Abstract
H. pylori is the major cause of human gastritis, duodenal ulcer and thus gastric adenocarcinoma. Many glycosphingolipid species have been postulated as receptors for H. pylori and it is likely that H. pylori attachment requires multiple, perhaps sequential receptor/ligand interactions. In this study, the binding of a number of H. pylori clinical isolates, as well as stock strains, to acid and neutral glycosphingolipids separated on thin-layer chromatograms was characterized under microaerobic conditions. All H. pylori clinical isolates, laboratory strains and type culture collection strains recognized galactosylceramide (Galβ1Cer) with ceramide containing sphingosine and hydroxylated fatty acid (type I), or non-hydroxylated fatty acid (type II), on thin-layer chromatograms and when incorporated into liposomes. The clinical isolates bound stronger to Galβ1Cer (type II) than Galβ1Cer (type I) on TLC, whereas lab and culture collection strains showed the opposite binding preference. A clear preference in binding to Galβ1Cer (type I) incorporated into liposome was shown by most tested strains. Clinical isolates bound well to glucosylceramide (Glcβ1Cer) with hydroxylated fatty acid, whereas weak binding to this glycolipid was detected with the lab and type collection strains. None of the tested strains bound Glcβ1Cer with non-hydroxylated fatty acid on the solid surface, but some strains of both clinical or type collection origins showed weak or very weak binding in the liposome assay. A clear distinction between the binding specificity of living organisms (under microaerobic conditions) as opposed to dying organisms (under normoxic conditions) illustrates the importance of cellular physiology in this process.
These studies illustrate lipid modulation of the potential receptor function of monohexosylceramides and the distinction between the receptor repertoire of H. pylori clinical isolates and cultured strains commonly used to study host-cell adhesion.
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References
Bode G, Malferthier P, Ditschuneit P, Kim Worchenscher 65, 144–6 (1987).
Price AB, J Gastroenterol Hepatol 6, 209–22 (1991).
Goodwin CS, Lancet ii, 1467–9 (1988).
Talley NJ, Zinseimer AR, Weaver A, Dimango EP, Carpenter HA, Pérez-Pérez GI, Blaser MJ, J Natl Cancer Inst 83, 1734–9 (1991).
Hussell T, Issacson PG, Crabtree JE, Spencer J, Lancet 342, 571–4 (1993).
Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, Issacson PG, Lancet 342, 575–7 (1993).
Evans DG, Evans DJ, Moulds JJ, Graham DY, Infect Immun 56, 2896–906 (1988).
Slomiany VL, Tiatrosky J, Samanta A, Van Horne K, Nurtey VLN, Slomiany A, Biochem Intl 19, 929–36 (1989).
Evans DG, Evans DJ, Jr. Graham DY, Infect Immun 57, 2272–8 (1989).
Simon PM, Goode PL, Mobasseri A, Zopf D, Infect Immun 65, 750–7 (1997).
Evans DG, Evans DJ, Jr. Graham DY, Gastroenterol 102, 1557–67 (1992).
Evans D, Karjalainen T, Evans D, Graham D, Lee C-H, J Bacteriol 175, 674–83 (1993).
Miller-Podraza H, Abul-Milh M, Teneberg S, Karlsson K-A, Infect Immun 65, 2480–2 (1997).
Gold B, Huesca M, Sherman P, Lingwood C, Infect Immun 61, 2632–8 (1993).
Bitzan MM, Gold BD, Philpot DJ, Huesca M, Sherman PM, Karch H, Lissner R, Lingwood CA, Karmali MA, J Infect Dis 177, 955–61 (1998).
Lingwood CA, Huesca M, Kuksis A, Infect Immun 60, 2470–4 (1992).
Borén T, Falk P, Roth KA, Larson G, Normark S, Science 262, 1892–5 (1993).
Ilver D, Arnqvist A, Ogren J, Frick I-M, Kersulyte D, Incecik ET, Covacci A, Engstrand L, Borén T, Science 279, 373–7 (1998).
Guruge JL, Falk PG, Lorenz RG, Dans M, Wirth H-P, Blaser MJ, Berg DE, Gordon JI, Proc Natl Acad Sci USA 95, 3925–30 (1998).
Clyne M, Drumm B, Gastroent 113, 72–80 (1997).
Osawa H, Sugano K, Iwamori M, Kawakami M, Tada M, Nakao M, Digest Dis Sci 46, 69–74 (2001).
