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. 1983 Feb;39(2):889–897. doi: 10.1128/iai.39.2.889-897.1983

Colonization factor antigens I and II and type 1 somatic pili in enterotoxigenic Escherichia coli: relation to enterotoxin type.

M M Levine, P Ristaino, R B Sack, J B Kaper, F Orskov, I Orskov
PMCID: PMC348031  PMID: 6131869

Abstract

Enterotoxigenic Escherichia coli (ETEC) isolates from 36 persons with acute traveler's diarrhea from whom no other pathogens were recovered were tested (after no more than three subcultures) for the presence of colonization factor antigens I and II (CFA/I and CFA/II) and type 1 somatic pili. CFA/I or CFA/II was identified in 7 of 10 strains with heat-labile and heat-stable enterotoxins (LT+/ST+), but in only 2 of 12 LT-/ST+ (P less than 0.05) and 0 of 14 LT+/ST- (P less than 0.02) strains. CFA pili were not found among 74 non-enterotoxigenic E. coli strains. Type 1 somatic pili were demonstrable in 42% of the 36 ETEC and in 49% of the 74 non-enterotoxigenic E. coli isolates. The nine ETEC isolates bearing a CFA were serially subcultured on 10 consecutive days and retested for CFA and toxin. After five subcultures only one strain had lost a CFA, but after 10 passages three strains were negative: two lost CFA/I and one lost CFA/II. The strain that lost CFA/II became negative for both LT and ST as well and was found to lack a 48- and a 60-megadalton plasmid. The two strains that lost CFA/I also became negative for ST, but plasmid analysis revealed no plasmid loss. Disappearance of the CFA/I phenotype without loss of a plasmid can be explained by phase variation, as exhibited by type 1 somatic pili, or by rearrangement of base sequences in the CFA/I plasmid genome. If purified pili vaccines are to provide broad-spectrum protection against ETEC diarrhea, the search must be intensified to identify the antigens responsible for adhesion to intestinal mucosa in the many ETEC strains that lack CFA/I and CFA/II.

