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Vol. 21, No. 1-2, 2011
Issue release date: January 2012
Section title: Paper
Editor's Choice -- Free Access
J Mol Microbiol Biotechnol 2011;21:8–19
(DOI:10.1159/000335354)

What Limits the Efficiency of Double-Strand Break-Dependent Stress-Induced Mutation in Escherichia coli

Shee C. · Ponder R. · Gibson J.L. · Rosenberg S.M.
Departments of Molecular and Human Genetics, Biochemistry and Molecular Biology, Molecular Virology and Microbiology, and Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, Tex., USA
email Corresponding Author

Abstract

Stress-induced mutation is a collection of molecular mechanisms in bacterial, yeast and human cells that promote mutagenesis specifically when cells are maladapted to their environment, i.e. when they are stressed. Here, we review one molecular mechanism: double-strand break (DSB)-dependent stress-induced mutagenesis described in starving Escherichia coli. In it, the otherwise high-fidelity process of DSB repair by homologous recombination is switched to an error-prone mode under the control of the RpoS general stress response, which licenses the use of error-prone DNA polymerase, DinB, in DSB repair. This mechanism requires DSB repair proteins, RpoS, the SOS response and DinB. This pathway underlies half of spontaneous chromosomal frameshift and base substitution mutations in starving E. coli [Proc Natl Acad Sci USA 2011;108:13659–13664], yet appeared less efficient in chromosomal than F′ plasmid-borne genes. Here, we demonstrate and quantify DSB-dependent stress-induced reversion of a chromosomal lac allele with DSBs supplied by I-SceI double-strand endonuclease. I-SceI-induced reversion of this allele was previously studied in an F′. We compare the efficiencies of mutagenesis in the two locations. When we account for contributions of an F′-borne extra dinB gene, strain background differences, and bypass considerations of rates of spontaneous DNA breakage by providing I-SceI cuts, the chromosome is still ∼100 times less active than F. We suggest that availability of a homologous partner molecule for recombinational break repair may be limiting. That partner could be a duplicated chromosomal segment or sister chromosome.

© 2012 S. Karger AG, Basel


  

Key Words

  • DNA repair
  • Double-strand break repair
  • Evolution
  • Mutation
  • Stress-induced mutation
  • Stress response

