Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1990 Nov;58(11):3717–3723. doi: 10.1128/iai.58.11.3717-3723.1990

Enterotoxin and cytotoxin production by enteroinvasive Escherichia coli.

A Fasano 1, B A Kay 1, R G Russell 1, D R Maneval Jr 1, M M Levin 1
PMCID: PMC313719  PMID: 2228242

Abstract

It has long been suspected that besides their ability to invade enterocytes, enteroinvasive Escherichia coli (EIEC) strains have the ability to elaborate an enterotoxin. We tested 35 EIEC strains for cytotoxins and 9 (1 per serogroup) for enterotoxins. All 35 strains exhibited low levels of Vero cell cytotoxins that are immunologically and genetically distinct from Shiga-like toxin I or II of enterohemorrhagic E. coli. Sterile supernatants and cell lysates of two EIEC strains were tested in rabbit ileal loops, and both stimulated moderate fluid accumulation (circa 0.5 ml/cm) without tissue damage; secretory activity was confirmed in Ussing chambers, where these two strains and the seven others tested significantly increased short circuit current without altering tissue conductance. Curing the 140-MDa invasiveness plasmid from an EIEC strain did not diminish enterotoxin production. Culture in minimal Fe2+ medium is necessary to detect expression of the enterotoxin which is circa 68 to 80 kDa in size and is distinct from the EIEC cytotoxin.

