Type 1 pilus-mediated bacterial invasion of bladder epithelial cells

EMBO Journal

Volumn 19, Issue 12, 2000, Pages 2803-2812

  Martinez, Juan J ^a   Mulvey, Matthew A ^a   Schilling, Joel D ^a   Pinkner, Jerome S ^a   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adhesin; Bladder; Invasion; Type 1 pili; Urinary tract infection

Indexed keywords

ACTIN; ADHESIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; TYROSINE; VINCULIN;

ARTICLE; BACTERIAL INFECTION; BACTERIUM ADHERENCE; BACTERIUM PILUS; BLADDER EPITHELIUM; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ESCHERICHIA COLI; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; URINARY TRACT INFECTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0034659834     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.12.2803     Document Type: Article

References (64)

1. Alrutz, M.A. and Isberg, R.R. (1998) Involvement of focal adhesion kinase in invasin mediated uptake. Prof. Natl Acad. Sci. USA, 95, 13658-13663.
2. Baorto, D.M., Gao, Z., Malaviya, R., Dustin, M.L., van der Merwe, A., Lublin, D.M. and Abraham, S.N. (1997) Survival of FimH-expressing enterobacteria in macrophages relies on glycolipid traffic. Nature, 389, 636-639.
3. Barnett, B.J. and Stephens, D.S. (1997) Urinary tract infection: an overview, Am. J. Med. Sci., 314, 245-249.
4. Bliska, J.B., Galan, J.E. and Falkow, S. (1993) Signal transduction in the mammalian cell during bacterial attachment and entry. Cell, 73, 903-920.
5. Blomfield, I.C., McClain, M.S. and Eisenstein, B.I. (1991) Type 1 fimbriae mutants of Escherichia coli K12: characterisation of recognized afimbriate strains and construction of new fim deletion mutants. Mol. Microbiol., 5, 1439-1445.
6. Braun, L., Ohayon, H. and Cossart, P. (1998) The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol. Microbiol., 27, 1077-1087.
7. Carpenter, C.L. and Cantley, L.C. (1996) Phosphoinositide kinases. Curr. Opin. Cell Biol., 8, 153-158.
8. Carpenter, C.L., Duckworth B.C., Auger, K.R., Cohen, B., Schaffhausen, B.S. and Cantley, L.C. (1990) Purification and characterization of phosphoinositide 3-kinase from rat liver. J. Biol. Chem., 265, 19704-19711.
9. Chen, H.-C. and Guan, J.-L. (1994) Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Pro Natl Acad. Sci. USA, 91, 10148-10152.
10. Chen, H.-C. and Guan J.-L. (1996) The association of focal adhesion kinase with a 200-kDa protein that is tyrosine phosphorylated in response to platelet-derived growth factor. Eur. J. Biochem., 235, 495-500.
11. Chen, H.-C., Appeddu, P.A., Isoda, H. and Guan, J.-L. (1996) Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J. Biol. Chem., 271, 26329-26334.
12. Choudhury, D., Thompson, A., Stojanoff V., Langermann, S., Pinkner, J., Hultgren, S.J. and Knight, S.D. (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science, 285, 1061-1066.
13. FAK. Mol. Cell. Biol., 14, 147-155.
14. Comolli, J.C., Waite, L.L., Mostov, K.E. and Engel, J.N. (1999) Pili binding to asialo-GMI on epithelial cells can mediate cytotoxicity or bacterial internalization by Pseudomnnas aeruginosa. Infect. Immun., 67, 3207-3214.
15. Connell, H., Agace, W., Klemm, P., Schembri, M., Marild, S. and Svanborg, C. (1996) Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl Acad. Sci. USA, 93, 9827-9832.
16. Cormack, B.P., Valdivia, R.H. and Falkow, S. (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene, 173, 33-38.
17. Dekker, L.V. and Segal, A.W. (2000) Signals to move cells. Science, 287, 982-985.
18. Dibb-Fuller, M.P., Allen-Vercoe, E., Thorns, C.J. and Woodward, M.J. (1999) Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology, 145, 1023-1031.
19. Dumenil, G., Olivo, J.C., Pellegrini, S., Fellous, M., Sansonetti, P.J. and Nhieu, G.T. (1998) Interferon a inhibits a Src-mediated pathway necessary for Shigella-induced cytoskeletal rearrangements in epithelial cells. J. Cell Biol., 143, 1003-1012.
20. Elsinghorst, E.A. (1994) Measurement of invasion by gentamicin resistance. Methods Enzymol., 236, 405-420.
21. Evans, D.J., Frank, D., Finek-Barbancon, V., Wu, C. and Fleiszig, S. (1998) Pseudomonas aeruginosa invasion and cytotoxicity are independent events, both of which involve protein tyrosine kinase activity. Infect. Immun., 66, 1453-1459.