References

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  2. Andersson DI, Koskiniemi S, Hughes D: Biological roles of translesion synthesis DNA polymerases in eubacteria. Mol Microbiol 2010;77:540–548.
  3. Bachmann BJ: Pedigrees of some mutant strains of Escherichia coli k-12. Bacteriol Rev 1972;36:525–557.
  4. Battesti A, Majdalani N, Gottesman S: The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 2011;65:189–213.
  5. Biery MC, Stewart FJ, Stellwagen AE, Raleigh EA, Craig NL: A simple in vitro Tn7-based transposition system with low target site selectivity for genome and gene analysis. Nucleic Acids Res 2000;28:1067–1077.
  6. Bindra RS, Crosby ME, Glazer, PM: Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev 2007;26:249–260.
  7. Bjedov I, Tenaillon O, Gerard B, Souza V, Denamur E, Radman M, Taddei F, Matic I: Stress-induced mutagenesis in bacteria. Science 2003;300:1404–1409.
  8. Blattner FR, Plunkett G, 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y: The complete genome sequence of Escherichia coli K-12. Science 1997;277:1453–1462.
  9. Boles BR, Singh PK: Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci USA 2008;105:12503–12508.
  10. Bull HJ, Lombardo MJ, Rosenberg SM: Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase I.V. dependence. Proc Natl Acad Sci USA 2001;98:8334–8341.
  11. Cairns J, Foster PL: Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 1991;128:695–701.
  12. Cirz RT, Romesberg FE: Controlling mutation: intervening in evolution as a therapeutic strategy. Crit Rev Biochem Mol Biol 2007;42:341–354.
  13. Coros CJ, Piazza CL, Chalamcharla VR, Smith D, Belfort M: Global regulators orchestrate group II intron retromobility. Mol Cell 2009;34:250–256.
  14. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC: Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 2001;158:41–64.
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  16. Fernandez De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, Ohmori H, Woodgate R: Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 2000;35:1560–1572.
  17. Forche A, Abbey D, Pisithkul T, Weinzierl MA, Ringstrom T, Bruck D, Petersen K, Berman J: Stress alters rates and types of loss of heterozygosity in Candida albicans. MBio 2011;2:e00129-11.
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  20. Foster PL, Trimarchi JM: Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation. Proc Natl Acad Sci USA 1995;92:5487–5490.
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  29. Harris RS, Longerich S, Rosenberg SM: Recombination in adaptive mutation. Science 1994;264:258–260.
  30. Hastings PJ, Bull HJ, Klump JR, Rosenberg SM: Adaptive amplification: an inducible chromosomal instability mechanism. Cell 2000;103:723–731.
  31. Hastings PJ, Hersh MN, Thornton PC, Fonville NC, Slack A, Frisch RL, Ray MP, Harris RS, Leal SM, Rosenberg SM: Competition of Escherichia coli DNA polymerases I, II and III with DNA Pol IV in stressed cells. PLoS One 2010;5:e10862.
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  33. Hastings PJ, Lupski JR, Rosenberg SM, Ira G: Mechanisms of change in gene copy number. Nat Rev Genet 2009b;10:551–564.
  34. Hastings PJ, Slack A, Petrosino JF, Rosenberg SM: Adaptive amplification and point mutation are independent mechanisms: evidence for various stress-inducible mutation mechanisms. PLoS Biol 2004;2:e399.
  35. Hicks WM, Kim M, Haber JE: Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 2010;329:82–85.
  36. Ilves H, Horak R, Kivisaar M: Involvement of sigma(s) in starvation-induced transposition of Pseudomonas putida transposon Tn4652. J Bacteriol 2001;183:5445–5448.
  37. Koskiniemi S, Hughes D, Andersson DI: Effect of translesion DNA polymerases, endonucleases and RpoS on mutation rates in Salmonella typhimurium. Genetics 2010;185:783–795.
  38. Kugelberg E, Kofoid E, Reams AB, Andersson DI, Roth JR: Multiple pathways of selected gene amplification during adaptive mutation. Proc Natl Acad Sci USA 2006;103:17319–17324.
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  40. Lamrani S, Ranquet C, Gama MJ, Nakai H, Shapiro JA, Toussaint A, Maenhaut-Michel G: Starvation-induced Mucts62-mediated coding sequence fusion: a role for ClpXP, Lon, RpoS and Crp. Mol Microbiol 1999;32:327–343.
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Author Contacts

Susan M. Rosenberg
Department of Molecular and Human Genetics, Baylor College of Medicine
One Baylor Plaza, Rm S809A Mail Stop BCM225
Houston, TX 77030-3411 (USA)
Tel. +1 713 798 6924, E-Mail smr@bcm.edu

  

Article Information

C.S. and R.P. have equally contributed to this work.

Published online: January 13, 2012
Number of Print Pages : 12
Number of Figures : 4, Number of Tables : 1, Number of References : 75

  

Publication Details

Journal of Molecular Microbiology and Biotechnology

Vol. 21, No. 1-2, Year 2011 (Cover Date: January 2012)

Journal Editor: Saier Jr. M.H. (La Jolla, Calif.)
ISSN: 1464-1801 (Print), eISSN: 1660-2412 (Online)

For additional information: http://www.karger.com/MMB


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Stress-induced mutation is a collection of molecular mechanisms in bacterial, yeast and human cells that promote mutagenesis specifically when cells are maladapted to their environment, i.e. when they are stressed. Here, we review one molecular mechanism: double-strand break (DSB)-dependent stress-induced mutagenesis described in starving Escherichia coli. In it, the otherwise high-fidelity process of DSB repair by homologous recombination is switched to an error-prone mode under the control of the RpoS general stress response, which licenses the use of error-prone DNA polymerase, DinB, in DSB repair. This mechanism requires DSB repair proteins, RpoS, the SOS response and DinB. This pathway underlies half of spontaneous chromosomal frameshift and base substitution mutations in starving E. coli [Proc Natl Acad Sci USA 2011;108:13659–13664], yet appeared less efficient in chromosomal than F′ plasmid-borne genes. Here, we demonstrate and quantify DSB-dependent stress-induced reversion of a chromosomal lac allele with DSBs supplied by I-SceI double-strand endonuclease. I-SceI-induced reversion of this allele was previously studied in an F′. We compare the efficiencies of mutagenesis in the two locations. When we account for contributions of an F′-borne extra dinB gene, strain background differences, and bypass considerations of rates of spontaneous DNA breakage by providing I-SceI cuts, the chromosome is still ∼100 times less active than F. We suggest that availability of a homologous partner molecule for recombinational break repair may be limiting. That partner could be a duplicated chromosomal segment or sister chromosome.

