Skip to main content
Clinical Microbiology Reviews logoLink to Clinical Microbiology Reviews
. 1997 Jul;10(3):466–476. doi: 10.1128/cmr.10.3.466

Toxin production by Campylobacter spp.

T M Wassenaar 1
PMCID: PMC172930  PMID: 9227862

Abstract

Of all the virulence factors that were proposed for Campylobacter jejuni and related species to cause disease in humans, the discovery of toxin production was the most promising but led to a rather confusing and even disappointing stream of data. The discussion of whether proteinaceous exotoxins are relevant in disease remains open. One important reason for this lack of consensus is the anecdotal nature of the literature reports. To provide a basis for an unbiased opinion, this review compiles all described exotoxins, compares their reported properties, and provides a summary of animal model studies and clinical data. The toxins are divided into enterotoxins and cytotoxins and are sorted according to their biochemical properties. Since many Campylobacter toxins have been compared with toxins of other species, some key examples of the latter are also discussed. Future directions of toxin research that appear promising are defined.

Full Text

The Full Text of this article is available as a PDF (229.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguero-Rosenfeld M. E., Yang X. H., Nachamkin I. Infection of adult Syrian hamsters with flagellar variants of Campylobacter jejuni. Infect Immun. 1990 Jul;58(7):2214–2219. doi: 10.1128/iai.58.7.2214-2219.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akhtar S. Q., Huq F. Effect of Campylobacter jejuni extracts and culture supernatants on cell culture. J Trop Med Hyg. 1989 Apr;92(2):80–85. [PubMed] [Google Scholar]
  3. Arimi S. M., Park R. W., Fricker C. R. Study of haemolytic activity of some Campylobacter spp. on blood agar plates. J Appl Bacteriol. 1990 Sep;69(3):384–389. doi: 10.1111/j.1365-2672.1990.tb01528.x. [DOI] [PubMed] [Google Scholar]
  4. Bag P. K., Ramamurthy T., Nair U. B. Evidence for the presence of a receptor for the cytolethal distending toxin (CLDT) of Campylobacter jejuni on CHO and HeLa cell membranes and development of a receptor-based enzyme-linked immunosorbent assay for detection of CLDT. FEMS Microbiol Lett. 1993 Dec 15;114(3):285–291. doi: 10.1111/j.1574-6968.1993.tb06587.x. [DOI] [PubMed] [Google Scholar]
  5. Baig B. H., Wachsmuth I. K., Morris G. K., Hill W. E. Probing of Campylobacter jejuni with DNA coding for Escherichia coli heat-labile enterotoxin. J Infect Dis. 1986 Sep;154(3):542–542. doi: 10.1093/infdis/154.3.542. [DOI] [PubMed] [Google Scholar]
  6. Beutin L., Bode L., Ozel M., Stephan R. Enterohemolysin production is associated with a temperate bacteriophage in Escherichia coli serogroup O26 strains. J Bacteriol. 1990 Nov;172(11):6469–6475. doi: 10.1128/jb.172.11.6469-6475.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Beutin L., Prada J., Zimmermann S., Stephan R., Orskov I., Orskov F. Enterohemolysin, a new type of hemolysin produced by some strains of enteropathogenic E. coli (EPEC). Zentralbl Bakteriol Mikrobiol Hyg A. 1988 Mar;267(4):576–588. doi: 10.1016/s0176-6724(88)80042-7. [DOI] [PubMed] [Google Scholar]
  8. Beutin L., Stroeher U. H., Manning P. A. Isolation of enterohemolysin (Ehly2)-associated sequences encoded on temperate phages of Escherichia coli. Gene. 1993 Sep 30;132(1):95–99. doi: 10.1016/0378-1119(93)90519-9. [DOI] [PubMed] [Google Scholar]
  9. Beutin L. The different hemolysins of Escherichia coli. Med Microbiol Immunol. 1991;180(4):167–182. doi: 10.1007/BF00215246. [DOI] [PubMed] [Google Scholar]
