Logo of cmrPermissionsJournals.ASM.orgJournalCMR ArticleJournal InfoAuthorsReviewers
Clin Microbiol Rev. Jul 1997; 10(3): 466–476.
PMCID: PMC172930

Toxin production by Campylobacter spp.


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 (229K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aguero-Rosenfeld ME, Yang XH, Nachamkin I. Infection of adult Syrian hamsters with flagellar variants of Campylobacter jejuni. Infect Immun. 1990 Jul;58(7):2214–2219. [PMC free article] [PubMed]
  • Akhtar SQ, Huq F. Effect of Campylobacter jejuni extracts and culture supernatants on cell culture. J Trop Med Hyg. 1989 Apr;92(2):80–85. [PubMed]
  • Arimi SM, Park RW, Fricker CR. Study of haemolytic activity of some Campylobacter spp. on blood agar plates. J Appl Bacteriol. 1990 Sep;69(3):384–389. [PubMed]
  • Bag PK, Ramamurthy T, Nair UB. 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. [PubMed]
  • Baig BH, Wachsmuth IK, Morris GK, Hill WE. Probing of Campylobacter jejuni with DNA coding for Escherichia coli heat-labile enterotoxin. J Infect Dis. 1986 Sep;154(3):542–542. [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Beutin L, Stroeher UH, Manning PA. Isolation of enterohemolysin (Ehly2)-associated sequences encoded on temperate phages of Escherichia coli. Gene. 1993 Sep 30;132(1):95–99. [PubMed]
  • Beutin L. The different hemolysins of Escherichia coli. Med Microbiol Immunol. 1991;180(4):167–182. [PubMed]
  • 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. [PubMed]
  • 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. [PubMed]
  • Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ. Experimental Campylobacter jejuni infection in humans. J Infect Dis. 1988 Mar;157(3):472–479. [PubMed]
  • Blaser MJ, Reller LB. Campylobacter enteritis. N Engl J Med. 1981 Dec 10;305(24):1444–1452. [PubMed]
  • Bok HE, Greeff AS, Crewe-Brown HH. Incidence of toxigenic Campylobacter strains in South Africa. J Clin Microbiol. 1991 Jun;29(6):1262–1264. [PMC free article] [PubMed]
  • Braun V, Focareta T. Pore-forming bacterial protein hemolysins (cytolysins). Crit Rev Microbiol. 1991;18(2):115–158. [PubMed]
  • Calva E, Torres J, Vázquez M, Angeles V, de la Vega H, Ruíz-Palacios GM. Campylobacter jejuni chromosomal sequences that hybridize to Vibrio cholerae and Escherichia coli LT enterotoxin genes. Gene. 1989 Feb 20;75(2):243–251. [PubMed]
  • 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. [PubMed]
  • Coote JG, Arain T. A rapid, colourimetric assay for cytotoxin activity in Campylobacter jejuni. FEMS Immunol Med Microbiol. 1996 Jan;13(1):65–70. [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • De Melo MA, Gabbiani G, Pechère JC. Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect Immun. 1989 Jul;57(7):2214–2222. [PMC free article] [PubMed]
  • de Melo MA, Pechère JC. Identification of Campylobacter jejuni surface proteins that bind to Eucaryotic cells in vitro. Infect Immun. 1990 Jun;58(6):1749–1756. [PMC free article] [PubMed]
  • Dillon ST, Rubin EJ, Yakubovich M, Pothoulakis C, LaMont JT, Feig LA, Gilbert RJ. 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. [PMC free article] [PubMed]
  • Dolg P, Yao R, Burr DH, Guerry P, Trust TJ. An environmentally regulated pilus-like appendage involved in Campylobacter pathogenesis. Mol Microbiol. 1996 May;20(4):885–894. [PubMed]
  • 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. [PubMed]
  • Everest PH, Goossens H, Butzler JP, Lloyd D, Knutton S, Ketley JM, Williams PH. 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. [PubMed]
  • Everest PH, Cole AT, Hawkey CJ, Knutton S, Goossens H, Butzler JP, Ketley JM, Williams PH. Roles of leukotriene B4, prostaglandin E2, and cyclic AMP in Campylobacter jejuni-induced intestinal fluid secretion. Infect Immun. 1993 Nov;61(11):4885–4887. [PMC free article] [PubMed]
  • Everest PH, Goossens H, Sibbons P, Lloyd DR, Knutton S, Leece R, Ketley JM, Williams PH. Pathological changes in the rabbit ileal loop model caused by Campylobacter jejuni from human colitis. J Med Microbiol. 1993 May;38(5):316–321. [PubMed]
