Stress-induced adaptive tolerance response and virulence gene expression in Campylobacter jejuni

Journal of Food Safety

Volumn 29, Issue 1, 2009, Pages 126-143

  Ma, Yue ^a   Hanning, Irene ^a   Slavik, Michael ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

EID: 58849143077     PISSN: 01496085     EISSN: 17454565     Source Type: Journal    
DOI: 10.1111/j.1745-4565.2008.00147.x     Document Type: Article

References (52)

1. ABEE, T. WOUTERS, J.A. 1999. Microbial stress response in minimal processing. Int. J. Food Microbiol. 50, 65 91.
2. ADAK, G.K., COWDEN, J.M., NICHOLAS, S. EVANS, H.S. 1995. The Public Health Laboratory Service national case-control study of primary indigenous sporadic cases of Campylobacter infection. Epidemiol. Infect. 115, 15 22.
3. ALVAREZ, G., HEREDIA, N. GARCIA, S. 2003. Relationship between the effects of stress induced by human bile juice and acid treatment in Vibrio cholerae. J. Food Prot. 66, 2283 2288.
4. BEUMER, R., VRIES, R.J. ROMBOUTS, F.M. 1992. Campylobacter jejuni non-culturable coccoid cells. Int. J. Food Microbiol. 15, 153 163.
5. BLACK, R., LEVINE, M., CLEMENTS, M., HUGHES, T. BLASER, M.J. 1988. Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 157, 472 479.
6. BRÁS, A.M., CHATTERJEE, S., WREN, B.W., NEWELL, D.G. KETLEY, J.M. 1999. A novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J. Bacteriol. 181, 3298 3302.
7. BRØNDSTED, L., THORUP ANDERSEN, M., PARKER, M., JØRGENSEN, K. INGMER, H. 2005. The HtrA protease of Campylobacter jejuni is required for heat and oxygen tolerance and for optimal interaction with human epithelial cells. Appl. Environ. Microbiol. 71, 3205 3212.
8. CAPPELIER, J.M., ROSSERO, A. FEDERIGHI, M. 2000. Demonstration of a protein systhesis in starved Campylobacter jejuni cells. Int. J. Food Microbiol. 55, 63 67.
9. CEELEN, L., DECOSTERE, A., DUCATELLE, R. HAESEBROUCK, F. 2006. Cytolethal distending toxin generates cell death by inducing a bottleneck in the cell cycle. Microbiol. Res. 161, 109 120.
10. CLOAK, O.M., SOLOW, B.T., BRIGGS, C.E., CHEN, C.Y. FRATAMICO, P.M. 2002. Quorum sensing and production of autoinducer-2 in Campylobacter spp., Escherichia coli O157:H7, and Salmonella enterica Serovar Typhimurium in foods. Appl. Environ. Microbiol. 68, 4666 4671.
11. CSONKA, L.N. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53, 121 147.
12. DENAGEL, D.C. PIERCE, S.K. 1993. Heat shock proteins in immune responses. Crit. Rev. Immunol 13, 71 81.
13. DORRELL, N., MANGAN, J.A., LAING, K.G., HINDS, J., LINTON, D., AL-GHUSEIN, H., BARRELL, B.G. PARKHILL, J. 2001. Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. Genome. Res. 11, 1706 1715.
14. FOSTER, J.W. HALL, H.K. 1991. Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J. Bacteriol. 173, 5129 5135.
15. GARREN, D.M., HARRISON, M.A. RUSSELL, S.M. 1998. Acid tolerance and acid shock response of Escherichia coli O157:H7 and non-O157 : H7 isolates provide cross-protection to sodium lactate and sodium chloride. J. Food Prot. 61, 158 161.
16. GAYNOR, E.C., WELLS, D.H., MACKICHAN, J.K. FALKOW, S. 2005. The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol. Microbiol. 56, 8 27.
17. GILBERT, C. SLAVIK, M. 2004. Determination of toxicity of Campylobacter jejuni isolated from humans and from poultry carcasses acquired at various stages of production. J. Appl. Microbiol. 97, 347 353.
