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Originally published In Press as doi:10.1074/jbc.M511496200 on April 19, 2006

J. Biol. Chem., Vol. 281, Issue 24, 16656-16663, June 16, 2006
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Catch Bond-mediated Adhesion without a Shear Threshold

TRIMANNOSE VERSUS MONOMANNOSE INTERACTIONS WITH THE FimH ADHESIN OF ESCHERICHIA COLI*Formula

Lina M. Nilsson{ddagger}§, Wendy E. Thomas§, Elena Trintchina, Viola Vogel{ddagger}§1, and Evgeni V. Sokurenko2

From the Departments of §Bioengineering and Microbiology, University of Washington, Seattle, Washington 98195 and the {ddagger}Laboratory for Biologically Oriented Materials, Department of Materials, Swiss Federal Institute of Technology, ETH Zurich, Hönggerberg, CH-8093 Zürich, Switzerland

The FimH protein is the adhesive subunit of Escherichia coli type 1 fimbriae. It mediates shear-dependent bacterial binding to monomannose (1M)-coated surfaces manifested by the existence of a shear threshold for binding, below which bacteria do not adhere. The 1M-specific shear-dependent binding of FimH is consistent with so-called catch bond interactions, whose lifetime is increased by tensile force. We show here that the oligosaccharide-specific interaction of FimH with another of its ligands, trimannose (3M), lacks a shear threshold for binding, since the number of bacteria binding under static conditions is higher than under any flow. However, similar to 1M, the binding strength of surface-interacting bacteria is enhanced by shear. Bacteria transition from rolling into firm stationary surface adhesion as the shear increases. The shear-enhanced bacterial binding on 3M is mediated by catch bond properties of the 1M-binding subsite within the extended oligosaccharide-binding pocket of FimH, since structural mutations in the putative force-responsive region and in the binding site affect 1M- and 3M-specific binding in an identical manner. A shear-dependent conversion of the adhesion mode is also exhibited by P-fimbriated E. coli adhering to digalactose surfaces.


Received for publication, October 24, 2005 , and in revised form, March 1, 2006.

* This work was supported by National Institutes of Health Grants A145820 (to E. V. S.) and A150940 (to E. V. S.), a National Science Foundation graduate fellowship (to L. N.), and the Swiss Federal Institute of Technology, ETH Zurich (to V. V.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Formula The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1 and S2.

1 To whom correspondence may be addressed: Dept. of Material Science, Laboratory for Biologically Oriented Materials, Swiss Federal Institute of Technology, ETH Wolfgang-Pauli-Str. 10, ETH Hönggerberg, HCI F443, CH-8093 Zürich, Switzerland. Tel.: 41-44-632-08-87; Fax: 41-44-632-10-73; E-mail: viola.vogel{at}mat.ethz.ch. 2 To whom correspondence may be addressed: Dept. of Microbiology, Rm. E309 HSB, University of Washington, Box 357242, Seattle, WA 98195-7242. Tel.: 206-685-2162; Fax: 206-543-8297; E-mail: evs{at}u.washington.edu.


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