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. 1997 Jul;4(4):429–434. doi: 10.1128/cdli.4.4.429-434.1997

Immune response to the mannose-sensitive hemagglutinin in patients with cholera due to Vibrio cholerae O1 and O0139.

F Qadri 1, G Jonson 1, Y A Begum 1, C Wennerås 1, M J Albert 1, M A Salam 1, A M Svennerholm 1
PMCID: PMC170545  PMID: 9220159

Abstract

The mannose-sensitive hemagglutinin (MSHA) is a type 4 pilus present in Vibrio cholerae O1 strains of the El Tor biotype, as well as in strains of serogroup O139. It has been shown to be a colonization antigen in animal models. The aim of this study was to investigate systemic and local antibody responses to MSHA in adult patients with cholera due to V. cholerae O1 and O139. Twenty-four of 28 (86%) patients with O1 cholera and 11 of 17 (65%) patients with O139 cholera showed significant increases in MSHA-specific immunoglobulin A (IgA) and IgM antibody-secreting cells (ASCs) 7 days after the onset of disease. However, the magnitude of the ASC response in O1 cholera patients was significantly higher than that in the O139 cholera patients in both IgA-producing (P = 0.015) and IgM-producing (P = 0.029) cells. Both groups of patients responded with antibody responses to MSHA in plasma, seroconverting with both IgA (63 to 70% of patients) and IgG (43 to 59% of patients) antibodies. Compared to the MSHA-specific antibody levels determined in healthy controls (n = 10), more than 90% of O1 and O139 cholera patients showed responses to MSHA of both the IgA and the IgG isotypes. About 70% of the patients in both groups also had antibody responses to MSHA in their feces. In summary, we demonstrated that MSHA is immunogenic, giving rise to both systemic and local antibodies in patients with cholera due to both O1 and O139 serogroups.

