Transcription-Associated mutagenesis

Annual Review of Genetics

Volumn 48, Issue , 2014, Pages 341-359

  Jinks Robertson, Sue ^a   Bhagwat, Ashok S ^b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

Author keywords

class switch recombination; cytosine deamination; DNA damage; somatic hypermutation; topoisomerase

Indexed keywords

DNA TOPOISOMERASE; MESSENGER RNA; MUTAGENIC AGENT; THYMINE; URACIL; SINGLE STRANDED DNA;

ARTICLE; BACTERIUM; CELL STRESS; DNA DAMAGE; DNA STRAND; DNA TRANSCRIPTION; EUKARYOTE; GENE REARRANGEMENT; MUTAGENESIS; NONHUMAN; RNA REPLICATION; RNA TRANSCRIPTION; SOMATIC HYPERMUTATION; STARVATION; STRESS; YEAST; DNA REPLICATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; SACCHAROMYCETALES;

BACTERIA; DNA DAMAGE; DNA REPLICATION; DNA, SINGLE-STRANDED; HUMANS; MUTAGENESIS; SACCHAROMYCETALES; TRANSCRIPTION, GENETIC;

EID: 84913596602     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-120213-092015     Document Type: Article

References (114)

1. Aguilera A, Garcia-Muse T. 2012. R loops: from transcription byproducts to threats to genome stability. Mol. Cell 46:115-24
2. Alexander MP, Begins KJ, Crall WC, Holmes MP, Lippert MJ. 2013. High levels of transcription stimulate transversions at GC base pairs in yeast. Environ. Mol. Mutagen. 54:44-53
3. Arakawa H, Hauschild J, Buerstedde JM. 2002. Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science 295:1301-6
4. Azvolinsky A, Giresi PG, Lieb JD, Zakian VA. 2009. Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol. Cell 34:722-34
5. Basu U, Meng FL, Keim C, Grinstein V, Pefanis E, et al. 2011. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell 144:353-63
6. 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 93:13919-24
7. Belotserkovskii BP, Mirkin SM, Hanawalt PC. 2013. DNA sequences that interfere with transcription: implications for genome function and stability. Chem. Rev. 113:8620-37
8. Bemark M, Neuberger MS. 2000. The c-MYC allele that is translocated into the IgH locus undergoes constitutive hypermutation in a Burkitt's lymphoma line. Oncogene 19:3404-10
9. Boiteux S, Jinks-Robertson S. 2013. DNA repair mechanisms and the bypass of DNA damage in Saccharomyces cerevisiae. Genetics 193:1025-64
10. Bransteitter R, Pham P, Scharff MD, Goodman MF. 2003. Activation-induced cytidine deaminase deaminates deoxycytidine on single-strandedDNAbut requires the action of RNase. Proc. Natl. Acad. Sci. USA 100:4102-7
11. Burkala E, Reimers JM, Schmidt KH, Davis N, Wei P, Wright BE. 2007. Secondary structures as predictors of mutation potential in the lacZ gene of Escherichia coli. Microbiology 153:2180-89
12. Burns MB, Lackey L, Carpenter MA, Rathore A, Land AM, et al. 2013. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494:366-70
13. Cerritelli SM, Crouch RJ. 2009. Ribonuclease H: the enzymes in eukaryotes. FEBS J. 276:1494-505
14. Chaudhuri J, Tian M, Khuong C, Chua K, Pinaud E, Alt FW. 2003. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422:726-30
15. Cho JE, Kim N, Li YC, Jinks-Robertson S. 2013. Two distinct mechanisms of topoisomerase 1-dependent mutagenesis in yeast. DNA Repair 12:205-11
16. Datta A, Jinks-Robertson S. 1995. Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268:1616-19
17. Davis BD. 1989. Transcriptional bias: a non-Lamarckian mechanism for substrate-induced mutations. Proc. Natl. Acad. Sci. USA 86:5005-9
18. de Morgan A, Brodsky L, Ronin Y, Nevo E, Korol A, Kashi Y. 2010. Genome-wide analysis of DNA turnover and gene expression in stationary-phase Saccharomyces cerevisiae. Microbiology 156:1758-71
19. Deshpande AM, Newlon CS. 1996. DNA replication fork pause sites dependent on transcription. Science 272:1030-33
20. Dickerson SK, Market E, Besmer E, Papavasiliou FN. 2003. AID mediates hypermutation by deaminating single stranded DNA. J. Exp. Med. 197:1291-96