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Selected References

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  1. Acres S. D., Isaacson R. E., Babiuk L. A., Kapitany R. A. Immunization of calves against enterotoxigenic colibacillosis by vaccinating dams with purified K99 antigen and whole cell bacterins. Infect Immun. 1979 Jul;25(1):121–126. doi: 10.1128/iai.25.1.121-126.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burrows M. R., Sellwood R., Gibbons R. A. Haemagglutinating and adhesive properties associated with the K99 antigen of bovine strains of Escherichia coli. J Gen Microbiol. 1976 Oct;96(2):269–275. doi: 10.1099/00221287-96-2-269. [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. G., Evans D. J., Jr New surface-associated heat-labile colonization factor antigen (CFA/II) produced by enterotoxigenic Escherichia coli of serogroups O6 and O8. Infect Immun. 1978 Aug;21(2):638–647. doi: 10.1128/iai.21.2.638-647.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Evans D. G., Evans D. J., Jr, Tjoa W. S., DuPont H. L. Detection and characterization of colonization factor of enterotoxigenic Escherichia coli isolated from adults with diarrhea. Infect Immun. 1978 Feb;19(2):727–736. doi: 10.1128/iai.19.2.727-736.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Evans D. G., Evans D. J., Jr, Tjoa W. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun. 1977 Nov;18(2):330–337. doi: 10.1128/iai.18.2.330-337.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Evans D. G., Silver R. P., Evans D. J., Jr, Chase D. G., Gorbach S. L. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect Immun. 1975 Sep;12(3):656–667. doi: 10.1128/iai.12.3.656-667.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gorbach S. L., Kean B. H., Evans D. G., Evans D. J., Jr, Bessudo D. Travelers' diarrhea and toxigenic Escherichia coli. N Engl J Med. 1975 May 1;292(18):933–936. doi: 10.1056/NEJM197505012921801. [DOI] [PubMed] [Google Scholar]
  10. Isaacson R. E., Fusco P. C., Brinton C. C., Moon H. W. In vitro adhesion of Escherichia coli to porcine small intestinal epithelial cells: pili as adhesive factors. Infect Immun. 1978 Aug;21(2):392–397. doi: 10.1128/iai.21.2.392-397.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jones G. W., Rutter J. M. Role of the K88 antigen in the pathogenesis of neonatal diarrhea caused by Escherichia coli in piglets. Infect Immun. 1972 Dec;6(6):918–927. doi: 10.1128/iai.6.6.918-927.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones G. W., Rutter J. M. The association of K88 antigen with haemagglutinating activity in porcine strains of Escherichia coli. J Gen Microbiol. 1974 Sep;84(1):135–144. doi: 10.1099/00221287-84-1-135. [DOI] [PubMed] [Google Scholar]
  13. Levine M. M., Rennels M. B., Daya V., Hughes T. P. Hemagglutination and colonization factors in enterotoxigenic and enteropathogenic Escherichia coli that cause diarrhea. J Infect Dis. 1980 Jun;141(6):733–737. doi: 10.1093/infdis/141.6.733. [DOI] [PubMed] [Google Scholar]
  14. McConnell M. M., Smith H. R., Willshaw G. A., Field A. M., Rowe B. Plasmids coding for colonization factor antigen I and heat-stable enterotoxin production isolated from enterotoxigenic Escherichia coli: comparison of their properties. Infect Immun. 1981 May;32(2):927–936. doi: 10.1128/iai.32.2.927-936.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Merson M. H., Morris G. K., Sack D. A., Wells J. G., Feeley J. C., Sack R. B., Creech W. B., Kapikian A. Z., Gangarosa E. J. Travelers' diarrhea in Mexico. A prospective study of physicians and family members attending a congress. N Engl J Med. 1976 Jun 10;294(24):1299–1305. doi: 10.1056/NEJM197606102942401. [DOI] [PubMed] [Google Scholar]
  16. Meyers J. A., Sanchez D., Elwell L. P., Falkow S. Simple agarose gel electrophoretic method for the identification and characterization of plasmid deoxyribonucleic acid. J Bacteriol. 1976 Sep;127(3):1529–1537. doi: 10.1128/jb.127.3.1529-1537.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Moon H. W., Nagy B., Isaacson R. E., Orskov I. Occurrence of K99 antigen on Escherichia coli isolated from pigs and colonization of pig ileum by K99+ enterotoxigenic E. coli from calves and pigs. Infect Immun. 1977 Feb;15(2):614–620. doi: 10.1128/iai.15.2.614-620.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Morgan R. L., Isaacson R. E., Moon H. W., Brinton C. C., To C. C. Immunization of suckling pigs against enterotoxigenic Escherichia coli-induced diarrheal disease by vaccinating dams with purified 987 or K99 pili: protection correlates with pilus homology of vaccine and challenge. Infect Immun. 1978 Dec;22(3):771–777. doi: 10.1128/iai.22.3.771-777.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Moseley S. L., Huq I., Alim A. R., So M., Samadpour-Motalebi M., Falkow S. Detection of enterotoxigenic Escherichia coli by DNA colony hybridization. J Infect Dis. 1980 Dec;142(6):892–898. doi: 10.1093/infdis/142.6.892. [DOI] [PubMed] [Google Scholar]
