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

Infection and Immunity

Volumn 72, Issue 7, 2004, Pages 3914-3924

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

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b SOUTH DAKOTA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROTOXIN; ESCHERICHIA COLI ENTEROTOXIN; NALIDIXIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; DEHYDRATION; DIARRHEA; ELECTROLYTE DISTURBANCE; ESCHERICHIA COLI; FIMBRIA; GNOTOBIOTICS; ILEUM; INOCULATION; JEJUNUM; METABOLIC ACIDOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SEPTICEMIA; SWINE; WEIGHT REDUCTION;

ANIMALS; BICARBONATES; CHLORIDES; DEHYDRATION; DIARRHEA; ENTEROTOXINS; ESCHERICHIA COLI; INTESTINES; MUTATION; POTASSIUM; SEQUENCE DELETION; SWINE; SWINE DISEASES; WEIGHT LOSS;

EID: 3042681631     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.7.3914-3924.2004     Document Type: Article

References (68)

1. Ausubel, F. R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1995. Short protocols in molecular biology. A compendium of methods from current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
2. 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.
3. Bertschinger, H. U., and J. M. Fairbrother. 1999. Escherichia coli infections, p. 431-468. In B. E. Straw, S. D'Allaire, W. L. Mengeling, and D. J. Taylor (ed.), Diseases of swine, 8th ed. Iowa State University Press, Ames.
4. 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. 66:1270-1272.
5. Chen, T.-M., A. J. Mazaitis, and W. K. Maas. 1985. Construction of a conjugative plasmid with potential use in vaccines against heat-labile enterotoxin. Infect. Immun. 47:5-10.
6. Chiu, C., A. H. McArdle, R. Brown, H. J. Scott, and F. N. Gurd. 1970. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch. Surg. 101:478-483.
7. 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.
8. Clark, D. R. 1979. Circulatory shock: etiology and pathophysiology. J. Am. Vet. Med. Assoc. 175:78-81.
9. Dallas, W. S. 1983. Conformity between heat-labile toxin genes from human and porcine enterotoxigenic Escherichia coli. Infect. Immun. 40:647-652.
10. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
11. Dubreuil, J. D. 1997. Escherichia coli STb enterotoxin. Microbiology 143:1783-1795.
12. Dubreuil, J. D., J. M. Fairbrother, R. Lallier, and S. Lariviere. 1991. Production and purification of heat-stable enterotoxin b from a porcine Escherichia coli strain. Infect. Immun. 59:198-203.
13. Fairbrother, J. M., and M. Ngeleka. 1994. Extraintestinal Escherichia coli infections in pigs, p. 221-236. In C. L. Gyles (ed.), Escherichia coli in domestic animals and humans. CAB International, Wallingford, United Kingdom.
14. Faubert, C., and R. Drolet. 1992. Hemorrhagic gastroenteritis caused by Escherichia coli in piglets: clinical, pathological and microbiological findings. Can. Vet. J. 33:251-256.
15. Field, M. 2003. Intestinal ion transport and the pathophysiology of diarrhea. J. Clin. Investig. 111:931-943.
16. + enterotoxigenic Escherichia coli, but adhesion of this bacterium to brush borders does not. Infect. Immun. 66:4050-4055.
17. Fusco, W. 2001. Ph.D. dissertation, University of Idaho, Moscow.
18. Geary, S. J., B. A. Marchlewicz, and R. A. Finkelstein. 1982. Comparison of heat-labile enterotoxins from porcine and human strains of Escherichia coli. Infect. Immun. 36:215-220.
19. George, J. W. 1994. Water, electrolytes, and acid base, p. 94-111. In J. R. Duncan and K. W. Prasse (ed.), Veterinary laboratory medicine: clinical pathology. Iowa State University Press, Ames.