22. Falkow, S., Isberg, R.R. and Portnoy, D.A. (1992) The interaction of bacteria with mammalian cells. Annu. Rev. Cell Biol., 8, 333-363.
23. Finlay, B.B. and Cossart, P. (1997) Exploitation of mammalian host cell function by bacterial pathogens. Science, 276, 718-725.
24. Finlay, B.B. and Falkow, S. (1997) Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev., 61, 136-169.
25. Finlay, B.B. Ruschkowski, S. and Dedhar, S. (1991) Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci., 99, 283-296.
26. Fukami, K., Endo, T., Imamura, M. and Takenawa, T. (1994) α-actinin and vinculin are PIP2-binding proteins involved in signaling by tyrosine kinase. J. Biol. Chem., 269, 1518-1522.
27. Fukushi, Y., Orikasa, S. and Kagayama, M. (1979) An electron microscopic study of the interaction between vesical epithelium and E.coli. Invest. Urol., 17, 61-68.
28. Gerwien, J., Nielsen, M., Labuda, T., Nissen, M.H., Svejgaard, A., Geisler, C., Ropke, C. and Odum, N. (1999) Cutting edge: TCR stimulation by antibody and bacterial superantigen induces Stat3 activation in human T cells. J. Immunol., 163, 1742-1745.
29. Gilmore, A.P., Jackson, P., Waites, G.T. and Critchley, D.R. (1992) Further characterisation of the talin-binding site in the cytoskeletal protein vinculin. J. Cell Sci., 103, 719-731.
30. Griffiss, J.M., Lammel, C.J., Wang, J., Dekker, N.P. and Brooks, G.F. (1999) Neisseria gonorrhoeae coordinately uses pili and Opa to activate HEC-I-B microvilli. which causes engulfment of the gonococci. Infect. Immun., 67, 3469-3480.
31. Guinebault, C., Payrastre, B., Racaud-Sultan, C., Mazarguil, H., Breton, M., Mauco, G., Plantavid, M. and Chap, H. (1995) Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interactions of p85 α with actin filaments and focal adhesion kinase. J. Cell Biol., 129, 831-842.
32. Hartwig, J.H., Bokoch, G.M., Carpenter, C.L., Janmey, P.A., Taylor, L.A., Toker, A. and Stossel, T.P. (1995) Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell, 82, 643-653.
33. Hooton, T.M. and Stamm, W.E. (1997) Diagnosis and treatment of uncomplicated urinary tract infection. Infect. Dis. Clin. North Am., 11, 551-581.
34. Hvidberg, H., Struve, C., Krogfelt, K.A., Christensen, N., Rasmussen, S.N. and Frimodt-Moller, N. (2000) Development of a long-term ascending urinary tract infection mouse model for antibiotic treatment studies. Antimicrob. Agents Chemother., 44, 156-163.
35. Ireton, K., Payrastre, B., Chap, H., Ogawa, W., Sakaue, H., Kasuga, M. and Cossart, P. (1996) A role for phosphoinositide 3-kinase in bacterial invasion. Science, 274, 780-784.
36. Ireton, K., Payrastre, B. and Cossart, P. (1999) The Listeria monocytogenes protein InIB is an agonist of mammalian phosphoinositide 3-kinase. J. Biol. Chem., 274, 17025-17032.
37. Isberg, R.R., Voorhis, D.L. and Falkow, S. (1987) Identification of invasin, a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell, 50, 769-778.
38. Jones, C.H., Pinkner, J.S., Roth, R., Heuser, J., Nicholes, A.V., Abraham, S.N. and Hultgren, S.J. (1995) FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc. Natl Acad. Sci. USA, 92, 2081-2085.
39. Kroemker, M., Rudiger, A.H., Jockusch, B.M. and Rudiger, M. (1994) Intramolecular interactions in vinculin control α-actinin binding to the vinculin head. FEBS Lett., 355, 259-262.
40. Kuhlman, P.A., Hemmings, L. and Critchley, D.R. (1992) The identification and characterization of an actin binding site in α-actinin by mutagenesis. FEBS Lett., 304, 201-206.
41. Langermann, S. et al. (1997) Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science, 276, 607-611.
42. Leevers, S.J., Vanhaesebroeck, B. and Waterfield, M.D. (1999) Signalling through phosphoinositide 3-kinases: the lipids take centre stage. Curr. Opin. Cell Biol., 11, 219-225.
43. Leffler, H. and Svanborg-Eden, C. (1980) Chemical identification of a glycosphingolipid receptor for Escherichia coli attaching to human urinary tract epithelial cells and agglutinating human erythrocytes. FEMS Microbiol. Lett., 8, 127-134.
