Comparison of the contributions of heat-labile enterotoxin and heat-stable enterotoxin b to the virulence of enterotoxigenic Escherichia coli in F4ac receptor-positive young pigs

Infection and Immunity

Volumn 76, Issue 7, 2008, Pages 3141-3149

  Erume, Joseph ^a   Berberov, Emil M ^a,d   Kachman, Stephen D ^a   Scott, Michael A ^b   Zhou, You ^a   Francis, David H ^c   Moxley, Rodney A ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c SOUTH DAKOTA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ENTEROTOXIN; ENTEROTOXIN B; PROTEIN ELTAB; PROTEIN ESTB; PROTEIN F4ACR; BACTERIAL TOXIN; ENTEROTOXIN LT; ESCHERICHIA COLI PROTEIN; HEAT STABLE TOXIN (E COLI); IMMUNOGLOBULIN RECEPTOR; PILI, BACTERIAL RECEPTOR;

ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CONTROLLED STUDY; DEHYDRATION; DIARRHEA; DISEASE SEVERITY; ENTEROTOXIGENIC ESCHERICHIA COLI; GENE DELETION; METABOLIC ACIDOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SWINE; THERMOSTABILITY; WEIGHT REDUCTION; ANIMAL; ANIMAL DISEASE; ENTEROBACTER INFECTION; FEMALE; GENETICS; GERMFREE ANIMAL; MALE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; SWINE DISEASE; VIRULENCE;

ANIMALS; BACTERIAL TOXINS; DIARRHEA; ENTEROTOXIGENIC ESCHERICHIA COLI; ENTEROTOXINS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FEMALE; GENE DELETION; GERM-FREE LIFE; MALE; RECEPTORS, IMMUNOLOGIC; SWINE; SWINE DISEASES; VIRULENCE;

EID: 46449123458     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01743-07     Document Type: Article

References (55)

