Double-Strand-Break Repair, Mutagenesis, and Stress

Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria

Volumn 1, Issue , 2016, Pages 185-195

  Rogers, Elizabeth ^a   Correa, Raul ^a   Barreto, Brittany ^a   Bravo Núñez, María Angélica ^a,b   Minnick, P J ^a   Vera Cruz, Diana ^a,c   Xia, Jun ^a   Hastings, P J ^a   Rosenberg, Susan M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

DNA repair; Double stranded breaks (DSBs); Evolution; Mutation; Recombination; RpoS; Stress response

Indexed keywords

EID: 85018221699     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781119004813.ch15     Document Type: Chapter

References (92)

1. Akerlund T, Nordstrom K, Bernander R. 1995. Analysis of cell size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia coli. Journal of Bacteriology 177: 6791-6797.
2. Al Mamun AA, Lombardo MJ, Shee C, Lisewski AM, Gonzalez C, et al. 2012. Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science 338: 1344-1348.
3. Avery OT, Macleod CM, McCarty M. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from Pneumococcus Type III. The Journal of Experimental Medicine 79: 137-158.
4. Battesti A, Majdalani N, Gottesman S. 2011. The RpoS-mediated general stress response in Escherichia coli. Annual Review of Microbiology 65: 189-213.
5. Bindra RS, Crosby ME, Glazer PM. 2007. Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Reviews 26: 249-260.
6. Bos J, Zhang Q, Vyawahare S, Rogers E, Rosenberg SM, et al. 2015. Emergence of antibiotic resistance from multinucleated bacterial fila-ments. Proceedings of the National Academy of Sciences 112: 178-483.
7. Bowater R, Doherty AJ. 2006. Making ends meet: repairing breaks in bacterial DNA by non-homologous end-joining. PLoS Genetics 2: e8.
8. Brown L, Elliott T. 1996. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded bythe hfq gene. Journal of Bacteriology 178: 3763-5770.
9. Bull HJ, McKenzie GJ, Hastings PJ, Rosenberg SM. 2000. Evidence that stationary-phase hypermutation in the Escherichia coli chromosome is promoted by recombination. Genetics 154: 1427-1437.
10. Burns MB, Lackey L, Carpenter MA, Rathore A, Land AM, Leonard B, et al. 2013a. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494: 366-370.
11. Burns MB, Temiz NA, Harris RS. 2013b. Evidence for APOBEC3B mutagenesis in multiple human cancers. Nature Genetics 45: 977-983.
12. Cairns J, Foster PL. 1991. Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128: 695-701.
13. Dartigalongue C, Missiakas D, Raina S. 2001. Characterization of the Escherichia coli sigma E regulon. The Journal of Biological Chemistry 276: 20866-20875.
14. De Las Penas A, Connolly L, Gross CA. 1997. SigmaE is an essential sigma factor in Escherichia coli. Journal of Bacteriology 179: 6862-6864.
15. Demerec M. 1962. "Selfers" - attributed to unequal crossovers in Salmonella. Proceedings of the National Academy of Sciences 48: 1696-1704.
16. Dillingham MS, Kowalczykowski SC. 2008. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiology and Molecular Biology Reviews 72: 642-671.
17. Drake JW. 1993. General antimutators are improbable. Journal of Molecular Biology 229: 8-13.
18. Esposito MS, Bruschi CV. 1993. Diploid yeast cells yield homozygous spontaneous mutations. Current Genetics 23: 430-434.
19. Foster PL. 1997. Nonadaptive mutations occur on the F' episome during adaptive mutation conditions in Escherichia coli. Journal of Bacte-riology 179: 1550-1554.
20. Foster PL, Trimarchi JM, Maurer RA. 1996. Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli. Genetics 142: 25-37.
