Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections

Antimicrobial Agents and Chemotherapy

Volumn 47, Issue 10, 2003, Pages 3222-3232

  Lindgren, Patricia Komp ^a   Karlsson, Åsa ^a,b   Hughes, Diarmaid ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b AB BIODISK   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL DNA; CARRIER PROTEIN; CHLORAMPHENICOL; CIPROFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING); MECILLINAM; NALIDIXIC ACID; NORFLOXACIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; QUINOLONE DERIVATIVE; TETRACYCLINE; TRIMETHOPRIM;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; DNA SEQUENCE; DRUG EFFECT; ESCHERICHIA COLI; GENE AMPLIFICATION; GENE GYRA; GENE GYRB; GENE MAROR; GENE MUTATION; GENE PARC; GENE PARE; GENETICS; GENOTYPE; HUMAN; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR EVOLUTION; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; URINARY TRACT INFECTION;

ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; CIPROFLOXACIN; DNA TOPOISOMERASES, TYPE II, BACTERIAL; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; FLUOROQUINOLONES; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MUTATION; NORFLOXACIN; URINARY TRACT INFECTIONS;

EID: 0141924871     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.47.10.3222-3232.2003     Document Type: Article

References (65)

1. Abdulkarim, F., and D. Hughes. 1996. Homologous recombination between the tuf genes of Salmonella typhimurium. J. Mol. Biol. 260:506-522.
2. Alekshun, M. N., and S. B. Levy. 1999. The mar regulon: multiple resistance to antibiotics and other toxic chemicals. Trends Microbiol. 7:410-413.
3. Alekshun, M. N., and S. B. Levy. 1997. Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob. Agents Chemother. 41:2067-2075.
4. Aono, R., M. Kobayashi, H. Nakajima, and H. Kobayashi. 1995. A close correlation between improvement of organic solvent tolerance levels and alteration of resistance toward low levels of multiple antibiotics in Escherichia coli. Biosci. Biotechnol. Biochem. 59:213-218.
5. Asako, H., H. Nakajima, K. Kobayashi, M. Kobayashi, and R. Aono. 1997. Organic solvent tolerance and antibiotic resistance increased by overexpression of marA in Escherichia coli. Appl. Environ. Microbiol. 63:1428-1433.
6. Bachoual, R., J. Tankovic, and C. J. Soussy. 1998. Analysis of the mutations involved in fluoroquinolone resistance of in vivo and in vitro mutants of Escherichia coli. Microb. Drug Resist. 4:271-276.
7. Ball, P. 2003. Adverse drug reactions: implications for the development of fluoroquinolones. J. Antimicrob. Chemother. 51(Suppl. 1):21-27.
8. Bebear, C. M., O. Grau, A. Charron, H. Renaudin, D. Gruson, and C. Bebear. 2000. Cloning and nucleotide sequence of the DNA gyrase (gyrA) gene from Mycoplasma hominis and characterization of quinolone-resistant mutants selected in vitro with trovafloxacin. Antimicrob. Agents Chemother. 44:2719-2727.
9. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
10. Breines, D. M., S. Ouabdesselam, E. Y. Ng, J. Tankovic, S. Shah, C. J. Soussy, and D. C. Hooper. 1997. Quinolone resistance locus nfxD of Escherichia coli is a mutant allele of the parE gene encoding a subunit of topoisomerase IV. Antimicrob. Agents Chemother. 41:175-179.
11. Clermont, O., S. Bonacorsi, and E. Bingen. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66:4555-4558.
