Genetic basis and functional consequences of differential expression of the CmeABC efflux pump in Campylobacter jejuni isolates

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Grinnage Pulley, Tara ^a,b   Zhang, Qijing ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CARRIER PROTEIN; CHLORAMPHENICOL; PRIMER DNA;

AMINO ACID SUBSTITUTION; ARTICLE; ASSAY; BACTERIAL GENE; BACTERIUM ISOLATE; CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; CARBOXY TERMINAL SEQUENCE; CMEABC GENE; CONTROLLED STUDY; DNA BINDING; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; NONHUMAN; PHENOTYPE; PROMOTER REGION; TRANSCRIPTIONAL FUSION ASSAY; ANIMAL; CHEMISTRY; CHICKEN; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; MUTATION; TURKEY (BIRD);

CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; GALLUS GALLUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CHICKENS; CHLORAMPHENICOL; CIPROFLOXACIN; DNA PRIMERS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MUTATION; PHENOTYPE; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; TURKEYS;

EID: 84938868788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131534     Document Type: Article

References (51)

1. Nikaido H, Pagès JM. Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol Rev. 2012; 36(2):340-63. doi: 10.1111/j.1574-6976.2011.00290.x PMID: 21707670; PubMed Central PMCID: PMCPMC3546547.
2. Li XZ, Nikaido H, Poole K. Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1995; 39(9):1948-53. PMID: 8540696; PubMed Central PMCID: PMCPMC162861.
3. Poole K, Krebes K, McNally C, Neshat S. Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon. J Bacteriol. 1993; 175(22):7363-72. PMID: 8226684; PubMed Central PMCID: PMCPMC206881.
4. Okusu H, Ma D, Nikaido H. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J Bacteriol. 1996; 178(1):306-8. PMID: 8550435; PubMed Central PMCID: PMCPMC177656.
5. Aires JR, Köhler T, Nikaido H, Plésiat P. Involvement of an active efflux system in the natural resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob Agents Chemother. 1999; 43(11):2624-8. PMID: 10543738; PubMed Central PMCID: PMCPMC89534.
6. Lin J, Michel L, Zhang Q. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob Agents Chemother. 2002; 46(7):2124-31. PMID: 12069964; PubMed Central PMCID: PMCPMC127319.
7. Lin J, Sahin O, Michel LO, Zhang Q. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect Immun. 2003; 71(8):4250-9. PMID: 12874300; PubMed Central PMCID: PMCPMC165992.
8. Luo N, Sahin O, Lin J, Michel LO, Zhang Q. 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. 2003; 47(1):390-4. PMID: 12499221; PubMed Central PMCID: PMCPMC148968.
9. Ge B, McDermott PF, White DG, Meng J. Role of efflux pumps and topoisomerase mutations in fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother. 2005; 49(8):3347-54. doi: 10.1128/AAC.49.8.3347-3354.2005 PMID: 16048946; PubMed Central PMCID: PMCPMC1196287.
10. Cagliero C, Mouline C, Cloeckaert A, Payot S. Synergy between efflux pump CmeABC and modifications in ribosomal proteins L4 and L22 in conferring macrolide resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother. 2006; 50(11):3893-6. doi: 10.1128/AAC.00616-06 PMID: 16940070; PubMed Central PMCID: PMCPMC1635205.
11. Gibreel A, Wetsch NM, Taylor DE. Contribution of the CmeABC efflux pump to macrolide and tetracycline resistance in Campylobacter jejuni. Antimicrob Agents Chemother. 2007; 51(9):3212-6. doi: 10.1128/AAC.01592-06 PMID: 17606685; PubMed Central PMCID: PMCPMC2043232.
12. Lin J, Akiba M, Sahin O, Zhang Q. CmeR functions as a transcriptional repressor for the multidrug efflux pump CmeABC in Campylobacter jejuni. Antimicrob Agents Chemother. 2005; 49(3):1067-75. doi: 49/3/1067 [pii] doi: 10.1128/AAC.49.3.1067-1075.2005 PMID: 15728904; PubMed Central PMCID: PMCPMC549222.
13. Guo B, Wang Y, Shi F, Barton Y, Plummer P, Reynolds D, et al. CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo. J Bacteriol. 2008; 190 (6):1879-90. doi: JB.01796-07 [pii] doi: 10.1128/JB.01796-07 PMID: 18178742; PubMed Central PMCID: PMCPMC2258875.
14. Cagliero C, Maurel M, Cloeckaert A, Payot S. Regulation of the expression of the CmeABC efflux pump in Campylobacter jejuni: identification of a point mutation abolishing the binding of the CmeR repressor in an in vitro-selected multidrug-resistant mutant. FEMS Microbiol Lett. 2007; 267(1):89-94. doi: FML558 [pii] doi: 10.1111/j.1574-6968.2006.00558.x PMID: 17166222.
