Rapid cytopathic effects of Clostridium perfringens beta-toxin on porcine endothelial cells

Infection and Immunity

Volumn 78, Issue 7, 2010, Pages 2966-2973

  Gurtner, Corinne ^a   Popescu, Francesca ^a   Wyder, Marianne ^a   Sutter, Esther ^a   Zeeh, Friederike ^a   Frey, Joachim ^a   Von Schubert, Conrad ^a   Posthaus, Horst ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM TOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DAMAGE; CELL STRUCTURE; CLOSTRIDIUM PERFRINGENS; CYTOPATHOGENIC EFFECT; CYTOTOXICITY; ENDOTHELIUM CELL; ENTERITIS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SWINE; THROMBOSIS; WESTERN BLOTTING;

ANIMALS; BACTERIAL TOXINS; BLOTTING, WESTERN; CELLS, CULTURED; CLOSTRIDIUM INFECTIONS; CLOSTRIDIUM PERFRINGENS; COLON; ENDOTHELIAL CELLS; ENTERITIS; NEUTRALIZATION TESTS; RECOMBINANT PROTEINS; STOMACH; SWINE;

EID: 77953951481     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01284-09     Document Type: Article

References (51)

1. Albini, S., I. Brodard, A. Jaussi, N. Wollschlaeger, J. Frey, R. Miserez, and C. Abril. 2008. Real-time multiplex PCR assays for reliable detection of Clostridium perfringens toxin genes in animal isolates. Vet. Microbiol. 127: 179-185.
2. Amimoto, K., T. Noro, E. Oishi, and M. Shimizu. 2007. A novel toxin homologous to large clostridial cytotoxins found in culture supernatant of Clostridium perfringens type C. Microbiology 153:1198-1206. (Pubitemid 46605818)
3. Awad, M. M., D. M. Ellemor, R. L. Boyd, J. J. Emmins, and J. I. Rood. 2001. Synergistic effects of alpha-toxin and perfringolysin O in Clostridium perfringens- mediated gas gangrene. Infect. Immun. 69:7904-7910.
4. Bouis, D., G. A. Hospers, C. Meijer, G. Molema, and N. H. Mulder. 2001. Endothelium in vitro: a review of human vascular endothelial cell lines for blood vessel-related research. Angiogenesis 4:91-102. (Pubitemid 34032695)
5. Bryant, A. E. 2003. Biology and pathogenesis of thrombosis and procoagulant activity in invasive infections caused by group A streptococci and Clostridium perfringens. Clin. Microbiol. Rev. 16:451-462.
6. Cooke, R. 1979. The pathology of pig bel. P. N. G. Med. J. 22:35-38.
7. Eason, R. J., and R. van Rij. 1984. Pigless pigbel: enteritis necroticans in the Solomon Islands. P. N. G. Med. J. 27:42-44.
8. Fisher, D. J., M. E. Fernandez-Miyakawa, S. Sayeed, R. Poon, V. Adams, J. I. Rood, F. A. Uzal, and B. A. McClane. 2006. Dissecting the contributions of Clostridium perfringens type C toxins to lethality in the mouse intravenous injection model. Infect. Immun. 74:5200-5210.
9. Geny, B., and M. R. Popoff. 2006. Bacterial protein toxins and lipids: pore formation or toxin entry into cells. Biol. Cell 98:667-678. (Pubitemid 44697058)
10. Gibert, M., C. Jolivet-Reynaud, and M. R. Popoff. 1997. Beta2 toxin, a novel toxin produced by Clostridium perfringens. Gene 203:65-73. (Pubitemid 27520654)
11. Hickey, M. J., R. Y. Kwan, M. M. Awad, C. L. Kennedy, L. F. Young, P. Hall, L. M. Cordner, D. Lyras, J. J. Emmins, and J. I. Rood. 2008. Molecular and cellular basis of microvascular perfusion deficits induced by Clostridium perfringens and Clostridium septicum. PLoS Pathog. 4:e1000045.
12. Hogh, P. 1969. Necrotizing infectious enteritis in piglets, caused by Clostridium perfringens type C. 3. Pathological changes. Acta Vet. Scand. 10:57-83.
13. Jacewicz, M. S., D. W. Acheson, D. G. Binion, G. A. West, L. L. Lincicome, C. Fiocchi, and G. T. Keusch. 1999. Responses of human intestinal microvascular endothelial cells to Shiga toxins 1 and 2 and pathogenesis of hemorrhagic colitis. Infect. Immun. 67:1439-1444.
