Catch bond-mediated adhesion without a shear threshold: trimannose versus monomannose interactions with the FimH adhesin of Escherichia coli.
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.
Nilsson
Lina M
LM
Departments of Bioengineering and Microbiology, University of Washington, Seattle, WA 98195, USA.
Thomas
Wendy E
WE
Trintchina
Elena
E
Vogel
Viola
V
Sokurenko
Evgeni V
EV
D018829:Adhesins, Bacterial / Q000737:chemistry; D018830:Adhesins, Escherichia coli / Q000737:chemistry* / Q000378:metabolism; D002448:Cell Adhesion; D004926:Escherichia coli / Q000378:metabolism*; D036781:Fimbriae Proteins / Q000737:chemistry* / Q000378:metabolism; D005690:Galactose / Q000737:chemistry; D037102:Lectins / Q000737:chemistry; D008024:Ligands; D008358:Mannose / Q000737:chemistry*; D008958:Models, Molecular; D009844:Oligosaccharides / Q000737:chemistry; D017434:Protein Structure, Tertiary; D013314:Stress, Mechanical
D018829:Adhesins, Bacterial; D018830:Adhesins, Escherichia coli; D037102:Lectins; D008024:Ligands; D009844:Oligosaccharides; C092426:PapG protein, E coli; C058769:fimH protein, E coli; D036781:Fimbriae Proteins; D008358:Mannose; D005690:Galactose