21. Duquette ML, Handa P, Vincent JA, Taylor AF, Maizels N. 2004. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev. 18:1618-29
22. Duquette ML, Pham P, Goodman MF, Maizels N. 2005. AID binds to transcription-induced structures in c-MYC that map to regions associated with translocation and hypermutation. Oncogene 24:5791-98
23. Eddy J, Vallur AC, Varma S, Liu H, Reinhold WC, et al. 2011. G4 motifs correlate with promoterproximal transcriptional pausing in human genes. Nucleic Acids Res. 39:4975-83
24. ENCODE Proj. Consort. , Bernstein BE, Birney E, Dunham I, Green ED, et al. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:57-74
25. Fix D, Canugovi C, Bhagwat AS. 2008. Transcription increases methylmethane sulfonate-induced mutations in alkB strains of Escherichia coli. DNA Repair 7:1289-97
26. Fix DF, Glickman BW. 1987. Asymmetric cytosine deamination revealed by spontaneous mutational specificity in an Ung-strain of Escherichia coli. Mol. Gen. Genet. 209:78-82
27. Fraenkel S, Mostoslavsky R, Novobrantseva TI, Pelanda R, Chaudhuri J, et al. 2007. Allelic "choice" governs somatic hypermutation in vivo at the immunoglobulin kappa-chain locus. Nat. Immunol. 8:715-22
28. Francino MP, Chao L, Riley MA, Ochman H. 1996. Asymmetries generated by transcription-coupled repair in enterobacterial genes. Science 272:107-9
29. Francino MP, Ochman H. 2001. Deamination as the basis of strand-Asymmetric evolution in transcribed Escherichia coli sequences. Mol. Biol. Evol. 18:1147-50
30. Frederico LA, Kunkel TA, Shaw BR. 1990. A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry 29:2532-37
31. Galhardo RS, Hastings PJ, Rosenberg SM. 2007. Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 42:399-435
32. Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD. 2001. Structural basis of transcription: an RNA polymerase II elongation complex at 3. 3A? resolution. Science 292:1876-82
33. Gomez-Gonzalez B, Aguilera A. 2007. Activation-induced cytidine deaminase action is strongly stimulated by mutations of the THO complex. Proc. Natl. Acad. Sci. USA 104:8409-14
34. Gowrishankar J, Harinarayanan R. 2004. Why is transcription coupled to translation in bacteria? Mol. Microbiol. 54:598-603
35. Green P, Ewing B, Miller W, Thomas PJ, Green ED, NISC Comp. Seq. , 2003. Transcription-Associated mutational asymmetry in mammalian evolution. Nat. Genet. 33:514-17
36. Hanawalt PC, Spivak G. 2008. Transcription-coupledDNArepair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 9:958-70
37. Harris RS, Sale JE, Petersen-Mahrt SK, Neuberger MS. 2002. AID is essential for immunoglobulin V gene conversion in a cultured B cell line. Curr. Biol. 12:435-38
38. Hartzog GA, Fu J. 2013. The Spt4-Spt5 complex: a multi-faceted regulator of transcription elongation. Biochim. Biophys. Acta 1829:105-15
39. Heidenreich E. 2007. Adaptive mutation in Saccharomyces cerevisiae. Crit. Rev. Biochem. Mol. Biol. 42:285-311
40. Helmrich A, Ballarino M, Nudler E, Tora L. 2013. Transcription-replication encounters, consequences and genomic instability. Nat. Struct. Mol. Biol. 20:412-18
41. Helmrich A, Ballarino M, Tora L. 2011. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 44:966-77
42. Hendriks G, Calleja F, Besaratinia A, Vrieling H, Pfeifer GP, et al. 2010. Transcription-dependent cytosine deamination is a novel mechanism in ultraviolet light-induced mutagenesis. Curr. Biol. 20:170-75
43. Herman RK, Dworkin NB. 1971. Effect of gene induction on the rate of mutagenesis by ICR-191 in Escherichia coli. J. Bacteriol. 106:543-50
44. Hicks WM, Kim M, Haber JE. 2010. Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329:82-85
