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. 1991 Dec;59(12):4473–4477. doi: 10.1128/iai.59.12.4473-4477.1991

Blocking of fimbria-mediated adherence of Haemophilus influenzae by sialyl gangliosides.

L van Alphen 1, L Geelen-van den Broek 1, L Blaas 1, M van Ham 1, J Dankert 1
PMCID: PMC259065  PMID: 1682262

Abstract

The structure of the receptor for the fimbriae of Haemophilus influenzae on human oropharyngeal epithelial cells and erythrocytes was determined in inhibition experiments with various sugars, glycolipids, and glycoproteins. Of 30 monosaccharides and disaccharides at a concentration of 0.1 M and of 3 polysaccharides at a concentration of 1 mg/ml, none inhibited fimbria-specific adherence and hemagglutination. Inhibition was obtained with gangliosides GM1, GM2, GM3, and GD1a in nanomolar concentrations, whereas the asialo derivative of GM1, sialyl-lactose, and sialoglycoproteins were poor inhibitors. These findings indicate that sialyl-lactosylceramide (GM3) is the minimal structure for the fimbria-dependent binding of H. influenzae to its receptor on oropharyngeal epithelial cells and erythrocytes. As is the case with GM2, substitution of GM3 with N-acetylgalactosamine makes the molecule a 10-fold-better receptor analog.

