Transcriptional regulation of the cmeABC multidrug efflux pump and the KatA catalase by cosR in campylobacter jejuni

Journal of Bacteriology

Volumn 194, Issue 24, 2012, Pages 6883-6891

  Hwang, Sunyoung ^b   Zhang, Qijing ^c   Ryu, Sangryeol ^b   Jeon, Byeonghwa ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b Seoul National University   (South Korea)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; CATALASE; CMEABC PROTEIN; COSR PROTEIN; DEOXYRIBONUCLEASE; KATA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; BIOGENESIS; CAMPYLOBACTER JEJUNI; DNA FOOTPRINTING; ENERGY YIELD; ENZYME ACTIVITY; ENZYME ASSAY; GEL MOBILITY SHIFT ASSAY; GENE REPRESSION; GENE SILENCING; LIPID METABOLISM; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FOLDING; PROTEIN SYNTHESIS; QUANTITATIVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BINDING SITES; CAMPYLOBACTER JEJUNI; DNA FOOTPRINTING; DNA-BINDING PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; PEROXIDASES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

CAMPYLOBACTER; CAMPYLOBACTER JEJUNI;

EID: 84870694009     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01636-12     Document Type: Article

References (47)

1. Akiba M, Lin J, Barton YW, Zhang Q. 2006. Interaction of CmeABC and CmeDEF in conferring antimicrobial resistance and maintaining cell viability in Campylobacter jejuni. J. Antimicrob. Chemother. 57:52-60.
2. Atack JM, Kelly DJ. 2009. Oxidative stress in Campylobacter jejuni: responses, resistance, and regulation. Future Microbiol. 4:677-690.
3. Baillon ML, van Vliet AH, Ketley JM, Constantinidou C, Penn CW. 1999. An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J. Bacteriol. 181:4798-4804.
4. Beier D, Frank R. 2000. Molecular characterization of two-component systems of Helicobacter pylori. J. Bacteriol. 182:2068-2076.
5. Butcher J, Sarvan S, Brunzelle JS, Couture JF, Stintzi A. 2012. Structure and regulon of Campylobacter jejuni ferric uptake regulator Fur define apo-Fur regulation. Proc. Natl. Acad. Sci. U. S. A. 109:10047-10052.
6. Chiang SM, Schellhorn HE. 2012. Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch. Biochem. Biophys. 525:161-169.
7. Day WA, Jr, Sajecki JL, Pitts TM, Joens LA. 2000. Role of catalase in Campylobacter jejuni intracellular survival. Infect. Immun. 68:6337-6345.
8. Delany I, Spohn G, Rappuoli R, Scarlato V. 2002. Growth phase-dependent regulation of target gene promoters for binding of the essential orphan response regulator HP1043 of Helicobacter pylori. J. Bacteriol. 184:4800-4810.
9. Garénaux A, et al. 2008. Role of the Cj1371 periplasmic protein and the Cj0355c two-component regulator in the Campylobacter jejuni NCTC 11168 response to oxidative stress caused by paraquat. Res. Microbiol. 159:718-726.
10. Good L, Awasthi SK, Dryselius R, Larsson O, Nielsen PE. 2001. Bactericidal antisense effects of peptide-PNA conjugates. Nat. Biotechnol. 19:360-364.
11. Grant KA, Park SF. 1995. Molecular characterization of katA from Campylobacter jejuni and generation of a catalase-deficient mutant of Campylobacter coli by interspecific allelic exchange. Microbiology 141:1369-1376.
12. Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B. 1990. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 87:6181-6185.
13. Gu M, Imlay JA. 2011. The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol. Microbiol. 79:1136-1150.
14. Holmes K, et al. 2005. Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151:243-257.
15. Hwang S, Kim M, Ryu S, Jeon B. 2011. Regulation of oxidative stress response by CosR, an essential response regulator in Campylobacter jejuni. PLoS One 6:e22300. doi:10.1371/journal.pone.0022300.
16. Imlay JA. 2008. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77:755-776.
17. Jeon B, Wang Y, Hao H, Barton YW, Zhang Q. 2011. Contribution ofCmeGto antibiotic and oxidative stress resistance in Campylobacter jejuni. J. Antimicrob. Chemother. 66:79-85.
18. Jeon B, Zhang Q. 2009. Sensitization of Campylobacter jejuni to fluoroquinolone and macrolide antibiotics by antisense inhibition of the CmeABC multidrug efflux transporter. J. Antimicrob. Chemother. 63:946-948.
19. Kehrenberg C, Cloeckaert A, Klein G, Schwarz S. 2009. Decreased fluoroquinolone susceptibility in mutants of Salmonella serovars other than Typhimurium: detection of novel mutations involved in modulated expression of ramA and soxS. J. Antimicrob. Chemother. 64:1175-1180.
