Elevated shear stress protects Escherichia coli cells adhering to surfaces via catch bonds from detachment by soluble inhibitors

Applied and Environmental Microbiology

Volumn 72, Issue 4, 2006, Pages 3005-3010

  Nilsson, Lina M ^a,b   Thomas, Wendy E ^b   Sokurenko, Evgeni V ^c   Vogel, Viola ^a,b  

^a ETH ZURICH   (Switzerland)

^b University of Washington   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DRUG PRODUCTS; FLOW OF FLUIDS; SHEAR STRESS; VIRUSES;

CATCH BONDS; EUKARYOTIC CELLS; SURFACE ADHESION; THERAPEUTIC IMPLICATIONS;

ESCHERICHIA COLI;

ADHESION; BACTERIUM; SHEAR STRESS; VIRUS;

ARTICLE; BACTERIUM ADHERENCE; CELL ADHESION; COMPETITIVE INHIBITION; DRUG SCREENING; ESCHERICHIA COLI; EUKARYOTE; FLUID FLOW; HOST PATHOGEN INTERACTION; NONHUMAN; SHEAR FLOW; SHEAR STRESS;

ADHESINS, ESCHERICHIA COLI; BACTERIAL ADHESION; ESCHERICHIA COLI; FIMBRIAE PROTEINS; HEAT-SHOCK RESPONSE; MANNOSE; METHYLMANNOSIDES; STRESS, MECHANICAL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 33646115449     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.72.4.3005-3010.2006     Document Type: Article

References (38)