Full text

PDF
3717

Images in this article

3720Image
on p.3720

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BUTCHER R. W., SUTHERLAND E. W. Adenosine 3',5'-phosphate in biological materials. I. Purification and properties of cyclic 3',5'-nucleotide phosphodiesterase and use of this enzyme to characterize adenosine 3',5'-phosphate in human urine. J Biol Chem. 1962 Apr;237:1244–1250. [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. Cleary T. G., Murray B. E. Lack of Shiga-like cytotoxin production by enteroinvasive Escherichia coli. J Clin Microbiol. 1988 Oct;26(10):2177–2179. doi: 10.1128/jcm.26.10.2177-2179.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DuPont H. L., Formal S. B., Hornick R. B., Snyder M. J., Libonati J. P., Sheahan D. G., LaBrec E. H., Kalas J. P. Pathogenesis of Escherichia coli diarrhea. N Engl J Med. 1971 Jul 1;285(1):1–9. doi: 10.1056/NEJM197107012850101. [DOI] [PubMed] [Google Scholar]
  5. Gentry M. K., Dalrymple J. M. Quantitative microtiter cytotoxicity assay for Shigella toxin. J Clin Microbiol. 1980 Sep;12(3):361–366. doi: 10.1128/jcm.12.3.361-366.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gomes T. A., Toledo M. R., Trabulsi L. R., Wood P. K., Morris J. G., Jr DNA probes for identification of enteroinvasive Escherichia coli. J Clin Microbiol. 1987 Oct;25(10):2025–2027. doi: 10.1128/jcm.25.10.2025-2027.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Guandalini S., Fasano A., Migliavacca M., Marchesano G., Ferola A., Rubino A. Effects of berberine on basal and secretagogue-modified ion transport in the rabbit ileum in vitro. J Pediatr Gastroenterol Nutr. 1987 Nov-Dec;6(6):953–960. doi: 10.1097/00005176-198711000-00023. [DOI] [PubMed] [Google Scholar]
  8. Hale T. L., Oaks E. V., Formal S. B. Identification and antigenic characterization of virulence-associated, plasmid-coded proteins of Shigella spp. and enteroinvasive Escherichia coli. Infect Immun. 1985 Dec;50(3):620–629. doi: 10.1128/iai.50.3.620-629.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hale T. L., Sansonetti P. J., Schad P. A., Austin S., Formal S. B. Characterization of virulence plasmids and plasmid-associated outer membrane proteins in Shigella flexneri, Shigella sonnei, and Escherichia coli. Infect Immun. 1983 Apr;40(1):340–350. doi: 10.1128/iai.40.1.340-350.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harris J. R., Wachsmuth I. K., Davis B. R., Cohen M. L. High-molecular-weight plasmid correlates with Escherichia coli enteroinvasiveness. Infect Immun. 1982 Sep;37(3):1295–1298. doi: 10.1128/iai.37.3.1295-1298.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Levine M. M., Bergquist E. J., Nalin D. R., Waterman D. H., Hornick R. B., Young C. R., Sotman S. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet. 1978 May 27;1(8074):1119–1122. doi: 10.1016/s0140-6736(78)90299-4. [DOI] [PubMed] [Google Scholar]
  12. Levine M. M. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987 Mar;155(3):377–389. doi: 10.1093/infdis/155.3.377. [DOI] [PubMed] [Google Scholar]
  13. Levine M. M., Kaper J. B., Lockman H., Black R. E., Clements M. L., Falkow S. Recombinant DNA risk assessment studies in humans: efficacy of poorly mobilizable plasmids in biologic containment. J Infect Dis. 1983 Oct;148(4):699–709. doi: 10.1093/infdis/148.4.699. [DOI] [PubMed] [Google Scholar]
  14. Levine M. M., Prado V., Robins-Browne R., Lior H., Kaper J. B., Moseley S. L., Gicquelais K., Nataro J. P., Vial P., Tall B. Use of DNA probes and HEp-2 cell adherence assay to detect diarrheagenic Escherichia coli. J Infect Dis. 1988 Jul;158(1):224–228. doi: 10.1093/infdis/158.1.224. [DOI] [PubMed] [Google Scholar]
  15. Maas R. An improved colony hybridization method with significantly increased sensitivity for detection of single genes. Plasmid. 1983 Nov;10(3):296–298. doi: 10.1016/0147-619x(83)90045-8. [DOI] [PubMed] [Google Scholar]
  16. Makino S., Sasakawa C., Yoshikawa M. Genetic relatedness of the basic replicon of the virulence plasmid in shigellae and enteroinvasive Escherichia coli. Microb Pathog. 1988 Oct;5(4):267–274. doi: 10.1016/0882-4010(88)90099-x. [DOI] [PubMed] [Google Scholar]
  17. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Marques L. R., Moore M. A., Wells J. G., Wachsmuth I. K., O'Brien A. D. Production of Shiga-like toxin by Escherichia coli. J Infect Dis. 1986 Aug;154(2):338–341. doi: 10.1093/infdis/154.2.338. [DOI] [PubMed] [Google Scholar]
  19. Newland J. W., Neill R. J. DNA probes for Shiga-like toxins I and II and for toxin-converting bacteriophages. J Clin Microbiol. 1988 Jul;26(7):1292–1297. doi: 10.1128/jcm.26.7.1292-1297.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. O'Brien A. D., LaVeck G. D., Thompson M. R., Formal S. B. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli. J Infect Dis. 1982 Dec;146(6):763–769. doi: 10.1093/infdis/146.6.763. [DOI] [PubMed] [Google Scholar]
  21. O'Brien A. D., Marques L. R., Kerry C. F., Newland J. W., Holmes R. K. Shiga-like toxin converting phage of enterohemorrhagic Escherichia coli strain 933. Microb Pathog. 1989 May;6(5):381–390. doi: 10.1016/0882-4010(89)90080-6. [DOI] [PubMed] [Google Scholar]
  22. Prado D., Cleary T. G., Pickering L. K., Ericsson C. D., Bartlett A. V., 3rd, DuPont H. L., Johnson P. C. The relation between production of cytotoxin and clinical features in shigellosis. J Infect Dis. 1986 Jul;154(1):149–155. doi: 10.1093/infdis/154.1.149. [DOI] [PubMed] [Google Scholar]
  23. Pál T., Formal S. B., Hale T. L. Characterization of virulence marker antigen of Shigella spp. and enteroinvasive Escherichia coli. J Clin Microbiol. 1989 Mar;27(3):561–563. doi: 10.1128/jcm.27.3.561-563.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. SERENY B. Experimental shigella keratoconjunctivitis; a preliminary report. Acta Microbiol Acad Sci Hung. 1955;2(3):293–296. [PubMed] [Google Scholar]
  25. Snyder J. D., Wells J. G., Yashuk J., Puhr N., Blake P. A. Outbreak of invasive Escherichia coli gastroenteritis on a cruise ship. Am J Trop Med Hyg. 1984 Mar;33(2):281–284. doi: 10.4269/ajtmh.1984.33.281. [DOI] [PubMed] [Google Scholar]
  26. Taylor D. N., Echeverria P., Pál T., Sethabutr O., Saiborisuth S., Sricharmorn S., Rowe B., Cross J. The role of Shigella spp., enteroinvasive Escherichia coli, and other enteropathogens as causes of childhood dysentery in Thailand. J Infect Dis. 1986 Jun;153(6):1132–1138. doi: 10.1093/infdis/153.6.1132. [DOI] [PubMed] [Google Scholar]
  27. Taylor D. N., Echeverria P., Sethabutr O., Pitarangsi C., Leksomboon U., Blacklow N. R., Rowe B., Gross R., Cross J. Clinical and microbiologic features of Shigella and enteroinvasive Escherichia coli infections detected by DNA hybridization. J Clin Microbiol. 1988 Jul;26(7):1362–1366. doi: 10.1128/jcm.26.7.1362-1366.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tulloch E. F., Jr, Ryan K. J., Formal S. B., Franklin F. A. Invasive enteropathic Escherichia coli dysentery. An outbreak in 28 adults. Ann Intern Med. 1973 Jul;79(1):13–17. doi: 10.7326/0003-4819-79-1-13. [DOI] [PubMed] [Google Scholar]
  29. Venkatesan M. M., Buysse J. M., Kopecko D. J. Characterization of invasion plasmid antigen genes (ipaBCD) from Shigella flexneri. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9317–9321. doi: 10.1073/pnas.85.23.9317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wood P. K., Morris J. G., Jr, Small P. L., Sethabutr O., Toledo M. R., Trabulsi L., Kaper J. B. Comparison of DNA probes and the Sereny test for identification of invasive Shigella and Escherichia coli strains. J Clin Microbiol. 1986 Sep;24(3):498–500. doi: 10.1128/jcm.24.3.498-500.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES