Salicylate functions as an efflux pump inducer and promotes the emergence of fluoroquinolone-resistant Campylobacter jejuni mutants

Applied and Environmental Microbiology

Volumn 77, Issue 20, 2011, Pages 7128-7133

  Shen, Zhangqi ^a   Pu, Xiao Ying ^a,b   Zhang, Qijing ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Hangzhou Center for Disease Control and Prevention   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORIES; ANTIBIOTIC RESISTANCE; CAMPYLOBACTERS; CIPROFLOXACIN; CULTURE MEDIUM; EFFLUX PUMPS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUOROQUINOLONE-RESISTANT CAMPYLOBACTER; IMMUNOBLOTTING; MOLECULAR MECHANISM; MULTIDRUG EFFLUX; SELECTION PRESSURES; TRANSCRIPTIONAL FUSION; TRANSCRIPTIONAL REPRESSORS;

ANTIBIOTICS; ELECTRIC RESISTANCE; ELECTROPHORETIC MOBILITY; IMPACT RESISTANCE;

POLYMERASE CHAIN REACTION;

ANTIINFECTIVE AGENT; BACTERIAL DNA; NONSTEROID ANTIINFLAMMATORY AGENT; QUINOLONE DERIVATIVE; REPRESSOR PROTEIN; SALICYLIC ACID DERIVATIVE;

ANTIBIOTIC RESISTANCE; BACTERIUM; BIOASSAY; EMERGENCE; FREQUENCY ANALYSIS; GENE EXPRESSION; GENETIC ANALYSIS; INHIBITION; MOBILITY; MOLECULAR ANALYSIS; MUTATION; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SELECTION;

ACTIVE TRANSPORT; ANTIBIOTIC RESISTANCE; ARTICLE; CAMPYLOBACTER JEJUNI; DRUG ANTAGONISM; DRUG EFFECT; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE FUSION; GENETICS; IMMUNOBLOTTING; METABOLISM; PROTEIN BINDING; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION;

ANTI-BACTERIAL AGENTS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ARTIFICIAL GENE FUSION; BIOLOGICAL TRANSPORT, ACTIVE; CAMPYLOBACTER JEJUNI; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUOROQUINOLONES; GENE EXPRESSION PROFILING; GENES, REPORTER; IMMUNOBLOTTING; PROTEIN BINDING; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALICYLATES; TRANSCRIPTIONAL ACTIVATION;

EID: 82955194478     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00763-11     Document Type: Article

References (35)