18. HOFREUTER, D., TSAI, J., WATSON, R., NOVIK, V., ALTMAN, B., BENITEZ, M., CLARK, C., PERBOST, C., JARVIE, T., DU, L. ET AL. 2006. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74, 4694 4707.
19. HOLMES, K., MULHOLLAND, F., PEARSON, B.M., PIN, C., MCNICHOLL-KENNEDY, J., KETLEY, J.M. WELLS, J.M. 2005. Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151, 243 257.
20. HUMPHREY, T., WILLIAMS, A., MCALPINE, K., LEVER, M., GUARD-PETTER, J. COX, J. 1996. Isolates of Salmonella enterica Enteritidis PT4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chickens. Epidemiol. Infect. 117, 79 88.
21. JONES, D.M., SUTCLIFFE, E.M., RIOS, R., FOX, A.J. CURRY, A. 1993. Campylobacter jejuni adapts to aerobic metabolism in the environment. J. Med. Microbiol. 38, 145 150.
22. JONES, M.A., MARSTON, K.L., WOODALL, C.A., MASKELL, D.J., LINTON, D., KARLYSHEV, A.V., DORRELL, N., WREN, B.W. BARROW, P.A. 2004. Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 72, 3769 3776.
23. KONKEL, M.E., GARVIS, S.G., TIPTON, S.L., ANDERSON, D.E. CIEPLAK, W. 1997. Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni. Mol. Microbiol. 24, 953 963.
24. KONKEL, M.E., KIM, B.J., RIVERA-AMILL, V. GARVIS, S.G. 1999. Identification of proteins required for the internalization of Campylobacter jejuni into cultured mammalian cells. Adv. Exp. Med. Biol. 473, 215 224.
25. KOUTSOUMANIS, K.P. SOFOS, J.N. 2004. Comparative acid stress response of Listeria monocytogenes, Escherichia coli O157:H7 and Salmonella Typhimurium after habituation at different pH conditions. Lett. Appl. Microbiol. 38, 321 326.
26. KOUTSOUMANIS, K.P., KENDALL, P.A. SOFOS, J.N. 2003. Effect of food processing-related stresses on acid tolerance of Listeria monocytogenes. Appl. Environ. Microbiol. 69, 7514 7516.
27. KRAUSE-GRUSZCZYNSKA, M., ROHDE, M., HARTIG, R., GENTH, H., SCHMIDT, G., KEO, T., KÖNIG, W., MILLER, W., KONKEL, M. BACKERT, S. 2007. Role of the small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni. Cell. Microbiol. 9, 2431 2444.
28. LEENANON, B., ELHANAFI, D. DRAKE, M. 2003. Acid adaptation and starvation effects on Shiga toxin production by Escherichia coli O157:H7. J. Food Prot. 66, 970 977.
29. LEYER, G.J. JOHNSON, E.A. 1993. Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Appl. Environ. Microbiol. 59, 1842 1847.
30. LIVAK, K. SCHMITTGEN, T. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402 408.
31. MARTINEZ-RODRIGUEZ, A. MACKEY, B.M. 2005. Physiological changes in Campylobacter jejuni on entry into stationary phase. Int. J. Food Microbiol. 101, 1 8.
32. MEKALANOS, J.J. 1992. Environmental signals controlling expression of virulence determinants in bacteria. J. Bacteriol. 174, 1 7.
33. MIHALJEVIC, R.R., SIKIC, M., KLANCNIK, A., BRUMINI, G., MOZINA, S.S. ABRAM, M. 2007. Environmental stress factors affecting survival and virulence of Campylobacter jejuni. Microb. Pathog. 43, 120 125.
34. MOORMAN, M., NETTLETON, W., RYSER, E., LINZ, J. PESTKA, J. 2005. Altered sensitivity to a quanternary ammonium sanitizer in stressed Listeria innocua. J. Food Prot. 68, 1659 1663.
35. MÜLLER, J., SCHULZE, F., MÜLLER, W. HÄNEL, I. 2006. PCR detection of virulence-associated genes in Campylobacter jejuni strains with differential ability to invade Caco-2 cells and to colonize the chick gut. Vet. Microbiol. 113, 123 129.