15. Lei HT, Shen Z, Surana P, Routh MD, Su CC, Zhang Q, et al. Crystal structures of CmeR-bile acid complexes from Campylobacter jejuni. Protein Sci. 2011; 20(4):712-23. doi: 10.1002/pro.602 PMID: 21328631; PubMed Central PMCID: PMCPMC3081549.
16. Lin J, Cagliero C, Guo B, Barton Y, Maurel M, Payot S, et al. Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J Bacteriol. 2005; 187(21):7417-24. doi: 187/21/7417 [pii] doi: 10.1128/JB.187.21.7417-7424.2005 PMID: 16237025; PubMed Central PMCID: PMCPMC1272998.
17. Centers for Disease Control and Prevention. Estimates of Foodborne Illness in the United States2011 18 June 2013; 2013. Available: http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html.
18. Janssen R, Krogfelt KA, Cawthraw SA, van Pelt W, Wagenaar JA, Owen RJ. Host-pathogen interactions in Campylobacter infections: the host perspective. Clin Microbiol Rev. 2008; 21(3):505-18. doi: 10.1128/CMR.00055-07 PMID: 18625685; PubMed Central PMCID: PMCPMC2493085.
19. Taylor EV, Herman KM, Ailes EC, Fitzgerald C, Yoder JS, Mahon BE, et al. Common source outbreaks of Campylobacter infection in the USA, 1997-2008. Epidemiol Infect. 2013; 141(5):987-96. doi: 10.1017/S0950268812001744 PMID: 22892294.
20. Ross AG, Olds GR, Cripps AW, Farrar JJ, McManus DP. Enteropathogens and chronic illness in returning travelers. N Engl J Med. 2013; 368(19):1817-25. doi: 10.1056/NEJMra1207777 PMID: 23656647.
21. Luo N, Pereira S, Sahin O, Lin J, Huang S, Michel L, et al. Enhanced in vivo fitness of fluoroquinoloneresistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc Natl Acad Sci U S A. 2005; 102(3):541-6. doi: 10.1073/pnas.0408966102 PMID: 15634738; PubMed Central PMCID: PMCPMC545549.
22. Han J, Wang Y, Sahin O, Shen Z, Guo B, Shen J, et al. A fluoroquinolone resistance associated mutation in gyrA Affects DNA supercoiling in Campylobacter jejuni. Front Cell Infect Microbiol. 2012; 2:21. doi: 10.3389/fcimb.2012.00021 PMID: 22919613; PubMed Central PMCID: PMCPMC3417464.
23. Yan M, Sahin O, Lin J, Zhang Q. Role of the CmeABC efflux pump in the emergence of fluoroquinolone-resistant Campylobacter under selection pressure. J Antimicrob Chemother. 2006; 58(6):1154-9. doi: dkl412 [pii] doi: 10.1093/jac/dkl412 PMID: 17023497.
24. Luangtongkum T, Morishita TY, Ison AJ, Huang S, McDermott PF, Zhang Q. Effect of conventional and organic production practices on the prevalence and antimicrobial resistance of Campylobacter spp.in poultry. Appl Environ Microbiol. 2006; 72(5):3600-7. doi: 10.1128/AEM.72.5.3600-3607.2006 PMID: 16672508; PubMed Central PMCID: PMCPMC1472326.
25. Huang S, Luangtongkum T, Morishita TY, Zhang Q. Molecular typing of Campylobacter strains using the cmp gene encoding the major outer membrane protein. Foodborne Pathog Dis. 2005; 2(1):12-23. doi: 10.1089/fpd.2005.2.12 PMID: 15992295.
26. Linton D, Lawson AJ, Owen RJ, Stanley J. PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. J Clin Microbiol. 1997; 35(10):2568-72. PMID: 9316909; PubMed Central PMCID: PMCPMC230012.
27. Linton D, Owen RJ, Stanley J. Rapid identification by PCR of the genus Campylobacter and of five Campylobacter species enteropathogenic for man and animals. Res Microbiol. 1996; 147(9):707-18. PMID: 9296105.
28. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature. 2000; 403 (6770):665-8. doi: 10.1038/35001088 PMID: 10688204.
29. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ. Experimental Campylobacter jejuni infection in humans. J Infect Dis. 1988; 157(3):472-9. PMID: 3343522.
30. McDermott PF, Bodeis SM, Aarestrup FM, Brown S, Traczewski M, Fedorka-Cray P, et al. Development of a standardized susceptibility test for Campylobacter with quality-control ranges for ciprofloxacin, doxycycline, erythromycin, gentamicin, and meropenem. Microb Drug Resist. 2004; 10(2):124-31. doi: 10.1089/1076629041310064 PMID: 15256027.
31. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; Approved Standard-Third Edition. CLSI document M31-A3 Wayne, Pennsylvania2008.
32. Wösten M, Boeve M, Koot M, van Nuenen A, van der Zeijst B. Identification of Campylobacter jejuni promoter sequences. J Bacteriol. 1998; 180(3):594-9. PMID: 9457862; PubMed Central PMCID: PMCPMC106926.