© 2012 S. Karger AG, Basel


  

Author Contacts

Susan M. Rosenberg
Department of Molecular and Human Genetics, Baylor College of Medicine
One Baylor Plaza, Rm S809A Mail Stop BCM225
Houston, TX 77030-3411 (USA)
Tel. +1 713 798 6924, E-Mail smr@bcm.edu

  

Article Information

C.S. and R.P. have equally contributed to this work.

Published online: January 13, 2012
Number of Print Pages : 12
Number of Figures : 4, Number of Tables : 1, Number of References : 75

  

Publication Details

Journal of Molecular Microbiology and Biotechnology

Vol. 21, No. 1-2, Year 2011 (Cover Date: January 2012)

Journal Editor: Saier Jr. M.H. (La Jolla, Calif.)
ISSN: 1464-1801 (Print), eISSN: 1660-2412 (Online)

For additional information: http://www.karger.com/MMB


Article / Publication Details

First-Page Preview
Abstract of Paper

Published online: 1/13/2012
Issue release date: January 2012

Number of Print Pages: 12
Number of Figures: 4
Number of Tables: 1

ISSN: 1464-1801 (Print)
eISSN: 1660-2412 (Online)

For additional information: http://www.karger.com/MMB


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Akerlund T, Nordstrom K, Bernander R: Analysis of cell size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia coli. J Bacteriol 1995;177:6791–6797.
  2. Andersson DI, Koskiniemi S, Hughes D: Biological roles of translesion synthesis DNA polymerases in eubacteria. Mol Microbiol 2010;77:540–548.
  3. Bachmann BJ: Pedigrees of some mutant strains of Escherichia coli k-12. Bacteriol Rev 1972;36:525–557.
  4. Battesti A, Majdalani N, Gottesman S: The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 2011;65:189–213.
  5. Biery MC, Stewart FJ, Stellwagen AE, Raleigh EA, Craig NL: A simple in vitro Tn7-based transposition system with low target site selectivity for genome and gene analysis. Nucleic Acids Res 2000;28:1067–1077.
  6. Bindra RS, Crosby ME, Glazer, PM: Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev 2007;26:249–260.
  7. Bjedov I, Tenaillon O, Gerard B, Souza V, Denamur E, Radman M, Taddei F, Matic I: Stress-induced mutagenesis in bacteria. Science 2003;300:1404–1409.
  8. Blattner FR, Plunkett G, 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y: The complete genome sequence of Escherichia coli K-12. Science 1997;277:1453–1462.
  9. Boles BR, Singh PK: Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci USA 2008;105:12503–12508.
  10. Bull HJ, Lombardo MJ, Rosenberg SM: Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase I.V. dependence. Proc Natl Acad Sci USA 2001;98:8334–8341.
  11. Cairns J, Foster PL: Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 1991;128:695–701.
  12. Cirz RT, Romesberg FE: Controlling mutation: intervening in evolution as a therapeutic strategy. Crit Rev Biochem Mol Biol 2007;42:341–354.
  13. Coros CJ, Piazza CL, Chalamcharla VR, Smith D, Belfort M: Global regulators orchestrate group II intron retromobility. Mol Cell 2009;34:250–256.
  14. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC: Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 2001;158:41–64.
  15. Deem A, Keszthelyi A, Blackgrove T, Vayl A, Coffey B, Mathur R, Chabes A, Malkova A: Break-induced replication is highly inaccurate. PLoS Biol 2011;9:e1000594.
  16. Fernandez De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, Ohmori H, Woodgate R: Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 2000;35:1560–1572.
