1887

Abstract

Heritable hypermutation in bacteria is mainly due to alterations in the methyl-directed mismatch repair (MMR) system. MMR-deficient strains have been described from several bacterial species, and all of the strains exhibit increased mutation frequency and recombination, which are important mechanisms for acquired drug resistance in bacteria. Antibiotics select for drug-resistant strains and refine resistance determinants on plasmids, thus stimulating DNA recombination via the MMR system. Antibiotics can also act as indirect promoters of antibiotic resistance by inducing the SOS system and certain error-prone DNA polymerases. These alterations have clinical consequences in that efficacious treatment of bacterial infections requires high doses of antibiotics and/or a combination of different classes of antimicrobial agents. There are currently few new drugs with low endogenous resistance potential, and the development of such drugs merits further research.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.024083-0
2011-05-01
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/jmm/60/5/563.html?itemId=/content/journal/jmm/10.1099/jmm.0.024083-0&mimeType=html&fmt=ahah

References

  1. Alonso A., Campanario E., Martínez J. L. 1999; Emergence of multidrug-resistant mutants is increased under antibiotic selective pressure in Pseudomonas aeruginosa . Microbiology 145:2857–2862[PubMed]
    [Google Scholar]
  2. Baquero M.-R., Nilsson A. I., Turrientes M. del C., Sandvang D., Galán J. C., Martínez J. L., Frimodt-Møller N., Baquero F., Andersson D. I. 2004; Polymorphic mutation frequencies in Escherichia coli: emergence of weak mutators in clinical isolates. J Bacteriol 186:5538–5542 [View Article][PubMed]
    [Google Scholar]
  3. Baquero M. R., Galán J. C., del Carmen Turrientes M., Cantón R., Coque T. M., Martínez J. L., Baquero F. 2005; Increased mutation frequencies in Escherichia coli isolates harboring extended-spectrum beta-lactamases. Antimicrob Agents Chemother 49:4754–4756 [View Article][PubMed]
    [Google Scholar]
  4. Bayliss C. D. 2009; Determinants of phase variation rate and the fitness implications of differing rates for bacterial pathogens and commensals. FEMS Microbiol Rev 33:504–520 [View Article][PubMed]
    [Google Scholar]
  5. Bayliss C. D., Hoe J. C., Makepeace K., Martin P., Hood D. W., Moxon E. R. 2008; Neisseria meningitidis escape from the bactericidal activity of a monoclonal antibody is mediated by phase variation of lgtG and enhanced by a mutator phenotype. Infect Immun 76:5038–5048 [View Article][PubMed]
    [Google Scholar]
  6. Besier S., Zander J., Kahl B. C., Kraiczy P., Brade V., Wichelhaus T. A. 2008; The thymidine-dependent small-colony-variant phenotype is associated with hypermutability and antibiotic resistance in clinical Staphylococcus aureus isolates. Antimicrob Agents Chemother 52:2183–2189 [View Article][PubMed]
    [Google Scholar]
  7. Blázquez J. 2003; Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. Clin Infect Dis 37:1201–1209 [View Article][PubMed]
    [Google Scholar]
  8. Bridges B. A. 2001; Hypermutation in bacteria and other cellular systems. Philos Trans R Soc Lond B Biol Sci 356:29–39 [View Article][PubMed]
    [Google Scholar]
  9. Cattoir V., Lesprit P., Lascols C., Denamur E., Legrand P., Soussy C. J., Cambau E. 2006; In vivo selection during ofloxacin therapy of Escherichia coli with combined topoisomerase mutations that confer high resistance to ofloxacin but susceptibility to nalidixic acid. J Antimicrob Chemother 58:1054–1057 [View Article][PubMed]
    [Google Scholar]
  10. Chen L., Paulsen D. B., Scruggs D. W., Banes M. M., Reeks B. Y., Lawrence M. L. 2003; Alteration of DNA adenine methylase (Dam) activity in Pasteurella multocida causes increased spontaneous mutation frequency and attenuation in mice. Microbiology 149:2283–2290 [View Article][PubMed]
    [Google Scholar]
