Adhesion of K99 fimbriated Escherichia coli to pig intestinal epithelium: correlation of adhesive and non-adhesive phenotypes with the sialoglycolipid content
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 Eschenchia coli. The enterocytes of the K99-receptive piglets displayed a characteristic sialoglycolipid pattern, with a higher content of the monosialoglyco-lipids II3 NeuGc-LacCer (GM3Gc), IV3NeuGc-nLcOse4Cer (SPGGc) and IV3NeuAc-nLcOse4Cer (SPG) and the oligosialogangliosides IV3NeuAc, II3NeuAc-GgOse4Cer (GD1a), II3(NeuAc)2-GgOse3Cer (GD2), II3 (NeuAc)2-GgOse4Cer (GD1b) and IV3NeuAc, II3(NeuAc)2-GgOse4Cer (GT1b) when compared to the gangliosides of non-receptive piglets. The gangliosides from enterocytes of the non-receptive piglets were mainly the monosialogangliosides II3NeuAc-GgOse3Cer (GM2) and II3NeuAc-LacCer (GM3), only traces of the other sialoglycolipids being detected. Adhesion of 14C-labelled K99-positive E. coli 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 E. coli correlated with the degree of sialylation of the brush border glycolipids.
BenajibaA.,
DesnuelleP.,
MarouxS.1982; Presence of free hydrophobic peptides in the brush border and basolateral membranes of pig enterocytes. Biochimica et Biophysica Acta 682:1–7
ChappuisJ. P.,
Duval-IflahY.,
DucluzeauR.,
RaibaudP.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
ChengK.,
CostertonJ. W.1986; Microbial adhesion and colonization within the digestive tract. Society for Applied Bacteriology Symposium Series 13:239–261
Duchet-SuchauxM.,
Le MaîtreC.,
BertinA.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
Duval-IflahY.,
ChappuisJ. P.1984; Entéropathogénicité de différentes souches de Escherichia coli chez le porcelet gnotoxénique. Im Diarrhée du Jeune167–176DesjeuxJ. F.,
DucluzeauR.
Paris: INSERM;
Duval-IflahY.,
ChappuisJ. P.,
DucluzeauR.,
RaibaudP.1983; Intraspecific interactions between E. coli strains in human newborns and gnotobiotic mice and piglets. Progress in Food and Nutrition Science 7:107–116
GhidoniR.,
SonninoS.,
TettamantiG.,
BaumannN.,
ReuterG.,
SchauerR.1980; Isolation and characterization of a trisialoganglioside from mouse brain, containing 9-O-acetyl-N-acetylneuraminic acid. Journal of Biological Chemistry 255:6990–6995
GibbonsR.,
SellwoodR.,
BurrowsM.,
HunterP.1977; Inheritance of resistance to neonatal diarrhea in the pig: examination of the genetic system. Theoretical and Applied Genetics 51:65–70
GuinéeP. A.,
VeldkampJ.,
JansenW. H.1977; Improved Minca medium for the detection of K99 antigen in calf enterotoxigenic strains of Escherichia coli
. Infection and Immunity 15:676–678
GustafssonB. E.,
KarlssonK. A.,
LarsonG.,
MidtvedtT.,
StrömbergN.,
TenebergS.,
ThurinJ.1986; Glycosphingo-lipid patterns of the gastrointestinal tract and feces of germ-free and conventional rats. Journal of Biological Chemistry 261:15294–15300
HanssonG. C.,
KarlssonK. A.,
LarsonG.,
StrömbergN.,
ThurinJ.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
HerrlerG.,
ReuterG.,
RottR.,
KlenkH.-D.,
SchauerR.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
HolmgrenJ.,
LönnrothJ.,
ManssonJ. E.,
SvennerholmL.1975; Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proceedings of the National Academy of Sciences of the United States of America722520–2524
KyogashimaM.,
GinsburgV.,
KrivanH.1989; Escherichia coliK99 binds to mM-glycoIylsialoparagloboside and N-glycolyI-GM3 found in piglet small intestine. Archives of Biochemistry and Biophysics 270:391–397
LindahlM.,
CarlstedtI.1990; Binding of K99 fimbriae of enterotoxigenic Escherichia coli to pig small intestinal mucin glycopeptides. Journal of General Microbiology 136:1609–1614
MouricoutM. A.,
JulienR. A.1987a; Pilus-mediated binding of bovine enterotoxigenic Escherichia coli to calf intestinal mucins. Infection and Immunity 55:1216–1223
MouricoutM.,
JulienR.1987b; Adhesion of enterotoxigenic Escherichia coli to epithelial cell and mucus glycoconjugates. Proceedings of the IX International Symposium on GlycoconjugatesG14MontreuilJ.,
VerbertA.,
SpikG.,
FournetB.
