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. 1984 Dec;46(3):639–643. doi: 10.1128/iai.46.3.639-643.1984

Effects of Escherichia coli heat-stable enterotoxin STb on intestines of mice, rats, rabbits, and piglets.

D J Kennedy, R N Greenberg, J A Dunn, R Abernathy, J S Ryerse, R L Guerrant
PMCID: PMC261589  PMID: 6094354

Abstract

There are at least two classes of Escherichia coli heat-stable enterotoxins, STa and STb. Unlike STa, which is active in suckling mice and piglets, STb is inactive in suckling mice but active in piglets and older, weaned pigs. This study examined the activity of STb in several animals and its effect on intestinal histology and cyclic GMP levels in intestinal mucosal cells. STb did not cause fluid secretion in suckling mice up to 12 days old or in rat or rabbit intestinal-loop preparations. STb-induced fluid secretion in weaned-pig intestinal loops occurred by 30 min and became maximal by 3 to 6 h. STb did not disrupt intestinal histology and did not alter cyclic GMP levels in intestinal mucosal cells from piglet intestinal loops after 0.5- and 6-h incubations. Our studies support the concept that STb is a second heat-stable E. coli enterotoxin with properties and a mechanism of action unlike those of STa.

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Selected References

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  1. Alderete J. F., Robertson D. C. Purification and chemical characterization of the heat-stable enterotoxin produced by porcine strains of enterotoxigenic Escherichia coli. Infect Immun. 1978 Mar;19(3):1021–1030. doi: 10.1128/iai.19.3.1021-1030.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burgess M. N., Bywater R. J., Cowley C. M., Mullan N. A., Newsome P. M. Biological evaluation of a methanol-soluble, heat-stable Escherichia coli enterotoxin in infant mice, pigs, rabbits, and calves. Infect Immun. 1978 Aug;21(2):526–531. doi: 10.1128/iai.21.2.526-531.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. DE S. N., BHATTACHARYA K., SARKAR J. K. A study of the pathogenicity of strains of Bacterium coli from acute and chronic enteritis. J Pathol Bacteriol. 1956 Jan;71(1):201–209. doi: 10.1002/path.1700710126. [DOI] [PubMed] [Google Scholar]
  4. Dean A. G., Ching Y. C., Williams R. G., Harden L. B. Test for Escherichia coli enterotoxin using infant mice: application in a study of diarrhea in children in Honolulu. J Infect Dis. 1972 Apr;125(4):407–411. doi: 10.1093/infdis/125.4.407. [DOI] [PubMed] [Google Scholar]
  5. Evans D. J., Jr, Chen L. C., Curlin G. T., Evans D. G. Stimulation of adenyl cyclase by Escherichia coli enterotoxin. Nat New Biol. 1972 Apr 5;236(66):137–138. doi: 10.1038/newbio236137a0. [DOI] [PubMed] [Google Scholar]
  6. Evans D. J., Jr, Evans D. G., Gorbach S. L. Production of vascular permeability factor by enterotoxigenic Escherichia coli isolated from man. Infect Immun. 1973 Nov;8(5):725–730. doi: 10.1128/iai.8.5.725-730.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Field M., Graf L. H., Jr, Laird W. J., Smith P. L. Heat-stable enterotoxin of Escherichia coli: in vitro effects on guanylate cyclase activity, cyclic GMP concentration, and ion transport in small intestine. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2800–2804. doi: 10.1073/pnas.75.6.2800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Frantz J. C., Robertson D. C. Immunological properties of Escherichia coli heat-stable enterotoxins: development of a radioimmunoassay specific for heat-stable enterotoxins with suckling mouse activity. Infect Immun. 1981 Jul;33(1):193–198. doi: 10.1128/iai.33.1.193-198.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Giannella R. A. Suckling mouse model for detection of heat-stable Escherichia coli enterotoxin: characteristics of the model. Infect Immun. 1976 Jul;14(1):95–99. doi: 10.1128/iai.14.1.95-99.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Greenberg R. N., Guerrant R. L., Chang B., Robertson D. C., Murad F. Inhibition of Escherichia coli heat-stable enterotoxin effects on intestinal guanylate cyclase and fluid secretion by quinacrine. Biochem Pharmacol. 1982 Jun 1;31(11):2005–2009. doi: 10.1016/0006-2952(82)90413-0. [DOI] [PubMed] [Google Scholar]
  11. Greenberg R. N., Guerrant R. L. E. coli heat-stable enterotoxin. Pharmacol Ther. 1981;13(3):507–531. doi: 10.1016/0163-7258(81)90027-9. [DOI] [PubMed] [Google Scholar]
  12. Guerrant R. L., Brunton L. L., Schnaitman T. C., Rebhun L. I., Gilman A. G. Cyclic adenosine monophosphate and alteration of Chinese hamster ovary cell morphology: a rapid, sensitive in vitro assay for the enterotoxins of Vibrio cholerae and Escherichia coli. Infect Immun. 1974 Aug;10(2):320–327. doi: 10.1128/iai.10.2.320-327.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gyles C. L. Limitations of the infant mouse test for Escherichia coli heat stable enterotoxin. Can J Comp Med. 1979 Oct;43(4):371–379. [PMC free article] [PubMed] [Google Scholar]
  14. Harper J. F., Brooker G. Femtomole sensitive radioimmunoassay for cyclic AMP and cyclic GMP after 2'0 acetylation by acetic anhydride in aqueous solution. J Cyclic Nucleotide Res. 1975;1(4):207–218. [PubMed] [Google Scholar]
