Interplay between plasmid-mediated and chromosomal-mediated fluoroquinolone resistance and bacterial fitness in Escherichia coli

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 12, 2014, Pages 3203-3215

  Machuca, Jesús ^a   Briales, Alejandra ^b,c   Labrador, Gema ^c,d   Díaz de Alba, Paula ^b   López Rojas, Rafael ^c,d   Docobo Pérez, Fernando ^a,c   Martínez Martínez, Luis ^c,e,f   Rodríguez Baño, Jesús ^a,b,c   Pachón, Maria Eugenia ^c,d   Pascual, Álvaro ^a,b,c   Rodríguez Martínez, José Manuel ^b,c  

^a HOSPITAL UNIVERSITARIO VIRGEN MACARENA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^e HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^f UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Bacterial fitness; Qnr; Quinolones

Indexed keywords

CIPROFLOXACIN; LEVOFLOXACIN; MOXIFLOXACIN; NORFLOXACIN; OFLOXACIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; REACTIVE OXYGEN METABOLITE; ANTIINFECTIVE AGENT; QUINOLONE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BROTH DILUTION; ESCHERICHIA COLI; FEMALE; GENE DELETION; GENE MUTATION; GENOTYPE; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; MOUSE; MUTANT; MUTATION RATE; NONHUMAN; PHENOTYPE; PLASMID; QNR GENE; QNRA1 GENE; QNRS1 GENE; ANIMAL; BACTERIAL LOAD; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; ESCHERICHIA COLI INFECTION; GENETIC RECOMBINATION; GROWTH, DEVELOPMENT AND AGING; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MUTATION; PHYSIOLOGY; VIRULENCE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL LOAD; CHROMOSOMES, BACTERIAL; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; FLUOROQUINOLONES; GENES, BACTERIAL; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; MUTATION; PLASMIDS; RECOMBINATION, GENETIC; VIRULENCE;

EID: 84929342177     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dku308     Document Type: Article

References (60)

