Strain-dependent induction of epithelial cell oncosis by Campylobacter jejuni is correlated with invasion ability and is independent of cytolethal distending toxin

Microbiology

Volumn 153, Issue 9, 2007, Pages 2952-2963

  Kalischuk, Lisa D ^a,b   Inglis, G Douglas ^b   Buret, Andre G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLETHAL DISTENDING TOXIN; DNA FRAGMENT;

APOPTOSIS; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CAMPYLOBACTER JEJUNI; CELL INVASION; CONTROLLED STUDY; CYTOTOXICITY; ENTERITIS; EPITHELIUM CELL; GENE DELETION; GENE FUNCTION; GENE ISOLATION; GENETIC ANALYSIS; GRAM NEGATIVE INFECTION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION;

BACTERIAL ADHESION; BACTERIAL TOXINS; CAMPYLOBACTER JEJUNI; CELL DEATH; CELL LINE; ENTEROCYTES; HUMANS; MEMBRANE POTENTIALS; MITOCHONDRIA; MUTATION; SPECIES SPECIFICITY;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

EID: 34948905287     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2006/003962-0     Document Type: Article

References (57)

1. Bang, D. D., Scheutz, F., Ahrens, P., Pedersen, K., Blom, J. & Madsen, M. (2001). Prevalence of cytolethal distending toxin (cdt) genes and CDT production in Campylobacter spp. isolated from Danish broilers. J Med Microbiol 50, 1087-1094.
2. Bielaszewska, M., Sinha, B., Kuczius, T. & Karch, H. (2005). Cytolethal distending toxin from Shiga toxin-producing Escherichia coli O157 causes irreversible G2/M arrest, inhibition of proliferation, and death of human endothelial cells. Infect Immun 73, 552-562.
3. Blanke, S. R. (2005). Micro-managing the executioner: pathogen targeting of mitochondria. Trends Microbiol 13, 64-71.
4. Brennan, M. A. & Cookson, B. T. (2000). Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38, 31-40.
5. Buret, A. G., Chin, A. C. & Scott K. G. (2003). Infection of human and bovine epithelial cells with Cryptosporidium andersoni induces apoptosis and disrupts tight junctional ZO-1: effects of epidermal growth factor. Int J Parasitol 33, 1363-1371.
6. Chin, A. C., Teoh, D. A., Scott, K. G., Meddings, J. B., Macnaughton, W. K. & Buret, A. G. (2002). Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect Immun 70, 3673-3680.
7. Chin, A. C., Vergnolle, N., MacNaughton, W. K., Wallace, J. L., Hollenberg, M. D. & Buret A. G. (2003). Proteinase-activated receptor 1 activation induces epithelial apoptosis and increases intestinal permeability. Proc Natl Acad Sci U S A 100, 11104-11109.
8. De Melo, M. A. & Pechere, J. C. (1988). Effect of mucin on Campylobacter jejuni association and invasion on HEp-2 cells. Microb Pathog 5, 71-76.
9. De Melo, M. A., Gabbiani, G. & Pechere, J. C. (1989). Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect Immun 57, 2214-2222.
10. Denis, M., Soumet, C., Rivoal, K., Ermel, G., Blivet, D., Salvat, G. & Colin, P. (1999). Development of a m-PCR assay for simultaneous identification of Campylobacter jejuni and C. coli. Lett Appl Microbiol 29, 406-410.
11. Dong, Z., Saikumar, P., Weinberg, J. M. & Venkatachalam, M. A. (1997). Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am J Pathol 151, 1205-1213.
12. Earnshaw, W. C., Martins, L. M. & Kaufmann, S. H. (1999). Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68, 383-424.
13. Eguchi, Y., Shimizu, S. & Tsujimoto, Y. (1997). Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57, 1835-1840.
14. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A. & Nagata, S. (1998). A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43-50.
15. Everest P. H., Goossens, H., Butzler, J. P., Lloyd, D., Knutton, S., Ketley, J. M. & Williams, P. H. (1992). Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J Med Microbiol 37, 319-325.
