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Erythrocyte and porcine intestinal glycosphingolipids recognized by F4 fimbriae of enterotoxigenic Escherichia coli

Annelies Coddens UGent, Erik Valis, John Benktander, Jonas Ångström, Michael E Breimer, Eric Cox UGent and Ssusann Teneberg (2011) PLOS ONE. 6(9).
abstract
Enterotoxigenic F4-fimbriated Escherichia coli is associated with diarrheal disease in neonatal and postweaning pigs. The F4 fimbriae mediate attachment of the bacteria to the pig intestinal epithelium, enabling an efficient delivery of diarrhea-inducing enterotoxins to the target epithelial cells. There are three variants of F4 fimbriae designated F4ab, F4ac and F4ad, respectively, having different antigenic and adhesive properties. In the present study, the binding of isolated F4ab, F4ac and F4ad fimbriae, and F4ab/ac/ad-fimbriated E. coli, to glycosphingolipids from erythrocytes and from porcine small intestinal epithelium was examined, in order to get a comprehensive view of the F4-binding glycosphingolipids involved in F4-mediated hemagglutination and adhesion to the epithelial cells of porcine intestine. Specific interactions between the F4ab, F4ac and F4ad fimbriae and both acid and non-acid glycosphingolipids were obtained, and after isolation of binding-active glycosphingolipids and characterization by mass spectrometry and proton NMR, distinct carbohydrate binding patterns were defined for each fimbrial subtype. Two novel glycosphingolipids were isolated from chicken erythrocytes, and characterized as GalNAc alpha 3GalNAc alpha beta 3Gal beta 4Glc beta 1Cer and GalNAc alpha 3GalNAc beta 3Gal beta 4GlcNAc beta 3Gal beta 4Glc beta 1Cer. These two compounds, and lactosylceramide (Gal beta 4Glc beta 1Cer) with phytosphingosine and hydroxy fatty acid, were recognized by all three variants of F4 fimbriae. No binding of the F4ad fimbriae or F4ad-fimbriated E. coli to the porcine intestinal glycosphingolipids occurred. However, for F4ab and F4ac two distinct binding patterns were observed. The F4ac fimbriae and the F4ac-expressing E. coli selectively bound to galactosylceramide (Gal beta 1Cer) with sphingosine and hydroxy 24: 0 fatty acid, while the porcine intestinal glycosphingolipids recognized by F4ab fimbriae and the F4ab-fimbriated bacteria were characterized as galactosylceramide, sulfatide (SO(3)-3Gal beta 1Cer), sulf-lactosylceramide (SO(3)-3Gal beta 4Glc beta 1Cer), and globotriaosylceramide (Gal alpha 4Gal beta 4Glc beta 1Cer) with phytosphingosine and hydroxy 24: 0 fatty acid. Finally, the F4ad fimbriae and the F4ad-fimbriated E. coli, but not the F4ab or F4ac subtypes, bound to reference gangliotriaosylceramide (GalNAc beta 4Gal beta 4Glc beta 1Cer), gangliotetraosylceramide (Gal beta 3GalNAc beta 4Gal beta 4Glc beta 1Cer), isoglobotriaosylceramide (Gal alpha 3-Gal beta 4Glc beta 1Cer), and neolactotetraosylceramide (Gal beta 4GlcNAc beta 3Gal beta 4Glc beta 1Cer).