  • Fauchère JL, 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. [PubMed]
  • Fernández H, Neto UF, Fernandes F, de Almeida Pedra M, Trabulsi LR. Culture supernatants of Campylobacter jejuni induce a secretory response in jejunal segments of adult rats. Infect Immun. 1983 Apr;40(1):429–431. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Gillespie MJ, Smutko J, Haraszthy GG, Zambon JJ. Isolation and partial characterization of the Campylobacter rectus cytotoxin. Microb Pathog. 1993 Mar;14(3):203–215. [PubMed]
  • Goossens H, Rummens E, Cadranel S, Butzler JP, Takeda Y. Cytotoxic activity on Chinese hamster ovary cells in culture filtrates of Campylobacter jejuni/coli. Lancet. 1985 Aug 31;2(8453):511–511. [PubMed]
  • Grant CC, Konkel ME, Cieplak W, Jr, Tompkins LS. 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. [PMC free article] [PubMed]
  • Guerrant RL, Wanke CA, Pennie RA, Barrett LJ, Lima AA, O'Brien AD. Production of a unique cytotoxin by Campylobacter jejuni. Infect Immun. 1987 Oct;55(10):2526–2530. [PMC free article] [PubMed]
  • Guerry P, Yao R, Alm RA, Burr DH, Trust TJ. Systems of experimental genetics for Campylobacter species. Methods Enzymol. 1994;235:474–481. [PubMed]
  • Hossain A, Stewart-Tull DE, Freer JH. Heat-labile and heat-stable haemolysins of Campylobacter jejuni. FEMS Immunol Med Microbiol. 1993 Apr;6(4):331–339. [PubMed]
  • Ichinose Y, Yamamoto K, Nakasone N, Tanabe MJ, 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. [PMC free article] [PubMed]
  • Johnson WM, Lior H. Toxins produced by Campylobacter jejuni and Campylobacter coli. Lancet. 1984 Jan 28;1(8370):229–230. [PubMed]
  • Johnson WM, Lior H. Cytotoxic and cytotonic factors produced by Campylobacter jejuni, Campylobacter coli, and Campylobacter laridis. J Clin Microbiol. 1986 Aug;24(2):275–281. [PMC free article] [PubMed]
  • Johnson WM, Lior H. A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. Microb Pathog. 1988 Feb;4(2):115–126. [PubMed]
  • 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. [PubMed]
  • Kanwar RK, Ganguly NK, Kanwar JR, Kumar L, Walia BN. 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. [PubMed]
  • Kaur R, Ganguly NK, Kumar L, Walia BN. 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. [PubMed]
  • Ketley JM. The 16th C. L. Oakley Lecture. Virulence of Campylobacter species: a molecular genetic approach. J Med Microbiol. 1995 May;42(5):312–327. [PubMed]
  • Khalil K, Lindblom GB, 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]
  • 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. [PubMed]
  • 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. [PubMed]
  • Klipstein FA, Engert RF. Properties of crude Campylobacter jejuni heat-labile enterotoxin. Infect Immun. 1984 Aug;45(2):314–319. [PMC free article] [PubMed]
  • Klipstein FA, Engert RF. Purification of Campylobacter jejuni enterotoxin. Lancet. 1984 May 19;1(8386):1123–1124. [PubMed]
  • Klipstein FA, Engert RF. Immunological relationship of the B subunits of Campylobacter jejuni and Escherichia coli heat-labile enterotoxins. Infect Immun. 1985 Jun;48(3):629–633. [PMC free article] [PubMed]
  • Klipstein FA, Engert RF, Short H, Schenk EA. Pathogenic properties of Campylobacter jejuni: assay and correlation with clinical manifestations. Infect Immun. 1985 Oct;50(1):43–49. [PMC free article] [PubMed]
  • Klipstein FA, Engert RF, Short HB. Enzyme-linked immunosorbent assays for virulence properties of Campylobacter jejuni clinical isolates. J Clin Microbiol. 1986 Jun;23(6):1039–1043. [PMC free article] [PubMed]
  • Konkel ME, Corwin MD, Joens LA, Cieplak W. Factors that influence the interaction of Campylobacter jejuni with cultured mammalian cells. J Med Microbiol. 1992 Jul;37(1):30–37. [PubMed]
  • Konkel ME, Hayes SF, Joens LA, 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. [PubMed]