21. Frisch RL, Su Y, Thornton PC, Gibson JL, Rosenberg SM, et al. 2010. Separate DNA Pol II- and Pol IV-dependent pathways of stress-induced mutation during double-strand-break repair in Escherichia coli are controlled by RpoS. Journal of Bacteriology 192: 4694-5700.
22. Galhardo RS, Do R, Yamada M, Friedberg EC, Hastings PJ, et al. 2009. DinB upregulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. Genetics 182: 55-68.
23. Gibson JL, Lombardo MJ, Thornton PC, Hu KH, Galhardo RS, et al. 2010. The sigma(E) stress response is required for stress-induced mutation and amplification in Escherichia coli. Molecular Micro-biology 77: 415-430.
24. Gumbiner-Russo LM, Lombardo MJ, Ponder RG, Rosenberg SM. 2001. The TGV transgenic vectors for single-copy gene expression from the Escherichia coli chromosome. Gene 273: 97-104.
25. Gutierrez A, Laureti L, Crussard S, Abida H, Rodriguez-Rojas A, et al. 2013. beta-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nature Communi-cations 4: 1610.
26. Harris RS, Longerich S, Rosenberg SM. 1994. Recombination in adaptive mutation. Science 264: 258-260.
27. Harris RS, Ross KJ, Rosenberg SM. 1996. Opposing roles of the Holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation. Genetics 142:681-691.
28. Hastings PJ, Bull HJ, Klump JR, Rosenberg SM. 2000. Adaptive ampli-fication: an inducible chromosomal instability mechanism. Cell 103: 723-731.
29. Hastings PJ, Ira G, Lupski JR. 2009a. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genetics 5: e1000327.
30. Hastings PJ, Lupski JR, Rosenberg SM, Ira G. 2009b. Mechanisms of change in gene copy number. Nature Reviews Genetics 10: 551-564.
31. Hastings PJ, Slack A, Petrosino JF, Rosenberg SM. 2004. Adaptive ampli-fication and point mutation are independent mechanisms: evidence for various stress-inducible mutation mechanisms. PLoS Biology 2: e399-e399.
32. Hengge-Aronis R, Lange R, Henneberg N, Fischer D. 1993. Osmotic reg-ulation of RpoS-dependent genes in Escherichia coli. Journal of Bac-teriology 175: 259-265.
33. Hernandez SB, Cota I, Ducret A, Aussel L, Casadesus J. 2012. Adaptation and preadaptation of Salmonella enterica to bile. PLoS Genetics 8: e1002459.
34. Hershey AD, Chase M. 1952. Independent functions of viral protein and nucleic acid in growth of bacteriophage. The Journal of General Physiology 36: 39-56.
35. Ito A, May T, Kawata K, Okabe S. 2008. Significance of RpoS during maturation of Escherichia coli biofilms. Biotechnology and Bioengineering 99: 1462-1471.
36. Kabir MS, Yamashita D, Koyama S, Oshima T, Kurokawa K, et al. 2005. Cell lysis directed by sigmaE in early stationary phase and effect of induction of the rpoE gene on global gene expression in Escherichia coli. Microbiology 151: 2721-2735.
37. Kim SR, Maenhaut-Michel G, Yamada M, Yamamoto Y, Matsui K. 1997. Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proceedings of the National Academy of Sciences 94: 13792-13797.
38. Klauck E, Lingnau M, Hengge-Aronis R. 2001. Role of the response regulator RssB in sigma recognition and initiation of sigma proteolysis in Escherichia coli. Molecular Microbiology 40: 1381-1390.
39. Kogoma T. 1997. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiology and Molecular Biology Reviews 61: 212-238.
40. Kuzminov A. 1995. Collapse and repair of replication forks in Escherichia coli. Molecular Microbiology 16: 373-384.
41. Kuzminov A. 2011. Homologous recombination-experimental systems, analysis and significance. EcoSal Plus 4(2). doi:10.1128/ ecosalplus.7.2.6.
42. Lange R, Hengge-Aronis R. 1991. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Molecular Microbiology 5: 49-59.