45. Hinnebusch AG. 1992. General and pathway-specific regulatory mechanisms controlling the synthesis of amino acid biosynthesis enzymes in Saccharomyces cerevisiae. In TheMolecular and Cellular Biology of the Yeast Saccharomyces: Gene Expression, ed. EW Jones, JR Pringle, JR Broach, pp. 319-414. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
46. Hudson RE, Bergthorsson U, Ochman H. 2003. Transcription increases multiple spontaneous point mutations in Salmonella enterica. Nucleic Acids Res. 31:4517-22
47. Kanehiro Y, Todo K, Negishi M, Fukuoka J, Gan W, et al. 2012. Activation-induced cytidine deaminase (AID)-dependent somatic hypermutation requires a splice isoform of the serine/arginine-rich (SR) protein SRSF1. Proc. Natl. Acad. Sci. USA 109:1216-21
48. Kim N, Abdulovic AL, Gealy R, Lippert MJ, Jinks-Robertson S. 2007. Transcription-Associated mutagenesis in yeast is directly proportional to the level of gene expression and influenced by the direction of DNA replication. DNA Repair 6:1285-96
49. Kim N, Cho JE, Li YC, Jinks-Robertson S. 2013. RNA:DNA hybrids initiate quasi-palindromeassociated mutations in highly transcribed yeast DNA. PLoS Genet. 9:e1003924
50. Kim N, Jinks-Robertson S. 2009. dUTP incorporation into genomic DNA is linked to transcription in yeast. Nature 459:1150-53
51. Kim N, Jinks-Robertson S. 2010. Abasic sites in the transcribed strand of yeast DNA are removed by transcription-coupled nucleotide excision repair. Mol. Cell. Biol. 30:3206-15
52. Klapacz J, Bhagwat AS. 2002. Transcription-dependent increase in multiple classes of base substitution mutations in Escherichia coli. J. Bacteriol. 184:6866-72
53. Klapacz J, Bhagwat AS. 2005. Transcription promotes guanine to thymine mutations in the nontranscribed strand of an Escherichia coli gene. DNA Repair 4:806-13
54. Kobayashi M, Sabouri Z, Sabouri S, Kitawaki Y, Pommier Y, et al. 2011. Decrease in topoisomerase I is responsible for activation-induced cytidine deaminase (AID)-dependent somatic hypermutation. Proc. Natl. Acad. Sci. USA 108:19305-10
55. Korogodin VI, Korogodin VL, Fajszi C, Chepurnoy AI, Mikhova-Tsenova N, Simonyan NV. 1991. On the dependence of spontaneous mutation rates on the functional state of genes. Yeast 7:105-17
56. Larijani M, Martin A. 2012. The biochemistry of activation-induced deaminase and its physiological functions. Semin. Immunol. 24:255-63
57. Li G, Zan H, Xu Z, Casali P. 2013. Epigenetics of the antibody response. Trends Immunol. 34:460-70
58. Li X, Manley JL. 2006. Cotranscriptional processes and their influence on genome stability. Genes Dev. 20:1838-47
59. Lin Y, Hubert L Jr, Wilson JH. 2009. Transcription destabilizes triplet repeats. Mol. Carcinog. 48:350-61
60. Lippert MJ, Chen Q, Liber HL. 1998. Increased transcription decreases the spontaneous mutation rate at the thymidine kinase locus in human cells. Mutat. Res. 401:1-10
61. Lippert MJ, Freedman JA, Barber MA, Jinks-Robertson S. 2004. Identification of a distinctive mutation spectrum associated with high levels of transcription in yeast. Mol. Cell. Biol. 24:4801-9 .
62. Lippert MJ, Kim N, Cho JE, Larson RP, Schoenly NE, et al. 2011. Role for topoisomerase 1 in transcription-Associated mutagenesis in yeast. Proc. Natl. Acad. Sci. USA 108:698-703
63. Liu LF, Wang JC. 1987. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84:7024-27
64. Liu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC, et al. 2008. Two levels of protection for the B cell genome during somatic hypermutation. Nature 451:841-45
65. Masani S, Han L, Yu K. 2013. Apurinic/apyrimidinic endonuclease 1 is the essential nuclease during immunoglobulin class switch recombination. Mol. Cell Biol. 33:1468-73
66. Merrikh H, Zhang Y, Grossman AD, Wang JD. 2012. Replication-transcription conflicts in bacteria. Nat. Rev. Microbiol. 10:449-58