  • Konkel ME, Joens LA. Adhesion to and invasion of HEp-2 cells by Campylobacter spp. Infect Immun. 1989 Oct;57(10):2984–2990. [PMC free article] [PubMed]
  • Lindblom GB, Cervantes LE, Sjögren E, Kaijser B, Ruiz-Palacios GM. 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]
  • Lindblom GB, Johny M, Khalil K, Mazhar K, Ruiz-Palacios GM, 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. [PubMed]
  • Lindblom GB, 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. [PMC free article] [PubMed]
  • Lyerly DM, Krivan HC, Wilkins TD. Clostridium difficile: its disease and toxins. Clin Microbiol Rev. 1988 Jan;1(1):1–18. [PMC free article] [PubMed]
  • Mahajan S, Rodgers FG. Isolation, characterization, and host-cell-binding properties of a cytotoxin from Campylobacter jejuni. J Clin Microbiol. 1990 Jun;28(6):1314–1320. [PMC free article] [PubMed]
  • Martin PM, Mathiot J, Ipero J, Georges AJ, Georges-Courbot MC. Antibody response to Campylobacter coli in children during intestinal infection and carriage. J Clin Microbiol. 1988 Jul;26(7):1421–1424. [PMC free article] [PubMed]
  • Martin PM, Mathiot J, Ipero J, Kirimat M, Georges AJ, Georges-Courbot MC. 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. [PMC free article] [PubMed]
  • Mathan VI, Rajan DP, Klipstein FA, Engert RF. Enterotoxigenic Campylobacter jejuni among children in South India. Lancet. 1984 Oct 27;2(8409):981–981. [PubMed]
  • McCardell BA, Madden JM, Lee EC. Production of cholera-like toxin by Campylobacter jejuni/coli. Lancet. 1984 Feb 25;1(8374):448–449. [PubMed]
  • McCardell BA, Madden JM, Stanfield JT. Effect of iron concentration on toxin production in Campylobacter jejuni and Campylobacter coli. Can J Microbiol. 1986 May;32(5):395–401. [PubMed]
  • McCardell BA, Madden JM, Stanfield JT. Production of cytotoxins by Campylobacter. Lancet. 1986 May 3;1(8488):1031–1031. [PubMed]
  • McFarland BA, Neill SD. Profiles of toxin production by thermophilic Campylobacter of animal origin. Vet Microbiol. 1992 Feb;30(2-3):257–266. [PubMed]
  • McSweegan E, Walker RI. Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect Immun. 1986 Jul;53(1):141–148. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • 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. [PubMed]
  • Mizuno K, Takama K, Suzuki S. Characteristics of cytotoxin produced by Campylobacter jejuni strains. Microbios. 1994;78(317):215–228. [PubMed]
  • Moore MA, Blaser MJ, Perez-Perez GI, O'Brien AD. Production of a Shiga-like cytotoxin by Campylobacter. Microb Pathog. 1988 Jun;4(6):455–462. [PubMed]
  • Morooka T, Umeda A, Amako K. Motility as an intestinal colonization factor for Campylobacter jejuni. J Gen Microbiol. 1985 Aug;131(8):1973–1980. [PubMed]
  • Morris GK, Merson MH, Sack DA, Wells JG, Martin WT, Dewitt WE, Feeley JC, Sack RB, Bessudo DM. 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. [PMC free article] [PubMed]
  • Newell DG, McBride H, Dolby JM. 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. [PMC free article] [PubMed]
  • Nishibuchi M, Fasano A, Russell RG, Kaper JB. Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect Immun. 1992 Sep;60(9):3539–3545. [PMC free article] [PubMed]
  • Obrig TG. Toxins that inhibit host protein synthesis. Methods Enzymol. 1994;235:647–656. [PubMed]
  • 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. [PubMed]
  • Olsnes S, Reisbig R, Eiklid K. Subunit structure of Shigella cytotoxin. J Biol Chem. 1981 Aug 25;256(16):8732–8738. [PubMed]
  • Olsvik O, Wachsmuth K, Morris G, Feeley JC. Genetic probing of Campylobacter jejuni for cholera toxin and Escherichia coli heat-labile enterotoxin. Lancet. 1984 Feb 25;1(8374):449–449. [PubMed]
  • Pang T, Wong PY, Puthucheary SD, Sihotang K, Chang WK. In-vitro and in-vivo studies of a cytotoxin from Campylobacter jejuni. J Med Microbiol. 1987 May;23(3):193–198. [PubMed]
  • Park SF, Richardson PT. Molecular characterization of a Campylobacter jejuni lipoprotein with homology to periplasmic siderophore-binding proteins. J Bacteriol. 1995 May;177(9):2259–2264. [PMC free article] [PubMed]