  20. Nagy B., Moon H. W., Isaacson R. E. Colonization of porcine intestine by enterotoxigenic Escherichia coli: selection of piliated forms in vivo, adhesion of piliated forms to epithelial cells in vitro, and incidence of a pilus antigen among porcine enteropathogenic E. coli. Infect Immun. 1977 Apr;16(1):344–352. doi: 10.1128/iai.16.1.344-352.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nagy B., Moon H. W., Isaacson R. E., To C. C., Brinton C. C. Immunization of suckling pigs against enteric enterotoxigenic Escherichia coli infection by vaccinating dams with purified pili. Infect Immun. 1978 Jul;21(1):269–274. doi: 10.1128/iai.21.1.269-274.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Old D. C. Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. J Gen Microbiol. 1972 Jun;71(1):149–157. doi: 10.1099/00221287-71-1-149. [DOI] [PubMed] [Google Scholar]
  23. Orskov F., Orskov I. Escherichia coli O:H serotypes isolated from human blood. Prevalence of the K1 antigen with technical details of O and H antigenic determination. Acta Pathol Microbiol Scand Suppl. 1975 Dec;83(6):595–600. [PubMed] [Google Scholar]
  24. Orskov I., Orskov F. Special O:K:H serotypes among enterotoxigenic E. coli strains from diarrhea in adults and children. Occurrence of the CF (colonization factor) antigen and of hemagglutinating abilities. Med Microbiol Immunol. 1977 Jul 18;163(2):99–110. doi: 10.1007/BF02121825. [DOI] [PubMed] [Google Scholar]
  25. Reis M. H., Heloiza M., Affonso T., Trabulsi L. R., Mazaitis A. J., Maas R., Maas W. K. Transfer of a CFA/I-ST plasmid promoted by a conjugative plasmid in a strain of Escherichia coli of serotype O128ac:H12. Infect Immun. 1980 Jul;29(1):140–143. doi: 10.1128/iai.29.1.140-143.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Reis M. H., Matos D. P., de Castro A. F., Toledo M. R., Trabulsi L. R. Relationship among enterotoxigenic phenotypes, serotypes, and sources of strains in enterotoxigenic Escherichia coli. Infect Immun. 1980 Apr;28(1):24–27. doi: 10.1128/iai.28.1.24-27.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rutter J. M., Jones G. W. Protection against enteric disease caused by Escherichia coli--a model for vaccination with a virulence determinant? Nature. 1973 Apr 20;242(5399):531–532. doi: 10.1038/242531a0. [DOI] [PubMed] [Google Scholar]
  28. Sack D. A., Kaminsky D. C., Sack R. B., Itotia J. N., Arthur R. R., Kapikian A. Z., Orskov F., Orskov I. Prophylactic doxycycline for travelers' diarrhea. Results of a prospective double-blind study of Peace Corps volunteers in Kenya. N Engl J Med. 1978 Apr 6;298(14):758–763. doi: 10.1056/NEJM197804062981402. [DOI] [PubMed] [Google Scholar]
  29. Sack D. A., Sack R. B. Test for enterotoxigenic Escherichia coli using Y-1 adrenal cells in miniculture. Infect Immun. 1975 Feb;11(2):334–336. doi: 10.1128/iai.11.2.334-336.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sack R. B., Froehlich J. L., Zulich A. W., Hidi D. S., Kapikian A. Z., Orskov F., Orskov I., Greenberg H. B. Prophylactic doxycycline for travelers' diarrhea: results of a prospective double-blind study of Peace Corps volunteers in Morocco. Gastroenterology. 1979 Jun;76(6):1368–1373. [PubMed] [Google Scholar]
  31. Salit I. E., Gotschlich E. C. Hemagglutination by purified type I Escherichia coli pili. J Exp Med. 1977 Nov 1;146(5):1169–1181. doi: 10.1084/jem.146.5.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith H. R., Willshaw G. A., Rowe B. Mapping of a plasmid, coding for colonization, factor antigen I and heat-stable enterotoxin production, isolated from an enterotoxigenic strain of Escherichia coli. J Bacteriol. 1982 Jan;149(1):264–275. doi: 10.1128/jb.149.1.264-275.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Smith H. W., Linggood M. A. Further observations on Escherichia coli enterotoxins with particular regard to those produced by atypical piglet strains and by calf and lamb strains: the transmissible nature of these enterotoxins and of a K antigen possessed by calf and lamb strains. J Med Microbiol. 1972 May;5(2):243–250. doi: 10.1099/00222615-5-2-243. [DOI] [PubMed] [Google Scholar]
  34. Smith H. W., Linggood M. A. Observations on the pathogenic properties of the K88, Hly and Ent plasmids of Escherichia coli with particular reference to porcine diarrhoea. J Med Microbiol. 1971 Nov;4(4):467–485. doi: 10.1099/00222615-4-4-467. [DOI] [PubMed] [Google Scholar]
  35. So M., Heffron F., McCarthy B. J. The E. coli gene encoding heat stable toxin is a bacterial transposon flanked by inverted repeats of IS1. Nature. 1979 Feb 8;277(5696):453–456. doi: 10.1038/277453a0. [DOI] [PubMed] [Google Scholar]
  36. Swaney L. M., Liu Y. P., To C. M., To C. C., Ippen-Ihler K., Brinton C. C., Jr Isolation and characterization of Escherichia coli phase variants and mutants deficient in type 1 pilus production. J Bacteriol. 1977 Apr;130(1):495–505. doi: 10.1128/jb.130.1.495-505.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thomas L. V., Cravioto A., Scotland S. M., Rowe B. New fimbrial antigenic type (E8775) that may represent a colonization factor in enterotoxigenic Escherichia coli in humans. Infect Immun. 1982 Mar;35(3):1119–1124. doi: 10.1128/iai.35.3.1119-1124.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]

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