Beta toxin is essential for the intestinal virulence of Clostridium perfringens type C disease isolate CN3685 in a rabbit ileal loop model

Molecular Microbiology

Volumn 67, Issue 1, 2008, Pages 15-30

  Sayeed, Sameera ^a   Uzal, Francisco A ^b   Fisher, Derek J ^a,e   Saputo, Juliann ^b   Vidal, Jorge E ^a   Chen, Yue ^c   Gupta, Phalguni ^c   Rood, Julian I ^d   McClane, Bruce A ^a,d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^d MONASH UNIVERSITY   (Australia)

^e UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; BETA TOXIN; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM ISOLATE; CLOSTRIDIUM; CLOSTRIDIUM PERFRINGENS TYPE C; CONTROLLED STUDY; NECROTIZING ENTERITIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RABBIT; WILD TYPE;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; ANTITOXINS; BACTERIAL TOXINS; CALCIUM-BINDING PROTEINS; CLOSTRIDIUM INFECTIONS; CLOSTRIDIUM PERFRINGENS; DISEASE MODELS, ANIMAL; FEMALE; GENOTYPE; HEMOLYSIN PROTEINS; HUMANS; ILEAL DISEASES; ILEUM; MALE; MUTAGENESIS, INSERTIONAL; PHENOTYPE; RABBITS; SHEEP DISEASES; TYPE C PHOSPHOLIPASES; VIRULENCE FACTORS;

ANIMALIA; CLOSTRIDIUM PERFRINGENS; ORYCTOLAGUS CUNICULUS;

EID: 36849034460     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.06007.x     Document Type: Article

References (37)