1. Andriole VT. The quinolones: past, present, and future. Clin Infect Dis 2005; 41 Suppl 2: S113-9.
2. Kohanski MA, Dwyer DJ, Collins JJ. How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 2010; 8: 423-35.
3. Kohanski MA, Dwyer DJ, Hayete B et al. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 2007; 130: 797-810.
4. Strahilevitz J, Jacoby GA, Hooper DC et al. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 2009; 22: 664-89.
5. Briales A, Rodriguez-Martinez JM, Velasco C et al. In vitro effect of qnrA1, qnrB1, and qnrS1 genes on fluoroquinolone activity against isogenic Escherichia coli isolates with mutations in gyrA and parC. Antimicrob Agents Chemother 2011; 55: 1266-9.
6. Marcusson LL, Frimodt-Moller N, Hughes D. Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 2009; 5: e1000541.
7. Andersson DI. The biological cost of mutational antibiotic resistance: any practical conclusions? Curr Opin Microbiol 2006; 9: 461-5.
8. Drlica K, Hiasa H, Kerns R et al. Quinolones: action and resistance updated. Curr Top Med Chem 2009; 9: 981-98.
9. Rodriguez-Martinez JM, Cano ME, Velasco C et al. Plasmid-mediated quinolone resistance: an update. J Infect Chemother 2011; 17: 149-82.
10. Robicsek A, Strahilevitz J, Jacoby GA et al. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 2006; 12: 83-8.
11. Hansen LH, Johannesen E, Burmolle M et al. Plasmid-encoded multidrug efflux pump conferring resistance to olaquindox in Escherichia coli. Antimicrob Agents Chemother 2004; 48: 3332-7.
12. Yamane K, Wachino J, Suzuki S et al. New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother 2007; 51: 3354-60.
13. Cambau E, Lascols C, Sougakoff W et al. Occurrence of qnrA-positive clinical isolates in French teaching hospitals during 2002-2005. Clin Microbiol Infect 2006; 12: 1013-20.
14. Tran JH, Jacoby GA. Mechanism of plasmid-mediated quinolone resistance. Proc Natl Acad Sci USA 2002; 99: 5638-42.
15. Andersson DI, Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 2010; 8: 260-71.
16. Komp Lindgren P, Marcusson LL, Sandvang D et al. Biological cost of single and multiple norfloxacin resistance mutations in Escherichia coli implicated in urinary tract infections. Antimicrob Agents Chemother 2005; 49: 2343-51.
17. Fernandez A, Perez A, Ayala JA et al. Expression of OXA-type and SFO-1 b-lactamases induces changes in peptidoglycan composition and affects bacterial fitness. Antimicrob Agents Chemother 2012; 56: 1877-84.
18. Jacoby GA. Mechanisms of resistance to quinolones. Clin Infect Dis 2005; 41 Suppl 2: S120-6.
19. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-third Informational Supplement M100-S23. CLSI, Wayne, PA, USA, 2013.
20. Posfai G, Kolisnychenko V, Bereczki Z et al. Markerless gene replacement in Escherichia coli stimulated by a double-strand break in the chromosome. Nucleic Acids Res 1999; 27: 4409-15.
21. Datsenko KA,Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97: 6640-5.
22. Rodriguez-Martinez JM, Velasco C, Garcia I et al. Mutant prevention concentrations of fluoroquinolones for Enterobacteriaceae expressing the plasmid-carried quinolone resistance determinant qnrA1. Antimicrob Agents Chemother 2007; 51: 2236-9.
23. Marcusson LL, Olofsson SK, Komp Lindgren P et al. Mutant prevention concentrations of ciprofloxacin for urinary tract infection isolates of Escherichia coli. J Antimicrob Chemother 2005; 55: 938-43.
24. Rodriguez-Martinez JM, Poirel L, Nordmann P. Extended-spectrum cephalosporinases in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2009; 53: 1766-71.
25. Michon A, Allou N, Chau F et al. Plasmidic qnrA3 enhances Escherichia coli fitness in absence of antibiotic exposure. PLoS One 2011; 6: e24552.
26. Dean AM, Dykhuizen DE, Hartl DL. Fitness effects of amino acid replacements in the b-galactosidase of Escherichia coli. Mol Biol Evol 1988; 5: 469-85.
27. Lopez-Rojas R, Jimenez-Mejias ME, Lepe JA et al. Acinetobacter baumannii resistant to colistin alters its antibiotic resistance profile: a case report from Spain. J Infect Dis 2011; 204: 1147-8.
28. Rodriguez-Martinez JM, Fernandez-Echauri P, Fernandez-Cuenca F et al. Genetic characterization of an extended-spectrum AmpC cephalosporinase with hydrolysing activity against fourth-generation cephalosporins in a clinical isolate of Enterobacter aerogenes selected in vivo. J Antimicrob Chemother 2012; 67: 64-8.
29. EUCAST. Clinical Breakpoints and Epidemiological Cut-off Values. 2013. http://www.eucast.org/clinical_breakpoints/.
30. Flach CF, Boulund F, Kristiansson E et al. Functional verification of computationally predicted qnr genes. Ann Clin Microbiol Antimicrob 2013; 12: 34.
31. Mandell GL, Bennet JE, Dolin R. Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases. Philadelphia, PA: Churchill Livingstone Press, 2010; 492.