  11. Chopra I., O’Neill A. J., Miller K. 2003; The role of mutators in the emergence of antibiotic-resistant bacteria. Drug Resist Updat 6:137–145 [View Article][PubMed]
    [Google Scholar]
  12. Chou H. H., Berthet J., Marx C. J. 2009; Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genet 5:e1000652 [View Article][PubMed]
    [Google Scholar]
  13. Ciofu O., Riis B., Pressler T., Poulsen H. E., Høiby N. 2005; Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob Agents Chemother 49:2276–2282 [View Article][PubMed]
    [Google Scholar]
  14. Cirz R. T., Romesberg F. E. 2006; Induction and inhibition of ciprofloxacin resistance-conferring mutations in hypermutator bacteria. Antimicrob Agents Chemother 50:220–225 [View Article][PubMed]
    [Google Scholar]
  15. Comité de l’Antibiogramme de la Société Française de Microbiologie 2009 http://www.sfm-microbiologie.org/UserFiles/file/CASFM/casfm_2009-1.pdf
  16. Cooper T. F. 2007; Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli . PLoS Biol 5:e225 [View Article][PubMed]
    [Google Scholar]
  17. Daurel C., Prunier A. L., Chau F., Garry L., Leclercq R., Fantin B. 2007; Role of hypermutability on bacterial fitness and emergence of resistance in experimental osteomyelitis due to Staphylococcus aureus . FEMS Immunol Med Microbiol 51:344–349 [View Article][PubMed]
    [Google Scholar]
  18. del Campo R., Morosini M. I., de la Pedrosa E. G., Fenoll A., Muñoz-Almagro C., Máiz L., Baquero F., Cantón R. the Spanish Pneumococcal Infection Study Network 2005; Population structure, antimicrobial resistance, and mutation frequencies of Streptococcus pneumoniae isolates from cystic fibrosis patients. J Clin Microbiol 43:2207–2214 [View Article][PubMed]
    [Google Scholar]
  19. Denamur E., Bonacorsi S., Giraud A., Duriez P., Hilali F., Amorin C., Bingen E., Andremont A., Picard B. et al. 2002; High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J Bacteriol 184:605–609 [View Article][PubMed]
    [Google Scholar]
  20. Dörr T., Lewis K., Vulić M. 2009; SOS response induces persistence to fluoroquinolones in Escherichia coli . PLoS Genet 5:e1000760 [View Article][PubMed]
    [Google Scholar]
  21. Dörr T., Vulić M., Lewis K. 2010; Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli . PLoS Biol 8:e1000317 [View Article][PubMed]
    [Google Scholar]
  22. Driffield K. L., Bostock J. M., Miller K., O’Neill A. J., Hobbs J. K., Chopra I. 2006; Evolution of extended-spectrum beta-lactamases in a MutS-deficient Pseudomonas aeruginosa hypermutator. J Antimicrob Chemother 58:905–907 [View Article][PubMed]
    [Google Scholar]
  23. Eisenstadt E., Carlton B. C., Brown B. J. 1994; Gene mutation. In Methods for General and Molecular Bacteriology pp. 297–316 Edited by Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  24. Ellington M. J., Livermore D. M., Pitt T. L., Hall L. M., Woodford N. 2006; Mutators among CTX-M beta-lactamase-producing Escherichia coli and risk for the emergence of fosfomycin resistance. J Antimicrob Chemother 58:848–852 [View Article][PubMed]
    [Google Scholar]
  25. Foster P. L. 2005; Stress responses and genetic variation in bacteria. Mutat Res 569:3–11[PubMed] [CrossRef]
    [Google Scholar]
  26. Galán J. C., Tato M., Baquero M. R., Turrientes C., Baquero F., Martinez J. L. 2004; Fosfomycin and rifampin disk diffusion tests for detection of Escherichia coli mutator strains. J Clin Microbiol 42:4310–4312 [View Article][PubMed]
    [Google Scholar]
  27. Giraud A., Matic I., Radman M., Fons M., Taddei F. 2002; Mutator bacteria as a risk factor in treatment of infectious diseases. Antimicrob Agents Chemother 46:863–865 [View Article][PubMed]
    [Google Scholar]
  28. Gutiérrez O., Juan C., Pérez J. L., Oliver A. 2004; Lack of association between hypermutation and antibiotic resistance development in Pseudomonas aeruginosa isolates from intensive care unit patients. Antimicrob Agents Chemother 48:3573–3575 [View Article][PubMed]