1. Allen, S.D. Baron, E.J. (1991) Clostridium. In Manual of Clinical Microbiology. Balows, A., Hausler, W.J., Jr., Herrmann, K.L., Isenberg, H.D. Shadomy, H.J. (eds). Washington, DC : American Society of Microbiology, pp. 505 521.
2. Amimoto, K., Noro, T., Oishi, E. Shimuzu, M. (2007) A novel toxin homologous to large clostridial cytotoxins found in culture supernatant of Clostridium perfringens type C. Microbiology 153 : 1198 1206.
3. Awad, M.M., Bryant, A.E., Stevens, D.L. Rood, J.I. (1995) Virulence studies on chromosomal alpha-toxin and theta toxin mutants constructed by allelic exchange provide genetic evidence for the essential role of alpha-toxin in Clostridium perfringens-mediated gas gangrene. Mol Microbiol 15 : 191 202.
4. Awad, M.M., Ellemor, D.M., Boyd, R.L., Emmins, J.J. Rood, J.I. (2001) Synergistic effects of alpha-toxin and perfringolysin O in Clostridium perfringens-mediated gas gangrene. Infect Immun 69 : 7904 7910.
5. Bannum, T.L. Rood, J.I. (1993) Clostridium perfringens-Escherichia coli shuttle vectors that carry single antibiotic resistance determinants. Plasmid 29 : 233 235.
6. Bergeland, M.E. (1972) Pathogenesis and immunity of Clostridium perfringens type C enteritis in swine. J Am Vet Med Assoc 160 : 568 571.
7. Chen, Y., McClane, B.A., Fisher, D.J., Rood, J.I. Gupta, P. (2005) Construction of an alpha toxin gene knockout mutant of Clostridium perfringens type A by use of a mobile group II intron. Appl Environ Microbiol 71 : 7542 7547.
8. Chen, Y., Caruso, L., McClane, B.A., Fisher, D.J. Gupta, P. (2007) Disruption of a toxin gene by introduction of a foreign gene into the chromosome of Clostridium perfringens using targetron-induced mutagenesis. Plasmid 58 : 182 189.
9. Fisher, D.J., Fernandez Miyakawa, M.F., Sayeed, S., Poon, R., Adams, V., Rood, J.I., et al. (2006) Dissecting the contributions of Clostridium perfringens Type C toxins to lethality in the mouse intravenous injection model. Infect Immun 74 : 5200 5210.
10. Gibert, M., Jolivet-Renaud C. Popoff M.R. (1997) Beta2 toxin, a novel toxin produced by Clostridium perfringens. Gene 203 : 65 73.
11. Ginter, A., Williamson, E.D., Dessy, F., Coppe, P., Bullifent, H., Howells, A. Titball, R.W. (1996) Molecular variation between the alpha-toxins from the type strain (NCTC 8237) and clinical isolates of Clostridium perfringens associated with disease in man and animals. Microbiology 42 : 191 198.
12. Gui, L., Subramony, C., Fratkin, J. Hughson, M.D. (2002) Fatal enteritis necroticans (Pigbel) in a diabetic adult. Mod Pathol 15 : 66 70.
13. Hall, T.A. (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41 : 95 98.
14. Heap, J.T., Pennington, O.J., Cartman, S.T., Carter, G.P. Minton, N.P. (2007) The ClosTron: a universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70 : 452 464.
15. Hughes, M.L., Poon, R., Adams, V., Sayeed, S., Saputo, J., Uzal, F.A., et al. (2007) Epsilon toxin plasmids of Clostridium perfringens are conjugative. J Bacteriol 189 : 7531 7538.
16. Hunter, S.E., Brown, J.E., Oyston, P.C., Sakurai, J. Titball, R.W. (1993) Molecular genetic analysis of beta-toxin of Clostridium perfringens reveals sequence homology with alpha-toxin, gamma-toxin, and leukocidin of Staphylococcus aureus. Infect Immun 61 : 3958 3965.
17. Johnson, S. Gerding, D.N. (1997) Enterotoxemic infections. In The Clostridia. Molecular Biology and Pathogenesis. Rood, J.I., McClane, B.A., Songer, J.G. Titball, R.W. (eds). London : Academic press, pp. 117 140.
18. Keyburn, A.L., Sheedy, S.A., Ford, M.E., Williamson, M.M., Awad, M.M., Rood, J.I. Moore, R.J. (2006) Alpha-toxin of Clostridium perfringens is not an essential virulence factor in necrotic enteritis in chickens. Infect Immun 74 : 6496 6500.
19. Kulkarni, R.R., Parreria, V.R., Sharif, S. Prescott, J.F. (2007) Immunization of broiler chickens against Clostridium perfringens-induced necrotic enteritis. Clin Vaccine Immunol 9 : 1070 1077.
20. Lawrence, G.W. (1997) The pathogenesis of enteritis necroticans. In The Clostridia. Molecular Biology and Pathogenesis. Rood, J.I., McClane, B.A., Songer, J.G. Titball, R.W. (eds). London : Academic press, pp. 197 207.
21. Lee, H., Bueschel, D.M. Nesheim, S.R. (2000) Enteritis necroticans (Pigbel) in a diabetic child. N Engl J Med 342 : 1250 1253.
22. Lowry, O.H., Rosebrough, N.J., Farr, A.L. Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193 : 265 275.
23. Lyras, D. Rood, J.I. (2006) Clostridial genetics. In Gram-Positive Pathogens. Fischetti, V.A., Novick, R.P., Ferretti, J.J., Portnoy, D.A. Rood, J.I. (eds). Washington, DC : American Society for Microbiology Press, pp. 672 687.
24. McClane, B.A., Uzal, F.A., Miyakawa, M.F., Lyerly, D. Wilkins, T. (2004) The enterotoxic clostridia. In The Prokaryotes. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. Stackebrandt, E. (eds). New York : Springer New York, pp. 698 752.
25. Matsuda, T., Okada, Y., Tanabe, Y., Shimizu, Y., Nagashima, K., Sakurai, J., et al. (2007) Enteritis necroticans 'pigbel' in a Japanese diabetic adult. Pathol Int 57 : 622 626.
26. Matsuura, M., Saldanha, R., Ma, H., Wank, H., Yang, J., Mohr, G., et al. (1997) A bacterial group II intron encoding reverse transcriptase, maturase, and DNA endonuclease activities: biochemical demonstration of maturase activity and insertion of new genetic information within the intron. Genes Dev 11 : 2910 2924.
27. Miyamoto, K., Fisher, D.J., Li, J., Sayeed, S., Akimoto, S. McClane, B.A. (2006) Complete sequencing and diversity analysis of the enterotoxin-encoding plasmids in Clostridium perfringens Type A non-food-borne human gastrointestinal disease isolates. J Bacteriol 188 : 1585 1598.
28. Sarker, M.R., Carman, R.J. McClane, B.A. (1999) Inactivation of the gene (cpe) encoding Clostridium perfringens enterotoxin eliminates the ability of two-cpe-positive C. perfringens type A human gastrointestinal disease isolates to affect rabbit ileal loops. Mol Microbiol 33 : 946 958.
29. Smedley, J.G., 3rd, Fisher, D.J., Sayeed, S., Chakrabarti, G. McClane, B.A. (2004) The enteric toxins of Clostridium perfringens. Rev Physiol Biochem Pharmacol 152 : 183 204.
30. Sobel, J., Mixter, C.G., Kolhe, P., Gupta, A., Guarner, J., Zaki, S., et al. (2005) Necrotizing enterocolitis associated with Clostridium perfringens type A in previously healthy North American adults. J Am Coll Surg 201 : 48 56.
31. Songer, J.G. (1996) Clostridial enteric diseases of domestic animals. Clin Microbiol Rev 9 : 216 234.
32. Songer, J.G. (1997) Bacterial phospholipases and their role in virulence. Trends Microbiol 5 : 156 161.
33. Steinthorsdottir, V., Fridriksdottir, V., Gunnarsson, E. Andresson, O.S. (1998) Site-directed mutagenesis of Clostridium perfringens beta-toxin: expression of wild-type and mutant toxins in Bacillus subtilis. FEMS Microbiol Lett 158 : 17 23.
34. Titball, R.W. (1998) Bacterial phospholipases. Symp Ser Soc Appl Microbiol 27 : 127S 137S.
35. Tweten, R.K. (2001) Clostridium perfringens beta-toxin and Clostridium septicum alpha toxin: their mechanisms and possible role in pathogenesis. Vet Microbiol 82 : 1 9.
36. Wen, Q. McClane, B.A. (2004) Detection of enterotoxigenic Clostridium perfringens type A isolates in American retail foods. Appl Environ Microbiol 70 : 2685 2691.
37. Yao, J., Zhong, J., Fang, Y., Geisinger, E., Novick, R.P. Lambowitz, A.M. (2006) Use of targetrons to disrupt essential and nonessential genes in Staphylococcus aureus reveals temperature sensitivity of Ll.LtrB group II intron splicing. RNA 12 : 1271 1281.