32. Webber MA, Ricci V, Whitehead R et al. Clinically relevant mutant DNA gyrase alters supercoiling, changes the transcriptome, and confers multidrug resistance. MBio 2013; 4: e00273-13.
33. Andersson DI, Hughes D. Evolution of antibiotic resistance at nonlethal drug concentrations. Drug Resist Updat 2012; 15: 162-72.
34. Luo N, Pereira S, Sahin O et al. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc Natl Acad Sci USA 2005; 102: 541-6.
35. Baker S, Duy PT, Nga TVet al. Fitness benefits in fluoroquinolone-resistant Salmonella typhi in the absence of antimicrobial pressure. Elife 2013; 2: e01229.
36. Hooper DC. Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis 2001; 7: 337-41.
37. Singh R, Swick MC, Ledesma KR et al. Temporal interplay between efflux pumps and target mutations in development of antibiotic resistance in Escherichia coli. Antimicrob Agents Chemother 2012; 56: 1680-5.
38. Cesaro A, Bettoni RR, Lascols C et al. Low selection of topoisomerase mutants from strains of Escherichia coli harbouring plasmid-borne qnr genes. J Antimicrob Chemother 2008; 61: 1007-15.
39. Komp Lindgren P, Karlsson A, Hughes D. Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother 2003; 47: 3222-32.
40. Rodriguez-Martinez JM, Velasco C, Briales A et al. Qnr-like pentapeptide repeat proteins in Gram-positive bacteria. J Antimicrob Chemother 2008; 61: 1240-3.
41. Tamae C, Liu A, Kim K et al. Determination of antibiotic hypersensitivity among 4,000 single-gene-knockout mutants of Escherichia coli. J Bacteriol 2008; 190: 5981-8.
42. Kohanski MA, DePristo MA, Collins JJ. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol Cell 2010; 37: 311-20.
43. Tran JH, Jacoby GA, Hooper DC. Interaction of the plasmid-encoded quinolone resistance protein QnrA with Escherichia coli topoisomerase IV. Antimicrob Agents Chemother 2005; 49: 3050-2.
44. Tran JH, Jacoby GA, Hooper DC. Interaction of the plasmid-encoded quinolone resistance protein qnr with Escherichia coli DNA gyrase. Antimicrob Agents Chemother 2005; 49: 118-25.
45. Merens A, Matrat S, Aubry A et al. The pentapeptide repeat proteins MfpAMt and QnrB4 exhibit opposite effects on DNA gyrase catalytic reactions and on the ternary gyrase-DNA-quinolone complex. J Bacteriol 2009; 191: 1587-94.
46. Arsene S, Leclercq R. Role of a qnr-like gene in the intrinsic resistance of Enterococcus faecalis to fluoroquinolones. Antimicrob Agents Chemother 2007; 51: 3254-8.
47. Hegde SS, Vetting MW, Mitchenall LA et al. Structural and biochemical analysis of the pentapeptide repeat protein EfsQnr, a potent DNA gyrase inhibitor. Antimicrob Agents Chemother 2011; 55: 110-7.
48. Hegde SS, Vetting MW, Roderick SL et al. A fluoroquinolone resistance protein from Mycobacterium tuberculosis that mimics DNA. Science 2005; 308: 1480-3.
49. Xiong X, Bromley EH, Oelschlaeger P et al. Structural insights into quinolone antibiotic resistance mediated by pentapeptide repeat proteins: conserved surface loops direct the activity of a Qnr protein from a Gram-negative bacterium. Nucleic Acids Res 2011; 39: 3917-27.
50. Sanchez MB, Martinez JL. Differential epigenetic compatibility of qnr antibiotic resistance determinants with the chromosome of Escherichia coli. PLoS One 2012; 7: e35149.
51. Tran QT, Nawaz MS, Deck J et al. Plasmid-mediated quinolone resistance in Pseudomonas putida isolates from imported shrimp. Appl Environ Microbiol 2011; 77: 1885-7.
52. Martinez-Martinez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet 1998; 351: 797-9.
53. Jlili N, Rejiba S, Smaoui H et al. Trend of plasmid-mediated quinolone resistance genes at the children's hospital in Tunisia. J Med Microbiol 2014; 63: 195-202.
54. Jones-Dias D, Manageiro V, Francisco AP et al. Assessing the molecular basis of transferable quinolone resistance in Escherichia coli and Salmonella spp. from food-producing animals and food products. Vet Microbiol 2013; 167: 523-31.
55. Weinreich DM, Delaney NF, Depristo MA et al. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 2006; 312: 111-4.
56. Wang M, Guo Q, Xu X et al. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 2009; 53: 1892-7.
57. Cavaco LM, Hasman H, Xia S et al. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and bovismorbificans strains of human origin. Antimicrob Agents Chemother 2009; 53: 603-8.
58. Rodriguez-Martinez JM, Velasco C, Pascual A et al. Correlation of quinolone resistance levels and differences in basal and quinolone-induced expression from three qnrA-containing plasmids. Clin Microbiol Infect 2006; 12: 440-5.
59. Briales A, Rodriguez-Martinez JM, Velasco C et al. Exposure to diverse antimicrobials induces the expression of qnrB1, qnrD and smaqnr genes by SOS-dependent regulation. J Antimicrob Chemother 2012; 67: 2854-9.
60. Chaveroche MK, Ghigo JM, d'Enfert C. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 2000; 28: E97.