Gerhard M, Lehn N, Neumayer N, Boren T, Rad R, Schepp W, Miehlke S, Classen M, Prinz C, Proc Natl Acad Sci USA 96, 12778–83 (1999).
Kamisago S, Iwamori M, Tai T, Mitamura K, Yazaki Y, Sugano K, Infect Immun 64, 624–8 (1996).
Miller-Podraza H, Milh MA, Bergström J, Karlsson K-A, Glycoconj J 13, 453–60 (1996).
Ångström J, Teneberg S, Milh A-M, Larsson T, Leonardsson I, Olsson B, Halvarsson M, Danielsson D, Naslund I, Ljung Å, Wadström T, Karlsson K-A, Glycobiol 8, 297–309 (1998).
Piotrowski J, Slominany A, Murty VLN, Fekete Z, Slomiany BL, Biochem Intl 24, 749–56 (1991).
Saitoh T, Natomi H, Zhao W, Okuzumi K, Sugano K, Iwamori M, Nagai Y, FEBS Lett 282, 385–7 (1991).
Huesca M, Borgia S, Hoffman P, Lingwood CA, Infect Immun 64, 2643–8 (1996).
Mamelak D, Mylvaganam M, Whetstone H, Hartmann E, Lennarz W, Wyrick P, Raulston J, Han H, Hoffman P, Lingwood C, Biochemistry 40, 3572–82 (2001).
Karlsson KA, Glycobiol 10, 761–71 (2000).
Lingwood CA, Current Biology 2, 695–700 (1998).
Levine M, Komblatt MJ, Murray RK, Can J Biochem 53, 679–89 (1975).
Strasberg P, Grey A, Warren I, Skomorowski M-A, J Lip Res 30, 121–7 (1989).
Yamakawa T, Irie R, Iwanaga M, J Biochem 48, 490–7 (1960).
Lingwood CA, Wasfy G, Han H, Huesca M, Infect Immun 61, 2474–8 (1993).
Waldi D. In Dünnschicht-Chromatographie, E. Stahl (ed), Berlin, Springer-Verlag, 1962, pp. 496–515.
Szoka F, Jr., Phabadjopouos D, Proc Natl Acad Sci 75, 4194–8 (1978).
Lingwood CA, Law H, Pellizzari A, Sherman P, Drumm B, Lancet ii, 238–41 (1989).
McGowan CC, Cover TL, Blaser M, Gastroenterol 110, 926–38 (1996).
Cheli R, Crespi M, Testino G, Citarda F, J Clin Gastroenterol 26, 3–6 (1998).
Krivan HC, Roberts DD, Ginsburg V, Proc Natl Acad Sci USA 85, 6157–61 (1988).
Lingwood CA, Biochim Biophys Acta 1455, 375–86 (1999).
Lingwood CA, Cheng M, Krivan HC, Woods D, Biochem Biophy Res Comm 173, 1076–81 (1991).
Foster DB, Philpott D, Abul-Milh M, Huesca M, Sherman PM, Lingwood CA, Microb Path 27, 289–301 (1999).
Foster DB, Abul-Milh M, Huesca M, Lingwood CA, Infect Immun 68, 3108–15 (2000).
Moran A, Sturegard E, Sjunnesson H, Wadstrom T, Hynes S, FEMS Immunol Med Micro 29, 263–70 (2000).
Pascher I, Sundell S, Chem Phys Lipids 20, 175–91 (1977).
Nyholm P-G, Pascher I, Biochem 32, 1225–34 (1993).
Strömberg N, Ryd N, Lindberg AA, Karlsson K-A, FEBS Lett 232, 193–8 (1988).
Blomberg L, Krivan H, Cohen P, Conway P, Infect Immun 61, 2526–31 (1993).
Payne D, O'Reilly M, Williamson D, Infect Immun 61, 3673–7 (1993).
Abul-Milh M, Paradis S-É, Dubreuil JD, Jacques M, Infect Immun 67, 4983–7 (1999).
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Abul-Milh, M., Foster, D.B. & Lingwood, C.A. In vitro binding of Helicobacter pylori to monohexosylceramides. Glycoconj J 18, 253–260 (2001). https://doi.org/10.1023/A:1012460824913
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DOI: https://doi.org/10.1023/A:1012460824913