1. Allen, K. P., M. M. Randolph, and J. M. Fleckenstein. 2006. Importance of heat-labile enterotoxin in colonization of the adult mouse small intestine by human enterotoxigenic Escherichia coli strains. Infect. Immun. 74:869-875.
2. Reference deleted.
3. Amezcua, R., R. M. Friendship, C. E. Dewey, C. Gyles, and J. M. Fairbrother. 2002. Presentation of postweaning Escherichia coli diarrhea in southern Ontario, prevalence of hemolytic E. coli serogroups involved, and their antimicrobial resistance patterns. Can. J. Vet. Res. 66:73-78.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1995. Short protocols in molecular biology. John Wiley & Sons, New York, NY.
5. Baker, D. R., L. O. Billey, and D. H. Francis. 1997. Distribution of K88 Escherichia coli-adhesive and nonadhesive phenotypes among pigs of four breeds. Vet. Microbiol. 54:123-132.
6. Berberov, E. M., Y. Zhou, D. H. Francis, M. A. Scott, S. D. Kachman, and R. A. Moxley. 2004. Relative importance of heat-labile enterotoxin in the causation of severe diarrheal disease in the gnotobiotic piglet model by a strain of enterotoxigenic Escherichia coli that produces multiple enterotoxins. Infect. Immun. 72:3914-3924.
7. Bijlsma, I. G., A. de Nijs, C. van der Meer, and J. F. Frik. 1982. Different pig phenotypes affect adherence of Escherichia coli to jejunal brush borders by K88ab, K88ac, or K88ad antigen. Infect. Immun. 37:891-894.
8. Billey, L. O., A. K. Ericsson, and D. H. Francis. 1998. Multiple receptors on porcine intestinal epithelial cells for the three variants of Escherichia coli K88 fimbrial adhesion. Vet. Microbiol. 59:203-212.
9. Casey, T. A., C. J. Herring, R. A. Schneider, B. T. Bosworth, and S. C. Whipp. 1998. Expression of heat-stable enterotoxin STb by adherent Escherichia coli is not sufficient to cause severe diarrhea in neonatal pigs. Infect. Immun. 66:270-272.
10. Chapman, P. A., and D. L. Swift. 1984. A simplified method for detecting the heat-labile enterotoxin of Escherichia coli. J. Med. Microbiol. 18:399-403.
11. Cherepanov, P. P., and W. Wackernagel. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
12. Choi, C., D. Kwon, and C. Chae. 2001. Prevalence of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene and its relationship with fimbrial and enterotoxin genes in E. coli isolated from diarrheic piglets. J. Vet. Diagn. Investig. 13:26-29.
13. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
14. Dorsey, F. C., J. F. Fischer, and J. M. Fleckenstein. 2006. Directed delivery of heat-labile enterotoxin by enterotoxigenic Escherichia coli. Cell. Microbiol. 8:1516-1527.
15. Erickson, A. K., J. A. Willgohs, S. Y. McFarland, D. A. Benfield, and D. H. Francis. 1992. Identification of two porcine brush border glycoproteins that bind the K88ac adhesion of Escherichia coli and correlation of these glycoproteins with the adhesive phenotype. Infect. Immun. 60:983-988.
16. Erickson, A. K., D. R. Baker, B. T. Bosworth, T. A. Casey, D. A. Benfield, and D. H. Francis. 1994. Characterization of porcine intestinal receptors for the K88ac fimbrial adhesin of Escherichia coli as mucin-type sialoglycoproteins. Infect. Immun. 62:5404-5410.
17. Fairbrother, J. M., E. Nadeau, and C. L. Gyles. 2005. Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim. Health Res. Rev. 6:17-39.
18. Francis, D. H. 2002. Enterotoxigenic Escherichia coli infection in pigs and its diagnosis. J. Swine Health Prod. 10:171-175.
19. + enterotoxigenic Escherichia coli, but adhesion of this bacterium to brush borders does not. Infect. Immun. 66:4050-4055.
20. Frydendahl, K. 2002. Prevalence of serogroups and virulence genes in Escherichia coli associated with postweaning diarrhoea and edema disease in pigs and a comparison of diagnostic approaches. Vet. Microbiol. 85:169-182.
21. Grange, P. A., A. K. Erickson, T. J. Anderson, and D. H. Francis. 1998. Characterization of the carbohydrate moiety of intestinal mucin-type sialoglycoprotein receptors for the K88ac fimbrial adhesin of Escherichia coli. Infect. Immun. 66:1613-1621.
22. Grange, P. A., and M. A. Mouricout. 1996. Transferrin associated with the porcine intestinal mucosa is a receptor specific for K88ab fimbriae of Escherichia coli. Infect. Immun. 64:606-610.
23. Gyles, C. L. 1992. Escherichia coli cytotoxins and enterotoxins. Can. J. Microbiol. 38:734-746.
24. Jensen, G. M., K. Frydendahl, O. Svendsen, C. B. Jorgensen, S. Cirera, M. Fredholm, J. P. Nielsen, and K. Moller. 2006. Experimental infection with Escherichia coli O149:F4ac in weaned piglets. Vet. Microbiol. 115:243-249.
25. Jorgensen, C. B., S. Cirera, A. L. Archibald, L. Anderson, M. Fredholm, and I. Edfors-Lilja. 2004. Porcine polymorphisms and methods for detecting them. International application published under the patent cooperation treaty (PCT). PCT/DK2003/000807 or WO2004/048606-A2.
26. Lasaro, M. A., J. F. Rodrigues, C. Mathias-Santos, B. E. Guth, A. Régua-Mangia, A. J. Piantino Ferreira, M. Takagi, J. Cabrera-Crespo, M. E. Sbrogio-Almeida, and L. C. de Souza Ferreira. 2006. Production and release of heat-labile toxin by wild-type human-derived enterotoxigenic Escherichia coli. FEMS Immunol. Med. Microbiol. 48:123-131.