14. Jaggi, M., N. Wollschlager, C. Abril, S. Albini, C. Brachelente, M. Wyder, and H. Posthaus. 2009. Retrospective study on necrotizing enteritis in piglets in Switzerland. Schweiz. Arch. Tierheilkd. 151:369-375.
15. Johannsen, U., S. Menger, W. Erwerth, and B. Kohler. 1986. Clostridium perfringens type C enterotoxemia (necrotizing enteritis) in suckling pigs. 2. Light and electron microscopic studies of the pathology and pathogenesis of experimental Clostridium perfringens type C toxin poisoning. Arch. Exp. Veterinaermed. 40:881-894.
16. Johannsen, U., S. Menger, W. Erwerth, and B. Kohler. 1986. Clostridium perfringens type C enterotoxemia (necrotizing enteritis) of suckling pigs. 3. Light and electron microscopic studies of the pathology and pathogenesis of experimental Clostridium perfringens type C infection. Arch. Exp. Veterinaermed. 40:895-909.
17. Johnson, S., P. Echeverria, D. N. Taylor, S. R. Paul, R. Coninx, J. Sakurai, B. Eampokalap, P. Jimakorn, R. A. Cooke, G. W. Lawrence, et al. 1987. Enteritis necroticans among Khmer children at an evacuation site in Thailand. Lancet ii:496-500.
18. Johnson, S., and D. N. Gerding. 1997. Enterotoxemic infections, p. 117-140. In J. I. Rood, B. A. McClaine, J. G. Songer, and R. W. Titball (ed.), The clostridia: molecular biology and pathogenesis. Academic Press, San Diego, CA.
19. Keyburn, A. L., J. D. Boyce, P. Vaz, T. L. Bannam, M. E. Ford, D. Parker, A. Di Rubbo, J. I. Rood, and R. J. Moore. 2008. NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathog. 4:e26.
20. Kreft, B., K. Dalhoff, and K. Sack. 2000. Necrotizing enterocolitis: a historical and current review. Med. Klin. 95:435-441.
21. Lawrence, G. 1979. The pathogenesis of pig-bel in Papua New Guinea. P. N. G. Med. J. 22:39-49.
22. Lawrence, G. 2005. The pathogenesis of pig-bel in Papua New Guinea. 1979. P. N. G. Med. J. 48:39-49.
23. Lawrence, G., and P. D. Walker. 1976. Pathogenesis of enteritis necroticans in Papua New Guinea. Lancet i:125-126.
24. Lawrence, G. W., D. Lehmann, G. Anian, C. A. Coakley, G. Saleu, M. J. Barker, and M. W. Davis. 1990. Impact of active immunisation against enteritis necroticans in Papua New Guinea. Lancet 336:1165-1167.
25. Li, D. Y., A. O. Scheimann, J. G. Songer, R. E. Person, M. Horwitz, L. Resar, and K. B. Schwarz. 2004. Enteritis necroticans with recurrent enterocutaneous fistulae caused by Clostridium perfringens in a child with cyclic neutropenia. J. Pediatr. Gastroenterol. Nutr. 38:213-215.
26. Mandrella, B. 2007. A recent outbreak of necrotizing enteritis in eastern Sri Lanka. Trop. Dr. 37:52-54.
27. Matsuda, T., Y. Okada, E. Inagi, Y. Tanabe, Y. Shimizu, K. Nagashima, J. Sakurai, M. Nagahama, and S. Tanaka. 2007. Enteritis necroticans 'pigbel' in a Japanese diabetic adult. Pathol. Int. 57:622-626.
28. Miclard, J., M. Jaggi, E. Sutter, M. Wyder, B. Grabscheid, and H. Posthaus. 2009. Clostridium perfringens beta-toxin targets endothelial cells in necrotizing enteritis in piglets. Vet. Microbiol. 137:320-325.
29. Miclard, J., J. van Baarlen, M. Wyder, B. Grabscheid, and H. Posthaus. 2009. Clostridium perfringens beta-toxin binding to vascular endothelial cells in a human case of enteritis necroticans. J. Med. Microbiol. 58:826-828.
30. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63. (Pubitemid 14203433)
31. Nagahama, M., S. Hayashi, S. Morimitsu, and J. Sakurai. 2003. Biological activities and pore formation of Clostridium perfringens beta toxin in HL 60 cells. J. Biol. Chem. 278:36934-36941.
32. Obrig, T. G., C. B. Louise, C. A. Lingwood, B. Boyd, L. Barley-Maloney, and T. O. Daniel. 1993. Endothelial heterogeneity in Shiga toxin receptors and responses. J. Biol. Chem. 268:15484-15488.