    [Google Scholar]
  29. Haber L. T., Pang P. P., Sobell D. I., Mankovich J. A., Walker G. C. 1988; Nucleotide sequence of the Salmonella typhimurium mutS gene required for mismatch repair: homology of MutS and HexA of Streptococcus pneumoniae . J Bacteriol 170:197–202[PubMed]
    [Google Scholar]
  30. Harris R. S., Longerich S., Rosenberg S. M. 1994; Recombination in adaptive mutation. Science 264:258–260 [View Article][PubMed]
    [Google Scholar]
  31. Henrichfreise B., Wiegand I., Pfister W., Wiedemann B. 2007; Resistance mechanisms of multiresistant Pseudomonas aeruginosa strains from Germany and correlation with hypermutation. Antimicrob Agents Chemother 51:4062–4070 [View Article][PubMed]
    [Google Scholar]
  32. Hogardt M., Hoboth C., Schmoldt S., Henke C., Bader L., Heesemann J. 2007; Stage-specific adaptation of hypermutable Pseudomonas aeruginosa isolates during chronic pulmonary infection in patients with cystic fibrosis. J Infect Dis 195:70–80 [View Article][PubMed]
    [Google Scholar]
  33. Itakura M., Tabata K., Eda S., Mitsui H., Murakami K., Yasuda J., Minamisawa K. 2008; Generation of Bradyrhizobium japonicum mutants with increased N2O reductase activity by selection after introduction of a mutated dnaQ gene. Appl Environ Microbiol 74:7258–7264 [View Article][PubMed]
    [Google Scholar]
  34. Jiricny J. 1998; Replication errors: cha(lle)nging the genome. EMBO J 17:6427–6436 [View Article][PubMed]
    [Google Scholar]
  35. Kang J. M., Iovine N. M., Blaser M. J. 2006; A paradigm for direct stress-induced mutation in prokaryotes. FASEB J 20:2476–2485 [View Article][PubMed]
    [Google Scholar]
  36. Komp Lindgren P., Karlsson A., Hughes D. 2003; Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother 47:3222–3232 [View Article][PubMed]
    [Google Scholar]
  37. Konstan M. W., Berger M. 1993; Infection and inflammation of the lung in cystic fibrosis. In Lung Biology in Health and Disease vol. 64 pp. 219–276 New York: Marcel Dekker;
    [Google Scholar]
  38. Labat F., Pradillon O., Garry L., Peuchmaur M., Fantin B., Denamur E. 2005; Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis. FEMS Immunol Med Microbiol 44:317–321 [View Article][PubMed]
    [Google Scholar]
  39. LeClerc J. E., Li B., Payne W. L., Cebula T. A. 1996; High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274:1208–1211 [View Article][PubMed]
    [Google Scholar]
  40. Le Gall S., Desbordes L., Gracieux P., Saffroy S., Bousarghin L., Bonnaure-Mallet M., Jolivet-Gougeon A. 2009; Distribution of mutation frequencies among Salmonella enterica isolates from animal and human sources and genetic characterization of a Salmonella Heidelberg hypermutator. Vet Microbiol 137:306–312 [View Article][PubMed]
    [Google Scholar]
  41. Lewin C. S., Amyes S. G. 1991; The role of the SOS response in bacteria exposed to zidovudine or trimethoprim. J Med Microbiol 34:329–332 [View Article][PubMed]
    [Google Scholar]
  42. Li B., Tsui H. C., LeClerc J. E., Dey M., Winkler M. E., Cebula T. A. 2003; Molecular analysis of mutS expression and mutation in natural isolates of pathogenic Escherichia coli . Microbiology 149:1323–1331 [View Article][PubMed]
    [Google Scholar]
  43. López E., Elez M., Matic I., Blázquez J. 2007; Antibiotic-mediated recombination: ciprofloxacin stimulates SOS-independent recombination of divergent sequences in Escherichia coli . Mol Microbiol 64:83–93 [View Article][PubMed]
    [Google Scholar]
  44. Maciá M. D., Borrell N., Pérez J. L., Oliver A. 2004; Detection and susceptibility testing of hypermutable Pseudomonas aeruginosa strains with the Etest and disk diffusion. Antimicrob Agents Chemother 48:2665–2672 [View Article][PubMed]
    [Google Scholar]
  45. Maciá M. D., Blanquer D., Togores B., Sauleda J., Pérez J. L., Oliver A. 2005; Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob Agents Chemother 49:3382–3386 [View Article][PubMed]
