Skip to main content
SpringerLink
Log in
Book cover

Stress-Induced Mutagenesis pp 21–39Cite as

Mutagenesis Associated with Repair of DNA Double-Strand Breaks Under Stress

  • Chapter
  • First Online:

Abstract

Evolutionary theory predicted that mutations occur randomly both in time and in genomic space. This expectation has been revised by the discoveries of stress-induced mutation mechanisms, which activate mutagenesis pathways under the control of stress responses. Stress-induced mutation mechanisms produce mutations preferentially when cells or organisms are maladapted to their environment, i.e., when they are stressed, potentially accelerating evolution. We review stress-­induced mutagenesis associated with repair of double-strand breaks in Escherichia coli. In this mechanism, the process of DNA break repair by homologous recombination is high-fidelity in unstressed cells, but is switched to a mutagenic mode using the error-prone DNA polymerase DinB, and other error-prone DNA polymerases, under the control of the RpoS general stress response. The switch to mutagenic repair occurs during starvation or if RpoS is upregulated artificially in unstressed cells, and presumably during the many different stresses that activate the RpoS response. Recent work shows that this mechanism accounts for most spontaneous base-substitution and frameshift mutagenesis during starvation in E. coli, acts not only in plasmid DNA but also in the chromosomes of plasmid-free cells, illustrates the generality of this mechanism in many organisms and circumstances, and resolves some other old tensions in the field. Stress-induced mutation mechanisms studied in the laboratory are likely to provide superior models for mutagenesis underlying pathogen-host adaptation, antibiotic resistance, and cancer progression and resistance mechanisms, all problems of evolution under stress driven by mutations.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Al Mamun AA, Lombardo MJ, Shee C, Lisewski AM, Gonzalez C, Lin D, Nehring R, Saint-Ruff C, Gibson GL, Frisch RL et al (2012) Identify and function of a large gene network underlying mutagenic repair of DNA breaks. Science 338:1344–1348

    Google Scholar 

  • Albano F, Anelli L, Zagaria A, Coccaro N, Casieri P, Rossi AR, Vicari L, Liso V, Rocchi M, Specchia G (2010) Non random distribution of genomic features in breakpoint regions involved in chronic myeloid leukemia cases with variant t(9;22) or additional chromosomal rearrangements. Mol Cancer 9:120

    PubMed  Google Scholar 

  • Andersson DI, Koskiniemi S, Hughes D (2010) Biological roles of translesion synthesis DNA polymerases in eubacteria. Mol Microbiol 77:540–548

    PubMed  CAS  Google Scholar 

  • Banach-Orlowska M, Fijalkowska IJ, Schaaper RM, Jonczyk P (2005) DNA polymerase II as a fidelity factor in chromosomal DNA synthesis in Escherichia coli. Mol Microbiol 58:61–70

    PubMed  CAS  Google Scholar 

  • Battesti A, Majdalani N, Gottesman S (2011) The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 65:189–213

    PubMed  CAS  Google Scholar 

  • Bindra RS, Schaffer PJ, Meng A, Woo J, Maseide K, Roth ME, Lizardi P, Hedley DW, Bristow RG, Glazer PM (2004) Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 24:8504–8518

    PubMed  CAS  Google Scholar 

  • Bindra RS, Gibson SL, Meng A, Westermark U, Jasin M, Pierce AJ, Bristow RG, Classon MK, Glazer PM (2005) Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res 65:11597–11604

    PubMed  CAS  Google Scholar 

  • Bindra RS, Crosby ME, Glazer PM (2007) Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev 26:249–260

    PubMed  CAS  Google Scholar 

  • Bjedov I, Tenaillon O, Gerard B, Souza V, Denamur E, Radman M, Taddei F, Matic I (2003) Stress-induced mutagenesis in bacteria. Science 300:1404–1409

    PubMed  CAS  Google Scholar 

  • Bridges BA (1997) Microbial genetics. Hypermutation under stress. Nature 387:557–558

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Cairns J, Foster PL (1991) Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128:695–701

    PubMed  CAS  Google Scholar 

  • Camerini-Otero RD, Hsieh P (1993) Parallel DNA triplexes, homologous recombination, and other homology-dependent DNA interactions. Cell 73:217–223

    PubMed  CAS  Google Scholar 

  • Caporale LH (2006) The implicit genome. Oxford University Press, USA

    Google Scholar 

  • Casadesus. J Pers Commun.