  10. Bhakdi S., Bayley H., Valeva A., Walev I., Walker B., Kehoe M., Palmer M. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch Microbiol. 1996 Feb;165(2):73–79. doi: 10.1007/s002030050300. [DOI] [PubMed] [Google Scholar]
  11. Bhakdi S., Grimminger F., Suttorp N., Walmrath D., Seeger W. Proteinaceous bacterial toxins and pathogenesis of sepsis syndrome and septic shock: the unknown connection. Med Microbiol Immunol. 1994 Jul;183(3):119–144. doi: 10.1007/BF00196048. [DOI] [PubMed] [Google Scholar]
  12. Black R. E., Levine M. M., Clements M. L., Hughes T. P., Blaser M. J. Experimental Campylobacter jejuni infection in humans. J Infect Dis. 1988 Mar;157(3):472–479. doi: 10.1093/infdis/157.3.472. [DOI] [PubMed] [Google Scholar]
  13. Blaser M. J., Reller L. B. Campylobacter enteritis. N Engl J Med. 1981 Dec 10;305(24):1444–1452. doi: 10.1056/NEJM198112103052404. [DOI] [PubMed] [Google Scholar]
  14. Bok H. E., Greeff A. S., Crewe-Brown H. H. Incidence of toxigenic Campylobacter strains in South Africa. J Clin Microbiol. 1991 Jun;29(6):1262–1264. doi: 10.1128/jcm.29.6.1262-1264.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Braun V., Focareta T. Pore-forming bacterial protein hemolysins (cytolysins). Crit Rev Microbiol. 1991;18(2):115–158. doi: 10.3109/10408419109113511. [DOI] [PubMed] [Google Scholar]
  16. Calva E., Torres J., Vázquez M., Angeles V., de la Vega H., Ruíz-Palacios G. M. Campylobacter jejuni chromosomal sequences that hybridize to Vibrio cholerae and Escherichia coli LT enterotoxin genes. Gene. 1989 Feb 20;75(2):243–251. doi: 10.1016/0378-1119(89)90270-9. [DOI] [PubMed] [Google Scholar]
  17. Collins S., O'Loughlin E., O'Rourke J., Li Z., Lee A., Howden M. A cytotonic, cholera toxin-like protein produced by Campylobacter jejuni. Comp Biochem Physiol B. 1992 Oct;103(2):299–303. doi: 10.1016/0305-0491(92)90295-3. [DOI] [PubMed] [Google Scholar]
  18. Coote J. G., Arain T. A rapid, colourimetric assay for cytotoxin activity in Campylobacter jejuni. FEMS Immunol Med Microbiol. 1996 Jan;13(1):65–70. doi: 10.1111/j.1574-695X.1996.tb00217.x. [DOI] [PubMed] [Google Scholar]
  19. Daikoku T., Kawaguchi M., Takama K., Suzuki S. Partial purification and characterization of the enterotoxin produced by Campylobacter jejuni. Infect Immun. 1990 Aug;58(8):2414–2419. doi: 10.1128/iai.58.8.2414-2419.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Daikoku T., Suzuki S., Oka S., Takama K. Profiles of enterotoxin and cytotoxin production in Campylobacter jejuni and C. coli. FEMS Microbiol Lett. 1989 Mar;49(1):33–36. doi: 10.1016/0378-1097(89)90337-6. [DOI] [PubMed] [Google Scholar]
  21. De Melo M. A., Gabbiani G., Pechère J. C. Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect Immun. 1989 Jul;57(7):2214–2222. doi: 10.1128/iai.57.7.2214-2222.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Dillon S. T., Rubin E. J., Yakubovich M., Pothoulakis C., LaMont J. T., Feig L. A., Gilbert R. J. Involvement of Ras-related Rho proteins in the mechanisms of action of Clostridium difficile toxin A and toxin B. Infect Immun. 1995 Apr;63(4):1421–1426. doi: 10.1128/iai.63.4.1421-1426.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Dolg P., Yao R., Burr D. H., Guerry P., Trust T. J. An environmentally regulated pilus-like appendage involved in Campylobacter pathogenesis. Mol Microbiol. 1996 May;20(4):885–894. doi: 10.1111/j.1365-2958.1996.tb02526.x. [DOI] [PubMed] [Google Scholar]
  24. Endo Y., Tsurugi K., Yutsudo T., Takeda Y., Ogasawara T., Igarashi K. Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem. 1988 Jan 15;171(1-2):45–50. doi: 10.1111/j.1432-1033.1988.tb13756.x. [DOI] [PubMed] [Google Scholar]