44. Malaviya, R. and Abraham, S.N. (1998) Clinical implications of mast cell-bacteria interactions. J. Mol. Med., 76, 617-623.
45. McTaggart, L.A., Rigby, R.C. and Elliot, T.S.J. (1990) The pathogenesis of urinary tract infections associated with Escherichia coli, Staphylococcus saprophyticus and S.epidermidis. J. Med. Microbiol., 32, 135-141.
46. Mecsas, J., Raupach, B. and Falkow, S. (1998) The Yersinia Yops inhibit invasion of Listeria, Shigella and Edwardsiella but not Salmonella into epithelial cells. Mol. Microbiol., 28, 1269-1281.
47. Menard, R., Dehio, C. and Sansonetti, P.J. (1996) Bacterial entry into epithelial cells: the paradigm of Shigella. Trends Microbiol., 4, 220-226.
48. Mengaud, J., Ohayon, H., Gounon, P., Mege, R.-M. and Cossart, P. (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L.monocytogenes into epithelial cells. Cell, 84, 923-932.
49. Minion, F.C., Abraham, S.N., Beachy, E.H. and Goguen, J.D. (1986) The genetic determinant of adhesive function in type 1 fimbriae of Escherichia coli is distinct from the gene encoding the fimbrial subunit. J. Bacteriol., 165, 1033-1036.
50. Mulvey, M.A., Lopez-Boado, Y.S., Wilson, C.L., Roth, R., Parks, W.C., Heuser, J. and Hultgren, S.J. (1998) Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science, 282, 1494-1497.
51. Mulvey, M.A., Schilling, J.D., Martinez, J.J. and Hultgren, S.J. (2000) Bad bugs and beleaguered bladders: interplay between uropathogenic E.coli and innate host defenses. Proc. Natl Acad. Sci. USA, in press.
52. Orndorff, P.E. and Falkow, S. (1984) Identification and characterization of a gene product that regulates type 1 piliation in Escherichia coli. J. Bacteriol., 160, 61-66.
53. Palmer, L.M., Reilly, T.J., Utsalo, S.J. and Donnenberg, M.S. (1997) Internalization of Escherichia coli by human renal epithelial cells is associated with tyrosine phosphorylation of specific host cell proteins. Infect. Immun., 65, 2570-2575.
54. Parsons, J.T. (1996) Integrin-mediated signaling: regulation by protein tyrosine kinases and small GTP-binding proteins. Curr. Opin. Cell Biol., 8, 146-152.
55. Russell, P.W. and Orndorff, P.E. (1992) Lesions in two Escherichia coli type 1 genes alter pilus number and length without affecting receptor binding. J. Bacteriol., 174, 5923-5935.
56. Sansonetti, P.J. (1991) Genetic and molecular basis of epithelial cell invasion by Shigella species. Rev. Infect. Dis., 13, 285-292.
57. Schulte, R., Zumbihl, R., Kampik, D., Fauconnier, A. and Autenrieth, I.B. (1998) Wortmannin blocks Yersinia invasin-triggered internalization, but not interleukin production by epithelial cells. Med. Microbiol. Immunol., 187, 53-60.
58. Shoelson, S.E., Sivaraja, M., Williams, K.P., Hu, P., Schlessinger, J. and Weiss, M.A. (1993) Specific phosphopeptide binding regulates a conformational change in the PI 3-kinase SH2 domain associated with enzyme activation. EMBO J., 12, 795-802.
59. Stromberg, N., Marklund, B.I., Lund, B., Ilver, D., Hamers, A., Gaastra, W., Karlsson, K.A. and Normark, S. (1990) Host-specificity of uropathogenic Escherichia coli depends on differences in binding specificity to Galα1-4Gal-containing isoreceptors. EMBO J., 9, 2001-2010.
60. Tewari, R., MacGregor, J.I., Ikeda, T., Little, J.R., Hultgren, S.J. and Abraham, S.N. (1993) Neutrophil activation by nascent FimH subunits of type 1 fimbriae purified from the periplasm of Escherichia coli. J. Biol. Chem., 268, 3009-3015.
61. Thankavel, K., Madison, B., Ikeda, T., Malaviya, R., Shah, A.H., Arumugan, P.M. and Abraham, S.N. (1997) Localization of a domain in the fimH adhesin of Echerichia coli type 1 fimbriae capable of receptor recognition and use of a domain-specific antibody to confer protection against experimental urinary tract infection. J. Clin. Invest., 100, 1123-1136.
62. Vanhaesebroeck, B. and Waterfield, M.D. (1999) Signaling by distinct classes of phosphoinositide 3-kinases. Exp. Cell Res., 253, 239-254.
63. Vlahos, C.J., Matter, W.F., Hui, K.Y. and Brown, R.F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem., 269, 5241-5248.
64. Weinberg, A., Belton, C.M., Park, Y. and Lamont, R.J. (1997) Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun., 65, 313-316.