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Originally published In Press as doi:10.1074/jbc.M111640200 on March 4, 2002

J. Biol. Chem., Vol. 277, Issue 20, 18198-18205, May 17, 2002
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Identification of Target Tissue Glycosphingolipid Receptors for Uropathogenic, F1C-fimbriated Escherichia coli and Its Role in Mucosal Inflammation*

Fredrik BäckhedDagger §, Björn Alsén§||, Niamh Roche||**, Jonas Ångström||, Anne von EulerDagger , Michael E. BreimerDagger Dagger , Benita Westerlund-Wikström§§, Susann Teneberg||¶¶, and Agneta Richter-DahlforsDagger ||||

From the Dagger  Microbiology and Tumorbiology Center, Karolinska Institute, SE 171 77 Stockholm, Sweden, the || Institute of Medical Biochemistry, Göteborg University, P. O. Box 440, SE 405 30 Göteborg, Sweden, the Dagger Dagger  Department of Surgery, Sahlgrenska University Hospital, SE 413 45 Göteborg, Sweden, and the §§ Division of General Microbiology, Department of Biosciences, P. O. Box 56, University of Helsinki, Helsinki FIN-00014 Finland

Bacterial adherence to mucosal cells is a key virulence trait of pathogenic bacteria. The type 1 fimbriae and the P-fimbriae of Escherichia coli have both been described to be important for the establishment of urinary tract infections. While P-fimbriae recognize kidney glycosphingolipids carrying the Galalpha 4Gal determinant, type 1 fimbriae bind to the urothelial mannosylated glycoproteins uroplakin Ia and Ib. The F1C fimbriae are one additional type of fimbria correlated with uropathogenicity. Although it was identified 20 years ago its receptor has remained unidentified. Here we report that F1C-fimbriated bacteria selectively interact with two minor glycosphingolipids isolated from rat, canine, and human urinary tract. Binding-active compounds were isolated and characterized as galactosylceramide, and globotriaosylceramide, both with phytosphingosine and hydroxy fatty acids. Comparison with reference glycosphingolipids revealed that the receptor specificity is dependent on the ceramide composition. Galactosylceramide was present in the bladder, urethers, and kidney while globotriaosylceramide was present only in the kidney. Using a functional assay, we demonstrate that binding of F1C-fimbriated Escherichia coli to renal cells induces interleukin-8 production, thus suggesting a role for F1C-mediated attachment in mucosal defense against bacterial infections.

* This work was supported in part by the Swedish Medical Research Council, the Swedish Cancer Foundation, and the Wallenberg Foundation.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Both authors contributed equally to this work.

Supported by grants from the program "Glycoconjugates in Biological Systems" sponsored by the Swedish Foundation for Strategic Research.

** Supported by grants from the program "Glycoconjugates in Biological Systems" sponsored by the Swedish Foundation for Strategic Research.

¶¶ To whom correspondence should be addressed: Institute of Medical Biochemistry, Göteborg University, P.O. Box 440, SE 405 30 Göteborg, Sweden. Tel.: 46-31-773-3492; Fax: 46-31-413-190; E-mail: Susann.Teneberg@medkem.gu.se.

|||| Recipient of special grants from The Royal Swedish Academy of Sciences and the Swedish Foundation for Strategic Research.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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