  17. Forche A, Abbey D, Pisithkul T, Weinzierl MA, Ringstrom T, Bruck D, Petersen K, Berman J: Stress alters rates and types of loss of heterozygosity in Candida albicans. MBio 2011;2:e00129-11.
  18. Foster PL: Nonadaptive mutations occur on the F′ episome during adaptive mutation conditions in Escherichia coli. J Bacteriol 1997;179:1550–1554.
  19. Foster PL, Rosche WA: Increased episomal replication accounts for the high rate of adaptive mutation in recD mutants of Escherichia coli. Genetics 1999;152:15–30.
  20. Foster PL, Trimarchi JM: Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation. Proc Natl Acad Sci USA 1995;92:5487–5490.
  21. Frisch RL, Su Y, Thornton PC, Gibson JL, Rosenberg SM, Hastings PJ: 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 2010;192:4694–4700.
  22. Galhardo RS, Do R, Yamada M, Friedberg E, Hastings P, Nohmi T, Rosenberg S: DinB up-regulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. Genetics 2009;182:55–68.
  23. Galhardo RS, Hastings PJ, Rosenberg SM: Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 2007;42:399–435.
  24. Gibson JL, Lombardo MJ, Thornton PC, Hu KH, Galhardo RS, Beadle B, Habib A, Magner DB, Frost LS, Herman C, Hastings PJ, Rosenberg SM: The sigma(e) stress response is required for stress-induced mutation and amplification in Escherichia coli. Mol Microbiol 2010;77:415–430.
  25. Godoy VG, Gizatullin FS, Fox MS: Some features of the mutability of bacteria during nonlethal selection. Genetics 2000;154:49–59.
  26. Gomez-Gomez JM, Blazquez J, Baquero F, Martinez JL: H-NS and RpoS regulate emergence of Lac Ara+ mutants of Escherichia coli MCS2. J Bacteriol 1997;179:4620–4622.
  27. Gumbiner-Russo LM, Lombardo M-J, Ponder RG, Rosenberg SM: The TGV transgenic vectors for single copy gene expression in the E. coli chromosome. Gene 2001;273:97–104.
  28. Hanahan D: Studies on transformation of Escherichia coli with plasmids. J Mol Biol 1983;166:557–580.
  29. Harris RS, Longerich S, Rosenberg SM: Recombination in adaptive mutation. Science 1994;264:258–260.
  30. Hastings PJ, Bull HJ, Klump JR, Rosenberg SM: Adaptive amplification: an inducible chromosomal instability mechanism. Cell 2000;103:723–731.
  31. Hastings PJ, Hersh MN, Thornton PC, Fonville NC, Slack A, Frisch RL, Ray MP, Harris RS, Leal SM, Rosenberg SM: Competition of Escherichia coli DNA polymerases I, II and III with DNA Pol IV in stressed cells. PLoS One 2010;5:e10862.
  32. Hastings PJ, Ira G, Lupski JR: A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet 2009a;5:e1000327.
  33. Hastings PJ, Lupski JR, Rosenberg SM, Ira G: Mechanisms of change in gene copy number. Nat Rev Genet 2009b;10:551–564.
  34. Hastings PJ, Slack A, Petrosino JF, Rosenberg SM: Adaptive amplification and point mutation are independent mechanisms: evidence for various stress-inducible mutation mechanisms. PLoS Biol 2004;2:e399.
  35. Hicks WM, Kim M, Haber JE: Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 2010;329:82–85.
  36. Ilves H, Horak R, Kivisaar M: Involvement of sigma(s) in starvation-induced transposition of Pseudomonas putida transposon Tn4652. J Bacteriol 2001;183:5445–5448.
  37. Koskiniemi S, Hughes D, Andersson DI: Effect of translesion DNA polymerases, endonucleases and RpoS on mutation rates in Salmonella typhimurium. Genetics 2010;185:783–795.
  38. Kugelberg E, Kofoid E, Reams AB, Andersson DI, Roth JR: Multiple pathways of selected gene amplification during adaptive mutation. Proc Natl Acad Sci USA 2006;103:17319–17324.
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