  25. Everest P. H., Cole A. T., Hawkey C. J., Knutton S., Goossens H., Butzler J. P., Ketley J. M., Williams P. H. Roles of leukotriene B4, prostaglandin E2, and cyclic AMP in Campylobacter jejuni-induced intestinal fluid secretion. Infect Immun. 1993 Nov;61(11):4885–4887. doi: 10.1128/iai.61.11.4885-4887.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Everest P. H., Goossens H., Butzler J. P., Lloyd D., Knutton S., Ketley J. M., Williams P. H. Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J Med Microbiol. 1992 Nov;37(5):319–325. doi: 10.1099/00222615-37-5-319. [DOI] [PubMed] [Google Scholar]
  27. Everest P. H., Goossens H., Sibbons P., Lloyd D. R., Knutton S., Leece R., Ketley J. M., Williams P. H. Pathological changes in the rabbit ileal loop model caused by Campylobacter jejuni from human colitis. J Med Microbiol. 1993 May;38(5):316–321. doi: 10.1099/00222615-38-5-316. [DOI] [PubMed] [Google Scholar]
  28. Fauchère J. L., Kervella M., Rosenau A., Mohanna K., Véron M. Adhesion to HeLa cells of Campylobacter jejuni and C. coli outer membrane components. Res Microbiol. 1989 Jul-Aug;140(6):379–392. doi: 10.1016/0923-2508(89)90014-4. [DOI] [PubMed] [Google Scholar]
  29. Fernández H., Neto U. F., Fernandes F., de Almeida Pedra M., Trabulsi L. R. Culture supernatants of Campylobacter jejuni induce a secretory response in jejunal segments of adult rats. Infect Immun. 1983 Apr;40(1):429–431. doi: 10.1128/iai.40.1.429-431.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Florin I., Antillon F. Production of enterotoxin and cytotoxin in Campylobacter jejuni strains isolated in Costa Rica. J Med Microbiol. 1992 Jul;37(1):22–29. doi: 10.1099/00222615-37-1-22. [DOI] [PubMed] [Google Scholar]
  31. Gillespie M. J., Smutko J., Haraszthy G. G., Zambon J. J. Isolation and partial characterization of the Campylobacter rectus cytotoxin. Microb Pathog. 1993 Mar;14(3):203–215. doi: 10.1006/mpat.1993.1020. [DOI] [PubMed] [Google Scholar]
  32. Goossens H., Rummens E., Cadranel S., Butzler J. P., Takeda Y. Cytotoxic activity on Chinese hamster ovary cells in culture filtrates of Campylobacter jejuni/coli. Lancet. 1985 Aug 31;2(8453):511–511. doi: 10.1016/s0140-6736(85)90454-4. [DOI] [PubMed] [Google Scholar]
  33. Grant C. C., Konkel M. E., Cieplak W., Jr, Tompkins L. S. Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect Immun. 1993 May;61(5):1764–1771. doi: 10.1128/iai.61.5.1764-1771.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Guerrant R. L., Wanke C. A., Pennie R. A., Barrett L. J., Lima A. A., O'Brien A. D. Production of a unique cytotoxin by Campylobacter jejuni. Infect Immun. 1987 Oct;55(10):2526–2530. doi: 10.1128/iai.55.10.2526-2530.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Guerry P., Yao R., Alm R. A., Burr D. H., Trust T. J. Systems of experimental genetics for Campylobacter species. Methods Enzymol. 1994;235:474–481. doi: 10.1016/0076-6879(94)35163-5. [DOI] [PubMed] [Google Scholar]
  36. Hossain A., Stewart-Tull D. E., Freer J. H. Heat-labile and heat-stable haemolysins of Campylobacter jejuni. FEMS Immunol Med Microbiol. 1993 Apr;6(4):331–339. doi: 10.1111/j.1574-695X.1993.tb00346.x. [DOI] [PubMed] [Google Scholar]
  37. Ichinose Y., Yamamoto K., Nakasone N., Tanabe M. J., Takeda T., Miwatani T., Iwanaga M. Enterotoxicity of El Tor-like hemolysin of non-O1 Vibrio cholerae. Infect Immun. 1987 May;55(5):1090–1093. doi: 10.1128/iai.55.5.1090-1093.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Johnson W. M., Lior H. A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. Microb Pathog. 1988 Feb;4(2):115–126. doi: 10.1016/0882-4010(88)90053-8. [DOI] [PubMed] [Google Scholar]
