eukaryotes. Science 335: 1235-1238
5. Kim N, Jinks-Robertson S (2012) Transcription as a source of genome instability. Nat Rev Genet 13: 204-214
6. Aguilera A (2002) The connection between transcription and genomic instability. EMBO J 21: 195-201 (Pubitemid 34137281)
7. Svejstrup JQ (2002) Mechanisms of transcription-coupled DNA repair. Nat Rev Mol Cell Biol 3: 21-29 (Pubitemid 135709915)
8. Hanawalt PC, Spivak G (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9: 958-970
9. Savic DJ, Kanazir DT (1972) The effect of a histidine operator-constitutive mutation on UV-induced mutability within the histidine operon of Salmonella typhimurium. Mol Gen Genet 118: 45-50
10. Herman RK, Dworkin NB (1971) Effect of gene induction on the rate of mutagenesis by ICR-191 in Escherichia coli. J Bacteriol 106: 543-550
11. Beletskii A, Bhagwat AS (1996) Transcription-induced mutations: increase in C to T mutations in the nontranscribed strand during transcription in Escherichia coli. Proc Natl Acad Sci USA 93: 13919-13924 (Pubitemid 26424221)
12. Takahashi T, Burguiere-Slezak G, Van der Kemp PA, Boiteux S (2011) Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 108: 692-697
13. Datta A, Jinks-Robertson S (1995) Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268: 1616-1619
14. Kim N, Jinks-Robertson S (2009) dUTP incorporation into genomic DNA is linked to transcription in yeast. Nature 459: 1150-1153
15. Lippert MJ, Kim N, Cho JE, Larson RP, Schoenly NE, O'Shea SH, Jinks-Robertson S (2011) Role for topoisomerase 1 in transcriptionassociated mutagenesis in yeast. Proc Natl Acad Sci USA 108: 698-703
16. Hendriks G, Calleja F, Besaratinia A, Vrieling H, Pfeifer GP, Mullenders LH, Jansen JG, de Wind N (2010) Transcription-dependent cytosine deamination is a novel mechanism in ultraviolet light-induced mutagenesis. Curr Biol 20: 170-175
17. Lynch M et al (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci USA 105: 9272-9277
18. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349 (Pubitemid 351929471)
19. Gojobori T, Li WH, Graur D (1982) Patterns of nucleotide substitution in pseudogenes and functional genes. J Mol Evol 18: 360-369 (Pubitemid 12023396)
20. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241-254 (Pubitemid 40852689)
21. Qian W, Yang JR, Pearson NM, Maclean C, Zhang J (2012) Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genet 8: e1002603
22. Hershberg R, Petrov DA (2008) Selection on codon bias. Annu Rev Genet 42: 287-299
23. Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134: 341-352 (Pubitemid 352010328)
24. Pal C, Papp B, Hurst LD (2001) Highly expressed genes in yeast evolve slowly. Genetics 158: 927-931 (Pubitemid 32552328)
25. Yang JR, Liao BY, Zhuang SM, Zhang J (2012) Protein misinteraction avoidance causes highly expressed proteins to evolve slowly. Proc Natl Acad Sci USA 109: E831-E840
26. Parenteau J, Durand M, Morin G, Gagnon J, Lucier JF, Wellinger RJ, Chabot B, Elela SA (2011) Introns within ribosomal protein genes regulate the production and function of yeast ribosomes. Cell 147: 320-331
27. Juneau K, Miranda M, Hillenmeyer ME, Nislow C, Davis RW (2006) Introns regulate RNA and protein abundance in yeast. Genetics 174: 511-518 (Pubitemid 44427691)
28. Hwang DG, Green P (2004) Bayesian Markov chain Monte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution. Proc Natl Acad Sci USA 101: 13994-14001 (Pubitemid 39305018)
29. Washietl S, Machne R, Goldman N (2008) Evolutionary footprints of nucleosome positions in yeast. Trends Genet 24: 583-587
30. Mugal CF, von Grunberg HH, Peifer M (2009) Transcription-induced mutational strand bias and its effect on substitution rates in human genes. Mol Biol Evol 26: 131-142
31. Fujita PA et al (2011) The UCSC Genome Browser database: update 2011. Nucleic Acids Res 39: D876-D882
32. Xiong Y, Chen X, Chen Z, Wang X, Shi S, Wang X, Zhang J, He X (2010) RNA sequencing shows no dosage compensation of the active X-chromosome. Nat Genet 42: 1043-1047
33. Brawand D et al (2011) The evolution of gene expression levels in mammalian organs. Nature 478: 343-348
34. Polak P, Arndt PF (2008) Transcription induces strand-specific mutations at the 5' end of human genes. Genome Res 18: 1216-1223
35. Green P, Ewing B, Miller W, Thomas PJ, Green ED (2003) Transcriptionassociated mutational asymmetry in mammalian evolution. Nat Genet 33: 514-517 (Pubitemid 36390015)
36. Cho RJ et al (1998) A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 2: 65-73 (Pubitemid 128378967)
37. Hoede C, Denamur E, Tenaillon O (2006) Selection acts on DNA secondary structures to decrease transcriptional mutagenesis. PLoS Genet 2: e176
38. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297
39. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114
40. Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH, Fink GR, Bartel DP (2009) RNAi in budding yeast. Science 326: 544-550
41. Lee W et al (2010) The mutation spectrum revealed by paired genome sequences from a lung cancer patient. Nature 465: 473-477
42. Pleasance ED et al (2010) A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 463: 191-196
43. Pleasance ED et al (2010) A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463: 184-190
44. Araten DJ, Golde DW, Zhang RH, Thaler HT, Gargiulo L, Notaro R, Luzzatto L (2005) A quantitative measurement of the human somatic mutation rate. Cancer Res 65: 8111-8117 (Pubitemid 41330573)
45. Zhang J, He X (2005) Significant impact of protein dispensability on the instantaneous rate of protein evolution. Mol Biol Evol 22: 1147-1155 (Pubitemid 40471427)
46. Kimura M (1967) On the evolutionary adjustment of spontaneous mutation rates. Genet Res 9: 23-34
47. Zhang J (2000) Protein-length distributions for the three domains of life. Trends Genet 16: 107-109 (Pubitemid 30122341)
48. Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22: 1365-1374 (Pubitemid 40734188)
49. Fraser HB, Hirsh AE, Giaever G, Kumm J, Eisen MB (2004) Noise minimization in eukaryotic gene expression. PLoS Biol 2: e137
50. Wang Z, Zhang J (2011) Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc Natl Acad Sci USA 108: E67-E76
51. Yang JR, Zhuang SM, Zhang J (2010) Impact of translational errorinduced and error-free misfolding on the rate of protein evolution. Mol Syst Biol 6: 421
52. Cherry JL (2010) Expression level, evolutionary rate, and the cost of expression. Genome Biol Evol 2: 757-769
53. Gout JF, Kahn D, Duret L (2010) The relationship among gene expression, the evolution of gene dosage, and the rate of protein evolution. PLoS Genet 6: e1000944
54. Martincorena I, Seshasayee AS, Luscombe NM (2012) Evidence of nonrandom mutation rates suggests an evolutionary risk management strategy. Nature 485: 95-98
55. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591 (Pubitemid 47236688)
56. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120 (Pubitemid 11166431)