    Google Scholar 

  • Chicurel M (2001) Genetics. Can organisms speed their own evolution? Science 292:1824–1827

    PubMed  CAS  Google Scholar 

  • Cirz RT, Romesberg FE (2007) Controlling mutation: intervening in evolution as a therapeutic strategy. Crit Rev Biochem Mol Biol 42:341–354

    PubMed  CAS  Google Scholar 

  • Cirz RT, Chin JK, Andes DR, de Crecy-Lagard V, Craig WA, Romesberg FE (2005) Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biol 3:e176

    PubMed  Google Scholar 

  • Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC (2001) Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158:41–64

    PubMed  CAS  Google Scholar 

  • Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74:417–433

    PubMed  CAS  Google Scholar 

  • Deem A, Keszthelyi A, Blackgrove T, Vayl A, Coffey B, Mathur R, Chabes A, Malkova A (2011) Break-induced replication is highly inaccurate. PLoS Biol 9:e1000594

    PubMed  CAS  Google Scholar 

  • Di Noia JM, Neuberger MS (2007) Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 76:1–22

    PubMed  Google Scholar 

  • Dillingham MS, Kowalczykowski SC (2008) RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol Mol Biol Rev 72:642–671

    PubMed  CAS  Google Scholar 

  • Drake JW (2007a) Mutations in clusters and showers. Proc Natl Acad Sci USA 104:8203–8204

    PubMed  CAS  Google Scholar 

  • Drake JW (2007b) Too many mutants with multiple mutations. Crit Rev Biochem Mol Biol 42:247–258

    PubMed  CAS  Google Scholar 

  • Dubnau D, Losick R (2006) Bistability in bacteria. Mol Microbiol 61:564–572

    PubMed  CAS  Google Scholar 

  • Erill I, Campoy S, Barbe J (2007) Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol Rev 31:637–656

    PubMed  CAS  Google Scholar 

  • Fonville NC, Ward RM, Mittelman D (2011) Stress-induced modulators of repeat instability and genome evolution. J Mol Microbiol Biotechnol 21:36–44

    PubMed  CAS  Google Scholar 

  • Foster PL, Trimarchi JM (1994) Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265:407–409

    PubMed  CAS  Google Scholar 

  • Foster PL, Trimarchi JM (1995) Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation. Proc Natl Acad Sci USA 92:5487–5490

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2005) DNA repair and mutagenesis. ASM Press, Washington, DC

    Google Scholar 

  • Frisch RL, Su Y, Thornton PC, Gibson JL, Rosenberg SM, Hastings PJ (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. J Bacteriol 192:4694–4700

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Galhardo RS, Do R, Yamada M, Friedberg E, Hastings P, Nohmi T, Rosenberg S (2009) DinB up-­regulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. Genetics 182:55–68

    PubMed  CAS  Google Scholar 

  • Galitski T, Roth JR (1995) Evidence that F plasmid transfer replication underlies apparent adaptive mutation. Science 268:421–423

    PubMed  CAS  Google Scholar 

  • Gibson JL, Lombardo MJ, Thornton PC, Hu KH, Galhardo RS, Beadle B, Habib A, Magner DB, Frost LS, Herman C et al (2010) The sigma(E) stress response is required for stress-induced mutation and amplification in Escherichia coli. Mol Microbiol 77:415–430

    PubMed  CAS  Google Scholar 

  • Godoy VG, Gizatullin FS, Fox MS (2000) Some features of the mutability of bacteria during nonlethal selection. Genetics 154:49–59