67. Morey NJ, Greene CN, Jinks-Robertson S. 2000. Genetic analysis of transcription-Associated mutation in Saccharomyces cerevisiae. Genetics 154:109-20
68. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553-63
69. Nagaoka H, Muramatsu M, Yamamura N, Kinoshita K, Honjo T. 2002. Activation-induced deaminase (AID)-directed hypermutation in the immunoglobulin Sμregion: implication of AID involvement in a common step of class switch recombination and somatic hypermutation. J. Exp. Med. 195:529-34
70. Nambu Y, Sugai M, Gonda H, Lee CG, Katakai T, et al. 2003. Transcription-coupled events associating with immunoglobulin switch region chromatin. Science 302:2137-40
71. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, et al. 2012. Mutational processes molding the genomes of 21 breast cancers. Cell 149:979-93
72. Palombo F, Kohfeldt E, Calcagnile A, Nehls P, Dogliotti E. 1992. N-methyl-N-nitrosourea-induced mutation in human cells: effects of the transcriptional activity of the target gene. J. Mol. Biol. 223:587-94
73. Papantonis A, Cook PR. 2013. Transcription factories: genome organization and gene regulation. Chem. Rev. 113:8683-705
74. Park C, Qian W, Zhang J. 2012. Genomic evidence for elevatedmutation rates in highly expressed genes. EMBO Rep. 13:1123-29
75. Pasqualucci L, Migliazza A, Fracchiolla N, William C, Neri A, et al. 1998. BCL-6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc. Natl. Acad. Sci. USA 95:11816-21
76. Paul S, Million-Weaver S, Chattopadhyay S, Sokurenko E, Merrikh H. 2013. Accelerated gene evolution through replication-transcription conflicts. Nature 495:512-15
77. Pavri R, Gazumyan A, Jankovic M, Di Virgilio M, Klein I, et al. 2010. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell 143:122-33
78. Peterlin BM, Price DH. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23:297-305
79. Polak P, Querfurth R, Arndt PF. 2010. The evolution of transcription-Associated biases of mutations across vertebrates. BMC Evol. Biol. 10:187
80. Prado F, Aguilera A. 2005. Impairment of replication fork progression mediatesRNApolII transcriptionassociated recombination. EMBO J. 24:1267-76
81. Pybus C, Pedraza-Reyes M, Ross CA, Martin H, Ona K, et al. 2010. Transcription-Associated mutation in Bacillus subtilis cells under stress. J. Bacteriol. 192:3321-28
82. Reimers JM, Schmidt KH, Longacre A, Reschke DK, Wright BE. 2004. Increased transcription rates correlatewith increased reversion rates in leuB and argH Escherichia coli auxotrophs. Microbiology 150:1457-66
83. Roberts SA, Gordenin DA. 2014. Clustered and genome-wide transient mutagenesis in human cancers: hypermutation without permanent mutators or loss of fitness. BioEssays 36:382-93
84. Roberts SA, Sterling J, Thompson C, Harris S, Mav D, et al. 2012. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol. Cell 46:424-35
85. Sakofsky CJ, Roberts SA, Malc E, Mieczkowski PA, Resnick MA, et al. 2014. Break-induced replication is a source of mutation clusters underlying kataegis. Cell Rep. 7:1640-48
86. Samaranayake M, Bujnicki JM, Carpenter M, Bhagwat AS. 2006. Evaluation of molecular models for the affinity maturation of antibodies: roles of cytosine deamination by AID and DNA repair. Chem. Rev. 106:700-19
87. 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
88. Schmidt KH, Reimers JM, Wright BE. 2006. The effect of promoter strength, supercoiling and secondary structure on mutation rates in Escherichia coli. Mol. Microbiol. 60:1251-61
89. Shen HM, Tanaka A, Bozek G, Nicolae D, Storb U. 2006. Somatic hypermutation and class switch recombination in Msh6?/?Ung?/? double-knockout mice. J. Immunol. 177:5386-92
90. Smith HC, Bennett RP, Kizilyer A, McDougall WM, Prohaska KM. 2012. Functions and regulation of the APOBEC family of proteins. Semin. Cell Dev. Biol. 23:258-68
