Evidence that the Agr-like quorum sensing system regulates the toxin production, cytotoxicity and pathogenicity of Clostridium perfringens type C isolate CN3685

Molecular Microbiology

Volumn 83, Issue 1, 2012, Pages 179-194

  Vidal, Jorge E ^a,b   Ma, Menglin ^b   Saputo, Julian ^c   Garcia, Jorge ^c   Uzal, Francisco A ^c   McClane, Bruce A ^b  

^a EMORY UNIVERSITY   (United States)

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

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CLOSTRIDIUM TOXIN; PROTEIN AGR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM PERFRINGENS TYPE C; CONTROLLED STUDY; CYTOTOXICITY; ENTEROTOXEMIA; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NECROTIZING ENTERITIS; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUORUM SENSING; RABBIT;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL LINE; CLOSTRIDIUM INFECTIONS; CLOSTRIDIUM PERFRINGENS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MALE; MICE; QUORUM SENSING; RABBITS;

CLOSTRIDIUM PERFRINGENS; MUS; ORYCTOLAGUS CUNICULUS;

EID: 84155162788     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07925.x     Document Type: Article

References (34)

1. Antunes, L.C., Ferreira, R.B., Buckner, M.M., and Finlay, B.B. (2010) Quorum sensing in bacterial virulence. Microbiology 156: 2271-2282.
2. Bannam, T.L., and Rood, J.I. (1993) Clostridium perfringens-Escherichia coli shuttle vectors that carry single antibiotic resistance determinants. Plasmid 29: 233-235.
3. Beier, D., and Gross, R. (2006) Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9: 143-152.
4. Calva, E., and Oropeza, R. (2006) Two-component signal transduction systems, environmental signals, and virulence. Microb Ecol 51: 166-176.
5. Chen, Y., McClane, B.A., Fisher, D.J., Rood, J.I., and 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.
6. Cooksley, C.M., Davis, I.J., Winzer, K., Chan, W.C., Peck, M.W., and Minton, N.P. (2010) Regulation of neurotoxin production and sporulation by a putative agrBD signaling system in proteolytic Clostridium botulinum. Appl Environ Microbiol 76: 4448-4460.
7. Fisher, D.J., Fernandez-Miyakawa, M.E., Sayeed, S., Poon, R., Adams, V., Rood, J.I., etal. (2006) Dissecting the contributions of Clostridium perfringens type C toxins to lethality in the mouse intravenous injection model. Infect Immun 74: 5200-5210.
8. Heuck, A.P., Moe, P.C., and Johnson, B.B. (2010) The cholesterol-dependent cytolysin family of gram-positive bacterial toxins. Subcell Biochem 51: 551-577.
9. Johnson, S., and Gerding, D.N. (1997) Enterotoxemic infections. In The Clostridia: Molecular Biology and Pathogenesis. Rood, J.I., McClane, B.A., Songer, J.G., and Titball, R.W. (eds). London: Academic Press, pp. 117-140.
10. Kaper, J.B., and Sperandio, V. (2005) Bacterial cell-to-cell signaling in the gastrointestinal tract. Infect Immun 73: 3197-3209.
11. 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., and Titball, R.W. (eds). London: Academic Press, pp. 198-207.
12. Li, J., and McClane, B.A. (2008) A novel small acid soluble protein variant is important for spore resistance of most Clostridium perfringens food poisoning isolates. PLoS Pathog 4: e1000056.
13. Li, J., Chen, J., Vidal, J.E., and McClane, B.A. (2011) The Agr-like quorum-sensing system regulates sporulation and production of enterotoxin and beta2 toxin by Clostridium perfringens type A non-food-borne human gastrointestinal disease strain F5603. Infect Immun 79: 2451-2459.
14. Lyon, G.J., Wright, J.S., Muir, T.W., and Novick, R.P. (2002) Key determinants of receptor activation in the agr autoinducing peptides of Staphylococcus aureus. Biochemistry 41: 10095-10104.