16. Eylgor, A., Dawson, K A., Langlois, B. E. & Pickett, C. L. (1999). Detection of cytolethal distending toxin activity and cdt genes in Campylobacter spp. isolated from chicken carcasses. Appl Environ Microbiol 65, 1501-1505.
17. Fernandez-Prada, C., Tall, B. D., Elliott, S. E., Hoover, D. L., Nataro, J. P. & Venkatesan, M. M. (1998). Hemolysin-positive enteroaggregative and cell-detaching Escherichia coli strains cause oncosis of human monocyte-derived macrophages and apoptosis of murine J774 cells. Infect Immun 66, 3918-3924.
18. Fiorentini, C., Fabbri, A., Falzano, L., Fattorossi, A., Matarrese, P., Rivabene, R. & Donelli, G. (1998). Clostridium difficile toxin B induces apoptosis in intestinal cultured cells. Infect Immun 66, 2660-2665.
19. Gao, J. X., Ma, B. L., Xie, Y. L. & Huang, D. S. (1991). Electron microscopic appearance of the chronic Campylobacter jejuni enteritis of mice. Chin Med J (Engl) 104, 1005-1010.
20. Gaynor, E. C., Cawthraw, S., Manning, G., MacKichan, J. K., Falkow, S. & Newell, D. G. (2004). The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J Bacteriol 186, 503-517.
21. Golstein, P. & Kroemer, G. (2007). Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32, 37-43.
22. Hickey, T. E., Majam, G. & Guerry, P. (2005). Intracellular survival of Campylobacter jejuni in human monocytic cells and induction of apoptotic death by cytholethal distending toxin. Infect Immun 73, 5194-5197.
23. Humphrey, C. D., Montag, D. M. & Pittman, F. E. (1986). Morphologic observations of experimental Campylobacter jejuni infection in the hamster intestinal tract. Am J Pathol 122, 152-159.
24. Ketley, J. M. (1997). Pathogenesis of enteric infection by Campylobacter. Microbiology 143, 5-21.
25. Kiechle, F. L. & Zhang, X. (2002). Apoptosis: biochemical aspects and clinical implications. Clin Chim Acta 326, 27-45.
26. Kim, J. M., Eckmann, L., Savidge, T. C., Lowe, D. C., Witthoft, T. & Kagnoff, M. F. (1998). Apoptosis of human intestinal epithelial cells after bacterial invasion. J Clin Invest 102, 1815-1823.
27. Kim, J. S., He, L. & Lemasters, J. J. (2003). Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 304, 463-470.
28. Klipstein, F. A., Engert, R. F., Short, H. & Schenk, E. A. (1985). Pathogenic properties of Campylobacter jejuni: assay and correlation with clinical manifestations. Infect Immun 50, 43-49.
29. Klipstein, F. A., Engert R. F. & Short H. B. (1986). Enzyme-linked inummosorbent assays for virulence properties of Campylobacter jejuni clinical isolates. J Clin Microbiol 23, 1039-1043.
30. Konkel, M. E., Klena, J. D., Rivera-Amill, V., Monteville, M. R., Biswas, D., Raphael, B. & Mickelson, J. (2004). Secretion of virulence proteins from Campylobacter jojuni is dependent on a functional flagellar export apparatus. J Bacteriol 186, 3296-3303.
31. Korlath, J. A., Osterholm, M. T., Judy, L. A., Forfang, J. C. & Robinson, R. A. (1985). A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152, 592-596.
32. Lara-Tejero, M. & Galan, J. E. (2001). CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal. distending toxin activity. Infect Immun 69, 4358-4365.
33. Leist M., Single, B., Castoldi, A. F., Kuhnie, S. & Nicotera, P. (1997). Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis.: J Exp Med 185, 1481-1486.
34. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S. & Wang, X. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.
35. Lindblom, G. B. & Kaijser, B. (1995). In vitro studies of Campylobacter jejuni/coli strains from hens and humans regarding adherence, invasiveness, and toxigenicity. Avian Dis 39, 718-722.
36. Los, M., Mozoluk, M., Ferrari, D., Stepczynska, A., Stroh, C., Renz, A., Herceg, Z., Wang, Z. M & Schulze-Osthoff, K. (2002). Activation and caspase-mediated inhibition of PARP: a molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol Biol Cell 13, 978-988.