Lille; Lerouge, France:
MullinB. R.,
PooreC. M.,
RuppB. H.1983; Quantitation of gangliosides by scanning densitometry of thin-layer chromatography plates. Journal of Chromatography 278:160–166
NakamuraY.,
HashimotoY.,
YamakawaT.,
SusukiA.1988; Age-dependent changes in GM1 and GD1a expression in mouse liver. Journal of Biochemistry 103:396–398
PohlentzG.,
KleinD.,
SchwarzmannG.,
SchmitzD.,
SandhoffK.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 America857044–7048
RapaczJ.,
Hasler-RapaczJ.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
RoosendaalB.,
Van Bergen en HenegouwenP.,
de GraafF. K.1986; Subcellar localization of K99 fimbrial subunits and effect of temperature on subunit synthesis and assembly. Journal of Bacteriology 165:1029–1032
RunnelsP. L.,
MoonH. W.,
SchneiderR. 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
SaitoM.,
KasaiN.,
YuR.1985; In situ immunological determination of basic carbohydrate structures of gangliosides on thin-layer plates. Analytical Biochemistry 148:54–58
SellwoodR.,
GibbonsR. A.,
JonesG. W.,
RutterJ. 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
ShawL.,
SchauerR.1988; The biosynthesis of N-glycolyl-neuraminic acid occurs by hydroxylation of the CMP-acetyl-neuraminic acid. Biological Chemistry Hoppe-Seyler 369:477–486
SmitH.,
GaastraW.,
KamerlingJ. P.,
VielgenthartJ. F. G.,
de GraafF. K.1984; Isolation and structural characterization of the equine erythrocyte receptor for enterotoxigenic Escherichia coli K99 fimbrial adhesin. Infection and Immunity 46:578–584
SnodgrassD. R.,
ChandlerD. S.,
MakinJ. J.1981; Inheritance of Escherichia coli adhesion in pigs: identification of nonadhesive phenotypes in a commercial herd. Veterinary Record 109:461–463
SuzukiY.,
SuzukiN.,
MichiH.,
MatsumotoM.1985; Characterization of gangliosides of porcine erythrocyte membranes : occurrence of ganglioside GD3 as major ganglioside. Lipids 20:588–593
SvennerholmL.1957; Quantitative estimation of sialic acids. II. A colorimetric resorcinol hydrochloric acid method. Biochimica et Biophysica Acta 24:604–611
TannoM.,
YamadaH.,
ShimadaH.,
OhashiM.1988; Ganglioside variations in human liver cirrhosis and hepatocellular carcinoma as shown by two-dimensional thin-layer chromatography. Clinical Biochemistry 21:333–339
TenebergS.,
WillemsenP.,
de GraafF. K.,
KarlssonK. 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
TixierG.,
GovetP.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
TrincheraM.,
VallenzascaC.,
GhidoniR.,
TettamentG.1990; Extensive precursor-product relationship between gangliosides formed from exogenous glucosylceramide in rat liver. FEBS Letters 260:23–26
Adhesion of K99 fimbriated Escherichia coli to pig intestinal epithelium: correlation of adhesive and non-adhesive phenotypes with the sialoglycolipid content