15. Lyristis, M., Bryant, A.E., Sloan, J., Awad, M.M., Nisbet, I.T., Stevens, D.L., and Rood, J.I. (1994) Identification and molecular analysis of a locus that regulates extracellular toxin production in Clostridium perfringens. Mol Microbiol 12: 761-777.
16. Ma, M., Vidal, J., Saputo, J., McClane, B.A., and Uzal, F. (2011) The VirS/VirR two-component system regulates the anaerobic cytotoxicity, intestinal pathogenicity, and enterotoxemic lethality of Clostridium perfringens Type C isolate CN3685. MBio 2: pii: e00338-00310.
17. McClane, B.A., Uzal, F.A., Fernandez-Miyakawa, M., Lyerly, D., and Wilkins, T.D. (2004) The enterotoxigenic Clostridia. In The Prokaryotes. Dworkin, M., Falkow, S., Rosenburg, E., Schleifer, K.F., and Stackebrandt, E. (eds). New York: Springer-Verlag, pp. 698-752.
18. Myers, G.S., Rasko, D.A., Cheung, J.K., Ravel, J., Seshadri, R., DeBoy, R.T., etal. (2006) Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. Genome Res 16: 1031-1040.
19. Novick, R.P., and Geisinger, E. (2008) Quorum sensing in staphylococci. Annu Rev Genet 42: 541-564.
20. Ohtani, K., Hayashi, H., and Shimizu, T. (2002) The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Mol Microbiol 44: 171-179.
21. Ohtani, K., Yuan, Y., Hassan, S., Wang, R., Wang, Y., and Shimizu, T. (2009) Virulence gene regulation by the agr system in Clostridium perfringens. J Bacteriol 191: 3919-3927.
22. Parker, C.T., and Sperandio, V. (2009) Cell-to-cell signalling during pathogenesis. Cell Microbiol 11: 363-369.
23. Petrillo, T.M., Beck-Sague, C.M., Songer, J.G., Abramowsky, C., Fortenberry, J.D., Meacham, L., etal. (2000) Enteritis necroticans (pigbel) in a diabetic child. N Engl J Med 342: 1250-1253.
24. Riedel, C.U., Monk, I.R., Casey, P.G., Waidmann, M.S., Gahan, C.G., and Hill, C. (2009) AgrD-dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes. Mol Microbiol 71: 1177-1189.
25. Sayeed, S., Uzal, F.A., Fisher, D.J., Saputo, J., Vidal, J.E., Chen, Y., etal. (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.
26. Shimizu, T., Ohtani, K., Hirakawa, H., Ohshima, K., Yamashita, A., Shiba, T., etal. (2002) Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci USA 99: 996-1001.
27. Smedley, J.G., 3rd, Fisher, D.J., Sayeed, S., Chakrabarti, G., and McClane, B.A. (2004) The enteric toxins of Clostridium perfringens. Rev Physiol Biochem Pharmacol 152: 183-204.
28. Sperandio, V., Mellies, J.L., Nguyen, W., Shin, S., and Kaper, J.B. (1999) Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci USA 96: 15196-15201.
29. Titball, R.W., Naylor, C.E., and Basak, A.K. (1999) The Clostridium perfringens alpha-toxin. Anaerobe 5: 51-64.
30. Uzal, F.A., and McClane, B.A. (2011) Recent progress in understanding the pathogenesis of Clostridium perfringens type C infections. Vet Microbiol 153: 37-43.
31. Uzal, F.A., Saputo, J., Sayeed, S., Vidal, J.E., Fisher, D.J., Poon, R., etal. (2009) Development and application of new mouse models to study the pathogenesis of Clostridium perfringens type C Enterotoxemias. Infect Immun 77: 5291-5299.
32. Vidal, J.E., McClane, B.A., Saputo, J., Parker, J., and Uzal, F.A. (2008) Effects of Clostridium perfringens beta-toxin on the rabbit small intestine and colon. Infect Immun 76: 4396-4404.
33. Vidal, J.E., Chen, J., Li, J., and McClane, B.A. (2009a) Use of an EZ-Tn5-based random mutagenesis system to identify a novel toxin regulatory locus in Clostridium perfringens strain 13. PLoS ONE 4: e6232.
34. Vidal, J.E., Ohtani, K., Shimizu, T., and McClane, B.A. (2009b) Contact with enterocyte-like Caco-2 cells induces rapid upregulation of toxin production by Clostridium perfringens type C isolates. Cell Microbiol 11: 1306-1328.