37. Ma, C., Wickham, M. E., Guttman, J. A., Deng, W., Walker, J., Madsen, K L., Jacobson, K, Vogl, W. A., Finlay, B. B. & Valiance, B. A. (2006). Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: role of mitochondrial associated protein (Map). Cell Microbiol 8, 1669-1686.
38. Majno, G. & Joris, I.(1995). Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146, 3-15.
39. Miller, J. F., Dower, W. J. & Tompkins, L S. (1988). High-voltage electroporation of bacteria: genetic transformation of Campylobacter jejuni with plasmid DNA. Proc Natl Acad Sci U S A 85, 856-860.
40. Monteville, M. R., Yoon, J. E. & Konkel, M. E. (2003). Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 149, 153-165.
41. Nadeau, E., Messier, S. & Quessy, S. (2003). Comparison of Campylobacter isolates from poultry and humans: association between in vitro virulence properties, biotypes, and pulsed-field gel electrophoresis clusters. Appl Environ Microbiol 69, 6316-6320.
42. Newell, D. G. & Pearson, A. (1984). The invasion of epithelial cell lines and the intestinal epithelium of infant mice by Campylobacter jejuni/coli. J Diarrhoeal Dis Res 2, 19-26.
43. Nonaka, T., Kuwabara, T., Mimuro, H., Kuwae, A. & Imajoh-Ohmi, S. (2003). Shigella-induced necrosis and apoptosis of U937 cells and J774 macrophages. Microbiology 149, 2513-2527.
44. Palomba, L., Sestill, P., Columbaro, M., Falcieri, E. & Cantoni, O. (1999). Apoptosis and necrosis following exposure of U937 cells to increasing concentrations of hydrogen peroxide: the effect of the poly(ADP-ribose)polymerase inhibitor 3-aminobenzamide. Biochem Pharmacol 58, 1743-1750.
45. Pickett, C. L., Pescl, E. C., Cottle, D. L., Russell, G., Erdem, A. N. & Zeytin, H. (1996). Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene. Infect Immun 64, 2070-2078.
46. Purdy, D., Buswell, C. M., Hodgson, A. E., McAlpine, K, Henderson, I. & Leach, S. A. (2000). Characterisation of cytolethal distending toxin (CDT) mutants of Campylobacterjejuni. J Med Microbiol 49, 473-479.
47. Ren, Y. & Savill, J. (1998). Apoptosis: the importance of being eaten. Cell Death Differ 5, 563-568.
48. Russell, R. G., O'Donnoghue, K, Blake, D. C., Jr, Zulty, J. & DeTolla, L. J. (1993). Early colonic damage and invasion of Campylobacter jejuni in experimentally challenged infant Macaca mulatta. J Infect Dis 168, 210-215.
49. Slegesmund, A. M., Konkel, M. E., Klena, J. D. & Mixter, P. F. (2004). Campylobacter jejuni infection of differentiated THP-1 macrophages results in interleukin 1 beta release and caspase-1-independent apoptosis. Microbiology 150, 561-569.
50. Smiley, S. T., Rears, M., Mottola-Hartshorn, C., Lin, M., Chen, A., Smith, T. W., Steele, G. D., Jr & Chen, L. B. (1991). Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci U S A 88, 3671-3675.
51. Stanfield, J. T., McCardell, B. A. & Madden, J. M. (1987). Campylobacter diarrhea in an adult mouse model. Microb Pathog 3, 155-165.
52. Vandenabeele, P., Vanden Berghe, T. & Festjens, N. (2006). Caspase inhibitors promote alternative cell death pathways. Sci STKE 2006, pe44.
53. Wassenaar, T. M. (1997). Toxin production by Campylobacter spp. Clin Microbiol Rev 10, 466-476.
54. Wassenaar, T. M. & Blaser, M. J. (1999). Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1, 1023-1033.
55. Whitehouse, C. A., Balbo, P. B., Pesci, E. C., Cottle, D. L., Mirabito, P. M. & Pickett, C. L. (1998). Campylobacter jejuni cytolethal. distending toxin causes a G2-phase cell cycle block. Infect Immun 66, 1934-1940.
56. Zhu, J., Meinersmann, R. J., Hiett, K. L. & Evans, D. L. (1999). Apoptotic effect of outer-membrane proteins from Campylobacter jejuni on chicken lymphocytes. Curr Microbiol 38, 244-249.
57. Zychlinsky, A. (1993). Programmed cell death in infectious diseases. Trends Microbiol 1, 114-117.