    PubMed  CAS  Google Scholar 

  • Gonzalez CP, Hadany L, Ponder RG, Price M, Hastings PJ, Rosenberg SM (2008) Mutability and importance of a hypermutable cell subpopulation that produces stress-induced mutants in Escherichia coli. PLoS Genet 4:e10000208

    Google Scholar 

  • Gumbiner-Russo LM, Lombardo M-J, Ponder RG, Rosenberg SM (2001) The TGV transgenic vectors for single copy gene expression in the Escherichia coli chromosome. Gene 273:97–104

    PubMed  CAS  Google Scholar 

  • Haber JE (1999) DNA repair. Gatekeepers of recombination. Nature 398:665–667

    Google Scholar 

  • Harris RS, Longerich S, Rosenberg SM (1994) Recombination in adaptive mutation. Science 264:258–260

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hastings PJ (2007) Adaptive amplification. Crit Rev Biochem Mol Biol 42:271–273

    PubMed  CAS  Google Scholar 

  • Hastings PJ, Bull HJ, Klump JR, Rosenberg SM (2000) Adaptive amplification: an inducible chromosomal instability mechanism. Cell 103:723–731

    PubMed  CAS  Google Scholar 

  • Hastings PJ, Ira G, Lupski JR (2009a) A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet 5:e1000327

    PubMed  CAS  Google Scholar 

  • Hastings PJ, Lupski JR, Rosenberg SM, Ira G (2009b) Mechanisms of change in gene copy number. Nat Rev Genet 10:551–564

    PubMed  CAS  Google Scholar 

  • Hastings PJ, Hersh MN, Thornton PC, Fonville NC, Slack A, Frisch RL, Ray MP, Harris RS, Leal SM, Rosenberg SM (2010) Competition of Escherichia coli DNA polymerases I, II and III with DNA Pol IV in stressed cells. PLoS One 5:e10862

    PubMed  CAS  Google Scholar 

  • Hefferin ML, Tomkinson AE (2005) Mechanism of DNA double-strand break repair by non-­homologous end joining. DNA Repair (Amst) 4:639–648

    CAS  Google Scholar 

  • Heidenreich E (2007) Adaptive mutation in Saccharomyces cerevisiae. Crit Rev Biochem Mol Biol 42:285–311

    PubMed  CAS  Google Scholar 

  • Hendrickson H, Slechta ES, Bergthorsson U, Andersson DI, Roth JR (2002) Amplification-­mutagenesis: evidence that "directed" adaptive mutation and general hypermutability result from growth with a selected gene amplification. Proc Natl Acad Sci USA 99:2164–2169

    PubMed  CAS  Google Scholar 

  • Hicks WM, Kim M, Haber JE (2010) Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329:82–85

    PubMed  CAS  Google Scholar 

  • Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411:366–374

    PubMed  CAS  Google Scholar 

  • Kenyon CJ, Walker GC (1980) DNA-damaging agents stimulate gene expression at specific loci in Escherichia coli. Proc Natl Acad Sci USA 77:2819–2823

    PubMed  CAS  Google Scholar 

  • Kim SR, Maenhaut-Michel G, Yamada M, Yamamoto Y, Matsui K, Sofuni T, Nohmi T, Ohmori H (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. Proc Natl Acad Sci USA 94:13792–13797

    PubMed  CAS  Google Scholar 

  • Kimura M (1991) The neutral theory of molecular evolution: a review of recent evidence. Jpn J Genet 66:367–386

    PubMed  CAS  Google Scholar 

  • Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797–810

    PubMed  CAS  Google Scholar 

  • Kohanski MA, DePristo MA, Collins JJ (2010) Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol Cell 37:311–320

    PubMed  CAS  Google Scholar 

  • Kowalczykowski SC, Eggleston AK (1994) Homologous pairing and DNA strand-exchange ­proteins. Annu Rev Biochem 63:991–1043

    PubMed  CAS  Google Scholar 

  • Layton JC, Foster PL (2003) Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol Microbiol 50:549–561

