Weak rolling adhesion enhances bacterial surface colonization

Journal of Bacteriology

Volumn 189, Issue 5, 2007, Pages 1794-1802

  Anderson, Brett N ^a   Ding, Albert M ^a   Nilsson, Lina M ^b   Kusuma, Kaoru ^a   Tchesnokova, Veronika ^c   Vogel, Viola ^b   Sokurenko, Evgeni V ^c   Thomas, Wendy E ^a  

^a University of Washington   (United States)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN FIMH; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BIOFILM; CELL MOTION; ESCHERICHIA COLI; FLOW RATE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; SURFACE PROPERTY;

ADHESINS, ESCHERICHIA COLI; BACTERIAL ADHESION; BIOFILMS; ESCHERICHIA COLI; FIMBRIAE PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33947434498     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00899-06     Document Type: Article

References (59)

1. Bollinger, R. R., M. L. Everett, D. Palestrant, S. D. Love, S. S. Lin, and W. Parker. 2003. Human secretory immunoglobulin A may contribute to biofilm formation in the gut. Immunology 109:580-587.
2. Brown, I. I., and C. C. Hase. 2001. Flagellum-independent surface migration of Vibrio cholerae and Escherichia coli. J. Bacteriol. 183:3784-3790.
3. Chiang, P., and L. L. Burrows. 2003. Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J. Bacteriol. 185:2374-2378.
4. Connell, I., W. Agace, P. Klemm, M. Schembri, S. Marild, and C. Svanborg. 1996. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl. Acad. Sci. USA 93:9827-9832.
5. Costerton, J. W., K. R. Rozee, and K. J. Cheng. 1983. Colonization of particulates, mucous, and intestinal tissue. Prog. Food Nutr. Sci. 7:91-105.
6. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
7. Davies, P. F. 1995. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519-560.
8. Dickinson, R. B., J. A. Nagel, D. McDevitt, T. J. Foster, R. A. Proctor, and S. L. Cooper. 1995. Quantitative comparison of clumping factor- and coagulase-mediated Staphylococcus aureus adhesion to surface-bound fibrinogen underflow. Infect. Immun. 63:3143-3150.
9. Donlan, R. M. 2001. Biofilm formation: a clinically relevant microbiological process. Clin. Infect. Dis. 33:1387-1392.
10. Donovan, W. H., R. Hull, and C. D. Rossi. 1996. Analysis of gram negative recolonization of the neuropathic bladder among patients with spinal cord injuries. Spinal Cord 34:587-591.
11. Fux, C. A., J. W. Costerton, P. S. Stewart, and P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:34-40.
12. Genevaux, P., P. Bauda, M. S. DuBow, and B, Oudega. 1999. Identification of TnIO insertions in the dsbA gene affecting Escherichia coli biofilm formation. FEMS Microbiol. Lett. 173:403-409.
13. Gristina, A. 2004. Biomaterial-centered infection: microbial adhesion versus tissue integration. 1987. Clin. Orthop. Relat. Res. 2004:4-12.
14. Gristina, A. G. 1987. Biomaterial-centered infection: microbial adhesion versus tissue integration. Science 237:1588-1595.
15. Guo, Z., M. Moreau, D. W. Rickey, P. A. Picot, and A. Fenster. 1995. Quantitative investigation of in vitro flow using three-dimensional colour Doppler ultrasound. Ultrasound Med. Biol. 21:807-816.
16. Henrichsen, J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36:478-503.
17. Hoffmann, N., T. B. Rasmussen, P. O. Jensen, C. Stub, M. Hentzer, S. Molin, O. Ciofu, M. Givskov, H. K. Johansen, and N. Hoiby. 2005. Novel mouse model of chronic Pseudomonas aeruginosa lung infection mimicking cystic fibrosis. Infect. Immun. 73:2504-2514.
18. Isberg, R. R., and P. Barnes. 2002. Dancing with the host; flow-dependent bacterial adhesion. Cell 110(1):1-4.
