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. 1988 Dec;56(12):3241–3250. doi: 10.1128/iai.56.12.3241-3250.1988

Vibrio cholerae O1 adherence to villi and lymphoid follicle epithelium: in vitro model using formalin-treated human small intestine and correlation between adherence and cell-associated hemagglutinin levels.

T Yamamoto 1, T Kamano 1, M Uchimura 1, M Iwanaga 1, T Yokota 1
PMCID: PMC259731  PMID: 2903129

Abstract

Formalin-fixed human small intestinal mucosa possessing villi and lymphoid follicle epithelium of Peyer's patches at the mucosal surface was used to test the adherence ability of clinically isolated strains of Vibrio cholerae O1. V. cholerae O1 grown on CFA agar for approximately 3 h at 37 degrees C had various levels of cellular hemagglutinins (HAs) and manifested adherence abilities that were roughly correlated with the cellular HA levels, irrespective of cellular HA types. V. cholerae O1 adhered better to epithelium over ileal lymphoid follicles than to epithelium of jejunal or ileal villi. Cells of different morphology which constituted lymphoid follicle epithelium were almost equal targets for adherence. In contrast, V. cholerae O1 grown on CFA agar for approximately 20 h at 37 degrees C in many cases had lower levels of cellular HAs and adherence abilities. Contrary to the above observations with cellular HAs and adherence, piliation of V. cholerae O1 was rather more extensive at approximately 20 h of incubation at 37 degrees C than at approximately 3 h of incubation at 37 degrees C. L-Fucose inhibited adherence to a varied extent depending on the cellular HA types, while D-mannose enhanced adherence in some strains. Heating of V. cholerae O1 diminished adherence ability. This adherence model system provides a tool by which various V. cholerae O1 strains can be preliminarily tested for adherence ability and site in human small intestine.