20. Kim M, Hwang S, Ryu S, Jeon B. 2011. Regulation of perR expression by iron and PerR in Campylobacter jejuni. J. Bacteriol. 193:6171-6178.
21. Kirkpatrick BD, Tribble DR. 2011. Update on human Campylobacter jejuni infections. Curr. Opin. Gastroenterol. 27:1-7.
22. Koutsolioutsou A, Martins EA, White DG, Levy SB, Demple B. 2001. A soxRS-constitutive mutation contributing to antibiotic resistance in a clinical isolate of Salmonella enterica serovar Typhimurium. Antimicrob. Agents Chemother. 45:38-43.
23. Li XZ, Nikaido H. 2009. Efflux-mediated drug resistance in bacteria: An update. Drugs 69:1555-1623.
24. Li Z, Demple B. 1994. SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. J. Biol. Chem. 269:18371-18377.
25. Lin J, Akiba M, Sahin O, Zhang Q. 2005. CmeR functions as a transcriptional repressor for the multidrug efflux pumpCmeABCin Campylobacter jejuni. Antimicrob. Agents Chemother. 49:1067-1075.
26. Lin J, et al. 2005. Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J. Bacteriol. 187:7417-7424.
27. Lin J, Michel LO, Zhang Q. 2002. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob. Agents Chemother. 46:2124-2131.
28. Lin J, Sahin O, Michel LO, Zhang Q. 2003. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect. Immun. 71:4250-4259.
29. -ΔΔCT method. Methods 25: 402-408.
30. Luangtongkum T, et al. 2009. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol. 4:189-200.
31. Metris A, Reuter M, Gaskin DJ, Baranyi J, van Vliet AH. 2011. In vivo and in silico determination of essential genes of Campylobacter jejuni. BMC Genomics 12:535. doi:10.1186/1471-2164-12-535.
32. Nikaido H, Takatsuka Y. 2009. Mechanisms of RND multidrug efflux pumps. Biochim. Biophys. Acta 1794:769-781.
33. Palyada K, et al. 2009. Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. BMC Genomics 10:481. doi: 10.1186/1471-2164-10-481.
34. Parkhill J, et al. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
35. Raphael BH, et al. 2005. The Campylobacter jejuni response regulator, CbrR, modulates sodium deoxycholate resistance and chicken colonization. J. Bacteriol. 187:3662-3670.
36. Schar J, Sickmann A, Beier D. 2005. Phosphorylation-independent activity of atypical response regulators of Helicobacter pylori. J. Bacteriol. 187:3100-3109.
37. Shen Z, Pu XY, Zhang Q. 2011. Salicylate functions as an efflux pump inducer and promotes the emergence of fluoroquinolone-resistant Campylobacter jejuni mutants. Appl. Environ. Microbiol. 77:7128-7133.
38. Stahl M, Stintzi A. 2011. Identification of essential genes in Campylobacter jejuni genome highlights hyper-variable plasticity regions. Funct. Integr. Genomics 11:241-257.
39. Tao K. 1999. In vivo oxidation-reduction kinetics of OxyR, the transcriptional activator for an oxidative stress-inducible regulon in Escherichia coli. FEBS Lett. 457:90-92.
40. Tao K, Fujita N, Ishihama A. 1993. Involvement of the RNA polymerase alpha subunit C-terminal region in co-operative interaction and transcriptional activation with OxyR protein. Mol. Microbiol. 7:859-864.
41. Tartaglia LA, Storz G, Ames BN. 1989. Identification and molecular analysis of oxyR-regulated promoters important for the bacterial adaptation to oxidative stress. J. Mol. Biol. 210:709-719.
42. van Vliet AH, Baillon ML, Penn CW, Ketley JM. 1999. Campylobacter jejuni contains two Fur homologs: characterization of iron-responsive regulation of peroxide stress defense genes by the PerR repressor. J. Bacteriol. 181:6371-6376.
43. van Vliet AH, Ketley JM, Park SF, Penn CW. 2002. The role of iron in Campylobacter gene regulation, metabolism and oxidative stress defense. FEMS Microbiol. Rev. 26:173-186.
44. Woodbury W, Spencer AK, Stahman MA. 1971. An improved procedure using ferricyanide for detecting catalase isozymes. Anal. Biochem. 44:301-305.
45. Wosten MM, Boeve M, Koot MG, van Nuenen AC, van der Zeijst BA. 1998. Identification of Campylobacter jejuni promoter sequences. J. Bacteriol. 180:594-599.
46. Wu J, Weiss B. 1992. Two-stage induction of the soxRS (superoxide response) regulon of Escherichia coli. J. Bacteriol. 174:3915-3920.
47. Yang SH, et al. 2003. Genome-scale analysis of resveratrol-induced gene expression profile in human ovarian cancer cells using a cDNA microarray. Int. J. Oncol. 22:741-750.