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
MASS-SPECTROMETRY, MAGNETIC-RESONANCE-SPECTROSCOPY, K88 FIMBRIAE, STRUCTURAL CHARACTERIZATION, CORRELATED SPECTROSCOPY, GLYCOLIPID RECEPTORS, HELICOBACTER-PYLORI, BINDING-SPECIFICITY, IDENTIFICATION, ADHESIN
journal title
PLOS ONE
PLoS One
volume
6
issue
9
article_number
e23309
pages
16 pages
Web of Science type
Article
Web of Science id
000295173800002
JCR category
BIOLOGY
JCR impact factor
4.092 (2011)
JCR rank
12/84 (2011)
JCR quartile
1 (2011)
ISSN
1932-6203
DOI
10.1371/journal.pone.0023309
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
1988782
handle
http://hdl.handle.net/1854/LU-1988782
date created
2012-01-17 09:46:59
date last changed
2012-01-31 11:37:16
@article{1988782,
  abstract     = {Enterotoxigenic F4-fimbriated Escherichia coli is associated with diarrheal disease in neonatal and postweaning pigs. The F4 fimbriae mediate attachment of the bacteria to the pig intestinal epithelium, enabling an efficient delivery of diarrhea-inducing enterotoxins to the target epithelial cells. There are three variants of F4 fimbriae designated F4ab, F4ac and F4ad, respectively, having different antigenic and adhesive properties. In the present study, the binding of isolated F4ab, F4ac and F4ad fimbriae, and F4ab/ac/ad-fimbriated E. coli, to glycosphingolipids from erythrocytes and from porcine small intestinal epithelium was examined, in order to get a comprehensive view of the F4-binding glycosphingolipids involved in F4-mediated hemagglutination and adhesion to the epithelial cells of porcine intestine. Specific interactions between the F4ab, F4ac and F4ad fimbriae and both acid and non-acid glycosphingolipids were obtained, and after isolation of binding-active glycosphingolipids and characterization by mass spectrometry and proton NMR, distinct carbohydrate binding patterns were defined for each fimbrial subtype. Two novel glycosphingolipids were isolated from chicken erythrocytes, and characterized as GalNAc alpha 3GalNAc alpha beta 3Gal beta 4Glc beta 1Cer and GalNAc alpha 3GalNAc beta 3Gal beta 4GlcNAc beta 3Gal beta 4Glc beta 1Cer. These two compounds, and lactosylceramide (Gal beta 4Glc beta 1Cer) with phytosphingosine and hydroxy fatty acid, were recognized by all three variants of F4 fimbriae. No binding of the F4ad fimbriae or F4ad-fimbriated E. coli to the porcine intestinal glycosphingolipids occurred. However, for F4ab and F4ac two distinct binding patterns were observed. The F4ac fimbriae and the F4ac-expressing E. coli selectively bound to galactosylceramide (Gal beta 1Cer) with sphingosine and hydroxy 24: 0 fatty acid, while the porcine intestinal glycosphingolipids recognized by F4ab fimbriae and the F4ab-fimbriated bacteria were characterized as galactosylceramide, sulfatide (SO(3)-3Gal beta 1Cer), sulf-lactosylceramide (SO(3)-3Gal beta 4Glc beta 1Cer), and globotriaosylceramide (Gal alpha 4Gal beta 4Glc beta 1Cer) with phytosphingosine and hydroxy 24: 0 fatty acid. Finally, the F4ad fimbriae and the F4ad-fimbriated E. coli, but not the F4ab or F4ac subtypes, bound to reference gangliotriaosylceramide (GalNAc beta 4Gal beta 4Glc beta 1Cer), gangliotetraosylceramide (Gal beta 3GalNAc beta 4Gal beta 4Glc beta 1Cer), isoglobotriaosylceramide (Gal alpha 3-Gal beta 4Glc beta 1Cer), and neolactotetraosylceramide (Gal beta 4GlcNAc beta 3Gal beta 4Glc beta 1Cer).},
  articleno    = {e23309},
  author       = {Coddens, Annelies and Valis, Erik and Benktander, John and {\AA}ngstr{\"o}m, Jonas and Breimer, Michael E and Cox, Eric and Teneberg, Ssusann},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {MASS-SPECTROMETRY,MAGNETIC-RESONANCE-SPECTROSCOPY,K88 FIMBRIAE,STRUCTURAL CHARACTERIZATION,CORRELATED SPECTROSCOPY,GLYCOLIPID RECEPTORS,HELICOBACTER-PYLORI,BINDING-SPECIFICITY,IDENTIFICATION,ADHESIN},
  language     = {eng},
  number       = {9},
  pages        = {16},
  title        = {Erythrocyte and porcine intestinal glycosphingolipids recognized by F4 fimbriae of enterotoxigenic Escherichia coli},
  url          = {http://dx.doi.org/10.1371/journal.pone.0023309},
  volume       = {6},
  year         = {2011},
}

Chicago
Coddens, Annelies, Erik Valis, John Benktander, Jonas Ångström, Michael E Breimer, Eric Cox, and Ssusann Teneberg. 2011. “Erythrocyte and Porcine Intestinal Glycosphingolipids Recognized by F4 Fimbriae of Enterotoxigenic Escherichia Coli.” Plos One 6 (9).
APA
Coddens, A., Valis, E., Benktander, J., Ångström, J., Breimer, M. E., Cox, E., & Teneberg, S. (2011). Erythrocyte and porcine intestinal glycosphingolipids recognized by F4 fimbriae of enterotoxigenic Escherichia coli. PLOS ONE, 6(9).
Vancouver
1.
Coddens A, Valis E, Benktander J, Ångström J, Breimer ME, Cox E, et al. Erythrocyte and porcine intestinal glycosphingolipids recognized by F4 fimbriae of enterotoxigenic Escherichia coli. PLOS ONE. 2011;6(9).
MLA
Coddens, Annelies, Erik Valis, John Benktander, et al. “Erythrocyte and Porcine Intestinal Glycosphingolipids Recognized by F4 Fimbriae of Enterotoxigenic Escherichia Coli.” PLOS ONE 6.9 (2011): n. pag. Print.