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Infection and Immunity, March 2002, p. 1530-1537, Vol. 70, No. 3
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.3.1530-1537.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Interaction of an Outer Membrane Protein of Enterotoxigenic Escherichia coli with Cell Surface Heparan Sulfate Proteoglycans

James M. Fleckenstein,1,2* James T. Holland,3 and David L. Hasty3,4

Medicine,1 Research Services, Veterans Affairs Medical Center, Memphis, Tennessee 38104,3 Department of Medicine,2 Department of Anatomy, University of Tennessee, Memphis, Tennessee 381634

Received 6 August 2001/ Returned for modification 13 September 2001/ Accepted 15 November 2001

We have previously shown that enterotoxigenic invasion protein A (Tia), a 25-kDa outer membrane protein encoded on an apparent pathogenicity island of enterotoxigenic Escherichia coli (ETEC) strain H10407, mediates attachment to and invasion into cultured human gastrointestinal epithelial cells. The epithelial cell receptor(s) for Tia has not been identified. Here we show that Tia interacts with cell surface heparan sulfate proteoglycans. Recombinant E. coli expressing Tia mediated invasion into wild-type epithelial cell lines but not invasion into proteoglycan-deficient cells. Furthermore, wild-type eukaryotic cells, but not proteoglycan-deficient eukaryotic cells, attached to immobilized polyhistidine-tagged recombinant Tia (rTia). Binding of epithelial cells to immobilized rTia was inhibited by exogenous heparan sulfate glycosaminoglycans but not by hyaluronic acid, dermatan sulfate, or chondroitin sulfate. Similarly, pretreatment of eukaryotic cells with heparinase I, but not pretreatment of eukaryotic cells with chrondroitinase ABC, inhibited attachment to rTia. In addition, we also observed heparin binding to both immobilized rTia and recombinant E. coli expressing Tia. Heparin binding was inhibited by a synthetic peptide representing a surface loop of Tia, as well as by antibodies directed against this peptide. Additional studies indicated that Tia, as a prokaryotic heparin binding protein, may also interact via sulfated proteoglycan molecular bridges with a number of mammalian heparan sulfate binding proteins. These findings suggest that the binding of Tia to host epithelial cells is mediated at least in part through heparan sulfate proteoglycans and that ETEC belongs on the growing list of pathogens that utilize these ubiquitous cell surface molecules as receptors.

* Corresponding author. Mailing address: Research Service (151), Veterans Affairs Medical Center, 1030 Jefferson Avenue, Memphis, TN 38104. Phone: (901) 448-5786. Fax: (901) 577-7273. E-mail: jflecke1{at}tennessee.edu.

Infection and Immunity, March 2002, p. 1530-1537, Vol. 70, No. 3
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.3.1530-1537.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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