20. 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.
21. Gyles, C. L., and D. A. Barnum. 1969. A heat-labile enterotoxin from strains of Escherichia coli enteropathogenic for pigs. J. Infect. Dis. 120:419-426.
22. Haglund, U., L. Hulten, C. Ahren, and O. Lundgren. 1975. Mucosal lesions in the human small intestine in shock. Gut 16:979-984.
23. Hirst, T. R., L. L. Randall, and S. J. Hardy. 1984. Cellular location of heat-labile enterotoxin in Escherichia coli. J. Bacteriol. 157:637-642.
24. Hohmann, A., and M. R. Wilson. 1975. Adherence of enteropathogenic Escherichia coli to intestinal epithelium in vivo. Infect. Immun. 12:866-880.
25. Kohler, E. M. 1971. Enterotoxic activity of whole cell lysates of Escherichia coli in young pigs. Am. J. Vet. Res. 32:731-737.
26. Kohler, E. M., and R. F. Cross. 1971. Feeding bacteria-free whole cell lysates of Escherichia coli to gnotobiotic pigs and the effects of giving antiserums. Am. J. Vet. Res. 32:739-748.
27. Lundgren, O. 2002. Enteric nerves and diarrhoea. Pharm. Toxicol. 90:109-120.
28. McVeigh, A., A. Fasano, D. A. Scott, S. Jelacic, S. L. Moseley, D. C. Robertson, and S. J. Savarino. 2000. IS1414, an Escherichia coli insertion sequence with a heat-stable enterotoxin gene embedded in a transposase-like gene. Infect. Immun. 68:5710-5715.
29. Ménard, L. P., and J. D. Dubreuil. 2002. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 (EAST1): a new toxin with an old twist. Crit. Rev. Microbiol. 28:43-60.
30. Meyer, R. C., and J. Simon. 1972. Experimental peracute colibacillosis: gastrointestinal lesions in gnotobiotic piglets. Vet. Pathol. 9:360-367.
31. Miller, V. L., and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
32. Miniats, O. P., and D. Jol. 1978. Gnotobiotic pigs-derivation and rearing. Can. J. Comp. Med. 42:428-437.
33. Moon, H. W., and T. O. Bunn. 1993. Vaccines for preventing enterotoxigenic Escherichia coli infections in farm animals. Vaccine 11:213-220.
34. Moon, H. W., E. M. Kohler, R. A. Schneider, and S. C. Whipp. 1980. Prevalence of pilus antigens, enterotoxin types, and enteropathogenicity among K88-negative enterotoxigenic Escherichia coli from neonatal pigs. Infect. Immun. 27:222-230.
35. Moon, H. W., N. O. Nielsen, and T. T. Kramer. 1970. Experimental enteric colibacillosis of the newborn pig: histopathology of the small intestine and changes in plasma electrolytes. Am. J. Vet. Res. 31:103-112.
36. 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.
37. Moon, H. W., S. C. Whipp, and A. L. Baetz. 1971. Comparative effects of enterotoxins from Escherichia coli and Vibrio cholerae on rabbit and swine small intestine. Lab. Investig. 25:133-140.
38. Morales, V. M., A. Backman, and M. Bagdasarian. 1991. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97:39-47.
39. Mourad, F. H., and C. F. Nassar. 2000. Effect of vasoactive intestinal polypeptide (VIP) antagonism on rat jejunal fluid and electrolyte secretion induced by cholera and Escherichia coli enterotoxins. Gut 47:382-386.
40. Moxley, R. A., E. M. Berberov, D. H. Francis, J. Xing, M. Moayeri, R. A. Welch, D. R. Baker, and R. G. Barletta. 1998. Pathogenicity of an enterotoxigenic Escherichia coli hemolysin (hlyA) mutant in gnotobiotic piglets. Infect. Immun. 66:5031-5035.
41. 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.
42. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
43. Pierce, N. F., J. B. Kaper, J. J. Mekalanos, and W. C. Cray, Jr. 1985. Role of cholera toxin in enteric colonization by Vibrio cholerae O1 in rabbits. Infect. Immun. 50:813-816.
44. 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.