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Selected References

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

  1. Attridge S. R., Rowley D. The role of the flagellum in the adherence of Vibrio cholerae. J Infect Dis. 1983 May;147(5):864–872. doi: 10.1093/infdis/147.5.864. [DOI] [PubMed] [Google Scholar]
  2. BARUA D., MUKHERJEE A. C. DIRECT BACTERIAL HAEMAGGLUTINATION TEST FOR DIFFERENTIATING EL TOR VIBRIOS FROM V. CHOLERAE. Bull Calcutta Sch Trop Med. 1963 Jul;11:85–86. [PubMed] [Google Scholar]
  3. BARUA D., MUKHERJEE A. C. HAEMAGGLUTINATING ACTIVITY OF EL TOR VIBRIOS AND ITS NATURE. Indian J Med Res. 1965 May;53:399–404. [PubMed] [Google Scholar]
  4. Beachey E. H. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis. 1981 Mar;143(3):325–345. doi: 10.1093/infdis/143.3.325. [DOI] [PubMed] [Google Scholar]
  5. Bhattacharjee J. W., Srivastava B. S. Mannose-sensitive haemagglutinins in adherence of Vibrio cholerae eltor to intestine. J Gen Microbiol. 1978 Aug;107(2):407–410. doi: 10.1099/00221287-107-2-407. [DOI] [PubMed] [Google Scholar]
  6. Booth B. A., Finkelstein R. A. Presence of hemagglutinin/protease and other potential virulence factors in O1 and non-O1 Vibrio cholerae. J Infect Dis. 1986 Jul;154(1):183–186. doi: 10.1093/infdis/154.1.183. [DOI] [PubMed] [Google Scholar]
  7. Ehara M., Ishibashi M., Ichinose Y., Iwanaga M., Shimotori S., Naito T. Purification and partial characterization of fimbriae of Vibrio cholerae O1. Vaccine. 1987 Dec;5(4):283–288. doi: 10.1016/0264-410x(87)90153-8. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Finkelstein R. A., Boesman-Finkelstein M., Holt P. Vibrio cholerae hemagglutinin/lectin/protease hydrolyzes fibronectin and ovomucin: F.M. Burnet revisited. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1092–1095. doi: 10.1073/pnas.80.4.1092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hanne L. F., Finkelstein R. A. Characterization and distribution of the hemagglutinins produced by Vibrio cholerae. Infect Immun. 1982 Apr;36(1):209–214. doi: 10.1128/iai.36.1.209-214.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holmgren J., Svennerholm A. M., Lindblad M. Receptor-like glycocompounds in human milk that inhibit classical and El Tor Vibrio cholerae cell adherence (hemagglutination). Infect Immun. 1983 Jan;39(1):147–154. doi: 10.1128/iai.39.1.147-154.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones G. W., Abrams G. D., Freter R. Adhesive properties of Vibrio cholerae: adhesion to isolated rabbit brush border membranes and hemagglutinating activity. Infect Immun. 1976 Jul;14(1):232–239. doi: 10.1128/iai.14.1.232-239.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jones G. W., Freter R. Adhesive properties of Vibrio cholerae: nature of the interaction with isolated rabbit brush border membranes and human erythrocytes. Infect Immun. 1976 Jul;14(1):240–245. doi: 10.1128/iai.14.1.240-245.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kabir S., Ali S. Characterization of surface properties of Vibrio cholerae. Infect Immun. 1983 Mar;39(3):1048–1058. doi: 10.1128/iai.39.3.1048-1058.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Levine M. M., Kaper J. B., Black R. E., Clements M. L. New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development. Microbiol Rev. 1983 Dec;47(4):510–550. doi: 10.1128/mr.47.4.510-550.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Levine M. M., Kaper J. B., Herrington D., Losonsky G., Morris J. G., Clements M. L., Black R. E., Tall B., Hall R. Volunteer studies of deletion mutants of Vibrio cholerae O1 prepared by recombinant techniques. Infect Immun. 1988 Jan;56(1):161–167. doi: 10.1128/iai.56.1.161-167.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nakasone N., Iwanaga M. Quantitative evaluation of colonizing ability of Vibrio cholerae O1. Microbiol Immunol. 1987;31(8):753–761. doi: 10.1111/j.1348-0421.1987.tb03137.x. [DOI] [PubMed] [Google Scholar]
  18. Nelson E. T., Clements J. D., Finkelstein R. A. Vibrio cholerae adherence and colonization in experimental cholera: electron microscopic studies. Infect Immun. 1976 Aug;14(2):527–547. doi: 10.1128/iai.14.2.527-547.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Owen R. L., Jones A. L. Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology. 1974 Feb;66(2):189–203. [PubMed] [Google Scholar]
  20. Owen R. L., Pierce N. F., Apple R. T., Cray W. C., Jr M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis. 1986 Jun;153(6):1108–1118. doi: 10.1093/infdis/153.6.1108. [DOI] [PubMed] [Google Scholar]
  21. Owen R. L. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology. 1977 Mar;72(3):440–451. [PubMed] [Google Scholar]
  22. Pierce N. F., Cray W. C., Jr, Kaper J. B., Mekalanos J. J. Determinants of immunogenicity and mechanisms of protection by virulent and mutant Vibrio cholerae O1 in rabbits. Infect Immun. 1988 Jan;56(1):142–148. doi: 10.1128/iai.56.1.142-148.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pierce N. F., Kaper J. B., Mekalanos J. J., Cray W. C., Jr, Richardson K. Determinants of the immunogenicity of live virulent and mutant Vibrio cholerae O1 in rabbit intestine. Infect Immun. 1987 Feb;55(2):477–481. doi: 10.1128/iai.55.2.477-481.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Svennerholm A. M., Strömberg G. J., Holmgren J. Purification of Vibrio cholerae soluble hemagglutinin and development of enzyme-linked immunosorbent assays for antigen and antibody quantitations. Infect Immun. 1983 Jul;41(1):237–243. doi: 10.1128/iai.41.1.237-243.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Taylor R. K., Miller V. L., Furlong D. B., Mekalanos J. J. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci U S A. 1987 May;84(9):2833–2837. doi: 10.1073/pnas.84.9.2833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yamamoto T., Yokota T. Electron microscopic study of Vibrio cholerae O1 adherence to the mucus coat and villus surface in the human small intestine. Infect Immun. 1988 Oct;56(10):2753–2759. doi: 10.1128/iai.56.10.2753-2759.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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