  39. Johnson W. M., Lior H. Cytotoxic and cytotonic factors produced by Campylobacter jejuni, Campylobacter coli, and Campylobacter laridis. J Clin Microbiol. 1986 Aug;24(2):275–281. doi: 10.1128/jcm.24.2.275-281.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Johnson W. M., Lior H. Toxins produced by Campylobacter jejuni and Campylobacter coli. Lancet. 1984 Jan 28;1(8370):229–230. doi: 10.1016/s0140-6736(84)92155-x. [DOI] [PubMed] [Google Scholar]
  41. Just I., Selzer J., Wilm M., von Eichel-Streiber C., Mann M., Aktories K. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature. 1995 Jun 8;375(6531):500–503. doi: 10.1038/375500a0. [DOI] [PubMed] [Google Scholar]
  42. Kanwar R. K., Ganguly N. K., Kanwar J. R., Kumar L., Walia B. N. Impairment of Na+,K(+)-ATPase activity following enterotoxigenic Campylobacter jejuni infection: changes in Na+, Cl- and 3-O-methyl-D-glucose transport in vitro, in rat ileum. FEMS Microbiol Lett. 1994 Dec 15;124(3):381–385. doi: 10.1111/j.1574-6968.1994.tb07312.x. [DOI] [PubMed] [Google Scholar]
  43. Kaur R., Ganguly N. K., Kumar L., Walia B. N. Studies on the pathophysiological mechanism of Campylobacter jejuni-induced fluid secretion in rat ileum. FEMS Microbiol Lett. 1993 Aug 1;111(2-3):327–330. doi: 10.1111/j.1574-6968.1993.tb06406.x. [DOI] [PubMed] [Google Scholar]
  44. Ketley J. M. The 16th C. L. Oakley Lecture. Virulence of Campylobacter species: a molecular genetic approach. J Med Microbiol. 1995 May;42(5):312–327. doi: 10.1099/00222615-42-5-312. [DOI] [PubMed] [Google Scholar]
  45. Khalil K., Lindblom G. B., Mazhar K., Sjögren E., Kaijser B. Frequency and enterotoxigenicity of Campylobacter jejuni and C. coli in domestic animals in Pakistan as compared to Sweden. J Trop Med Hyg. 1993 Feb;96(1):35–40. [PubMed] [Google Scholar]
  46. Kita E., Nishikawa F., Kamikaidou N., Nakano A., Katsui N., Kashiba S. Mononuclear cell response in the liver of mice infected with hepatotoxigenic Campylobacter jejuni. J Med Microbiol. 1992 Nov;37(5):326–331. doi: 10.1099/00222615-37-5-326. [DOI] [PubMed] [Google Scholar]
  47. Kita E., Oku D., Hamuro A., Nishikawa F., Emoto M., Yagyu Y., Katsui N., Kashiba S. Hepatotoxic activity of Campylobacter jejuni. J Med Microbiol. 1990 Nov;33(3):171–182. doi: 10.1099/00222615-33-3-171. [DOI] [PubMed] [Google Scholar]
  48. Klipstein F. A., Engert R. F. Immunological relationship of the B subunits of Campylobacter jejuni and Escherichia coli heat-labile enterotoxins. Infect Immun. 1985 Jun;48(3):629–633. doi: 10.1128/iai.48.3.629-633.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Klipstein F. A., Engert R. F. Properties of crude Campylobacter jejuni heat-labile enterotoxin. Infect Immun. 1984 Aug;45(2):314–319. doi: 10.1128/iai.45.2.314-319.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Klipstein F. A., Engert R. F. Purification of Campylobacter jejuni enterotoxin. Lancet. 1984 May 19;1(8386):1123–1124. doi: 10.1016/s0140-6736(84)92536-4. [DOI] [PubMed] [Google Scholar]
  51. Klipstein F. A., Engert R. F., Short H. B. Enzyme-linked immunosorbent assays for virulence properties of Campylobacter jejuni clinical isolates. J Clin Microbiol. 1986 Jun;23(6):1039–1043. doi: 10.1128/jcm.23.6.1039-1043.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Klipstein F. A., Engert R. F., Short H., Schenk E. A. Pathogenic properties of Campylobacter jejuni: assay and correlation with clinical manifestations. Infect Immun. 1985 Oct;50(1):43–49. doi: 10.1128/iai.50.1.43-49.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Konkel M. E., Corwin M. D., Joens L. A., Cieplak W. Factors that influence the interaction of Campylobacter jejuni with cultured mammalian cells. J Med Microbiol. 1992 Jul;37(1):30–37. doi: 10.1099/00222615-37-1-30. [DOI] [PubMed] [Google Scholar]