    [Google Scholar]
  46. Maciá M. D., Borrell N., Segura M., Gómez C., Pérez J. L., Oliver A. 2006; Efficacy and potential for resistance selection of antipseudomonal treatments in a mouse model of lung infection by hypermutable Pseudomonas aeruginosa . Antimicrob Agents Chemother 50:975–983 [View Article][PubMed]
    [Google Scholar]
  47. Maciá M. D., Mena A., Borrell N., Pérez J. L., Oliver A. 2007; Increased susceptibility to colistin in hypermutable Pseudomonas aeruginosa strains from chronic respiratory infections. Antimicrob Agents Chemother 51:4531–4532 [View Article][PubMed]
    [Google Scholar]
  48. Maiques E., Úbeda C., Campoy S., Salvador N., Lasa I., Novick R. P., Barbé J., Penadés J. R. 2006; β-Lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus . J Bacteriol 188:2726–2729 [View Article][PubMed]
    [Google Scholar]
  49. Marinus M. G. 2010; DNA methylation and mutator genes in Escherichia coli K-12. Mutat Res 705:71–76 [View Article][PubMed]
    [Google Scholar]
  50. Matic I., Radman M., Taddei F., Picard B., Doit C., Bingen E., Denamur E., Elion J. 1997; Highly variable mutation rates in commensal and pathogenic Escherichia coli . Science 277:1833–1834 [View Article][PubMed]
    [Google Scholar]
  51. Mena A., Maciá M. D., Borrell N., Moya B., de Francisco T., Pérez J. L., Oliver A. 2007; Inactivation of the mismatch repair system in Pseudomonas aeruginosa attenuates virulence but favors persistence of oropharyngeal colonization in cystic fibrosis mice. J Bacteriol 189:3665–3668 [View Article][PubMed]
    [Google Scholar]
  52. Mena A., Smith E. E., Burns J. L., Speert D. P., Moskowitz S. M., Perez J. L., Oliver A. 2008; Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J Bacteriol 190:7910–7917 [View Article][PubMed]
    [Google Scholar]
  53. Mérino D., Réglier-Poupet H., Berche P. The European Listeria Genome Consortium Charbit A. 2002; A hypermutator phenotype attenuates the virulence of Listeria monocytogenes in a mouse model. Mol Microbiol 44:877–887 [View Article][PubMed]
    [Google Scholar]
  54. Meyers L. A., Levin B. R., Richardson A. R., Stojiljkovic I. 2003; Epidemiology, hypermutation, within-host evolution and the virulence of Neisseria meningitidis . Proc Biol Sci 270:1667–1677 [View Article][PubMed]
    [Google Scholar]
  55. Miller K., O’Neill A. J., Chopra I. 2002; Response of Escherichia coli hypermutators to selection pressure with antimicrobial agents from different classes. J Antimicrob Chemother 49:925–934 [View Article][PubMed]
    [Google Scholar]
  56. Montanari S., Oliver A., Salerno P., Mena A., Bertoni G., Tümmler B., Cariani L., Conese M., Döring G., Bragonzi A. 2007; Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 153:1445–1454 [View Article][PubMed]
    [Google Scholar]
  57. Morosini M. I., Baquero M. R., Sánchez-Romero J. M., Negri M. C., Galán J. C., del Campo R., Pérez-Díaz J. C., Baquero F. 2003; Frequency of mutation to rifampin resistance in Streptococcus pneumoniae clinical strains: hexA and hexB polymorphisms do not account for hypermutation. Antimicrob Agents Chemother 47:1464–1467 [View Article][PubMed]
    [Google Scholar]
  58. NCCLS 2003 Performance Standards for Antimicrobial Disk Susceptibility Tests Approved Standard , 8th edn..M2–A8 Villanova, PA: National Committee for Clinical Laboratory Standards;
    [Google Scholar]
  59. Negri M.-C., Morosini M.-I., Baquero M.-R., del Campo R., Blázquez J., Baquero F. 2002; Very low cefotaxime concentrations select for hypermutable Streptococcus pneumoniae populations. Antimicrob Agents Chemother 46:528–530 [View Article][PubMed]
    [Google Scholar]
  60. Nouvel L. X., Dos Vultos T., Kassa-Kelembho E., Rauzier J., Gicquel B. 2007; A non-sense mutation in the putative anti-mutator gene ada/alkA of Mycobacterium tuberculosis and M. bovis isolates suggests convergent evolution. BMC Microbiol 7:39 [View Article][PubMed]