91. Sohail A, Klapacz J, Samaranayake M, Ullah A, Bhagwat AS. 2003. Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations. Nucleic Acids Res. 31:2990-94
92. Sparks JL, Chon H, Cerritelli SM, Kunkel TA, Johansson E, et al. 2012. RNase H2-initiated ribonucleotide excision repair. Mol. Cell 47:980-86
93. Srivatsan A, Tehranchi A, MacAlpine DM, Wang JD. 2010. Co-orientation of replication and transcription preserves genome integrity. PLoS Genet. 6:e1000810
94. Storb U. 2014. Why does somatic hypermutation by AID require transcription of its target genes? Adv. Immunol. 122:253-77
95. Storb U, Shen HM, Michael N, Kim N. 2001. Somatic hypermutation of immunoglobulin and nonimmunoglobulin genes. Philos. Trans. R. Soc. Lond. B 356:13-19
96. Strathern JN, Shafer B, McGill CB. 1995. DNA synthesis errors associated with double-strand-break repair. Genetics 140:965-72 .
97. 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 108:692-97
98. Wang JC. 2002. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3:430-40
99. Wang X, Fan M, Kalis S, Wei L, Scharff MD. 2014. A source of the single-stranded DNA substrate for activation-induced deaminase during somatic hypermutation. Nat. Commun. 5:4137
100. Westover KD, Bushnell DA, Kornberg RD. 2004. Structural basis of transcription: separation of RNA from DNA by RNA polymerase II. Science 303:1014-16
101. Wimberly H, Shee C, Thornton PC, Sivaramakrishnan P, Rosenberg SM, Hastings PJ. 2013. R-loops and nicks initiate DNA breakage and genome instability in non-growing Escherichia coli. Nat. Commun. 4:2115
102. Woo CJ, Martin A, Scharff MD. 2003. Induction of somatic hypermutation is associated with modifications in immunoglobulin variable region chromatin. Immunity 19:479-89
103. Wright BE. 1996. The effect of the stringent response on mutation rates in Escherichia coli K-12. Mol. Microbiol. 19:213-19
104. Wright BE. 2004. Stress-directed adaptive mutations and evolution. Mol. Microbiol. 52:643-50
105. Wright BE, Longacre A, Reimers JM. 1999. Hypermutation in derepressed operons of Escherichia coli K12. Proc. Natl. Acad. Sci. USA 96:5089-94
106. Wright BE, Reschke DK, Schmidt KH, Reimers JM, Knight W. 2003. Predicting mutation frequencies in stem-loop structures of derepressed genes: implications for evolution. Mol. Microbiol. 48:429-41
107. Wright BE, Schmidt KH, Davis N, Hunt AT, Minnick MF. 2008. II. Correlations between secondary structure stability and mutation frequency during somatic hypermutation. Mol. Immunol. 45:3600-8
108. Wright BE, Schmidt KH, Hunt AT, Lodmell JS, Minnick MF, Reschke DK. 2011. The roles of transcription and genotoxins underlying p53 mutagenesis in vivo. Carcinogenesis 32:1559-67
109. Wright BE, Schmidt KH, Minnick MF, Davis N. 2008. I. VH gene transcription creates stabilized secondary structures for coordinatedmutagenesis during somatic hypermutation. Mol. Immunol. 45:3589-99
110. Xue K, Rada C, Neuberger MS. 2006. The in vivo pattern of AID targeting to immunoglobulin switch regions deduced from mutation spectra in msh2?/? ung?/? mice. J. Exp. Med. 203:2085-94
111. Yamaguchi Y, Shibata H, Handa H. 2013. Transcription elongation factorsDSIF and NELF: promoterproximal pausing and beyond. Biochim. Biophys. Acta 1829:98-104
112. Yamane A, Resch W, Kuo N, Kuchen S, Li Z, et al. 2011. Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat. Immunol. 12:62-69
113. Yu K, Roy D, Bayramyan M, Haworth IS, Lieber MR. 2005. Fine-structure analysis of activation-induced deaminase accessibility to class switch region R-loops. Mol. Cell. Biol. 25:1730-36
114. Zhang Y, Shishkin AA, Nishida Y, Marcinkowski-Desmond D, Saini N, et al. 2012. Genome-wide screen identifies pathways that govern GAA/TTC repeat fragility and expansions in dividing and nondividing yeast cells. Mol. Cell 48:254-65