    PubMed  CAS  Google Scholar 

  • Lombardo MJ, Aponyi I, Rosenberg SM (2004) General stress response regulator RpoS in adaptive mutation and amplification in Escherichia coli. Genetics 166:669–680

    PubMed  CAS  Google Scholar 

  • Luria SE, Delbrück M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491–511

    PubMed  CAS  Google Scholar 

  • Lynch M (2010) Evolution of the mutation rate. Trends Genet 26:345–352

    PubMed  CAS  Google Scholar 

  • Mayr E (1982) The Growth of Biological Thought: Diversity, Evolution, and Inheritance. Harvard University Press, Cambridge, MA, pp 738–744

    Google Scholar 

  • McKenzie GJ, Lombardo MJ, Rosenberg SM (1998) Recombination-dependent mutation in Escherichia coli occurs in stationary phase. Genetics 149:1163–1165

    PubMed  CAS  Google Scholar 

  • McKenzie GJ, Harris RS, Lee PL, Rosenberg SM (2000) The SOS response regulates adaptive mutation. Proc Natl Acad Sci USA 97:6646–6651

    PubMed  CAS  Google Scholar 

  • McKenzie GJ, Lee PL, Lombardo MJ, Hastings PJ, Rosenberg SM (2001) SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol Cell 7:571–579

    PubMed  CAS  Google Scholar 

  • McPartland A, Green L, Echols H (1980) Control of recA gene RNA in E. coli: regulatory and signal genes. Cell 20:731–737

    PubMed  CAS  Google Scholar 

  • Meulle A, Salles B, Daviaud D, Valet P, Muller C (2008) Positive regulation of DNA double strand break repair activity during differentiation of long life span cells: the example of adipogenesis. PLoS One 3:e3345

    PubMed  Google Scholar 

  • Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, Cohen SN (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305:1629–1631

    PubMed  CAS  Google Scholar 

  • 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 Dev 13:2889–2903

    PubMed  CAS  Google Scholar 

  • Moxon ER, Rainey PB, Nowak MA, Lenski RE (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4:24–33

    PubMed  CAS  Google Scholar 

  • Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, Jones D, Hinton J, Marshall J, Stebbings LA et al (2012) Mutational processes molding the genomes of 21 breast cancers. Cell 149:979–993

    PubMed  CAS  Google Scholar 

  • Ninio J (1996) Gene conversion as a focusing mechanism for correlated mutations: a hypothesis. Mol Gen Genet 251:503–508

    PubMed  CAS  Google Scholar 

  • Nohmi T (2006) Environmental stress and lesion-bypass DNA polymerases. Annu Rev Microbiol 60:231–253

    PubMed  CAS  Google Scholar 

  • Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T et al (2001) The Y-family of DNA polymerases. Mol Cell 8:7–8

    PubMed  CAS  Google Scholar 

  • Pennington JM, Rosenberg SM (2007) Spontaneous DNA breakage in single living Escherichia coli cells. Nat Genet 39:797–802

    PubMed  CAS  Google Scholar 

  • Perez-Capilla T, Baquero MR, Gomez-Gomez JM, Ionel A, Martin S, Blazquez J (2005) SOS-­independent induction of dinB transcription by beta-lactam-mediated inhibition of cell wall synthesis in Escherichia coli. J Bacteriol 187:1515–1518

    PubMed  CAS  Google Scholar 

  • 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. J Bacteriol 191:5881–5889

    PubMed  CAS  Google Scholar 

  • Ponder RG, Fonville NC, Rosenberg SM (2005) A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol Cell 19:791–804

    PubMed  CAS  Google Scholar 

  • Prieto AI, Ramos-Morales F, Casadesus J (2006) Repair of DNA damage induced by bile salts in Salmonella enterica. Genetics 174:575–584

    PubMed  CAS  Google Scholar 

  • Radicella JP, Park PU, Fox MS (1995) Adaptive mutation in Escherichia coli: a role for ­conjugation. Science 268:418–420