    [Google Scholar]
  61. Oliver A. 2010; Mutators in cystic fibrosis chronic lung infection: prevalence, mechanisms, and consequences for antimicrobial therapy. Int J Med Microbiol 300:563–572 [View Article][PubMed]
    [Google Scholar]
  62. Oliver A., Cantón R., Campo P., Baquero F., Blázquez J. 2000; High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–1253 [View Article][PubMed]
    [Google Scholar]
  63. Oliver A., Baquero F., Blázquez J. 2002; The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol Microbiol 43:1641–1650 [View Article][PubMed]
    [Google Scholar]
  64. Oliver A., Levin B. R., Juan C., Baquero F., Blázquez J. 2004; Hypermutation and the preexistence of antibiotic-resistant Pseudomonas aeruginosa mutants: implications for susceptibility testing and treatment of chronic infections. Antimicrob Agents Chemother 48:4226–4233 [View Article][PubMed]
    [Google Scholar]
  65. O’Neill A. J., Chopra I. 2002; Insertional inactivation of mutS in Staphylococcus aureus reveals potential for elevated mutation frequencies, although the prevalence of mutators in clinical isolates is low. J Antimicrob Chemother 50:161–169 [View Article][PubMed]
    [Google Scholar]
  66. O’Neill A. J., Chopra I. 2003; Lack of evidence for involvement of hypermutability in emergence of vancomycin-intermediate Staphylococcus aureus . Antimicrob Agents Chemother 47:1484–1485, author reply 1485 [View Article][PubMed]
    [Google Scholar]
  67. O’Neill A. J., Cove J. H., Chopra I. 2001; Mutation frequencies for resistance to fusidic acid and rifampicin in Staphylococcus aureus . J Antimicrob Chemother 47:647–650 [View Article][PubMed]
    [Google Scholar]
  68. Pal C., Maciá M. D., Oliver A., Schachar I., Buckling A. 2007; Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450:1079–1081 [View Article][PubMed]
    [Google Scholar]
  69. Picard B., Duriez P., Gouriou S., Matic I., Denamur E., Taddei F. 2001; Mutator natural Escherichia coli isolates have an unusual virulence phenotype. Infect Immun 69:9–14 [View Article][PubMed]
    [Google Scholar]
  70. Prudhomme M., Méjean V., Martin B., Claverys J. P. 1991; Mismatch repair genes of Streptococcus pneumoniae: HexA confers a mutator phenotype in Escherichia coli by negative complementation. J Bacteriol 173:7196–7203[PubMed]
    [Google Scholar]
  71. Prunier A. L., Malbruny B., Laurans M., Brouard J., Duhamel J. F., Leclercq R. 2003; High rate of macrolide resistance in Staphylococcus aureus strains from patients with cystic fibrosis reveals high proportions of hypermutable strains. J Infect Dis 187:1709–1716 [View Article][PubMed]
    [Google Scholar]
  72. Quillardet P., Hofnung M. 1993; The SOS chromotest: a review. Mutat Res 297:235–279[PubMed] [CrossRef]
    [Google Scholar]
  73. Reenan R. A., Kolodner R. D. 1992; Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins. Genetics 132:963–973[PubMed]
    [Google Scholar]
  74. Richardson A. R., Yu Z., Popovic T., Stojiljkovic I. 2002; Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. Proc Natl Acad Sci U S A 99:6103–6107 [View Article][PubMed]
    [Google Scholar]
  75. Rodríguez-Rojas A., Blázquez J. 2009; The Pseudomonas aeruginosa pfpI gene plays an antimutator role and provides general stress protection. J Bacteriol 191:844–850 [View Article][PubMed]
    [Google Scholar]
  76. Rosche W. A., Foster P. L. 1999; The role of transient hypermutators in adaptive mutation in Escherichia coli . Proc Natl Acad Sci U S A 96:6862–6867 [View Article][PubMed]
    [Google Scholar]
  77. Sakai A., Nakanishi M., Yoshiyama K., Maki H. 2006; Impact of reactive oxygen species on spontaneous mutagenesis in Escherichia coli . Genes Cells 11:767–778 [View Article][PubMed]
    [Google Scholar]
  78. Saumaa S., Tover A., Tark M., Tegova R., Kivisaar M. 2007; Oxidative DNA damage defense systems in avoidance of stationary-phase mutagenesis in Pseudomonas putida . J Bacteriol 189:5504–5514 [View Article][PubMed]