  54. Konkel M. E., Hayes S. F., Joens L. A., Cieplak W., Jr Characteristics of the internalization and intracellular survival of Campylobacter jejuni in human epithelial cell cultures. Microb Pathog. 1992 Nov;13(5):357–370. doi: 10.1016/0882-4010(92)90079-4. [DOI] [PubMed] [Google Scholar]
  55. Konkel M. E., Joens L. A. Adhesion to and invasion of HEp-2 cells by Campylobacter spp. Infect Immun. 1989 Oct;57(10):2984–2990. doi: 10.1128/iai.57.10.2984-2990.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Lindblom G. B., Cervantes L. E., Sjögren E., Kaijser B., Ruiz-Palacios G. M. Adherence, enterotoxigenicity, invasiveness and serogroups in Campylobacter jejuni and Campylobacter coli strains from adult humans with acute enterocolitis. APMIS. 1990 Feb;98(2):179–184. [PubMed] [Google Scholar]
  57. Lindblom G. B., Johny M., Khalil K., Mazhar K., Ruiz-Palacios G. M., Kaijser B. Enterotoxigenicity and frequency of Campylobacter jejuni, C. coli and C. laridis in human and animal stool isolates from different countries. FEMS Microbiol Lett. 1990 Jan 1;54(1-3):163–167. doi: 10.1111/j.1574-6968.1990.tb03990.x. [DOI] [PubMed] [Google Scholar]
  58. Lindblom G. B., Kaijser B., Sjögren E. Enterotoxin production and serogroups of Campylobacter jejuni and Campylobacter coli from patients with diarrhea and from healthy laying hens. J Clin Microbiol. 1989 Jun;27(6):1272–1276. doi: 10.1128/jcm.27.6.1272-1276.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Lyerly D. M., Krivan H. C., Wilkins T. D. Clostridium difficile: its disease and toxins. Clin Microbiol Rev. 1988 Jan;1(1):1–18. doi: 10.1128/cmr.1.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Mahajan S., Rodgers F. G. Isolation, characterization, and host-cell-binding properties of a cytotoxin from Campylobacter jejuni. J Clin Microbiol. 1990 Jun;28(6):1314–1320. doi: 10.1128/jcm.28.6.1314-1320.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Martin P. M., Mathiot J., Ipero J., Georges A. J., Georges-Courbot M. C. Antibody response to Campylobacter coli in children during intestinal infection and carriage. J Clin Microbiol. 1988 Jul;26(7):1421–1424. doi: 10.1128/jcm.26.7.1421-1424.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Martin P. M., Mathiot J., Ipero J., Kirimat M., Georges A. J., Georges-Courbot M. C. Immune response to Campylobacter jejuni and Campylobacter coli in a cohort of children from birth to 2 years of age. Infect Immun. 1989 Aug;57(8):2542–2546. doi: 10.1128/iai.57.8.2542-2546.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Mathan V. I., Rajan D. P., Klipstein F. A., Engert R. F. Enterotoxigenic Campylobacter jejuni among children in South India. Lancet. 1984 Oct 27;2(8409):981–981. doi: 10.1016/s0140-6736(84)91193-0. [DOI] [PubMed] [Google Scholar]
  64. McCardell B. A., Madden J. M., Lee E. C. Production of cholera-like toxin by Campylobacter jejuni/coli. Lancet. 1984 Feb 25;1(8374):448–449. doi: 10.1016/s0140-6736(84)91772-0. [DOI] [PubMed] [Google Scholar]
  65. McCardell B. A., Madden J. M., Stanfield J. T. Effect of iron concentration on toxin production in Campylobacter jejuni and Campylobacter coli. Can J Microbiol. 1986 May;32(5):395–401. doi: 10.1139/m86-075. [DOI] [PubMed] [Google Scholar]
  66. McCardell B. A., Madden J. M., Stanfield J. T. Production of cytotoxins by Campylobacter. Lancet. 1986 May 3;1(8488):1031–1031. doi: 10.1016/s0140-6736(86)91297-3. [DOI] [PubMed] [Google Scholar]
  67. McFarland B. A., Neill S. D. Profiles of toxin production by thermophilic Campylobacter of animal origin. Vet Microbiol. 1992 Feb;30(2-3):257–266. doi: 10.1016/0378-1135(92)90119-e. [DOI] [PubMed] [Google Scholar]