43. Layton JC and Foster PL. 2003. Error-prone DNA polymerase IV is controlledbythe stress-response sigmafactor, RpoS, in Escherichia coli. Molecular Microbiology 50: 549-561.
44. Lederberg J, Lederberg EM. 1952. Replica plating and indirect selection of bacterial mutants. Journal of Bacteriology 63: 399-406.
45. Lee IS, Lin J, Hall HK, Bearson B, Foster JW. 1995. The stationary-phase sigma factor sigma S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Molecular Microbi-ology 17: 155-167.
46. Lee JA, Carvalho CM, Lupski JR. 2007. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131: 1235-1247.
47. Liu P, Carvalho CM, Hastings PJ, Lupski JR. 2012. Mechanisms for recurrent and complex human genomic rearrangements. Current Opinion in Genetics &Development 22: 211-220.
48. Liu P, Erez A, Nagamani SC, Dhar SU, Kolodziejska KE, et al. 2011. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 146: 889-903.
49. Lombardo MJ, Aponyi I, Rosenberg SM. 2004. General stress response regulator RpoS in adaptive mutation and amplification in Escherichia coli. Genetics 166: 669-680.
50. Luria SE, Delbruck M. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491-511.
51. Magni GE, Von Borstel RC. 1962. Different rates of spontaneous mutation during mitosis and meiosis in yeast. Genetics 47: 1097-1108.
52. Malkova A, Haber JE. 2012. Mutations arising during repair of chromosome breaks. Annual Review of Genetics 46: 455-473.
53. Mayr E. 1982. The growth of biological thought: diversity, evolution, and inheritance. Harvard, MA: Belknap Press.
54. McHenry CS. 2011. DNA replicases from a bacterial perspective. Annual Review of Biochemistry 80: 403-436.
55. McKenzie GJ, Harris RS, Lee PL, Rosenberg SM. 2000. The SOS response regulates adaptive mutation. Proceedings of the National Academy of Sciences 97: 6646-6651.
56. McKenzie GJ, Lee PL, Lombardo MJ, Hastings PJ, Rosenberg SM. 2001. SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Molecular Cell 7: 9-9.
57. McPartland A, Green L, Echols H. 1980. Control of recA gene RNA in E. coli: regulatory and signal genes. Cell 20: 731-737.
58. Merrikh H, Zhang Y, Grossman AD, Wang JD. 2012. Replication transcription conflicts in bacteria. Nature Reviews Microbiology 10: 449-458.
59. Meselson M and Stahl FW. 1958. The replication of DNA in Escherichia coli. Proceedings of the National Academy of Sciences 44: 671-682.
60. Mika F, Hengge R. 2005. A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. Genes & Development 19: 2770-2781.
61. Motamedi MR, Szigety SK, Rosenberg SM. 1999. Double-strand-break repair recombination in Escherichia coli: physical evidence for a DNA replication mechanism in vivo. Genes & Development 13: 2889-2903.
62. Muffler A, Fischer D, Altuvia S, Storz G, Hengge-Aronis R. 1996. The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. The EMBO Journal 15: 1333-1339.
63. 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(5): 979-993.
64. Nohmi T. 2006. Environmental stress and lesion-bypass DNA polymerases. Annual Review of Microbiology 60: 231-253.
65. Paszewski A, Surzycki S. 1964. "Selfers" and high mutation rate during meiosis in Ascobolus immersus. Nature 204: 809.
66. Pennington JM, Rosenberg SM. 2007. Spontaneous DNA breakage in single living Escherichia coli cells. Nature Genetics 39: 797-802.
67. Petrosino JF, Galhardo RS, Morales LD, Rosenberg SM. 2009. Stress induced beta-lactam antibiotic resistance mutation and sequences of stationary-phase mutations in the Escherichia coli chromosome. Journal of Bacteriology 191: 5881-5889.