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Selected References

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

  1. Aniansson G., Andersson B., Lindstedt R., Svanborg C. Anti-adhesive activity of human casein against Streptococcus pneumoniae and Haemophilus influenzae. Microb Pathog. 1990 May;8(5):315–323. doi: 10.1016/0882-4010(90)90090-d. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Crook S. J., Boggs J. M., Vistnes A. I., Koshy K. M. Factors affecting surface expression of glycolipids: influence of lipid environment and ceramide composition on antibody recognition of cerebroside sulfate in liposomes. Biochemistry. 1986 Nov 18;25(23):7488–7494. doi: 10.1021/bi00371a035. [DOI] [PubMed] [Google Scholar]
  4. Evans D. G., Evans D. J., Jr, Moulds J. J., Graham D. Y. N-acetylneuraminyllactose-binding fibrillar hemagglutinin of Campylobacter pylori: a putative colonization factor antigen. Infect Immun. 1988 Nov;56(11):2896–2906. doi: 10.1128/iai.56.11.2896-2906.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Guerina N. G., Langermann S., Clegg H. W., Kessler T. W., Goldman D. A., Gilsdorf J. R. Adherence of piliated Haemophilus influenzae type b to human oropharyngeal cells. J Infect Dis. 1982 Oct;146(4):564–564. doi: 10.1093/infdis/146.4.564. [DOI] [PubMed] [Google Scholar]
  6. Karlsson K. A. Animal glycosphingolipids as membrane attachment sites for bacteria. Annu Rev Biochem. 1989;58:309–350. doi: 10.1146/annurev.bi.58.070189.001521. [DOI] [PubMed] [Google Scholar]
  7. Korhonen T. K., Väisänen-Rhen V., Rhen M., Pere A., Parkkinen J., Finne J. Escherichia coli fimbriae recognizing sialyl galactosides. J Bacteriol. 1984 Aug;159(2):762–766. doi: 10.1128/jb.159.2.762-766.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Krivan H. C., Roberts D. D., Ginsburg V. Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc beta 1-4Gal found in some glycolipids. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6157–6161. doi: 10.1073/pnas.85.16.6157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Loeb M. R., Connor E., Penney D. A comparison of the adherence of fimbriated and nonfimbriated Haemophilus influenzae type b to human adenoids in organ culture. Infect Immun. 1988 Feb;56(2):484–489. doi: 10.1128/iai.56.2.484-489.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mason E. O., Jr, Kaplan S. L., Wiedermann B. L., Norrod E. P., Stenback W. A. Frequency and properties of naturally occurring adherent piliated strains of Haemophilus influenzae type b. Infect Immun. 1985 Jul;49(1):98–103. doi: 10.1128/iai.49.1.98-103.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Parkkinen J., Korhonen T. K., Pere A., Hacker J., Soinila S. Binding sites in the rat brain for Escherichia coli S fimbriae associated with neonatal meningitis. J Clin Invest. 1988 Mar;81(3):860–865. doi: 10.1172/JCI113395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Pichichero M. E. Adherence of Haemophilus influenzae to human buccal and pharyngeal epithelial cells: relationship to pilation. J Med Microbiol. 1984 Aug;18(1):107–116. doi: 10.1099/00222615-18-1-107. [DOI] [PubMed] [Google Scholar]
  13. Pichichero M. E., Loeb M., Anderson, Smith D. H. Do pili play a role in pathogenicity of Haemophilus influenzae type B? Lancet. 1982 Oct 30;2(8305):960–962. doi: 10.1016/s0140-6736(82)90161-1. [DOI] [PubMed] [Google Scholar]
  14. Poole J., Van Alphen L. Haemophilus influenzae receptor and the AnWj antigen. Transfusion. 1988 May-Jun;28(3):289–289. doi: 10.1046/j.1537-2995.1988.28388219164.x. [DOI] [PubMed] [Google Scholar]
  15. Sable N. S., Connor E. M., Hall C. B., Loeb M. R. Variable adherence of fimbriated Haemophilus influenzae type b to human cells. Infect Immun. 1985 Apr;48(1):119–123. doi: 10.1128/iai.48.1.119-123.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Skarjune R., Oldfield E. Physical studies of cell surface and cell membrane structure. Deuterium nuclear magnetic resonance studies of N-palmitoylglucosylceramide (cerebroside) head group structure. Biochemistry. 1982 Jun 22;21(13):3154–3160. doi: 10.1021/bi00256a019. [DOI] [PubMed] [Google Scholar]
  17. Smith D. F., Zopf D. A., Ginsburg V. Fractionation of sialyl oligosaccharides of human milk by ion-exchange chromatography. Anal Biochem. 1978 Apr;85(2):602–608. doi: 10.1016/0003-2697(78)90261-0. [DOI] [PubMed] [Google Scholar]
  18. Sterk L. M., Van Alphen L., Geelen-van den Broek L., Houthoff H. J., Dankert J. Differential binding of Haemophilus influenzae to human tissues by fimbriae. J Med Microbiol. 1991 Sep;35(3):129–138. doi: 10.1099/00222615-35-3-129. [DOI] [PubMed] [Google Scholar]
  19. Strömberg N., Ryd M., Lindberg A. A., Karlsson K. A. Studies on the binding of bacteria to glycolipids. Two species of Propionibacterium apparently recognize separate epitopes on lactose of lactosylceramide. FEBS Lett. 1988 May 9;232(1):193–198. doi: 10.1016/0014-5793(88)80415-0. [DOI] [PubMed] [Google Scholar]
  20. Stull T. L., Mendelman P. M., Haas J. E., Schoenborn M. A., Mack K. D., Smith A. L. Characterization of Haemophilus influenzae type b fimbriae. Infect Immun. 1984 Dec;46(3):787–796. doi: 10.1128/iai.46.3.787-796.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Takala A. K., van Alphen L., Eskola J., Palmgren J., Bol P., Mäkelä P. H. Haemophilus influenzae type b strains of outer membrane subtypes 1 and 1c cause different types of invasive disease. Lancet. 1987 Sep 19;2(8560):647–650. doi: 10.1016/s0140-6736(87)92440-8. [DOI] [PubMed] [Google Scholar]
  22. Turk D. C. The pathogenicity of Haemophilus influenzae. J Med Microbiol. 1984 Aug;18(1):1–16. doi: 10.1099/00222615-18-1-1. [DOI] [PubMed] [Google Scholar]
  23. van Alphen L., Levene C., Geelen-van den Broek L., Poole J., Bennett M., Dankert J. Combined inheritance of epithelial and erythrocyte receptors for Haemophilus influenzae. Infect Immun. 1990 Nov;58(11):3807–3809. doi: 10.1128/iai.58.11.3807-3809.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. van Alphen L., Poole J., Geelen L., Zanen H. C. The erythrocyte and epithelial cell receptors for Haemophilus influenzae are expressed independently. Infect Immun. 1987 Oct;55(10):2355–2358. doi: 10.1128/iai.55.10.2355-2358.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. van Alphen L., Riemens T., Poolman J., Hopman C., Zanen H. C. Homogeneity of cell envelope protein subtypes, lipopolysaccharide serotypes, and biotypes among Haemophilus influenzae type b from patients with meningitis in The Netherlands. J Infect Dis. 1983 Jul;148(1):75–81. doi: 10.1093/infdis/148.1.75. [DOI] [PubMed] [Google Scholar]
  26. van Ham S. M., Mooi F. R., Sindhunata M. G., Maris W. R., van Alphen L. Cloning and expression in Escherichia coli of Haemophilus influenzae fimbrial genes establishes adherence to oropharyngeal epithelial cells. EMBO J. 1989 Nov;8(11):3535–3540. doi: 10.1002/j.1460-2075.1989.tb08519.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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