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Selected References

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  1. Ahrén C., Wennerås C., Holmgren J., Svennerholm A. M. Intestinal antibody response after oral immunization with a prototype cholera B subunit-colonization factor antigen enterotoxigenic Escherichia coli vaccine. Vaccine. 1993;11(9):929–934. doi: 10.1016/0264-410x(93)90380-g. [DOI] [PubMed] [Google Scholar]
  2. Albert M. J., Siddique A. K., Islam M. S., Faruque A. S., Ansaruzzaman M., Faruque S. M., Sack R. B. Large outbreak of clinical cholera due to Vibrio cholerae non-O1 in Bangladesh. Lancet. 1993 Mar 13;341(8846):704–704. doi: 10.1016/0140-6736(93)90481-u. [DOI] [PubMed] [Google Scholar]
  3. Albert M. J. Vibrio cholerae O139 Bengal. J Clin Microbiol. 1994 Oct;32(10):2345–2349. doi: 10.1128/jcm.32.10.2345-2349.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Attridge S. R., Manning P. A., Holmgren J., Jonson G. Relative significance of mannose-sensitive hemagglutinin and toxin-coregulated pili in colonization of infant mice by Vibrio cholerae El Tor. Infect Immun. 1996 Aug;64(8):3369–3373. doi: 10.1128/iai.64.8.3369-3373.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. BENENSON A. S., ISLAM M. R., GREENOUGH W. B., 3rd RAPID IDENTIFICATION OF VIBRIO CHOLERAE BY DARKFIELD MICROSCOPY. Bull World Health Organ. 1964;30:827–831. [PMC free article] [PubMed] [Google Scholar]
  6. Czerkinsky C., Moldoveanu Z., Mestecky J., Nilsson L. A., Ouchterlony O. A novel two colour ELISPOT assay. I. Simultaneous detection of distinct types of antibody-secreting cells. J Immunol Methods. 1988 Nov 25;115(1):31–37. doi: 10.1016/0022-1759(88)90306-7. [DOI] [PubMed] [Google Scholar]
  7. Ferguson A., Humphreys K. A., Croft N. M. Technical report: results of immunological tests on faecal extracts are likely to be extremely misleading. Clin Exp Immunol. 1995 Jan;99(1):70–75. doi: 10.1111/j.1365-2249.1995.tb03474.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Franzon V. L., Barker A., Manning P. A. Nucleotide sequence encoding the mannose-fucose-resistant hemagglutinin of Vibrio cholerae O1 and construction of a mutant. Infect Immun. 1993 Jul;61(7):3032–3037. doi: 10.1128/iai.61.7.3032-3037.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jertborn M., Svennerholm A. M., Holmgren J. Saliva, breast milk, and serum antibody responses as indirect measures of intestinal immunity after oral cholera vaccination or natural disease. J Clin Microbiol. 1986 Aug;24(2):203–209. doi: 10.1128/jcm.24.2.203-209.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jonson G., Holmgren J., Svennerholm A. M. Identification of a mannose-binding pilus on Vibrio cholerae El Tor. Microb Pathog. 1991 Dec;11(6):433–441. doi: 10.1016/0882-4010(91)90039-d. [DOI] [PubMed] [Google Scholar]
  11. Jonson G., Lebens M., Holmgren J. Cloning and sequencing of Vibrio cholerae mannose-sensitive haemagglutinin pilin gene: localization of mshA within a cluster of type 4 pilin genes. Mol Microbiol. 1994 Jul;13(1):109–118. doi: 10.1111/j.1365-2958.1994.tb00406.x. [DOI] [PubMed] [Google Scholar]
  12. Jonson G., Osek J., Svennerholm A. M., Holmgren J. Immune mechanisms and protective antigens of Vibrio cholerae serogroup O139 as a basis for vaccine development. Infect Immun. 1996 Sep;64(9):3778–3785. doi: 10.1128/iai.64.9.3778-3785.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jonson G., Sanchez J., Svennerholm A. M. Expression and detection of different biotype-associated cell-bound haemagglutinins of Vibrio cholerae O1. J Gen Microbiol. 1989 Jan;135(1):111–120. doi: 10.1099/00221287-135-1-111. [DOI] [PubMed] [Google Scholar]
  14. Kantele A. M., Takanen R., Arvilommi H. Immune response to acute diarrhea seen as circulating antibody-secreting cells. J Infect Dis. 1988 Nov;158(5):1011–1016. doi: 10.1093/infdis/158.5.1011. [DOI] [PubMed] [Google Scholar]
  15. MONSUR K. A. A highly selective gelatin-taurocholate-tellurite medium for the isolation of Vibrio cholerae. Trans R Soc Trop Med Hyg. 1961 Sep;55:440–442. doi: 10.1016/0035-9203(61)90090-6. [DOI] [PubMed] [Google Scholar]
  16. Mukhopadhyay S., Ghosh C., Ghose A. C. Phenotypic expression of a mannose-sensitive hemagglutinin by a Vibrio cholerae O1 E1Tor strain and evaluation of its role in intestinal adherence and colonization. FEMS Microbiol Lett. 1996 May 1;138(2-3):227–232. doi: 10.1111/j.1574-6968.1996.tb08162.x. [DOI] [PubMed] [Google Scholar]
  17. Nandy R. K., Sengupta T. K., Mukhopadhyay S., Ghose A. C. A comparative study of the properties of Vibrio cholerae O139, O1 and other non-O1 strains. J Med Microbiol. 1995 Apr;42(4):251–257. doi: 10.1099/00222615-42-4-251. [DOI] [PubMed] [Google Scholar]
  18. Osek J., Jonson G., Svennerholm A. M., Holmgren J. Role of antibodies against biotype-specific Vibrio cholerae pili in protection against experimental classical and El Tor cholera. Infect Immun. 1994 Jul;62(7):2901–2907. doi: 10.1128/iai.62.7.2901-2907.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Osek J., Svennerholm A. M., Holmgren J. Protection against Vibrio cholerae El Tor infection by specific antibodies against mannose-binding hemagglutinin pili. Infect Immun. 1992 Nov;60(11):4961–4964. doi: 10.1128/iai.60.11.4961-4964.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Qadri F., Azim T., Chowdhury A., Hossain J., Sack R. B., Albert M. J. Production, characterization, and application of monoclonal antibodies to Vibrio cholerae O139 synonym Bengal. Clin Diagn Lab Immunol. 1994 Jan;1(1):51–54. doi: 10.1128/cdli.1.1.51-54.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Qadri F., Mohi G., Hossain J., Azim T., Khan A. M., Salam M. A., Sack R. B., Albert M. J., Svennerholm A. M. Comparison of the vibriocidal antibody response in cholera due to Vibrio cholerae O139 Bengal with the response in cholera due to Vibrio cholerae O1. Clin Diagn Lab Immunol. 1995 Nov;2(6):685–688. doi: 10.1128/cdli.2.6.685-688.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Quiding M., Nordström I., Kilander A., Andersson G., Hanson L. A., Holmgren J., Czerkinsky C. Intestinal immune responses in humans. Oral cholera vaccination induces strong intestinal antibody responses and interferon-gamma production and evokes local immunological memory. J Clin Invest. 1991 Jul;88(1):143–148. doi: 10.1172/JCI115270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rahman M., Sack D. A., Mahmood S., Hossain A. Rapid diagnosis of cholera by coagglutination test using 4-h fecal enrichment cultures. J Clin Microbiol. 1987 Nov;25(11):2204–2206. doi: 10.1128/jcm.25.11.2204-2206.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sack R. B., Albert M. J. Summary of cholera vaccine workshop. J Diarrhoeal Dis Res. 1994 Jun;12(2):138–143. [PubMed] [Google Scholar]
  25. Stoll B. J., Svennerholm A. M., Gothefors L., Barua D., Huda S., Holmgren J. Local and systemic antibody responses to naturally acquired enterotoxigenic Escherichia coli diarrhea in an endemic area. J Infect Dis. 1986 Mar;153(3):527–534. doi: 10.1093/infdis/153.3.527. [DOI] [PubMed] [Google Scholar]
  26. Svennerholm A. M., Jertborn M., Gothefors L., Karim A. M., Sack D. A., Holmgren J. Mucosal antitoxic and antibacterial immunity after cholera disease and after immunization with a combined B subunit-whole cell vaccine. J Infect Dis. 1984 Jun;149(6):884–893. doi: 10.1093/infdis/149.6.884. [DOI] [PubMed] [Google Scholar]
  27. Svennerholm A. M., Johnson G., Yan C. A method for studies of an El Tor-associated antigen of Vibrio cholerae O1. FEMS Microbiol Lett. 1991 Apr 15;63(2-3):179–185. doi: 10.1016/0378-1097(91)90082-l. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Thelin K. H., Taylor R. K. Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect Immun. 1996 Jul;64(7):2853–2856. doi: 10.1128/iai.64.7.2853-2856.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Voss E., Manning P. A., Attridge S. R. The toxin-coregulated pilus is a colonization factor and protective antigen of Vibrio cholerae El Tor. Microb Pathog. 1996 Mar;20(3):141–153. doi: 10.1006/mpat.1996.0013. [DOI] [PubMed] [Google Scholar]
  31. Wennerås C., Svennerholm A. M., Ahrén C., Czerkinsky C. Antibody-secreting cells in human peripheral blood after oral immunization with an inactivated enterotoxigenic Escherichia coli vaccine. Infect Immun. 1992 Jul;60(7):2605–2611. doi: 10.1128/iai.60.7.2605-2611.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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