33. Miller WG, Bates AH, Horn ST, Brandl MT, Wachtel MR, Mandrell RE. Detection on surfaces and in Caco-2 cells of Campylobacter jejuni cells transformed with new gfp, yfp, and cfp marker plasmids. Appl Environ Microbiol. 2000; 66(12):5426-36. PMID: 11097924; PubMed Central PMCID: PMCPMC92478.
34. Hao H, Yuan Z, Shen Z, Han J, Sahin O, Liu P, et al. Mutational and transcriptomic changes involved in the development of macrolide resistance in Campylobacter jejuni. Antimicrob Agents Chemother. 2013; 57(3):1369-78. doi: 10.1128/AAC.01927-12 PMID: 23274667; PubMed Central PMCID: PMCPMC3591901.
35. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29(9):e45. PMID: 11328886; PubMed Central PMCID: PMCPMC55695.
36. Cagliero C, Cloix L, Cloeckaert A, Payot S. High genetic variation in the multidrug transporter cmeB gene in Campylobacter jejuni and Campylobacter coli. J Antimicrob Chemother. 2006; 58(1):168-72. doi: 10.1093/jac/dkl212 PMID: 16735430.
37. Oakland M, Jeon B, Sahin O, Shen Z, Zhang Q. Functional characterization of a lipoprotein-encoding operon in Campylobacter jejuni. PLoS One. 2011; 6(5):e20084. doi: PONE-D-11-01403 [pii] doi: 10.1371/journal.pone.0020084 PMID: 21625391; PubMed Central PMCID: PMCPMC3100323.
38. Alekshun MN, Kim YS, Levy SB. Mutational analysis of MarR, the negative regulator of marRAB expression in Escherichia coli, suggests the presence of two regions required for DNA binding. Mol Microbiol. 2000; 35(6):1394-404. PMID: 10760140.
39. Miller JH. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1992.
40. Qiagen. The QIAexpressionist. A handbook for high lelevel expresson and purification of 6x His-tagged proteins. Third ed: Qiagen Worldwide; 2003.
41. Luria S, Delbrück M. Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics. 1943; 28(6):491-511. PMID: 17247100; PubMed Central PMCID: PMCPMC1209226.
42. Crane G, Thomas S, Jones M. A modified Luria-Delbrück fluctuation assay for estimating and comparing mutation rates. Mutat Res. 1996; 354(2):171-82. doi: 0027510796000097 [pii]. PMID: 8764946.
43. Rosche W, Foster P. Determining mutation rates in bacterial populations. Methods. 2000; 20(1):4-17. doi: S1046-2023(99)90901-5 [pii] doi: 10.1006/meth.1999.0901 PMID: 10610800; PubMed Central PMCID: PMCPMC2932672.
44. Pope C, O'Sullivan D, McHugh T, Gillespie S. A practical guide to measuring mutation rates in antibiotic resistance. Antimicrob Agents Chemother. 2008; 52(4):1209-14. doi: AAC.01152-07 [pii] doi: 10.1128/AAC.01152-07 PMID: 18250188; PubMed Central PMCID: PMCPMC2292516.
45. Foster P. Methods for determining spontaneous mutation rates. Methods Enzymol. 2006; 409:195-213. doi: S0076-6879(05)09012-9 [pii] doi: 10.1016/S0076-6879(05)09012-9 PMID: 16793403; PubMed Central PMCID: PMCPMC2041832.
46. Wang G, Wilson TJ, Jiang Q, Taylor DE. Spontaneous mutations that confer antibiotic resistance in Helicobacter pylori. Antimicrob Agents Chemother. 2001; 45(3):727-33. doi: 10.1128/AAC.45.3.727-733.2001 PMID: 11181351; PubMed Central PMCID: PMCPMC90364.
47. Hall BM, Ma CX, Liang P, Singh KK. Fluctuation analysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics. 2009; 25(12):1564-5. doi: 10.1093/bioinformatics/btp253 PMID: 19369502; PubMed Central PMCID: PMCPMC2687991.
48. Han J, Sahin O, Barton YW, Zhang Q. Key role of Mfd in the development of fluoroquinolone resistance in Campylobacter jejuni. PLoS Pathog. 2008; 4(6):e1000083. doi: 10.1371/journal.ppat.1000083 PMID: 18535657; PubMed Central PMCID: PMCPMC2390758.
49. Chen CY, Nace GW, Irwin PL. A 6 x 6 drop plate method for simultaneous colony counting and MPN enumeration of Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli. J Microbiol Methods. 2003; 55(2):475-9. doi: S0167701203001945 [pii]. PMID: 14529971.
50. Gu R, Su CC, Shi F, Li M, McDermott G, Zhang Q, et al. Crystal structure of the transcriptional regulator CmeR from Campylobacter jejuni. J Mol Biol. 2007; 372(3):583-93. doi: 10.1016/j.jmb.2007.06.072 PMID: 17686491; PubMed Central PMCID: PMCPMC2104645.
51. Hyytiäinen H, Hänninen ML. Quality control strain Campylobacter jejuni ATCC 33560 contains a frameshift mutation in the CmeR regulator. Antimicrob Agents Chemother. 2012; 56(2):1148. doi: 10.1128/AAC.06228-11 PMID: 22143527; PubMed Central PMCID: PMCPMC3264221.