    [Google Scholar]
  79. Schaaff F., Reipert A., Bierbaum G. 2002; An elevated mutation frequency favors development of vancomycin resistance in Staphylococcus aureus . Antimicrob Agents Chemother 46:3540–3548 [View Article][PubMed]
    [Google Scholar]
  80. Schofield M. J., Hsieh P. 2003; DNA mismatch repair: molecular mechanisms and biological function. Annu Rev Microbiol 57:579–608 [View Article][PubMed]
    [Google Scholar]
  81. Scott J., Thompson-Mayberry P., Lahmamsi S., King C. J., McShan W. M. 2008; Phage-associated mutator phenotype in group A streptococcus . J Bacteriol 190:6290–6301 [View Article][PubMed]
    [Google Scholar]
  82. Siegel E. C., Bryson V. 1967; Mutator gene of Escherichia coli B. J Bacteriol 94:38–47[PubMed]
    [Google Scholar]
  83. Taddei F., Radman M., Maynard-Smith J., Toupance B., Gouyon P. H., Godelle B. 1997; Role of mutator alleles in adaptive evolution. Nature 387:700–702 [View Article][PubMed]
    [Google Scholar]
  84. Tompkins J. D., Nelson J. L., Hazel J. C., Leugers S. L., Stumpf J. D., Foster P. L. 2003; Error-prone polymerase, DNA polymerase IV, is responsible for transient hypermutation during adaptive mutation in Escherichia coli . J Bacteriol 185:3469–3472 [View Article][PubMed]
    [Google Scholar]
  85. Tsui H. C., Feng G., Winkler M. E. 1997; Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J Bacteriol 179:7476–7487[PubMed]
    [Google Scholar]
  86. Turrientes M. C., Baquero M. R., Sánchez M. B., Valdezate S., Escudero E., Berg G., Cantón R., Baquero F., Galán J. C., Martínez J. L. 2010; Polymorphic mutation frequencies of clinical and environmental Stenotrophomonas maltophilia populations. Appl Environ Microbiol 76:1746–1758 [View Article][PubMed]
    [Google Scholar]
  87. Úbeda C., Maiques E., Knecht E., Lasa I., Novick R. P., Penadés J. R. 2005; Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol 56:836–844 [View Article][PubMed]
    [Google Scholar]
  88. Watson M. E. Jr, Burns J. L., Smith A. L. 2004; Hypermutable Haemophilus influenzae with mutations in mutS are found in cystic fibrosis sputum. Microbiology 150:2947–2958 [View Article][PubMed]
    [Google Scholar]
  89. Willems R. J., Top J., Smith D. J., Roper D. I., North S. E., Woodford N. 2003; Mutations in the DNA mismatch repair proteins MutS and MutL of oxazolidinone-resistant or -susceptible Enterococcus faecium . Antimicrob Agents Chemother 47:3061–3066 [View Article][PubMed]
    [Google Scholar]
  90. Worth L. Jr, Clark S., Radman M., Modrich P. 1994; Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc Natl Acad Sci U S A 91:3238–3241 [View Article][PubMed]
    [Google Scholar]
  91. Wright B. E. 1996; The effect of the stringent response on mutation rates in Escherichia coli K-12. Mol Microbiol 19:213–219 [View Article][PubMed]
    [Google Scholar]
  92. Ysern P., Clerch B., Castańo M., Gibert I., Barbé J., Llagostera M. 1990; Induction of SOS genes in Escherichia coli and mutagenesis in Salmonella typhimurium by fluoroquinolones. Mutagenesis 5:63–66 [View Article][PubMed]
    [Google Scholar]
  93. Zahrt T. C., Mora G. C., Maloy S. 1994; Inactivation of mismatch repair overcomes the barrier to transduction between Salmonella typhimurium and Salmonella typhi . J Bacteriol 176:1527–1529[PubMed]
    [Google Scholar]
  94. Zaleski P., Piekarowicz A. 2004; Characterization of a dam mutant of Haemophilus influenzae Rd. Microbiology 150:3773–3781 [View Article][PubMed]
    [Google Scholar]
  95. Zeibell K., Aguila S., Yan Shi V., Chan A., Yang H., Miller J. H. 2007; Mutagenesis and repair in Bacillus anthracis: the effect of mutators. J Bacteriol 189:2331–2338 [View Article][PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.024083-0
Loading
/content/journal/jmm/10.1099/jmm.0.024083-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error