36. MURPHY, C., CARROLL, C. JORDAN, K.N. 2003a. Induction of an adaptive tolerance response in the foodborne pathogen Campylobacter jejuni. FEMS Microbiol. Lett. 223, 89 93.
37. MURPHY, C., CARROLL, C. JORDAN, K.N. 2003b. Identification of a novel stress resistance mechanism in Campylobacter jejuni. J. Appl. Microbiol. 95, 704 708.
38. MURPHY, C., CARROLL, C. JORDAN, K.N. 2005. The effect of different media on the survival and induction of stress responses by Campylobacter jejuni. J. Microbiol. Methods 62, 161 166.
39. NEIDHARDT, F.C. VANBOGELEN, R.A. 2000. Proteomic analysis of bacterial stress responses. In Bacterial Stress Response (G. Storz R. Hennge-Aronis, eds.) pp. 445 452, ASM Press, Washington, DC.
40. PARKHILL, J., WREN, B.W., MUNGALL, K., KETLEY, J.M., CHURCHER, C., BASHAM, D., CHILLINGWORTH, T., DAVIES, R.M., FELTWELL, T., HOLROYD, S. ET AL. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665 668.
41. PICKETT, C., PESCI, E., COTTLE, D., RUSSELL, G., ERDEM, A. ZEYTIN, H. 1996. Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene. Infect. Immun. 64, 2070 2078.
42. RAPHAEL, B.H., PEREIRA, S., FLOM, G.A., ZHANG, Q., KETLEY, J.M. KONKEL, M.E. 2005. The Campylobacter jejuni response regulator, CbrR, modulates sodium deoxycholate resistance and chicken colonization. J. Bacteriol. 187, 3662 3670.
43. ROLLINS, D.M. COLWELL, R.R. 1986. Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Appl. Environ. Microbiol. 52, 531 538.
44. SHAHEEN, B., MILLER, M. OYARZABAL, O. 2007. In vitro survival at low pH and acid adaptation response of Campylobacter jejuni and Campylobacter coli. J. Food Safety 27, 326 343.
45. SNELLING, W., MATSUDA, M., MOORE, J. DOOLEY, J. 2005. Campylobacter jejuni. Lett. Appl. Microbiol. 41, 297 302.
46. TAUXE, R.V. 1992. Epidemiology of Campylobacter jejuni infections in the United States and other industrial nations. In Campylobacter jejuni: Current and Future Trends (I. Nachamkin, M.J. Blaser L.S. Tompkins, eds.) pp. 9 12, American Society for Microbiology, Washington, DC.
47. TRAN VAN NHIEU, G. ISBERG, R. 1994. Isolation and identification of eukaryotic receptors promoting bacterial internalization. Meth. Enzymol. 236, 307 318.
48. WHITEHOUSE, C., BALBO, P., PESCI, E., COTTLE, D., MIRABITO, P. PICKETT, C. 1998. Campylobacter jejuni cytolethal distending toxin causes a G2-phase cell cycle block. Infect. Immun. 66, 1934 1940.
49. WONG, H., PENG, P., HAN, J., CHANG, C. LAN, S. 1998. Effect of mild acid treatment on the survival, enteropathogenicity, and protein production in Vibrio parahaemolyticus. Infect. Immun. 66, 3066 3071.
50. WU, Y.L., LEE, L.H., ROLLINS, D.M. CHING, W.M. 1994. Heat shock and alkaline pH-induced proteins of Campylobacter jejuni: Characterization and immunological properties. Infect. Immun. 62, 4256 4260.
51. ZIPRIN, R.L., YOUNG, C., BYRD, J., STANKER, L., HUME, M., GRAY, S., KIM, B. KONKEL, M. 2001. Role of Campylobacter jejuni potential virulence genes in cecal colonization. Avian Dis. 45, 549 557.
52. ZIPRIN, R.L., DROLESKEY, R., HUME, M. HARVEY, H. 2003. Failure of viable nonculturable Campylobacter jejuni to colonize the cecum of newly hatched leghorn chicks. Avian Dis. 47, 753 758.