  • Perez-Perez GI, Cohn DL, Guerrant RL, Patton CM, Reller LB, Blaser MJ. 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. [PubMed]
  • Pickett CL, Auffenberg T, Pesci EC, Sheen VL, Jusuf SS. Iron acquisition and hemolysin production by Campylobacter jejuni. Infect Immun. 1992 Sep;60(9):3872–3877. [PMC free article] [PubMed]
  • Pickett CL, Cottle DL, Pesci EC, Bikah G. Cloning, sequencing, and expression of the Escherichia coli cytolethal distending toxin genes. Infect Immun. 1994 Mar;62(3):1046–1051. [PMC free article] [PubMed]
  • Pickett CL, Pesci EC, Cottle DL, Russell G, Erdem AN, 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. [PMC free article] [PubMed]
  • Raimondi F, Kao JP, Kaper JB, 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. [PubMed]
  • 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]
  • Rowe GE, Welch RA. Assays of hemolytic toxins. Methods Enzymol. 1994;235:657–667. [PubMed]
  • Ruiz-Palacios GM, 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. [PubMed]
  • Ruiz-Palacios GM, Torres J, Torres NI, Escamilla E, Ruiz-Palacios BR, Tamayo J. Cholera-like enterotoxin produced by Campylobacter jejuni. Characterisation and clinical significance. Lancet. 1983 Jul 30;2(8344):250–253. [PubMed]
  • Saha SK, Saha S, Sanyal SC. Recovery of injured Campylobacter jejuni cells after animal passage. Appl Environ Microbiol. 1991 Nov;57(11):3388–3389. [PMC free article] [PubMed]
  • Saha SK, Singh NP, Sanyal SC. Enterotoxigenicity of chicken isolates of Campylobacter jejuni in ligated ileal loops of rats. J Med Microbiol. 1988 Jun;26(2):87–91. [PubMed]
  • Scott DA, Kaper JB. Cloning and sequencing of the genes encoding Escherichia coli cytolethal distending toxin. Infect Immun. 1994 Jan;62(1):244–251. [PMC free article] [PubMed]
  • Sears CL, Kaper JB. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol Rev. 1996 Mar;60(1):167–215. [PMC free article] [PubMed]
  • Spangler BD. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev. 1992 Dec;56(4):622–647. [PMC free article] [PubMed]
  • Spira WM, Sack RB, Froehlich JL. Simple adult rabbit model for Vibrio cholerae and enterotoxigenic Escherichia coli diarrhea. Infect Immun. 1981 May;32(2):739–747. [PMC free article] [PubMed]
  • Stroeher UH, Bode L, Beutin L, Manning PA. Characterization and sequence of a 33-kDa enterohemolysin (Ehly 1)-associated protein in Escherichia coli. Gene. 1993 Sep 30;132(1):89–94. [PubMed]
  • 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. [PubMed]
  • Tay ST, Devi S, Puthucheary SD, Kautner IM. Detection of haemolytic activity of campylobacters by agarose haemolysis and microplate assay. J Med Microbiol. 1995 Mar;42(3):175–180. [PubMed]
  • Taylor DE, Johnson WM, 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. [PMC free article] [PubMed]
  • Taylor NS, Thorne GM, Bartlett JG. Comparison of two toxins produced by Clostridium difficile. Infect Immun. 1981 Dec;34(3):1036–1043. [PMC free article] [PubMed]
  • Triadafilopoulos G, Pothoulakis C, O'Brien MJ, LaMont JT. Differential effects of Clostridium difficile toxins A and B on rabbit ileum. Gastroenterology. 1987 Aug;93(2):273–279. [PubMed]
  • Wadström T, Baloda SB, 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. [PubMed]
  • Walker RI, Caldwell MB, Lee EC, Guerry P, Trust TJ, Ruiz-Palacios GM. Pathophysiology of Campylobacter enteritis. Microbiol Rev. 1986 Mar;50(1):81–94. [PMC free article] [PubMed]
  • Wassenaar TM, Bleumink-Pluym NM, van der Zeijst BA. 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. [PMC free article] [PubMed]
  • Welch RA. Pore-forming cytolysins of gram-negative bacteria. Mol Microbiol. 1991 Mar;5(3):521–528. [PubMed]
  • Yeen WP, Puthucheary SD, Pang T. Demonstration of a cytotoxin from Campylobacter jejuni. J Clin Pathol. 1983 Nov;36(11):1237–1240. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PubMed]

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


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...