19. Iwahi, T., Y. Abe, M. Nakao, A. Imada, and K. Tsuchiya. 1983. Role of type 1 fimbriae in the pathogenesis of ascending urinary tract infection induced by Escherichia coli in mice. Infect. Immun. 39:1307-1315.
20. Jarvis, W. R., and W. J. Martone. 1992. Predominant pathogens in hospital infections. J. Antimicrob. Chemother. 29(Suppl. A):19-24.
21. Jesaitis, A. J., M. J. Franklin, D. Berglund, M. Sasaki, C. I. Lord, J. B. Bleazard, J. E. Duffy, H. Beyenal, and Z. Lewandowski. 2003. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neu-trophil and biofilm interactions. J. Immunol. 171:4329-4339.
22. Johnson, J. R. 1991. Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev. 4:80-128.
23. Johnson, J. R., N. Kaster, M. A. Kuskowski, and G. V. Ling. 2003. Identification of urovirulence traits in Escherichia coli by comparison of urinary and rectal E. coli isolates from dogs with urinary tract infection. J. Clin. Microbiol. 41:337-345.
24. Johnson, J. R., S. J. Weissman, A. L. Stell, E. Trintchina, D. E. Dykhuizen, and E. V. Sokurenko. 2001. Clonal and pathotypic analysis of archetypal Escherichia coli cystitis isolate NU14. J. Infect. Dis. 184:1556-1565.
25. Keith, B. R., L. Maurer, P. A. Spears, and P. E. Orndorff. 1986. Receptor-binding function of type 1 pili effects bladder colonization by a clinical isolate of Escherichia coli. Infect. Immun. 53:693-696.
26. Klausen, M., A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50:61-68.
27. Klausen, M., A. Heydorn, P. Ragas, L. Lambertsen, A. Aaes-Jorgensen, S. Molin, and T. Tolker-Nielsen. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 48:1511-1524.
28. Kolari, M., U. Schmidt, E. Kuismanen, and M. S. Salkinoja-Salonen. 2002. Firm but slippery attachment of Deinococcus geothermalis. J. Bacteriol. 184:2473-2480.
29. Kunin, C. M., S. Douthitt, J. Dancing, J. Anderson, and M. Moeschberger. 1992. The association between the use of urinary catheters and morbidity and mortality among elderly patients in nursing homes. Am. J. Epidemiol. 135:291-301.
30. Langermann, S., R. Mollby, J. E. Burlein, S. R. Palaszynski, C. G. Auguste, A. DeFusco, R. Strouse, M. A. Schenerman, S. J. Hultgren, J. S. Pinkner, J. Winberg, L. Guldevall, M. Soderhall, K. Ishikawa, S. Normark, and S. Koenig. 2000. Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J. Infect. Dis. 181:774-778.
31. Langermann, S., S. Palaszynski, M. Barnhart, G. Auguste, J. S. Pinkner, J. Burlein, P. Barren, S. Koenig, S. Leath, C. H. Jones, and S. J. Hultgren. 1997. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276:607-611.
32. Leid, J. G., M. E. Shirtliff, J. W. Costerton, and A. P. Stoodley. 2002. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect. Immun. 70:6339-6345.
33. Maki, D. G., and P. A. Tambyah. 2001. Engineering out the risk for infection with urinary catheters. Emerg. Infect. Dis. 7:342-347.
34. Mittelman, M. 1995. Adhesion to biomaterials, p. 89-127. In M. Fletcher (ed.), Bacterial adhesion: molecular and ecological diversity. Wiley-Liss, Inc, New York, NY.
35. 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.
36. Nilsson, L. M., W. E. Thomas, E. V. Sokurenko, and V. Vogel. 2006. Elevated shear stress protects Escherichia coli cells adhering to surfaces via catch bonds from detachment by soluble inhibitors. Appl. Environ. Microbiol. 72:3005-3010.
37. Nilsson, L. M., W. E. Thomas, E. Trintchina, V. Vogel, and E. V. Sokurenko. 2006. Catch bond-mediated adhesion without a shear threshold: trimannose versus monomannose interactions with the FimH adhesin of Escherichia coli. J. Biol. Chem. 281:16656-166663.
