Adhesion of K99 fimbriated to pig intestinal epithelium: correlation of adhesive and non-adhesive phenotypes with the sialoglycolipid content Free

Abstract

Summary: Evidence for the existence of two phenotypes of piglets born to experimental herds was obtained based on the susceptibility of intestinal brush borders to adhesion of K99-positive . The enterocytes of the K99-receptive piglets displayed a characteristic sialoglycolipid pattern, with a higher content of the monosialoglyco-lipids II NeuGc-LacCer (GM3Gc), IVNeuGc-nLcOseCer (SPGGc) and IVNeuAc-nLcOseCer (SPG) and the oligosialogangliosides IVNeuAc, IINeuAc-GgOseCer (GD1a), II(NeuAc)-GgOseCer (GD2), II (NeuAc)-GgOseCer (GD1b) and IVNeuAc, II(NeuAc)-GgOseCer (GT1b) when compared to the gangliosides of non-receptive piglets. The gangliosides from enterocytes of the non-receptive piglets were mainly the monosialogangliosides IINeuAc-GgOseCer (GM2) and IINeuAc-LacCer (GM3), only traces of the other sialoglycolipids being detected. Adhesion of C-labelled K99-positive cells to the piglet small intestinal sialoglycolipids, as tested by the thin-layer chromatogram overlay assay, revealed that the receptive enterocyte membrane was richer in glycolipids containing K99 receptor structures than the non-receptive enterocyte. Adhesion of K99-positive correlated with the degree of sialylation of the brush border glycolipids.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-137-7-1591
1991-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/137/7/mic-137-7-1591.html?itemId=/content/journal/micro/10.1099/00221287-137-7-1591&mimeType=html&fmt=ahah