27. Mainil, J. G., G. Daube, E. Jacquemin, P. Pohl, and A. Kaeckenbeeck. 1998. Virulence plasmids of enterotoxigenic Escherichia coli isolates from piglets. Vet. Microbiol. 62:291-301.
28. Maniats, O. P., and D. Jol. 1978. Gnotobiotic pigs - derivation and rearing. Can. J. Comp. Med. 42:428-437.
29. Mateo, K. S., P. R. Hardwidge, W. Zhang, R. S. Kaushik, R. A. Moxley, and D. H. Francis. 2007. Effect of heat-labile enterotoxin expression on the ability of enterotoxigenic Escherichia coli to adhere to the IPEC-J2 porcine epithelial cell line, abstr. 9. Proc. Conf. Res. Workers Anim. Dis., Chicago, IL, 1 to 3 December 2007.
30. Moon, H. W., R. A. Schneider, and S. L. Moseley. 1986. Comparative prevalence of four enterotoxin genes among Escherichia coli isolated from swine. Am. J. Vet. Res. 47:210-212.
31. Murphy, K. C. 1998. Use of bacteriophage lambda recombination functions to promote gene replacement in Escherichia coli. J. Bacteriol. 180:2063-2071.
32. Murphy, K. C., and K. G. Campellone. 2003. Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol. Biol. 13:4-11.
33. Nagy, B., T. A. Casey, and H. W. Moon. 1990. Phenotype and genotype of Escherichia coli isolated from pigs with postweaning diarrhea in Hungary. J. Clin. Microbiol. 28:651-653.
34. Nagy, B., and P. Z. Fekete. 2005. Enterotoxigenic Escherichia coli in veterinary medicine. Int. J. Med. Microbiol. 295:443-454.
35. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
36. Noamani, B. N., J. M. Fairbrother, and C. L. Gyles. 2003. Virulence genes of O149 enterotoxigenic Escherichia coli from outbreaks of postweaning diarrhea in pigs. Vet. Microbiol. 97:87-101.
37. Osek, J. 1999. Prevalence of Shiga toxin genes among Escherichia coli strains isolated from pigs. Vet. Rec. 145:557-558.
38. Peng, Q. L., J. Ren, X. M. Yan, X. Huang, H. Tang, Y. Z. Wang, B. Zhang, and L. S. Huang. 2007. The g.243A>G mutation in intron 17 of MUC4 is significantly associated with susceptibility/resistance to ETEC F4ab/ac infection in pigs. Anim. Genet. 38:397-400.
39. Qadri, F., A. M. Svennerholm, A. S. G. Faruque, and R. B. Sack. 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin. Microbiol. Rev. 18:465-483.
40. Rasschaert, K., F. Verdonck, B. M. Goddeeris, L. Duchateau, and E. Cox. 2007. Screening of pigs resistant to F4 enterotoxigenic Escherichia coli (ETEC) infection. Vet. Microbiol. 123:249-253.
41. Ristaino, P. A., M. M. Levine, and C. R. Young. 1983. Improved GM1-enzyme-linked immunosorbent assay for detection of Escherichia coli heat-labile enterotoxin. J. Clin. Microbiol. 18:808-815.
42. Rogers, D. G., A. A. Andersen, and B. D. Hunsaker. 1996. Lung and nasal lesions caused by a swine chlamydial isolate in gnotobiotic pigs. J. Vet. Diagn. Investig. 8:45-55.
43. Sack, D. A., and R. B. Sack. 1975. Test for enterotoxigenic Escherichia coli using Y-1 adrenal cells in miniculture. Infect. Immun. 11:334-336.
44. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Sears, C. L., and J. B. Kaper. 1996. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60:167-215.
46. Smith, H. W., and M. A. Linggood. 1971. Observations on the pathogenic properties of the K88, Hly and Ent plasmids of Escherichia coli with particular reference to porcine diarrhea. J. Med. Microbiol. 4:467-485.
47. Taneja, N., P. Rao, D. S. V. R. Rao, M. Singh, and M. Sharma. 2006. Enterotoxigenic Escherichia coli causing choleragenic syndrome during an interepidemic period of cholera in North India. Jpn. J. Infect. Dis. 59:245-248.
48. Urban, R. G., E. M. Pipper, L. A. Dreyfus, and S. C. Whipp. 1990. High-level production of Escherichia coli STb heat-stable enterotoxin and quantification by a direct enzyme-linked immunosorbent assay. J. Clin. Microbiol. 28:2383-2388.
49. Van den Broeck, W., E. Cox, B. Oudega, and B. M. Goddeeris. 2000. The F4 fimbrial antigen of Escherichia coli and its receptors. Vet. Microbiol. 71:223-244.
50. Walker, R. I., D. Steele, T. Aguado, and the Ad Hoc ETEC Technical Expert Committee. 2007. Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease. Vaccine 25:2545-2566.
51. Whipp, S. C., S. L. Moseley, and H. W. Moon. 1986. Microscopic alterations in jejunal epithelium of 3-week-old pigs induced by pig-specific, mouse-negative, heat-stable Escherichia coli enterotoxin. Am. J. Vet. Res. 47:615-618.
52. Willemsen, P. T., and F. K. de Graaf. 1992. Age and serotype dependent binding of K88 fimbriae to porcine intestinal receptors. Microb. Pathog. 12:367-375.
53. Yamamoto, T., and M. Nakazawa. 1997. Detection and sequences of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene in enterotoxigenic E. coli strains isolated from piglets and calves with diarrhea. J. Clin. Microbiol. 35:223-227.
54. Zhang, W., E. M. Berberov, J. Freeling, D. He, R. A. Moxley, and D. H. Francis. 2006. Significance of heat-stable and heat-labile enterotoxins in porcine colrbacillosis in an additive model for pathogenicity studies. Infect. Immun. 74:3107-3114.
55. Zhang, W., M. Zhao, L. Ruesch, A. Omot, and D. Francis. 2007. Prevalence of virulence genes in Escherichia coli strains recently isolated from young pigs with diarrhea in the US. Vet. Microbiol. 123:145-152.