  68. McSweegan E., Walker R. I. Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect Immun. 1986 Jul;53(1):141–148. doi: 10.1128/iai.53.1.141-148.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Misawa N., Hirayama K., Itoh K., Takahashi E. Detection of alpha- and beta-hemolytic-like activity from Campylobacter jejuni. J Clin Microbiol. 1995 Mar;33(3):729–731. doi: 10.1128/jcm.33.3.729-731.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Misawa N., Ohnishi T., Itoh K., Takahashi E. Cytotoxin detection in Campylobacter jejuni strains of human and animal origin with three tissue culture assay systems. J Med Microbiol. 1995 Nov;43(5):354–359. doi: 10.1099/00222615-43-5-354. [DOI] [PubMed] [Google Scholar]
  71. Misawa N., Ohnishi T., Itoh K., Takahashi E. Development of a tissue culture assay system for Campylobacter jejuni cytotoxin and the influence of culture conditions on cytotoxin production. J Med Microbiol. 1994 Oct;41(4):224–230. doi: 10.1099/00222615-41-4-224. [DOI] [PubMed] [Google Scholar]
  72. Mizuno K., Takama K., Suzuki S. Characteristics of cytotoxin produced by Campylobacter jejuni strains. Microbios. 1994;78(317):215–228. [PubMed] [Google Scholar]
  73. Moore M. A., Blaser M. J., Perez-Perez G. I., O'Brien A. D. Production of a Shiga-like cytotoxin by Campylobacter. Microb Pathog. 1988 Jun;4(6):455–462. doi: 10.1016/0882-4010(88)90030-7. [DOI] [PubMed] [Google Scholar]
  74. Morooka T., Umeda A., Amako K. Motility as an intestinal colonization factor for Campylobacter jejuni. J Gen Microbiol. 1985 Aug;131(8):1973–1980. doi: 10.1099/00221287-131-8-1973. [DOI] [PubMed] [Google Scholar]
  75. Morris G. K., Merson M. H., Sack D. A., Wells J. G., Martin W. T., Dewitt W. E., Feeley J. C., Sack R. B., Bessudo D. M. Laboratory investigation of diarrhea in travelers to Mexico: evaluation of methods for detecting enterotoxigenic Echerichia coli. J Clin Microbiol. 1976 May;3(5):486–495. doi: 10.1128/jcm.3.5.486-495.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Newell D. G., McBride H., Dolby J. M. Investigations on the role of flagella in the colonization of infant mice with Campylobacter jejuni and attachment of Campylobacter jejuni to human epithelial cell lines. J Hyg (Lond) 1985 Oct;95(2):217–227. doi: 10.1017/s0022172400062653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Nishibuchi M., Fasano A., Russell R. G., Kaper J. B. Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect Immun. 1992 Sep;60(9):3539–3545. doi: 10.1128/iai.60.9.3539-3545.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Obrig T. G. Toxins that inhibit host protein synthesis. Methods Enzymol. 1994;235:647–656. doi: 10.1016/0076-6879(94)35178-3. [DOI] [PubMed] [Google Scholar]
  79. Ohya T., Tominaga K., Nakazawa M. Production of cytolethal distending toxin (CLDT) by Campylobacter fetus subsp. fetus isolated from calves. J Vet Med Sci. 1993 Jun;55(3):507–509. doi: 10.1292/jvms.55.507. [DOI] [PubMed] [Google Scholar]
  80. Olsnes S., Reisbig R., Eiklid K. Subunit structure of Shigella cytotoxin. J Biol Chem. 1981 Aug 25;256(16):8732–8738. [PubMed] [Google Scholar]
  81. Olsvik O., Wachsmuth K., Morris G., Feeley J. C. Genetic probing of Campylobacter jejuni for cholera toxin and Escherichia coli heat-labile enterotoxin. Lancet. 1984 Feb 25;1(8374):449–449. doi: 10.1016/s0140-6736(84)91773-2. [DOI] [PubMed] [Google Scholar]
  82. Pang T., Wong P. Y., Puthucheary S. D., Sihotang K., Chang W. K. In-vitro and in-vivo studies of a cytotoxin from Campylobacter jejuni. J Med Microbiol. 1987 May;23(3):193–198. doi: 10.1099/00222615-23-3-193. [DOI] [PubMed] [Google Scholar]