References

  1. Benajiba A., Desnuelle P., Maroux S. 1982; Presence of free hydrophobic peptides in the brush border and basolateral membranes of pig enterocytes. Biochimica et Biophysica Acta 682:1–7
    [Google Scholar]
  2. Chappuis J. P., Duval-Iflah Y., Ducluzeau R., Raibaud P. 1985; Resistance of gnotobiotic Large White and Chinese piglets to in vivo attachment of a K88ab enterotoxigenic Escherichia coli strain. Reproduction, Nutrition et Dèvelopment 25:49–60
    [Google Scholar]
  3. Cheng K., Costerton J. W. 1986; Microbial adhesion and colonization within the digestive tract. Society for Applied Bacteriology Symposium Series 13:239–261
    [Google Scholar]
  4. Duchet-Suchaux M., Le Maître C., Bertin A. 1990; Differences in susceptibility of inbred and outbred infant mice to enterotoxigenic Escherichia coli of bovine, porcine and human origin. Journal of Medical Microbiology 31:185–190
    [Google Scholar]
  5. Duval-Iflah Y., Chappuis J. P. 1984; Entéropathogénicité de différentes souches de Escherichia coli chez le porcelet gnotoxénique. Im Diarrhée du Jeune167–176 Desjeux J. F., Ducluzeau R. Paris: INSERM;
    [Google Scholar]
  6. Duval-Iflah Y., Chappuis J. P., Ducluzeau R., Raibaud P. 1983; Intraspecific interactions between E. coli strains in human newborns and gnotobiotic mice and piglets. Progress in Food and Nutrition Science 7:107–116
    [Google Scholar]
  7. Gaastra W., De Graaf F. K. 1982; Host-specific fimbrial adhesins of noninvasive enterotoxigenic Escherichia coli strains. Microbiological Reviews 46:334–352
    [Google Scholar]
  8. Ghidoni R., Sonnino S., Tettamanti G., Baumann N., Reuter G., Schauer R. 1980; Isolation and characterization of a trisialoganglioside from mouse brain, containing 9-O-acetyl-N-acetylneuraminic acid. Journal of Biological Chemistry 255:6990–6995
    [Google Scholar]
  9. Gibbons R., Sellwood R., Burrows M., Hunter P. 1977; Inheritance of resistance to neonatal diarrhea in the pig: examination of the genetic system. Theoretical and Applied Genetics 51:65–70
    [Google Scholar]
  10. Guinée P. A., Veldkamp J., Jansen W. H. 1977; Improved Minca medium for the detection of K99 antigen in calf enterotoxigenic strains of Escherichia coli . Infection and Immunity 15:676–678
    [Google Scholar]
  11. Gustafsson B. E., Karlsson K. A., Larson G., Midtvedt T., Strömberg N., Teneberg S., Thurin J. 1986; Glycosphingo-lipid patterns of the gastrointestinal tract and feces of germ-free and conventional rats. Journal of Biological Chemistry 261:15294–15300
    [Google Scholar]
  12. Hansson G. C., Karlsson K. A., Larson G., Strömberg N., Thurin J. 1985; Carbohydrate-specific adhesion of bacteria to thin-layer chromatograms: a rationalized approach to the study of host cell glycolipid receptors. Analytical Biochemistry 146:158–163
    [Google Scholar]
  13. Herrler G., Reuter G., Rott R., Klenk H.-D., Schauer R. 1987; N-Acetyl-9-O-acetylneuraminic acid, the receptor for influenza C virus, is a differentiation marker on chicken erythrocytes. Biological Chemistry Hoppe-Seyler 368:451–454
    [Google Scholar]
  14. Holmgren J., Lönnroth J., Mansson J. E., Svennerholm L. 1975; Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proceedings of the National Academy of Sciences of the United States of America 722520–2524
    [Google Scholar]
  15. IUPAC-IUB 1986; Joint Commission on biochemical nomenclature. European Journal of Biochemistry 159:1–6
    [Google Scholar]
  16. Kyogashima M., Ginsburg V., Krivan H. 1989; Escherichia coliK99 binds to mM-glycoIylsialoparagloboside and N-glycolyI-GM3 found in piglet small intestine. Archives of Biochemistry and Biophysics 270:391–397
    [Google Scholar]
  17. Ledeen R. W., Yu R. K. 1982; Gangliosides: structure, isolation and analysis. Methods in Enzymology 83:139–191
    [Google Scholar]
  18. Lindahl M., Carlstedt I. 1990; Binding of K99 fimbriae of enterotoxigenic Escherichia coli to pig small intestinal mucin glycopeptides. Journal of General Microbiology 136:1609–1614
    [Google Scholar]
  19. Lindahl M., Brossmer R., Wadström T. 1987; Carbohydrate receptor specificity of K99 fimbriae of enterotoxigenic Escherichia coli. Glycoconjugate Journal 4:51–58
    [Google Scholar]
  20. Miettinen T., Takki-Lukkainen I. T. 1959; Use of butyl acetate in determination of sialic acid. Acta Chemica Scandinavica 13:856–858
    [Google Scholar]
  21. Mouricout M. A., Julien R. A. 1987a; Pilus-mediated binding of bovine enterotoxigenic Escherichia coli to calf intestinal mucins. Infection and Immunity 55:1216–1223
    [Google Scholar]
  22. Mouricout M., Julien R. 1987b; Adhesion of enterotoxigenic Escherichia coli to epithelial cell and mucus glycoconjugates. Proceedings of the IX International Symposium on GlycoconjugatesG14 Montreuil J., Verbert A., Spik G., Fournet B. Lille; Lerouge, France:
    [Google Scholar]