12. Cohen, S. P., L. M. McMurry, and S. B. Levy. 1988. marA locus causes decreased expression of OmpF porin in multiple-antibiotic-resistant (Mar) mutants of Escherichia coli. J. Bacteriol. 170:5416-5422.
13. Denamur, E., S. Bonacorsi, A. Giraud, P. Duriez, F. Hilali, C. Amorin, E. Bingen, A. Andremont, B. Picard, F. Taddei, and I. Matic. 2002. High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J. Bacteriol. 184:605-609.
14. Everett, M. J., Y. F. Jin, V. Ricci, and L. J. Piddock. 1996. Contributions of individual mechanisms to fluoroquinolone resistance in 36 Escherichia coli strains isolated from humans and animals. Antimicrob. Agents Chemother. 40:2380-2386.
15. Fournier, B., and D. C. Hooper. 1998. Mutations in topoisomerase IV and DNA gyrase of Staphylococcus aureus: novel pleiotropic effects on quinolone and coumarin activity. Antimicrob. Agents Chemother. 42:121-128.
16. Friedman, S. M., T. Lu, and K. Drlica. 2001. Mutation in the DNA gyrase A gene of Escherichia coli that expands the quinolone resistance-determining region. Antimicrob. Agents Chemother. 45:2378-2380.
17. Giraud, A., I. Matic, M. Radman, M. Fons, and F. Taddei. 2002. Mutator bacteria as a risk factor in treatment of infectious diseases. Antimicrob. Agents Chemother. 46:863-865.
18. Giraud, A., I. Matic, O. Tenaillon, A. Clara, M. Radman, M. Fons, and F. Taddei. 2001. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291:2606-2608.
19. Giraud, A., M. Radman, I. Matic, and F. Taddei. 2001. The rise and fall of mutator bacteria. Curr. Opin. Microbiol. 4:582-585.
20. Goettsch, W., W. van Pelt, N. Nagelkerke, M. G. Hendrix, A. G. Buiting, P. L. Petit, L. J. Sabbe, A. J. van Griethuysen, and A. J. de Neeling. 2000. Increasing resistance to fluoroquinolones in Escherichia coli from urinary tract infections in The Netherlands. J. Antimicrob. Chemother. 46:223-228.
21. Gootz, T. D., R. P. Zaniewski, S. L. Haskell, F. S. Kaczmarek, and A. E. Maurice. 1999. Activities of trovafloxacin compared with those of other fluoroquinolones against purified topoisomerases and gyrA and grlA mutants of Staphylococcus aureus. Antimicrob. Agents Chemother. 43:1845-1855.
22. Grkovic, S., M. H. Brown, and R. A. Skurray. 2002. Regulation of bacterial drug export systems. Microbiol. Mol. Biol. Rev. 66:671-701.
23. Heisig, P. 1996. Genetic evidence for a role of parC mutations in development of high-level fluoroquinolone resistance in Escherichia coli. Antimicrob. Agents Chemother. 40:879-885.
24. Heisig, P., and R. Tschorny. 1994. Characterization of fluoroquinolone-resistant mutants of Escherichia coli selected in vitro. Antimicrob. Agents Chemother. 38:1284-1291.
25. Hooper, D. C. 1999. Mechanisms of fluoroquinolone resistance. Drug Resist. Update 2:38-55.
26. Hooper, D. C., J. S. Wolfson, M. A. Bozza, and E. Y. Ng. 1992. Genetics and regulation of outer membrane protein expression by quinolone resistance loci nfxB, nfxC, and cfxB. Antimicrob. Agents Chemother. 36:1151-1154.
27. Hooton, T. M. 2000. Pathogenesis of urinary tract infections: an update. J. Antimicrob. Chemother. 46(Suppl. 1):1-7.
28. Hooton, T. M., D. Scholes, J. P. Hughes, C. Winter, P. L. Roberts, A. E. Stapleton, A. Stergachis, and W. E. Stamm. 1996. A prospective study of risk factors for symptomatic urinary tract infection in young women. N. Engl. J. Med. 335:468-474.