    PubMed  CAS  Google Scholar 

  • Radman M (1975) SOS repair hypothesis: phenomenology of an inducible DNA repair which is accompanied by mutagenesis. Basic Life Sci 5A:355–367

    PubMed  CAS  Google Scholar 

  • Roberts SA, Sterling J, Thompson C, Harris S, Mav D, Shah R, Klimczak LJ, Kryukov GV, Malc E, Mieczkowski PA et al (2012) Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol Cell 46:424–435

    PubMed  CAS  Google Scholar 

  • Rosche WA, Foster PL (1999) The role of transient hypermutators in adaptive mutation in Escherichia coli. Proc Natl Acad Sci USA 96:6862–6867

    PubMed  CAS  Google Scholar 

  • Rosenberg SM, Longerich S, Gee P, Harris RS (1994) Adaptive mutation by deletions in small mononucleotide repeats. Science 265:405–407

    PubMed  CAS  Google Scholar 

  • Rosenberg SM, Shee C, Frisch RL, Hastings PJ (2012) Stress-induced mutation via DNA breaks in E. coli: a molecular mechanism with implications for evolution and medicine. Bioessays 34:885–892

    Google Scholar 

  • Roth JR (2010) The joys and terrors of fast adaptation: new findings elucidate antibiotic resistance and natural selection. Mol Microbiol 79:279–282

    Google Scholar 

  • Roth JR, Andersson DI (2004) Adaptive mutation: how growth under selection stimulates Lac(+) reversion by increasing target copy number. J Bacteriol 186:4855–4860

    PubMed  CAS  Google Scholar 

  • Roth JR, Kugelberg E, Reams AB, Kofoid E, Andersson DI (2006) Origin of mutations under selection: the adaptive mutation controversy. Annu Rev Microbiol 60:477–501

    PubMed  CAS  Google Scholar 

  • Saint-Ruf C, Pesut J, Sopta M, Matic I (2007) Causes and consequences of DNA repair activity modulation during stationary phase in Escherichia coli. Crit Rev Biochem Mol Biol 42: 259–270

    PubMed  CAS  Google Scholar 

  • Shee C, Gibson JL, Darrow MC, Gonzalez C, Rosenberg SM (2011a) Impact of a stress-inducible switch to mutagenic repair of DNA breaks on mutation in Escherichia coli. Proc Natl Acad Sci USA 108:13659–13664

    PubMed  CAS  Google Scholar 

  • Shee C, Gibson JL, Rosenberg SM (2012) Two mechanisms produce mutation hotspots at DNA breaks in Escherichia coli. Cell Reports 2:714–721

    PubMed  CAS  Google Scholar 

  • Shee C, Ponder R, Gibson JL, Rosenberg SM (2011b) What limits the efficiency of double-strand break-dependent stress-induced mutation in Escherichia coli? J Mol Microbiol Biotechnol 21:8–19

    PubMed  CAS  Google Scholar 

  • Slack A, Thornton PC, Magner DB, Rosenberg SM, Hastings PJ (2006) On the mechanism of gene amplification induced under stress in Escherichia coli. PLoS Genet 2:e48

    PubMed  Google Scholar 

  • Slechta ES, Harold J, Andersson DI, Roth JR (2002a) The effect of genomic position on reversion of a lac frameshift mutation (lacIZ33) during non-lethal selection (adaptive mutation). Mol Microbiol 44:1017–1032

    PubMed  CAS  Google Scholar 

  • Slechta ES, Liu J, Andersson DI, Roth JR (2002b) Evidence that selected amplification of a bacterial lac frameshift allele stimulates Lac(+) reversion (adaptive mutation) with or without ­general hypermutability. Genetics 161:945–956

    PubMed  CAS  Google Scholar 

  • Slechta ES, Bunny KL, Kugelberg E, Kofoid E, Andersson DI, Roth JR (2003) Adaptive mutation: general mutagenesis is not a programmed response to stress but results from rare coamplification of dinB with lac. Proc Natl Acad Sci USA 100:12847–12852