  83. Park S. F., Richardson P. T. Molecular characterization of a Campylobacter jejuni lipoprotein with homology to periplasmic siderophore-binding proteins. J Bacteriol. 1995 May;177(9):2259–2264. doi: 10.1128/jb.177.9.2259-2264.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Perez-Perez G. I., Cohn D. L., Guerrant R. L., Patton C. M., Reller L. B., Blaser M. J. Clinical and immunologic significance of cholera-like toxin and cytotoxin production by Campylobacter species in patients with acute inflammatory diarrhea in the USA. J Infect Dis. 1989 Sep;160(3):460–468. doi: 10.1093/infdis/160.3.460. [DOI] [PubMed] [Google Scholar]
  85. Pickett C. L., Auffenberg T., Pesci E. C., Sheen V. L., Jusuf S. S. Iron acquisition and hemolysin production by Campylobacter jejuni. Infect Immun. 1992 Sep;60(9):3872–3877. doi: 10.1128/iai.60.9.3872-3877.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Pickett C. L., Cottle D. L., Pesci E. C., Bikah G. Cloning, sequencing, and expression of the Escherichia coli cytolethal distending toxin genes. Infect Immun. 1994 Mar;62(3):1046–1051. doi: 10.1128/iai.62.3.1046-1051.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Pickett C. L., Pesci E. C., Cottle D. L., Russell G., Erdem A. N., Zeytin H. Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene. Infect Immun. 1996 Jun;64(6):2070–2078. doi: 10.1128/iai.64.6.2070-2078.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Raimondi F., Kao J. P., Kaper J. B., Guandalini S., Fasano A. Calcium-dependent intestinal chloride secretion by Vibrio parahaemolyticus thermostable direct hemolysin in a rabbit model. Gastroenterology. 1995 Aug;109(2):381–386. doi: 10.1016/0016-5085(95)90324-0. [DOI] [PubMed] [Google Scholar]
  89. Reisbig R., Olsnes S., Eiklid K. The cytotoxic activity of Shigella toxin. Evidence for catalytic inactivation of the 60 S ribosomal subunit. J Biol Chem. 1981 Aug 25;256(16):8739–8744. [PubMed] [Google Scholar]
  90. Rowe G. E., Welch R. A. Assays of hemolytic toxins. Methods Enzymol. 1994;235:657–667. doi: 10.1016/0076-6879(94)35179-1. [DOI] [PubMed] [Google Scholar]
  91. Ruiz-Palacios G. M., López-Vidal Y., Torres J., Torres N. Serum antibodies to heat-labile enterotoxin of Campylobacter jejuni. J Infect Dis. 1985 Aug;152(2):413–416. doi: 10.1093/infdis/152.2.413. [DOI] [PubMed] [Google Scholar]
  92. Ruiz-Palacios G. M., Torres J., Torres N. I., Escamilla E., Ruiz-Palacios B. R., Tamayo J. Cholera-like enterotoxin produced by Campylobacter jejuni. Characterisation and clinical significance. Lancet. 1983 Jul 30;2(8344):250–253. doi: 10.1016/s0140-6736(83)90234-9. [DOI] [PubMed] [Google Scholar]
  93. Saha S. K., Saha S., Sanyal S. C. Recovery of injured Campylobacter jejuni cells after animal passage. Appl Environ Microbiol. 1991 Nov;57(11):3388–3389. doi: 10.1128/aem.57.11.3388-3389.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Saha S. K., Singh N. P., Sanyal S. C. Enterotoxigenicity of chicken isolates of Campylobacter jejuni in ligated ileal loops of rats. J Med Microbiol. 1988 Jun;26(2):87–91. doi: 10.1099/00222615-26-2-87. [DOI] [PubMed] [Google Scholar]
  95. Scott D. A., Kaper J. B. Cloning and sequencing of the genes encoding Escherichia coli cytolethal distending toxin. Infect Immun. 1994 Jan;62(1):244–251. doi: 10.1128/iai.62.1.244-251.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Sears C. L., Kaper J. B. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol Rev. 1996 Mar;60(1):167–215. doi: 10.1128/mr.60.1.167-215.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Spangler B. D. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev. 1992 Dec;56(4):622–647. doi: 10.1128/mr.56.4.622-647.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Spira W. M., Sack R. B., Froehlich J. L. Simple adult rabbit model for Vibrio cholerae and enterotoxigenic Escherichia coli diarrhea. Infect Immun. 1981 May;32(2):739–747. doi: 10.1128/iai.32.2.739-747.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Stroeher U. H., Bode L., Beutin L., Manning P. A. Characterization and sequence of a 33-kDa enterohemolysin (Ehly 1)-associated protein in Escherichia coli. Gene. 1993 Sep 30;132(1):89–94. doi: 10.1016/0378-1119(93)90518-8. [DOI] [PubMed] [Google Scholar]