33. Petit, L., M. Gibert, A. Gourch, M. Bens, A. Vandewalle, and M. R. Popoff. 2003. Clostridium perfringens epsilon toxin rapidly decreases membrane barrier permeability of polarized MDCK cells. Cell. Microbiol. 5:155-164.
34. Petit, L., M. Gibert, and M. R. Popoff. 1999. Clostridium perfringens: toxinotype and genotype. Trends Microbiol. 7:104-110.
35. Ribatti, D., B. Nico, A. Vacca, L. Roncali, and F. Dammacco. 2002. Endothelial cell heterogeneity and organ specificity. J. Hematother. Stem Cell Res. 11:81-90.
36. Rood, J. I. 1998. Virulence genes of Clostridium perfringens. Annu. Rev. Microbiol. 52:333-360.
37. Rood, J. I., B. A. McClaine, J. G. Songer, and R. W. Titball (ed.). 1997. The clostridia: molecular biology and pathogenesis. Academic Press, San Diego, CA.
38. Sayeed, S., F. A. Uzal, D. J. Fisher, J. Saputo, J. E. Vidal, Y. Chen, P. Gupta, J. I. Rood, and B. A. McClane. 2008. Beta toxin is essential for the intestinal virulence of Clostridium perfringens type C disease isolate CN3685 in a rabbit ileal loop model. Mol. Microbiol. 67:15-30.
39. Severin, W. P., A. A. de la Fuente, and M. F. Stringer. 1984. Clostridium perfringens type C causing necrotising enteritis. J. Clin. Pathol. 37:942-944.
40. Shatursky, O., R. Bayles, M. Rogers, B. H. Jost, J. G. Songer, and R. K. Tweten. 2000. Clostridium perfringens beta-toxin forms potential-dependent, cation-selective channels in lipid bilayers. Infect. Immun. 68:5546-5551.
41. Songer, J. G. 2010. Clostridia as agents of zoonotic disease. Vet. Microbiol. 140:399-404.
42. Songer, J. G. 1996. Clostridial enteric diseases of domestic animals. Clin. Microbiol. Rev. 9:216-234.
43. Songer, J. G., and F. A. Uzal. 2005. Clostridial enteric infections in pigs. J. Vet. Diagn. Invest. 17:528-536.
44. Steinthorsdottir, V., H. Halldorsson, and O. S. Andresson. 2000. Clostridium perfringens beta-toxin forms multimeric transmembrane pores in human endothelial cells. Microb. Pathog. 28:45-50.
45. Stevens, D. L. 1997. Necrotizing clostridial soft tissue infections, p. 141-151. In J. I. Rood, B. A. McClaine, J. G. Songer, and R. W. Titball (ed.), The clostridia: molecular biology and pathogenesis. Academic Press, San Diego, CA.
46. Tsai, S. H., Y. W. Liu, W. C. Tang, Z. W. Zhou, C. Y. Hwang, G. Y. Hwang, B. R. Ou, C. P. Hu, V. C. Yang, and J. K. Chen. 2007. Characterization of porcine arterial endothelial cells cultured on amniotic membrane, a potential matrix for vascular tissue engineering. Biochem. Biophys. Res. Commun. 357:984-990.
47. Uzal, F. A., J. Saputo, S. Sayeed, J. E. Vidal, D. J. Fisher, R. Poon, V. Adams, M. E. Fernandez-Miyakawa, J. I. Rood, and B. A. McClane. 2009. Development and application of new mouse models to study the pathogenesis of Clostridium perfringens type C enterotoxemias. Infect. Immun. 77:5291-5299.
48. van Hinsbergh, V. W. 2001. The endothelium: vascular control of haemostasis. Eur. J. Obstet. Gynecol. Reprod. Biol. 95:198-201.
49. Vidal, J. E., B. A. McClane, J. Saputo, J. Parker, and F. A. Uzal. 2008. Effects of Clostridium perfringens beta-toxin on the rabbit small intestine and colon. Infect. Immun. 76:4396-4404.
50. Vidal, J. E., K. Ohtani, T. Shimizu, and B. A. McClane. 2009. Contact with enterocyte-like Caco-2 cells induces rapid upregulation of toxin production by Clostridium perfringens type C isolates. Cell. Microbiol. 11:1306-1328.
51. Watson, D. A., J. H. Andrew, S. Banting, J. R. Mackay, R. G. Stillwell, and M. Merrett. 1991. Pig-bel but no pig: enteritis necroticans acquired in Australia. Med. J. Aust. 155:47-50.