1. Bell, G. I. 1978. Models for specific adhesion of cells to cells. Science 200:618-627.
2. Bouckaert, J., J. Berglund, M. Schembri, E. De Genst, L. Cools, M. Wuhrer, C. S. Hung, J. Pinkner, R. Slattegard, A. Zavialov, D. Choudhury, S. Langermann, S. J. Hultgren, L. Wyns, P. Klemm, S. Oscarson, S. D. Knight, and H. De Greve. 2005. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol. Microbiol. 55:441-455.
3. Cai, S., V. S. Dole, W. Bergmeier, J. Scafidi, H. Feng, D. D. Wagner, and A. E. Davis III. 2005. A direct role for C1 inhibitor in regulation of leukocyte adhesion. J. Immunol. 174:6462-6466.
4. Chigaev, A., G. J. Zwartz, T. Buranda, B. S. Edwards, E. R. Prossnitz, and L. A. Sklar. 2004. Conformational regulation of alpha 4 beta 1-integrin affinity by reducing agents. "Inside-out" signaling is independent of and additive to reduction-regulated integrin activation. J. Biol. Chem. 279:32435-32443.
5. Dickinson, R. B., J. A. Nagel, R. A. Proctor, and S. L. Cooper. 1997. Quantitative comparison of shear-dependent Staphylococcus aureus adhesion to three polyurethane ionomer analogs with distinct surface properties. J. Biomed. Mater. Res. 36:152-162.
6. Evans, E. 1999. Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. Biophys. Chem. 82:83-97.
7. Firon, N., S. Ashkenazi, D. Mirelman, I. Ofek, and N. Sharon. 1987. Aromatic alpha-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal epithelial cells. Infect. Immun. 55:472-476.
8. Forero, M., W. E. Thomas, C. Bland, L. M. Nilsson, E. V. Sokurenko, and V. Vogel. 2004. A catch-bond based nanoadhesive sensitive to shear stress. Nano Lett. 4:1593-1597.
9. Fu, D. T., L. Chen, and R. A. Oneill. 1994. A detailed structural characterization of ribonuclease-B oligosaccharides by H-1-NMR spectroscopy and mass-spectrometry. Carbohydr. Res. 261:173-186.
10. Hicks, A. E., A. Leppanen, R. D. Cummings, R. P. McEver, P. G. Hellewell, and K. E. Norman. 2002. Glycosulfopeptides modeled on P-selectin glycoprotein ligand 1 inhibit P-selectin-dependent leukocyte rolling in vivo. FASEB J. 16:1461-1462.
11. Hung, C. S., J. Bouckaert, D. Hung, J. Pinkner, C. Widberg, A. DeFusco, C. G. Auguste, R. Strouse, S. Langermann, G. Waksman, and S. J. Hultgren. 2002. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol. Microbiol. 44:903-915.
12. Jin, M., I. Andricioaei, and T. A. Springer. 2004. Conversion between three conformational states of integrin I domains with a C-terminal pull spring studied with molecular dynamics. Structure 12:2137-2147.
13. Joosten, J. A., V. Loimaranta, C. C. Appeldoorn, S. Haataja, F. A. El Maate, R. M. Liskamp, J. Finne, and R. J. Pieters. 2004. Inhibition of Streptococcus suis adhesion by dendritic galabiose compounds at low nanomolar concentration. J. Med. Chem. 47:6499-6508.
14. Karlsson, K. A., J. Angstrom, J. Bergstrom, and B. Lanne. 1992. Microbial interaction with animal cell surface carbohydrates. APMIS Suppl. 27:71-83.
15. Konstantopoulos, K., W. D. Hanley, and D. Wirtz. 2003. Receptor-ligand binding: 'catch' bonds finally caught. Curr. Biol. 13:R611-R613.
16. Langer, R., M. Wang, S. M. Stepkowski, W. W. Hancock, R. Han, P. Li, L. Feng, R. A. Kirken, K. L. Berens, B. Dupre, H. Podder, R. A. Dixon, and B. D. Kahan. 2004. Selectin inhibitor bimosiamose prolongs survival of kidney allografts by reduction in intragraft production of cytokines and chemokines. J. Am. Soc. Nephrol. 15:2893-2901.
17. Lindhorst, T. K., C. Kieburg, and U. Krallmann-Wenzel. 1998. Inhibition of the type 1 fimbriae-mediated adhesion of Escherichia coli to erythrocytes by multiantennary alpha-mannosyl clusters: the effect of multivalency. Glycoconj. J. 15:605-613.
18. Magnani, J. L. 2004. The discovery, biology, and drug development of sialyl Lea and sialyl Lex. Arch. Biochem. Biophys. 426:122-131.
19. Marshall, B. T., M. Long, J. W. Piper, T. Yago, R. P. McEver, and C. Zhu. 2003. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190-193.
20. Mascari, L., P. Ymele-Leki, C. D. Eggleton, P. Speziale, and J. M. Ross. 2003. Fluid shear contributions to bacteria cell detachment initiated by a monoclonal antibody. Biotechnol. Bioeng. 83:65-74.
21. Moshier, A., M. S. Reddy, and F. A. Scannapieco. 1996. Role of type 1 fimbriae in the adhesion of Escherichia coli to salivary mucin and secretory immunoglobulin A. Curr. Microbiol. 33:200-208.
22. Nagahori, N., R. T. Lee, S. Nishimura, D. Page, R. Roy, and Y. C. Lee. 2002. Inhibition of adhesion of type 1 fimbriated Escherichia coli to highly mannosylated ligands. ChemBioChem 3:836-844.
23. Nilsson, L. M., W. E. Thomas, E. Trintchina, V. Vogel, and E. Sokurenko. Submitted for publication.
24. Ofek, I., and N. Sharon. 1990. Adhesins as lectins: specificity and role in infection. Curr. Top. Microbiol. Immunol. 151:91-113.
25. Pak, J., Y. Pu, Z. T. Zhang, D. L. Hasty, and X. R. Wu. 2001. Tamm-Horsfall protein binds to type 1 fimbriated Escherichia coli and prevents E. coli from binding to uroplakin Ia and Ib receptors. J. Biol. Chem. 276:9924-9930.
26. Rockendorf, N., O. Sperling, and T. K. Lindhorst. 2002. Trivalent cluster mannosides with aromatic partial structure as ligands for the type 1 fimbrial lectin of Escherichia coli. Aust. J. Chem. 55:87-93.
27. Sarangapani, K. K., T. Yago, A. G. Klopocki, M. B. Lawrence, C. B. Fieger, S. D. Rosen, R. P. McEver, and C. Zhu. 2004. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279:2291-2298.
28. Serafini-Cessi, F., F. Dall'Olio, and N. Malagolini. 1984. High-mannose oligosaccharides from human Tamm-Horsfall glycoprotein. Biosci. Rep. 4:269-274.
29. Sharon, N. 1987. Bacterial lectins, cell-cell recognition and infectious-disease. FEBS Lett. 217:145-157.
30. Shive, M. S., S. M. Hasan, and J. M. Anderson. 1999. Shear stress effects on bacterial adhesion, leukocyte adhesion, and leukocyte oxidative capacity on a polyetherurethane. J. Biomed. Mater. Res. 46:511-519.
31. Sokurenko, E. V., V. Chesnokova, R. J. Doyle, and D. L. Hasty. 1997. Diversity of the Escherichia coli type 1 fimbrial lectin-differential binding to mannosides and uroepithelial cells. J. Biol. Chem. 272:17880-17886.
32. Thomas, W., M. Forero, O. Yakovenko, L. Nilsson, P. Vicini, E. Sokurenko, and V. Vogel. 2006. Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J. 90:753-764.
33. Thomas, W. E., L. M. Nilsson, M. Forero, E. V. Sokurenko, and V. Vogel. 2004. Shear-dependent 'stick-and-roll' adhesion of type 1 fimbriated Escherichia coli. Mol. Microbiol. 53:1545-1557.
34. Thomas, W. E., E. Trintchina, M. Forero, V. Vogel, and E. V. Sokurenko. 2002. Bacterial adhesion to target cells enhanced by shear force. Cell 109:913-923.
35. Wang, I. W., J. M. Anderson, M. R. Jacobs, and R. E. Marchant. 1995. Adhesion of Staphylococcus epidermidis to biomedical polymers: contributions of surface thermodynamics and hemodynamic shear conditions. J. Biomed. Mater. Res. 29:485-493.
36. Wold, A. E., J. Mestecky, M. Tomana, A. Kobata, H. Ohbayashi, T. Endo, and C. S. Eden. 1990. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect. Immun. 58:3073-3077.
37. Wu, X. R., T. T. Sun, and J. J. Medina. 1996. In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections. Proc. Natl. Acad. Sci. USA 93:9630-9635.
38. Zhou, G., W. Mo, P. Sebbel, G. Min, T. Neubert, R. Glockshuber, X. Wu, T. Sun, and X. Kong. 2001. Uroplakin la is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J. Cell Sci. 114:4095-4103.