  15. Hughes J. M., Murad F., Chang B., Guerrant R. L. Role of cyclic GMP in the action of heat-stable enterotoxin of Escherichia coli. Nature. 1978 Feb 23;271(5647):755–756. doi: 10.1038/271755a0. [DOI] [PubMed] [Google Scholar]
  16. Jacks T. M., Wu B. J., Braemer A. C., Bidlack D. E. Properties of the enterotoxic component in Escherichia coli enteropathogenic for swine. Infect Immun. 1973 Feb;7(2):178–189. doi: 10.1128/iai.7.2.178-189.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kashiwazaki M., Akaike Y., Miyachi T., Ogawa T., Sugawara M., Isayama Y. Production of heat-stable enterotoxic component by Escherichia coli strains enteropathogenic for swine. Natl Inst Anim Health Q (Tokyo) 1981 Spring;21(1):21–25. [PubMed] [Google Scholar]
  18. Kashiwazaki M., Nakamura K., Sugimoto C., Isayama Y., Akaike Y. Diarrhea in piglets due to Escherichia coli that produce only porcine ileal loop-positive heat-stable enterotoxic component. Natl Inst Anim Health Q (Tokyo) 1981 Fall;21(3):148–149. [PubMed] [Google Scholar]
  19. Katsuki S., Murad F. Regulation of adenosine cyclic 3',5'-monophosphate and guanosine cyclic 3',5'-monophosphate levels and contractility in bovine tracheal smooth muscle. Mol Pharmacol. 1977 Mar;13(2):330–341. [PubMed] [Google Scholar]
  20. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  21. Lathe R., Hirth P., DeWilde M., Harford N., Lecocq J. P. Cell-free synthesis of enterotoxin of E. coli from a cloned gene. Nature. 1980 Apr 3;284(5755):473–474. doi: 10.1038/284473a0. [DOI] [PubMed] [Google Scholar]
  22. Lee C. H., Moseley S. L., Moon H. W., Whipp S. C., Gyles C. L., So M. Characterization of the gene encoding heat-stable toxin II and preliminary molecular epidemiological studies of enterotoxigenic Escherichia coli heat-stable toxin II producers. Infect Immun. 1983 Oct;42(1):264–268. doi: 10.1128/iai.42.1.264-268.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moon H. W., Kohler E. M., Schneider R. A., Whipp S. C. Prevalence of pilus antigens, enterotoxin types, and enteropathogenicity among K88-negative enterotoxigenic Escherichia coli from neonatal pigs. Infect Immun. 1980 Jan;27(1):222–230. doi: 10.1128/iai.27.1.222-230.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Moon H. W., Sorensen D. K., Sautter J. H., Higbee J. M. Association of Escherichia coli with diarrheal disease of the newborn pig. Am J Vet Res. 1966 Jul;27(119):1007–1011. [PubMed] [Google Scholar]
  25. Olsson E., Söderlind O. Comparison of different assays for definition of heat-stable enterotoxigenicity of Escherichia coli porcine strains. J Clin Microbiol. 1980 Jan;11(1):6–15. doi: 10.1128/jcm.11.1.6-15.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Picken R. N., Mazaitis A. J., Maas W. K., Rey M., Heyneker H. Nucleotide sequence of the gene for heat-stable enterotoxin II of Escherichia coli. Infect Immun. 1983 Oct;42(1):269–275. doi: 10.1128/iai.42.1.269-275.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Richardson S. H., Giles J. C., Kruger K. S. Sealed adult mice: new model for enterotoxin evaluation. Infect Immun. 1984 Feb;43(2):482–486. doi: 10.1128/iai.43.2.482-486.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Smith H. W., Gyles C. L. The relationship between two apparently different enterotoxins produced by enteropathogenic strains of Escherichia coli of porcine origin. J Med Microbiol. 1970 Aug;3(3):387–401. doi: 10.1099/00222615-3-3-387. [DOI] [PubMed] [Google Scholar]
  29. Smith H. W., Halls S. Studies on Escherichia coli enterotoxin. J Pathol Bacteriol. 1967 Apr;93(2):531–543. doi: 10.1002/path.1700930212. [DOI] [PubMed] [Google Scholar]
  30. So M., McCarthy B. J. Nucleotide sequence of the bacterial transposon Tn1681 encoding a heat-stable (ST) toxin and its identification in enterotoxigenic Escherichia coli strains. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4011–4015. doi: 10.1073/pnas.77.7.4011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Staples S. J., Asher S. E., Giannella R. A. Purification and characterization of heat-stable enterotoxin produced by a strain of E. coli pathogenic for man. J Biol Chem. 1980 May 25;255(10):4716–4721. [PubMed] [Google Scholar]
  32. Steiner A. L., Parker C. W., Kipnis D. M. Radioimmunoassay for cyclic nucleotides. I. Preparation of antibodies and iodinated cyclic nucleotides. J Biol Chem. 1972 Feb 25;247(4):1106–1113. [PubMed] [Google Scholar]
  33. TRABULSI L. R. REVELA C AO DE COLIBACILOS ASSOCIADOS 'AS DIARR'EIAS INFANTIS PELO M'ETODO DA INFEC C AO EXPERIMENTAL DA AL CA LIGADA DO INTESTINO DO COELHO. Rev Inst Med Trop Sao Paulo. 1964 Sep-Oct;6:197–203. [PubMed] [Google Scholar]
  34. Takeda Y., Takeda T., Yano T., Yamamoto K., Miwatani T. Purification and partial characterization of heat-stable enterotoxin of enterotoxigenic Escherichia coli. Infect Immun. 1979 Sep;25(3):978–985. doi: 10.1128/iai.25.3.978-985.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Whipp S. C., Moon H. W., Argenzio R. A. Comparison of enterotoxic activities of heat-stable enterotoxins from class 1 and class 2 Escherichia coli of swine origin. Infect Immun. 1981 Jan;31(1):245–251. doi: 10.1128/iai.31.1.245-251.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

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