    PubMed  CAS  Google Scholar 

  • Sniegowski PD, Gerrish PJ, Johnson T, Shaver A (2000) The evolution of mutation rates: separating causes from consequences. Bioessays 22:1057–1066

    PubMed  CAS  Google Scholar 

  • Strathern JN, Shafer BK, McGill CB (1995) DNA synthesis errors associated with double-strand-break repair. Genetics 140:965–972

    PubMed  CAS  Google Scholar 

  • Sung HM, Yasbin RE (2002) Adaptive, or stationary-phase, mutagenesis, a component of bacterial differentiation in Bacillus subtilis. J Bacteriol 184:5641–5653

    PubMed  CAS  Google Scholar 

  • Sutton MD, Smith BT, Godoy VG, Walker GC (2000) The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu Rev Genet 34:479–497

    PubMed  CAS  Google Scholar 

  • Tiligada E (2006) Chemotherapy: induction of stress responses. Endocr Relat Cancer 13(Suppl 1):S115–124

    PubMed  CAS  Google Scholar 

  • Tiligada E, Miligkos V, Delitheos A (2002) Cross-talk between cellular stress, cell cycle and anticancer agents: mechanistic aspects. Curr Med Chem Anticancer Agents 2:553–566

    PubMed  CAS  Google Scholar 

  • Torkelson J, Harris RS, Lombardo MJ, Nagendran J, Thulin C, Rosenberg SM (1997) Genome-­wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-­dependent adaptive mutation. EMBO J 16:3303–3311

    PubMed  CAS  Google Scholar 

  • Wagner J, Gruz P, Kim SR, Yamada M, Matsui K, Fuchs RP, Nohmi T (1999) The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell 4:281–286

    CAS  Google Scholar 

  • Wang J, Gonzalez KD, Scaringe WA, Tsai K, Liu N, Gu D, Li W, Hill KA, Sommer SS (2007) Evidence for mutation showers. Proc Natl Acad Sci USA 104:8403–8408

    PubMed  CAS  Google Scholar 

  • Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591–1603

    PubMed  CAS  Google Scholar 

  • West SC (2003) Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 4:435–445

    PubMed  CAS  Google Scholar 

  • Weterings E, van Gent DC (2004) The mechanism of non-homologous end-joining: a synopsis of synapsis. DNA Repair (Amst) 3:1425–1435

    CAS  Google Scholar 

  • Wyman C, Kanaar R (2004) Homologous recombination: down to the wire. Curr Biol 14: R629–631

    PubMed  CAS  Google Scholar 

  • Yang Y, Sterling J, Storici F, Resnick MA, Gordenin DA (2008) Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS Genet 4:e1000264

    PubMed  Google Scholar 

  • Yao Y, Kovalchuk I (2011) Abiotic stress leads to somatic and heritable changes in homologous recombination frequency, point mutation frequency and microsatellite stability in Arabidopsis plants. Mutat Res 707:61–66

    PubMed  CAS  Google Scholar 

Download references

Acknowledgment

Supported by National Institutes of Health grant R01-GM53158.

Author information

Authors and Affiliations

  1. Departments of Molecular and Human Genetics, Biochemistry and Molecular Biology, Molecular Virology and Microbiology, Dan L Duncan Cancer Center, Baylor College of Medicine, Houston, TX, USA

    Chandan Shee & Susan M. Rosenberg

  2. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA

    P. J. Hastings

Authors
  1. Chandan Shee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. J. Hastings
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan M. Rosenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susan M. Rosenberg .

Editor information

Editors and Affiliations

  1. , Department of Biological Sciences, Virginia Tech, 4100 Derring Lab, Blacksburg, 24061, Virginia, USA

    David Mittelman

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Shee, C., Hastings, P.J., Rosenberg, S.M. (2013). Mutagenesis Associated with Repair of DNA Double-Strand Breaks Under Stress. In: Mittelman, D. (eds) Stress-Induced Mutagenesis. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6280-4_2

Download citation

Publish with us

Policies and ethics

Search

Navigation