29. Hultgren, S. J., W. R. Schwan, A. J. Schaeffer, and J. L. Duncan. 1986. Regulation of production of type 1 pili among urinary tract isolates of Escherichia coli. Infect. Immun. 54:613-620.
30. Jacoby, G. A., N. Chow, and K. B. Waites. 2003. Prevalence of plasmid-mediated quinolone resistance. Antimicrob. Agents Chemother. 47:559-562.
31. Jellen-Ritter, A. S., and W. V. Kern. 2001. Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants selected with a fluoroquinolone. Antimicrob. Agents Chemother. 45:1467-1472.
32. Jin, D. J., and C. A. Gross. 1988. Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance. J. Mol. Biol. 202:45-58.
33. Kahlmeter, G. 2000. The ECO.SENS Project: a prospective, multinational, multicentre epidemiological survey of the prevalence and antimicrobial susceptibility of urinary tract pathogens - interim report. J. Antimicrob. Chemother. 46(Suppl. 1):15-22.
34. Kahlmeter, G. 2003. An international survey of the antimicrobial susceptibility of pathogens from uncomplicated urinary tract infections: the ECO.SENS Project. J. Antimicrob. Chemother. 51:69-76.
35. Kern, W. V., M. Oethinger, A. S. Jellen-Ritter, and S. B. Levy. 2000. Non-target gene mutations in the development of fluoroquinolone resistance in Escherichia coli. Antimicrob. Agents Chemother. 44:814-820.
36. Kumagai, Y., J. I. Kato, K. Hoshino, T. Akasaka, K. Sato, and H. Ikeda. 1996. Quinolone-resistant mutants of Escherichia coli DNA topoisomerase IV parC gene. Antimicrob. Agents Chemother. 40:710-714.
37. Langermann, S., R. Mollby, J. E. Burlein, S. R. Palaszynski, C. G. Auguste, A. DeFusco, R. Strouse, M. A. Schenerman, S. J. Hultgren, J. S. Pinkner, J. Winberg, L. Guldevall, M. Soderhall, K. Ishikawa, S. Normark, and S. Koenig. 2000. Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J. Infect. Dis. 181:774-778.
38. LeClerc, J. E., B. Li, W. L. Payne, and T. A. Cebula. 1996. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274:1208-1211.
39. Linde, H. J., F. Notka, M. Metz, B. Kochanowski, P. Heisig, and N. Lehn. 2000. In vivo increase in resistance to ciprofloxacin in Escherichia coli associated with deletion of the C-terminal part of MarR. Antimicrob. Agents Chemother. 44:1865-1868.
40. Luria, S. E., and M. Delbrück. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491-511.
41. Maneewannakul, K., and S. B. Levy. 1996. Identification for mar mutants among quinolone-resistant clinical isolates of Escherichia coli. Antimicrob. Agents Chemother. 40:1695-1698.
42. Martin, R. G., K. W. Jair, R. E. Wolf, Jr., and J. L. Rosner. 1996. Autoactivation of the marRAB multiple antibiotic resistance operon by the MarA transcriptional activator in Escherichia coli. J. Bacteriol. 178:2216-2223.
43. Martinez-Martinez, L., A. Pascual, and G. A. Jacoby. 1998. Quinolone resistance from a transferable plasmid. Lancet 351:797-799.
44. Matic, I., M. Radman, F. Taddei, B. Picard, C. Doit, E. Bingen, E. Denamur, and J. Elion. 1997. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277:1833-1834.
45. Naber, K. G. 2000. Survey on antibiotic usage in the treatment of urinary tract infections. J. Antimicrob. Chemother. 46(Suppl. 1):49-52.
46. Naber, K. G. 2000. Treatment options for acute uncomplicated cystitis in adults. J. Antimicrob. Chemother. 46(Suppl. 1):23-27.
47. Oethinger, M., W. V. Kern, J. D. Goldman, and S. B. Levy. 1998. Association of organic solvent tolerance and fluoroquinolone resistance in clinical isolates of Escherichia coli. J. Antimicrob. Chemother. 41:111-114.