1. Akiba, M., J. Lin, Y. W. Barton, and Q. Zhang. 2006. Interaction of CmeABC and CmeDEF in conferring antimicrobial resistance and maintaining cell viability in Campylobacter jejuni. J. Antimicrob. Chemother. 57:52-60.
2. Alekshun, M. N., and S. B. Levy. 1997. Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob. Agents Chemother. 41:2067-2075.
3. Baigent, C., et al. 2009. Aspirin in the primary and secondary prevention of vascular disease: collaborative meta-analysis of individual participant data from randomised trials. Lancet 373:1849-1860.
4. Cohen, S. P., S. B. Levy, J. Foulds, and J. L. Rosner. 1993. Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar-independent pathway. J. Bacteriol. 175:7856-7862.
5. Domenico, P., T. Hopkins, and B. A. Cunha. 1990. The effect of sodium salicylate on antibiotic susceptibility and synergy in Klebsiella pneumoniae. J. Antimicrob. Chemother. 26:343-351.
6. Ge, B., P. F. McDermott, D. G. White, and J. Meng. 2005. Role of efflux pumps and topoisomerase mutations in fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob. Agents Chemother. 49:3347-3354.
7. George, A. M., R. M. Hall, and H. W. Stokes. 1995. Multidrug resistance in Klebsiella pneumoniae: a novel gene, ramA, confers a multidrug resistance phenotype in Escherichia coli. Microbiology 141:1909-1920.
8. Gu, R., et al. 2007. Crystal structure of the transcriptional regulator CmeR from Campylobacter jejuni. J. Mol. Biol. 372:583-593.
9. Guo, B., et al. 2008. CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo. J. Bacteriol. 190:1879-1890.
10. Hannula, M., and M. L. Hanninen. 2008. Effect of putative efflux pump inhibitors and inducers on the antimicrobial susceptibility of Campylobacter jejuni and Campylobacter coli. J. Med. Microbiol. 57:851-855.
11. Hartog, E., O. Menashe, E. Kler, and S. Yaron. 2010. Salicylate reduces the antimicrobial activity of ciprofloxacin against extracellular Salmonella enterica serovar Typhimurium, but not against Salmonella in macrophages. J. Antimicrob. Chemother. 65:888-896.
12. Huff, G. R., W. E. Huff, J. M. Balog, N. C. Rath, and R. S. Izard. 2004. The effects of water supplementation with vitamin E and sodium salicylate (Uni-Sol) on the resistance of turkeys to Escherichia coli respiratory infection. Avian Dis. 48:324-331.
13. Janssen, P. L., P. C. Hollman, D. P. Venema, W. A. van Staveren, and M. B. Katan. 1996. Salicylates in foods. Nutr. Rev. 54:357-359.
14. Lei, H. T., et al. 2011. Crystal structures of CmeR-bile acid complexes from Campylobacter jejuni. Protein Sci. 20:712-723.
15. Lin, J., M. Akiba, O. Sahin, and Q. Zhang. 2005. CmeR functions as a transcriptional repressor for the multidrug efflux pump CmeABC in Campylobacter jejuni. Antimicrob. Agents Chemother. 49:1067-1075.
16. Lin, J., et al. 2005. Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J. Bacteriol. 187:7417-7424.
17. Lin, J., L. O. Michel, and Q. Zhang. 2002. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob. Agents Chemother. 46: 2124-2131.
18. Luangtongkum, T., et al. 2009. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol. 4:189-200.
19. Luo, N., et al. 2005. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl. Acad. Sci. U. S. A. 102:541-546.
20. Luo, N., O. Sahin, J. Lin, L. O. Michel, and Q. Zhang. 2003. In vivo selection of Campylobacter isolates with high levels of fluoroquinolone resistance associated with gyrA mutations and the function of the CmeABC efflux pump. Antimicrob. Agents Chemother. 47:390-394.
21. Oakland, M., B. Jeon, O. Sahin, Z. Shen, and Q. Zhang. 2011. Functional characterization of a lipoprotein-encoding operon in Campylobacter jejuni. PLoS One 6:e20084.
22. Parkhill, J., et al. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
23. Payot, S., et al. 2004. Relative contribution of target gene mutation and efflux to fluoroquinolone and erythromycin resistance, in French poultry and pig isolates of Campylobacter coli. Int. J. Antimicrob. Agents 23:468-472.
24. Payot, S., et al. 2006. Mechanisms of fluoroquinolone and macrolide resistance in Campylobacter spp. Microbes Infect. 8:1967-1971.
25. Price, C. T., I. R. Lee, and J. E. Gustafson. 2000. The effects of salicylate on bacteria. Int. J. Biochem. Cell Biol. 32:1029-1043.
26. Randall, L. P., et al. 2003. Prevalence of multiple antibiotic resistance in 443 Campylobacter spp. isolated from humans and animals. J. Antimicrob. Chemother. 52:507-510.
27. Rosner, J. L. 1985. Nonheritable resistance to chloramphenicol and other antibiotics induced by salicylates and other chemotactic repellents in Escherichia coli K-12. Proc. Natl. Acad. Sci. U. S. A. 82:8771-8774.
28. Ruiz-Palacios, G. M. 2007. The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken. Clin. Infect. Dis. 44:701-703.
29. Scallan, E., et al. 2011. Foodborne illness acquired in the United States- major pathogens. Emerg. Infect. Dis. 17:7-15.
30. Slutsker, L., S. F. Altekruse, and D. L. Swerdlow. 1998. Foodborne diseases. Emerging pathogens and trends. Infect. Dis. Clin. North Am. 12:199-216.
31. Sulavik, M. C., M. Dazer, and P. F. Miller. 1997. The Salmonella typhimurium mar locus: molecular and genetic analyses and assessment of its role in virulence. J. Bacteriol. 179:1857-1866.
32. Warner, T. D., and J. A. Mitchell. 2002. Cyclooxygenase-3 (COX-3): filling in the gaps toward a COX continuum? Proc. Natl. Acad. Sci. U. S. A. 99:13371- 13373.
33. Wood, A., G. Baxter, F. Thies, J. Kyle, and G. Duthie. 2011. A systematic review of salicylates in foods: estimated daily intake of a Scottish population. Mol. Nutr. Food Res. 55(Suppl. 1):S7-S14.
34. Wosten, M. M., M. Boeve, M. G. Koot, A. C. van Nuenen, and B. A. van der Zeijst. 1998. Identification of Campylobacter jejuni promoter sequences. J. Bacteriol. 180:594-599.
35. Yan, M., O. Sahin, J. Lin, and Q. Zhang. 2006. Role of the CmeABC efflux pump in the emergence of fluoroquinolone-resistant Campylobacter under selection pressure. J. Antimicrob. Chemother. 58:1154-1159.