68. Pomerantz RT, Kurth I, Goodman MF, O'Donnell ME. 2013. Preferential D-loop extension by a translesion DNA polymerase underlies error-prone recombination. Nature Structural & Molecular Biology 20: 748-755.
69. Ponder RG, Fonville NC, Rosenberg SM. 2005. A switch from highfidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Molecular Cell 19: 791-804.
70. Prieto AI, Ramos-Morales F, Casadesus J. 2006. Repair of DNA damage inducedbybile salts in Salmonella enterica. Genetics 174: 575-584.
71. Rattray AJ, Strathern JN. 2003. Error-prone DNA polymerases: when making a mistake is the only way to get ahead. Annual Review of Genetics 37: 31-66.
72. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. 2006. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biology 4: e2.
73. 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. Molecular Cell 46(4): 424-435.
74. Rosenberg SM, Longerich S, Gee P, Harris RS. 1994. Adaptive mutation by deletions in small mononucleotide repeats. Science 265:405-407.
75. Rosenberg SM, Queitsch C. 2014. Medicine. Combating evolution to fight disease. Science 343: 1088-1089.
76. Rosenberg SM, Shee C, Frisch RL, Hastings PJ. 2012. Stress-induced mutation via DNA breaks in Escherichia coli: a molecular mechanism with implications for evolution and medicine. BioEssays 34: 885-892.
77. Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y, et al. 2013. Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature 502: 389-392.
78. 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 Reports 7: 1640-1648.
79. Sassanfar M and Roberts JW. 1990. Nature of the SOS-inducing signal in Escherichia coli: the involvement of DNA replication. Journal of Molecular Biology 212: 79-96.
80. Shee C, Cox BD, Gu F, Luengas EM, Joshi MC, et al. 2013. Engineered proteins detect spontaneous DNA breakage in human and bacterial cells. eLife 2: e01222.
81. Shee C, Gibson JL, Darrow MC, Gonzalez C, Rosenberg SM. 2011. Impact of a stress-inducible switch to mutagenic repair of DNA breaks on mutation in Escherichia coli. Proceedings of the National Academy of Sciences 108: 13659-13664.
82. Shee C, Gibson JL, Rosenberg SM. 2012. Two mechanisms produce mutation hotspots at DNA breaks in Escherichia coli. Cell Reports 2: 714-721.
83. Shor E, Fox CA, Broach JR. 2013. The yeast environmental stress response regulates mutagenesis induced by proteotoxic stress. PLoS Genetics 9: e1003680.
84. Simmons LA, Foti JJ, Cohen SE, Walker GC. 2008. The SOS regulatory network. EcoSal Plus 3(1). doi:10.1128/ecosalplus.5.4.3.
85. Slack A, Thornton PC, Magner DB, Rosenberg SM, Hastings PJ. 2006. On the mechanism of gene amplification induced under stress in Escherichia coli. PLoS Genetics 2: e48-e48.
86. Smith CE, Llorente B, Symington LS. 2007. Template switching during break-induced replication. Nature 447: 102-105.
87. Strathern JN, Shafer BK, McGill CB. 1995. DNA synthesis errors associated with double-strand-break repair. Genetics 140: 965-972.
88. Tang M, Pham P, Shen X, Taylor JS, O'Donnell M, et al. 2000. Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature 404: 1014-1018.
89. Watson JD, Crick FH. 1953. Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171: 737-738.
90. West SC. 1997. Processing of recombination intermediates by the RuvABC proteins. Annual Review of Genetics 31: 213-244.
91. Wimberly H, Shee C, Thornton PC, Sivaramakrishnan P, Rosenberg SM, et al. 2013. R-loops and nicks initiate DNA breakage and genome instability in non-growing Escherichia coli. Nature Communications 4: 2115.
92. Yang Y, Sterling J, Storici F, Resnick MA, Gordenin DA. 2008. Hyper-mutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS Genetics 4: e1000264.