38. Ofek, I., D. L. Hasty, and N. Sharon. 2003. Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunol. Med. Microbiol. 38:181-191.
39. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
40. Platt, R., B. F. Polk, B. Murdock, and B. Rosner. 1982. Mortality associated with nosocomial urinary-tract infection. N. Engl. J. Med. 307:637-642.
41. Pouttu, R., T. Puustinen, R. Virkola, J. Hacker, P. Klemm, and T. K. Korhonen. 1999. Amino acid residue Ala-62 in the FimH fimbrial adhesin is critical for the adhesiveness of meningitis-associated Escherichia coli to collagens. Mol. Microbiol. 31:1747-1757.
42. Pratt, L. A., and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30:285-293.
43. Rupp, C. J., C. A. Fux, and P. Stoodley. 2005. Viscoelasticity of Staphylococcus aureus biofilms in response to fluid shear allows resistance to detachment and facilitates rolling migration. Appl. Environ. Microbiol. 71:2175-2178.
44. Sauer, K., A. K. Camper, G. D. Ehrlich, J. W. Costerton, and D. G. Davies. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184:1140-1154.
45. Schembri, M. A., M. Givskov, and P. Klemm. 2002. An attractive surface: gram-negative bacterial biofilms. Sci. STKE 2002:RE6.
46. Schembri, M. A., and P. Klemm. 2001. Biofilm formation in a hydrodynamic environment by novel FimH variants and ramifications for virulence. Infect. Immun. 69:1322-1328.
47. Serafini-Cessi, F., N. Malagolini, and D. Cavallone. 2003. Tamm-Horsfall glycoprotein: biology and clinical relevance. Am. J. Kidney Dis. 42:658-676.
48. 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.
49. Sokurenko, E. V., V. Chesnokova, D. E. Dykhuizen, I. Ofek, X. R. Wu, K. A. Krogfelt, C. Struve, M. A. Schembri, and D. L. Hasty. 1998. Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc. Natl. Acad. Sci. USA 95:8922-8926.
50. Sokurenko, E. V., M. Feldgarden, E. Trintchina, S. J. Weissman, S. Avagyan, S. Chattopadhyay, J. R. Johnson, and D. E. Dykhuizen. 2004. Selection footprint in the FimH adhesin shows pathoadaptive niche differentiation in Escherichia coli. Mol. Biol. Evol. 21:1373-1383.
51. Steinberg, D., S. Poran, and L. Shapira. 1999. The effect of extracellular polysaccharides from Streptococcus mutans on the bactericidal activity of human neutrophils. Arch. Oral Biol. 44:437-444.
52. Stewart, P. S., and J. W. Costerton. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:135-138.
53. Thomas, W. E., M. Forero, O. Yakovenko, L. Nilsson, P. Vicini, E. V. Sokurenko, and V. Vogel. 2006. Catch bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J. 90:753-764.
54. Thomas, W. E., L. Nilsson, M. Forero, E. V. Sokurenko, and V. Vogel. 2004. 'Stick-and-roll' bacterial adhesion mediated by catch-bonds. Mol. Microbiol. 53:1545.
55. 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.
56. Thormann, K. M., R. M. Saville, S. Shukla, D. A. Pelletier, and A. M. Spormann. 2004. Initial phases of biofilm formation in Shewanella oneidensis MR-1. J. Bacteriol. 186:8096-8104.
57. Weissman, S. J., S. Chattopadhyay, P. Aprikian, M. Obata-Yasuoka, Y. Yarova-Yarovaya, A. Stapleton, W. Ba-Thein, D. Dykhuizen, J. R. Johnson, and E. V. Sokurenko. 2006. Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli. Mol. Microbiol. 59:975-988.
58. Wood, T. K., A. F. Gonzalez Barrios, M. Herzberg, and J. Lee. 2006. Motility influences biofilm architecture in Escherichia coli. Appl. Microbiol. Biotechnol. 72:361-367.
59. Zhu, C., J. Lou, and R. P. McEver. 2005. Catch bonds: physical models, structural bases, biological function and rheological relevance. Biorheology 42:443-462.