  100. Suzuki S., Kawaguchi M., Mizuno K., Takama K., Yuki N. Immunological properties and ganglioside recognitions by Campylobacter jejuni-enterotoxin and cholera toxin. FEMS Immunol Med Microbiol. 1994 Mar;8(3):207–211. doi: 10.1111/j.1574-695X.1994.tb00444.x. [DOI] [PubMed] [Google Scholar]
  101. Tay S. T., Devi S., Puthucheary S. D., Kautner I. M. Detection of haemolytic activity of campylobacters by agarose haemolysis and microplate assay. J Med Microbiol. 1995 Mar;42(3):175–180. doi: 10.1099/00222615-42-3-175. [DOI] [PubMed] [Google Scholar]
  102. Taylor D. E., Johnson W. M., Lior H. Cytotoxic and enterotoxic activities of Campylobacter jejuni are not specified by tetracycline resistance plasmids pMAK175 and pUA466. J Clin Microbiol. 1987 Jan;25(1):150–151. doi: 10.1128/jcm.25.1.150-151.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Taylor N. S., Thorne G. M., Bartlett J. G. Comparison of two toxins produced by Clostridium difficile. Infect Immun. 1981 Dec;34(3):1036–1043. doi: 10.1128/iai.34.3.1036-1043.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Triadafilopoulos G., Pothoulakis C., O'Brien M. J., LaMont J. T. Differential effects of Clostridium difficile toxins A and B on rabbit ileum. Gastroenterology. 1987 Aug;93(2):273–279. doi: 10.1016/0016-5085(87)91014-6. [DOI] [PubMed] [Google Scholar]
  105. Wadström T., Baloda S. B., Krovacek K., Faris A., Bengtson S., Walder M. Swedish isolates of Campylobacter jejuni/coli do not produce cytotonic or cytotoxic enterotoxins. Lancet. 1983 Oct 15;2(8355):911–911. doi: 10.1016/s0140-6736(83)90893-0. [DOI] [PubMed] [Google Scholar]
  106. Walker R. I., Caldwell M. B., Lee E. C., Guerry P., Trust T. J., Ruiz-Palacios G. M. Pathophysiology of Campylobacter enteritis. Microbiol Rev. 1986 Mar;50(1):81–94. doi: 10.1128/mr.50.1.81-94.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Wassenaar T. M., Bleumink-Pluym N. M., van der Zeijst B. A. Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO J. 1991 Aug;10(8):2055–2061. doi: 10.1002/j.1460-2075.1991.tb07736.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Welch R. A. Pore-forming cytolysins of gram-negative bacteria. Mol Microbiol. 1991 Mar;5(3):521–528. doi: 10.1111/j.1365-2958.1991.tb00723.x. [DOI] [PubMed] [Google Scholar]
  109. Yamamoto K., Ichinose Y., Shinagawa H., Makino K., Nakata A., Iwanaga M., Honda T., Miwatani T. Two-step processing for activation of the cytolysin/hemolysin of Vibrio cholerae O1 biotype El Tor: nucleotide sequence of the structural gene (hlyA) and characterization of the processed products. Infect Immun. 1990 Dec;58(12):4106–4116. doi: 10.1128/iai.58.12.4106-4116.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Yeen W. P., Puthucheary S. D., Pang T. Demonstration of a cytotoxin from Campylobacter jejuni. J Clin Pathol. 1983 Nov;36(11):1237–1240. doi: 10.1136/jcp.36.11.1237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Zitzer A., Walev I., Palmer M., Bhakdi S. Characterization of Vibrio cholerae El Tor cytolysin as an oligomerizing pore-forming toxin. Med Microbiol Immunol. 1995 May;184(1):37–44. doi: 10.1007/BF00216788. [DOI] [PubMed] [Google Scholar]
  112. de Melo M. A., Pechère J. C. Identification of Campylobacter jejuni surface proteins that bind to Eucaryotic cells in vitro. Infect Immun. 1990 Jun;58(6):1749–1756. doi: 10.1128/iai.58.6.1749-1756.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Clinical Microbiology Reviews are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES