Quantitative contributions of target alteration and decreased drug accumulation to pseudomonas aeruginosa fluoroquinolone resistance

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 3, 2013, Pages 1361-1368

  Bruchmann, Sebastian ^a,b   Dötsch, Andreas ^a,b   Nouri, Bianka ^a,b   Chaberny, Iris F ^c   Häussler, Susanne ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CIPROFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING) A; DNA TOPOISOMERASE (ATP HYDROLYSING) B; MEROPENEM; MEXAB OPRM PROTEIN; MEXCD OPRJ PROTEIN; MEXEF OPRN PROTEIN; MEXR PROTEIN; MEXS PROTEIN; MEXXY OPRM PROTEIN; MEXZ PROTEIN; NFXB PROTEIN; PROTEIN PARC; PROTEIN PARE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; ESCHERICHIA COLI; GENE EXPRESSION; GENE INACTIVATION; GENE MUTATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; SINGLE NUCLEOTIDE POLYMORPHISM;

ANTI-BACTERIAL AGENTS; BIOLOGICAL TRANSPORT; DNA GYRASE; DNA TOPOISOMERASE IV; DRUG RESISTANCE, BACTERIAL; FLUOROQUINOLONES; GENE EXPRESSION; MICROBIAL SENSITIVITY TESTS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION; PSEUDOMONAS AERUGINOSA;

EID: 84874027222     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01581-12     Document Type: Article

References (54)

1. Drlica K, Zhao X. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Mol. Biol. Rev. 61:377-392.
2. Hooper DC, Wolfson JS. 1991. Fluoroquinolone antimicrobial agents. N. Engl. J. Med. 324:384 -394.
3. Shorr AF. 2009. Review of studies of the impact of Gram-negative bacterial resistance on outcomes in the intensive care unit. Crit. Care Med. 37:1463-1469.
4. Gasink LB, Fishman NO, Weiner MG, Nachamkin I, Bilker WB, Lautenbach E. 2006. Fluoroquinolone-resistant Pseudomonas aeruginosa: assessment of risk factors and clinical impact. Am. J. Med. 119:526.e519- 526.e525. doi:10.1016/j.amjmed.2005.11.029.
5. Obritsch MD, Fish DN, MacLaren R, Jung R. 2005. Nosocomial infections due to multidrug-resistant Pseudomonas aeruginosa: epidemiology and treatment options. Pharmacotherapy 25:1353-1364.
6. Drlica K, Hiasa H, Kerns R, Malik M, Mustaev A, Zhao X. 2009. Quinolones: action and resistance updated. Curr. Top. Med. Chem. 9:981-998.
7. Ruiz J. 2003. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J. Antimicrob. Chemother. 51:1109 -1117.
8. Hooper DC, Wolfson JS. 1989. Bacterial resistance to the quinolone antimicrobial agents. Am. J. Med. 87(6C):17S-23S.
9. Poole K. 2005. Efflux-mediated antimicrobial resistance. J. Antimicrob. Chemother. 56:20 -51.
10. Yoshida H, Bogaki M, Nakamura M, Nakamura S. 1990. Quinolone resistance-determining region in the DNA gyrase gyrA gene of Escherichia coli. Antimicrob. Agents Chemother. 34:1271-1272.
11. Barnard FM, Maxwell A. 2001. Interaction between DNA gyrase and quinolones: effects of alanine mutations at GyrA subunit residues Ser83 and Asp87. Antimicrob. Agents Chemother. 45:1994 -2000.
12. Tran JH, Jacoby GA. 2002. Mechanism of plasmid-mediated quinolone resistance. Proc. Natl. Acad. Sci. U.S.A. 99:5638 -5642.
13. Perichon B, Courvalin P, Galimand M. 2007. Transferable resistance to aminoglycosides by methylation of G1405 in 16S rRNA and to hydrophilic fluoroquinolones by QepA-mediated efflux in Escherichia coli. Antimicrob. Agents Chemother. 51:2464 -2469.
14. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, Bush K, Hooper DC. 2006. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat. Med. 12:83- 88.
15. Doostzadeh J, Shokralla S, Absalan F, Jalili R, Mohandessi S, Langston JW, Davis RW, Ronaghi M, Gharizadeh B. 2008. High throughput automated allele frequency estimation by pyrosequencing. PLoS One 3:e2693. doi:10.1371/journal. pone.0002693.
16. Royo JL, Hidalgo M, Ruiz A. 2007. Pyrosequencing protocol using a universal biotinylated primer for mutation detection and SNP genotyping. Nat. Protoc. 2:1734 -1739.
17. Rozen S, Skaletsky H. 2000. Primer3 on theWWWfor general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
18. Tomás M, Doumith M, Warner M, Turton JF, Beceiro A, Bou G, Livermore DM, Woodford N. 2010. Efflux pumps, OprD porin, AmpC beta-lactamase, and multiresistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob. Agents Chemother. 54:2219- 2224.
19. Cabot G, Ocampo-Sosa AA, Tubau F, Macia MD, Rodriguez C, Moya B, Zamorano L, Suarez C, Pena C, Martinez-Martinez L, Oliver A, Spanish Network for Research in Infectious Diseases. 2011. Overexpression of AmpC and efflux pumps in Pseudomonas aeruginosa isolates from bloodstream infections: prevalence and impact on resistance in a Spanish multicenter study. Antimicrob. Agents Chemother. 55:1906 -1911.
20. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77- 86.
21. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
22. Wiegand I, Hilpert K, Hancock RE. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3:163-175.
23. Heeb S, Itoh Y, Nishijyo T, Schnider U, Keel C, Wade J, Walsh U, O'Gara F, Haas D. 2000. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in Gram-negative, plant-associated bacteria. Mol. Plant Microbe Interact. 13:232-237.
24. Gorgani N, Ahlbrand S, Patterson A, Pourmand N. 2009. Detection of point mutations associated with antibiotic resistance in Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 34:414-418.
25. Yoshida H, Nakamura M, Bogaki M, Nakamura S. 1990. Proportion of DNA gyrase mutants among quinolone-resistant strains of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 34:1273-1275.
26. Nakano M, Deguchi T, Kawamura T, Yasuda M, Kimura M, Okano Y, Kawada Y. 1997. Mutations in the gyrA and parC genes in fluoroquinolone- resistant clinical isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 41:2289 -2291.
27. Jalal S, Wretlind B. 1998. Mechanisms of quinolone resistance in clinical strains of Pseudomonas aeruginosa. Microb. Drug Resist. 4:257-261.
28. Mouneimne H, Robert J, Jarlier V, Cambau E. 1999. Type II topoisomerase mutations in ciprofloxacin-resistant strains of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 43:62- 66.
29. Takenouchi T, Sakagawa E, Sugawara M. 1999. Detection of gyrA mutations among 335 Pseudomonas aeruginosa strains isolated in Japan and their susceptibilities to fluoroquinolones. Antimicrob. Agents Chemother. 43:406-409.
30. Lee JK, Lee YS, Park YK, Kim BS. 2005. Alterations in the GyrA and GyrB subunits of topoisomerase II and the ParC and ParE subunits of topoisomerase IV in ciprofloxacin-resistant clinical isolates of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 25:290 -295.
31. Cambau E, Perani E, Dib C, Petinon C, Trias J, Jarlier V. 1995. Role of mutations in DNA gyrase genes in ciprofloxacin resistance of Pseudomonas aeruginosa susceptible or resistant to imipenem. Antimicrob. Agents Chemother. 39:2248 -2252.
32. Oh H, Stenhoff J, Jalal S, Wretlind B. 2003. Role of efflux pumps and mutations in genes for topoisomerases II and IV in fluoroquinoloneresistant Pseudomonas aeruginosa strains. Microb. Drug Resist. 9:323-328.
33. Akasaka T, Tanaka M, Yamaguchi A, Sato K. 2001. Type II topoisomerase mutations in fluoroquinolone-resistant clinical strains of Pseudomonas aeruginosa isolated in 1998 and 1999: role of target enzyme in mechanism of fluoroquinolone resistance. Antimicrob. Agents Chemother. 45: 2263-2268.
34. Jalal S, Ciofu O, Hoiby N, Gotoh N, Wretlind B. 2000. Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob. Agents Chemother. 44: 710-712.
35. Wong A, Kassen R. 2011. Parallel evolution and local differentiation in quinolone resistance in Pseudomonas aeruginosa. Microbiology 157:937- 944.
36. 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.
37. Pedersen SS, Jensen T, Hvidberg EF. 1987. Comparative pharmacokinetics of ciprofloxacin and ofloxacin in cystic fibrosis patients. J. Antimicrob. Chemother. 20:575-583.
38. Bagel S, Hullen V, Wiedemann B, Heisig P. 1999. Impact of gyrA and parC mutations on quinolone resistance, doubling time, and supercoiling degree of Escherichia coli. Antimicrob. Agents Chemother. 43:868-875.
39. Higgins PG, Fluit AC, Milatovic D, Verhoef J, Schmitz FJ. 2003. Mutations in GyrA, ParC, MexR and NfxB in clinical isolates of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 21:409-413.
40. Wang DD, Sun TY, Hu YJ. 2007. Contributions of efflux pumps to high level resistance of Pseudomonas aeruginosa to ciprofloxacin. Chin. Med. J. 120:68 -70.
41. Rejiba S, Aubry A, Petitfrere S, Jarlier V, Cambau E. 2008. Contribution of ParE mutation and efflux to ciprofloxacin resistance in Pseudomonas aeruginosa clinical isolates. J. Chemother. 20:749 -752.
42. Dunham SA, McPherson CJ, Miller AA. 2010. The relative contribution of efflux and target gene mutations to fluoroquinolone resistance in recent clinical isolates of Pseudomonas aeruginosa. Eur. J. Clin. Microbiol. Infect. Dis. 29:279 -288.
43. El Amin N, Giske CG, Jalal S, Keijser B, Kronvall G, Wretlind B. 2005. Carbapenem resistance mechanisms in Pseudomonas aeruginosa: alterations of porin OprD and efflux proteins do not fully explain resistance patterns observed in clinical isolates. APMIS 113:187-196.
44. Pai H, Kim J, Lee JH, Choe KW, Gotoh N. 2001. Carbapenem resistance mechanisms in Pseudomonas aeruginosa clinical isolates. Antimicrob. Agents Chemother. 45:480-484.
45. Mulet X, Moya B, Juan C, Macia MD, Perez JL, Blazquez J, Oliver A. 2011. Antagonistic interactions of Pseudomonas aeruginosa antibiotic resistance mechanisms in planktonic but not biofilm growth. Antimicrob. Agents Chemother. 55:4560-4568.
46. Lomovskaya O, Lee A, Hoshino K, Ishida H, Mistry A, Warren MS, Boyer E, Chamberland S, Lee VJ. 1999. Use of a genetic approach to evaluate the consequences of inhibition of efflux pumps in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 43:1340 -1346.
47. Breidenstein EB, Khaira BK, Wiegand I, Overhage J, Hancock RE. 2008. Complex ciprofloxacin resistome revealed by screening a Pseudomonas aeruginosa mutant library for altered susceptibility. Antimicrob. Agents Chemother. 52:4486-4491.
48. Dötsch A, Becker T, Pommerenke C, Magnowska Z, Jänsch L, Häussler S. 2009. Genomewide identification of genetic determinants of antimicrobial drug resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 53:2522-2531.
49. Robicsek A, Jacoby GA, Hooper DC. 2006. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect. Dis. 6:629-640.
50. Li X, Mariano N, Rahal JJ, Urban CM, Drlica K. 2004. Quinoloneresistant Haemophilus influenzae: determination of mutant selection window for ciprofloxacin, garenoxacin, levofloxacin, and moxifloxacin. Antimicrob. Agents Chemother. 48:4460-4462.
51. Heisig P, Tschorny R. 1994. Characterization of fluoroquinoloneresistant mutants of Escherichia coli selected in vitro. Antimicrob. Agents Chemother. 38:1284 -1291.
52. Singh R, Swick MC, Ledesma KR, Yang Z, Hu M, Zechiedrich L, Tam VH. 2012. Temporal interplay between efflux pumps and target mutations in development of antibiotic resistance in Escherichia coli. Antimicrob. Agents Chemother. 56:1680 -1685.
53. Drlica K. 2003. The mutant selection window and antimicrobial resistance. J. Antimicrob. Chemother. 52:11-17.
54. Gullberg E, Cao S, Berg OG, Ilback C, Sandegren L, Hughes D, Andersson DI. 2011. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog. 7:e1002158. doi:10.1371/journal.ppat.1002158.