  23. Mullin B. R., Poore C. M., Rupp B. H. 1983; Quantitation of gangliosides by scanning densitometry of thin-layer chromatography plates. Journal of Chromatography 278:160–166
    [Google Scholar]
  24. Nakamura Y., Hashimoto Y., Yamakawa T., Susuki A. 1988; Age-dependent changes in GM1 and GD1a expression in mouse liver. Journal of Biochemistry 103:396–398
    [Google Scholar]
  25. Ono E., Abe K., Nakazawa M., Naiki M. 1989; Ganglioside epitope recognized by K99 fimbriae from enterotoxigenic Escherichia coli. Infection and Immunity 57:907–911
    [Google Scholar]
  26. Pohlentz G., Klein D., Schwarzmann G., Schmitz D., Sandhoff K. 1988; Both GA2, GM2, and GD2 synthases and GM1b, GD1a, and GT1b synthases are single enzymes in Golgi vesicles from rat liver. Proceedings of the National Academy of Sciences of United States of America 857044–7048
    [Google Scholar]
  27. Rapacz J., Hasler-Rapacz J. 1986; Polymorphism and inheritance of swine small intestinal receptors mediating adhesion of three serological variants of Escherichia co/i-producing K88 pilus antigen. Animal Genetics 17:305–321
    [Google Scholar]
  28. Roosendaal B., Van Bergen en Henegouwen P., de Graaf F. K. 1986; Subcellar localization of K99 fimbrial subunits and effect of temperature on subunit synthesis and assembly. Journal of Bacteriology 165:1029–1032
    [Google Scholar]
  29. Runnels P. L., Moon H. W., Schneider R. A. 1980; Development of resistance with host age to adhesion of K99+Escherichia coli to isolated intestinal epithelial cells. Infection and Immunity 28:298–300
    [Google Scholar]
  30. Saito M., Kasai N., Yu R. 1985; In situ immunological determination of basic carbohydrate structures of gangliosides on thin-layer plates. Analytical Biochemistry 148:54–58
    [Google Scholar]
  31. Schauer R. 1978; Characterization of sialic acids. Methods in Enzymology 50:64–92
    [Google Scholar]
  32. Sellwood R., Gibbons R. A., Jones G. W., Rutter J. M. 1975; Adhesion of enteropathogenic Escherichia coli to pig intestinal brush borders: the existence of two pig phenotypes. Journal of Medical Microbiology 8:405–411
    [Google Scholar]
  33. Shaw L., Schauer R. 1988; The biosynthesis of N-glycolyl-neuraminic acid occurs by hydroxylation of the CMP-acetyl-neuraminic acid. Biological Chemistry Hoppe-Seyler 369:477–486
    [Google Scholar]
  34. Smit H., Gaastra W., Kamerling J. P., Vielgenthart J. F. G., de Graaf F. K. 1984; Isolation and structural characterization of the equine erythrocyte receptor for enterotoxigenic Escherichia coli K99 fimbrial adhesin. Infection and Immunity 46:578–584
    [Google Scholar]
  35. Smith M. W., Peacock M. A. 1980; Anomalous replacement of foetal enterocytes in the neonatal pig. Proceedings of the Royal Society of LondonB206411–420
    [Google Scholar]
  36. Snodgrass D. R., Chandler D. S., Makin J. J. 1981; Inheritance of Escherichia coli adhesion in pigs: identification of nonadhesive phenotypes in a commercial herd. Veterinary Record 109:461–463
    [Google Scholar]
  37. Suzuki Y., Suzuki N., Michi H., Matsumoto M. 1985; Characterization of gangliosides of porcine erythrocyte membranes : occurrence of ganglioside GD3 as major ganglioside. Lipids 20:588–593
    [Google Scholar]
  38. Svennerholm L. 1957; Quantitative estimation of sialic acids. II. A colorimetric resorcinol hydrochloric acid method. Biochimica et Biophysica Acta 24:604–611
    [Google Scholar]
  39. Svennerholm L. 1963; Chromatographic separation of human brain gangliosides. Journal of Neurochemistry 10:613–623
    [Google Scholar]
  40. Tanno M., Yamada H., Shimada H., Ohashi M. 1988; Ganglioside variations in human liver cirrhosis and hepatocellular carcinoma as shown by two-dimensional thin-layer chromatography. Clinical Biochemistry 21:333–339
    [Google Scholar]
  41. Teneberg S., Willemsen P., de Graaf F. K., Karlsson K. A. 1990; Receptor-active glycolipids of epithelial cells of the small intestine of young and adult pigs to susceptibility to infection with Escherichia coli. FEBS Letters 263:10–14
    [Google Scholar]
  42. Tixier G., Govet P. 1975; Mise en évidence d’une structure agglutinant les hématies de cheval en présence de mannose et spécifique des souches d’E. coli entérotoxiques d’origine bovine. Comptes Rendus de l’Academie des Sciences de Paris 281:1641–1644
    [Google Scholar]
  43. Trinchera M., Vallenzasca C., Ghidoni R., Tettament G. 1990; Extensive precursor-product relationship between gangliosides formed from exogenous glucosylceramide in rat liver. FEBS Letters 260:23–26
    [Google Scholar]
  44. Yamakawa T., Susuki A., Hashimoto Y. 1986; Genetic control of glycolipid expression. Chemistry and Physics of Lipids 42:75–90
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-137-7-1591
Loading
/content/journal/micro/10.1099/00221287-137-7-1591
Loading

Data & Media loading...

Most cited Most Cited RSS feed