45. 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.
46. + Escherichia coli to isolated intestinal epithelial cells. Infect. Immun. 28:298-300.
47. Sack, D. A., and R. B. Sack. 1975. Test for enterotoxigenic Escherichia coli using Y1 adrenal cells in miniculture. Infect. Immun. 11:334-336.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Saunders, C. N., A. J. Stevens, J. B. Spence, and W. J. Sojka. 1960. Escherichia coli infection in piglets. Res. Vet. Sci. 1:28-35.
50. Savarino, S. J., A. Fasano, J. Watson, B. M. Martin, M. M. Levine, S. Guandalini, and P. Guerry. 1993. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 represents another subfamily of E. coli heat-stable toxin. Proc. Natl. Acad. Sci. USA 90:3093-3097.
51. Savarino, S. J., A. McVeigh, J. Watson, A. Cravioto, J. Molina, P. Echeverria, M. K. Bhan, M. M. Levine, and A. Fasano. 1996. Enteroaggregative Escherichia coli heat-stable enterotoxin is not restricted to enteroaggregative E. coli. J. Infect. Dis. 173:1019-1022.
52. Sears, C. L., and J. B. Kaper. 1996. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60:167-215.
53. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-791.
54. Smith, H. W., and C. L. Gyles. 1970. The relationship between two apparently different enterotoxins produced by enteropathogenic strains of Escherichia coli of porcine origin. J. Med. Microbiol. 3:387-401.
55. 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.
56. Stawski, G., L. Nielsen, F. Orskov, and I. Orskov. 1990. Serum sensitivity of a diversity of Escherichia coli antigenic reference strains. APMIS 98:828-838.
57. Swank, R. T., and K. D. Munkres. 1971. Molecular weight analysis of oligopeptide by electrophoresis in polyacrylamide gel with sodium dodecyl sulfate. Anal. Biochem. 39:462-477.
58. Tauschek, M., R. J. Gorrell, R. A. Strugnell, and R. M. Robins-Browne. 2002. Identification of a protein secretory pathway for the secretion of heat-labile enterotoxin by an enterotoxigenic strain of Escherichia coli. Proc. Natl. Acad. Sci. USA 99:7066-7071.
59. Taylor, L. A., and R. E. Rose. 1988. A correction in the nucleotide sequence of the Tn903 kanamycin resistance determinant in pUC4K. Nucleic Acids Res. 16:358.
60. Tuomanen, E., and A. Weiss. 1985. Characterization of two adhesins of Bordetella pertussis for human ciliated respiratory-epithelial cells. J. Infect. Dis. 152:118-125.
61. Wang, F., T. Butler, G. H. Rabbani, and P. K. Jones. 1986. The acidosis of cholera: contributions of hyperproteinemia, lactic acidemia, and hyperphosphatemia to an increased serum anion gap. N. Engl. J. Med. 315:1591-1595.
62. Wang, Z., and T. G. Rossman. 1994. Large scale supercoiled plasmid preparation by acidic phenol extraction. BioTechniques 16:460-463.
63. Weikel, C. S., H. N. Nellans, and R. L. Guerrant. 1986. In vivo and in vitro effects of a novel enterotoxin, STb, produced by Escherichia coli. J. Infect. Dis. 153:893-901.
64. Whipp, S. C. 1987. Protease degradation of Escherichia coli heat-stable, mouse-negative, pig-positive enterotoxin. Infect. Immun. 55:2057-2060.
65. 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.
66. Wilson, R. A., and D. H. Francis. 1986. Fimbriae and enterotoxins associated with Escherichia coli serogroups isolated from pigs with colibacillosis. Am. J. Vet. Res. 47:213-217.
67. Yamamoto, T., and P. Echeverria. 1996. Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene sequences in enterotoxigenic E. coli strains pathogenic for humans. Infect. Immun. 64:1441-1445.
68. 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.