48. Oethinger, M., I. Podglajen, W. V. Kern, and S. B. Levy. 1998. Overexpression of the marA or soxS regulatory gene in clinical topoisomerase mutants of Escherichia coli. Antimicrob. Agents Chemother. 42:2089-2094.
49. Okusu, H., D. Ma, and H. Nikaido. 1996. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J. Bacteriol. 178:306-308.
50. Oliver, A., R. Canton, P. Campo, F. Baquero, and J. Blazquez. 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251-1254.
51. Pan, X. S., and L. M. Fisher. 1998. DNA gyrase and topoisomerase IV are dual targets of clinafloxacin action in Streptococcuspneumoniae. Antimicrob. Agents Chemother. 42:2810-2816.
52. Park, Y. H., J. H. Yoo, D. H. Huh, Y. K. Cho, J. H. Choi, and W. S. Shin. 1998. Molecular analysis of fluoroquinolone-resistance in Escherichia coli on the aspect of gyrase and multiple antibiotic resistance (mar) genes. Yonsei Med. J. 39:534-540.
53. Perichon, B., J. Tankovic, and P. Courvalin. 1997. Characterization of a mutation in the parE gene that confers fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 41:1166-1167.
54. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
55. Schmitz, F. J., M. E. Jones, B. Hofmann, B. Hansen, S. Scheuring, M. Luckefahr, A. Fluit, J. Verhoef, U. Hadding, H. P. Heinz, and K. Kohrer. 1998. Characterization of grlA, grlB, gyrA, and gyrB mutations in 116 unrelated isolates of Staphylococcus aureus and effects of mutations on ciprofloxacin MIC. Antimicrob. Agents Chemother. 42:1249-1252.
56. Taddei, F., M. Radman, J. Maynard-Smith, B. Toupance, P. H. Gouyon, and B. Godelle. 1997. Role of mutator alleles in adaptive evolution. Nature 387:700-702.
57. Travis, J. M., and E. R. Travis. 2002. Mutator dynamics in fluctuating environments. Proc. R. Soc. London Ser. B Biol. Sci. 269:591-597.
58. Walsh, C. 2000. Molecular mechanisms that confer antibacterial drug resistance. Nature 406:775-781.
59. Wang, H., J. L. Dzink-Fox, M. Chen, and S. B. Levy. 2001. Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: role of acrR mutations. Antimicrob. Agents Chemother. 45:1515-1521.
60. Webber, M. A., and L. J. Piddock. 2001. Absence of mutations in marRAB or soxRS in acrB-overexpressing fluoroquinolone-resistant clinical and veterinary isolates of Escherichia coli. Antimicrob. Agents Chemother. 45:1550-1552.
61. White, D. G., J. D. Goldman, B. Demple, and S. B. Levy. 1997. Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or roba in Escherichia coli. J. Bacteriol. 179:6122-6126.
62. Yamagishi, J., H. Yoshida, M. Yamayoshi, and S. Nakamura. 1986. Nalidixic acid-resistant mutations of the gyrB gene of Escherichia coli. Mol. Gen. Genet. 204:367-373.
63. Yang, S., S. R. Clayton, and E. L. Zechiedrich. 2003. Relative contributions of the AcrAB, MdfA and NorE efflux pumps to quinolone resistance in Escherichia coli. J. Antimicrob. Chemother. 51:545-556.
64. Yoshida, H., M. Bogaki, M. Nakamura, and S. Nakamura. 1990. Quinolone resistance-determining region in the DNA gyrase gyrA gene of Escherichia coli. Antimicrob. Agents Chemother. 34:1271-1272.
65. Yoshida, H., M. Bogaki, M. Nakamura, L. M. Yamanaka, and S. Nakamura. 1991. Quinolone resistance-determining region in the DNA gyrase gyrB gene of Escherichia coli. Antimicrob. Agents Chemother. 35:1647-1650.