FimH-mediated Escherichia coli K1 invasion of human brain microvascular endothelial cells

Cellular Microbiology

Volumn 9, Issue 1, 2007, Pages 169-178

  Khan, Naveed Ahmed ^a,b   Kim, Yuri ^a   Shin, Sooan ^a   Kim, Kwang Sik ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; CD48 ANTIGEN; FIMBRIA PROTEIN; PROTEIN FIMH; RHO KINASE;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BLOOD BRAIN BARRIER; BRAIN CELL; CALCIUM CELL LEVEL; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ESCHERICHIA COLI; ESCHERICHIA COLI K1; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

ADHESINS, ESCHERICHIA COLI; ANTIBODIES, BACTERIAL; ANTIGENS, CD; BACTERIAL ADHESION; BLOOD-BRAIN BARRIER; BRAIN; CALCIUM; CELL SEPARATION; CYTOSOL; ENDOTHELIAL CELLS; ESCHERICHIA COLI; FIMBRIAE PROTEINS; HUMANS; MANNOSE; PHOSPHORYLATION; RHOA GTP-BINDING PROTEIN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33845384412     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00779.x     Document Type: Article

References (48)

1. 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 (London) 389: 636-639.
2. 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-usher complex from uropathogenic Escherichia coli. Science 285: 1061-1066.
3. Comolli, J.C., Waite, L.L., Mostov, K.E., and Engel, J.N. (1999) Pili binding to asialo-GM1 on epithelial cells can mediate cytotoxicity or bacterial internalization by Pseudomonas aeruginosa. Infect Immun 67: 3207-3214.
4. 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.
5. 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.
6. Falzano, L., Fiorentini, C., Donelli, G., Michel, E., Kocks, C., Cossart, P, et.al. (1993) Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type 1. Mol Microbiol 9: 1247-1254.
7. Fiorentini, C., Fabbri, A., Matarrese, P., and Falzano, L. (1998) Hinderance of apoptosis and phagocytic behaviour induced by Escherichia coli cytotoxic necrotizing factor 1: Two related activities in epithelial cells. Biochem Biophys Res Commun 241: 341-346.
8. Gbarah, A., Gahmberg, C.G., Ofek, I., Jacobi, U., and Sharon, N. (1991) Identification of the leukocyte adhesion molecules CD11 and CD18 as receptors for type 1-fimbriated (mannose-specific) Escherichia coli. Infect Immun 59: 4524-4530.
9. Gladstone, I.M., Ehrenkranz, R.A., Edberg, S.C., and Baltimore, R.S. (1990) A ten-year review of neonatal sepsis and comparison with the previous fifty-year experience. Pediatr Infect Dis J 9: 819-825.
10. 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-1-B microvilli, which causes engulfment of the gonococci. Infect Immun 67: 3469-3480.
11. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514.
12. Huang, S.H., Wass, C.A., Fu, Q., Prasadarao, N.V., Stins, M., and Kim, K.S. (1995) E.coli invasion of brain microvascular endothelial cells in vitro and in vivo: Molecular cloning and characterization of E.coli invasion gene ibe10. Infect Immun 63: 4470-4475.
13. Khan, N.A., Wang, Y., Kim, K.J., Woong, J., Wass, C.A., and Kim, K.S. (2002) Role of cytotoxic necrotizing factor-1 in Escherichia coli K1 invasion into the central nervous system. J Biol Chem 277: 15607-15612.
14. Killeen, N., Moessner, R., Arvieux, J., Willis, A., and Williams, A.F. (1988) The MRC OX-45 antigen of rat leukocytes and endothelium is in a subset of the immunoglobulin superfamily with CD2, LFA-3 and carcinoembryonic antigens. EMBO J 7: 3087-3091.
15. Kim, K.S. (2001) Escherichia coli translocation at the blood-brain barrier. Infect Immun 69: 5217-5222.
16. Kim, K.S. (2003) Pathogenesis of bacterial meningitis: From bacteraemia to neuronal injury. Nat Rev Neurosci 4: 376-385.
17. Kim, K.S. (2006) Microbial translocation of the blood-brain barrier. Int J Parasitol 36: 607-614.
18. Kim, Y.V., Di Cello, F., Hillaire, C.S., and Kim, K.S. (2004) Differential Ca2+ signaling by thrombin and protease-activated receptor-1-activating peptide in human brain microvascular endothelial cells. Am J Physiol Cell Physiol 286: C31-C42.
19. Klemm, P., and Christiansen, G. (1987) Three fim genes required for the regulation of length and mediation of adhesion of Escherichia coli type 1 fimbriae. Mol Gen Genet 208: 439-455.
20. Lacerda, H.M., Pullinger, G.D., Lax, A.J., and Rozengurt, E. (1997) Cytotoxic necrotizing factor 1 from Escherichia coli and dermonecrotic toxin from Bordetella bronchiseptica induce p21 (rho)-dependent tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 cells. J Biol Chem 272: 9587-9596.
21. Langermann, S., Palaszynski, S., Barnhart, M., Auguste, G., Pinkner, J.S., Burlein, J., et.al. (1997) Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276: 607-611.
22. Lee, J., Shin, S., Teng, C.H., Hong, S.J., and Kim, K.S. (2005) FimH adhesin of Escherichia coli K1 type 1 fimbriae activates BV-2 microglia. Biochem Biophys Res Commun 334: 917-923.
23. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A, et.al. (1999) Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285: 895-898.
24. Martinez, J.J., Mulvey, M.A., Schilling, J.D., Pinkner, J.S., and Hultgren, S.J. (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19: 2803-2812.
25. Matsui, T., Maeda, M., Doi, Y., Yonemura, S., Amano, M., Kaibuchi, K, et.al. (1998) Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J Cell Biol 140: 647-657.
26. 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.
27. Prasadarao, N.V., Wass, C.A., and Kim, K.S. (1997) Identification and characterization of S fimbria-binding sialoglycoproteins on brain microvascular endothelial cells. Infect Immun 65: 2852-2860.
28. Prasadarao, N.V., Wass, C.A., Huang, S.H., and Kim, K.S. (1999) Identification and characterization of a novel Ibe10 binding protein that contributes to Escherichia coli invasion of brain microvascular endothelial cells. Infect Immun 67: 1131-1138.
29. Reddy, M.A., Wass, C.A., Kim, K.S., Schlaepfer, D.D., and Prasadarao, N.V. (2000a) Involvement of focal adhesion kinase in Escherichia coli invasion of human brain microvascular endothelial cells. Infect Immun 68: 6423-6430.
30. Reddy, M.A., Prasadarao, N.V., Wass, C.A., and Kim, K.S. (2000b) Phosphatidylinositol 3-kinase activation and interaction with focal adhesion kinase in Escherichia coli K1 invasion of human brain microvascular endothelial cells. J Biol Chem 275: 36769-36774.
31. Sauter, S.L., Rutherfurd, S.M., Wagener, C., Shively, J.E., and Hefta, S.A. (1991) Binding of nonspecific cross-reacting antigen, a granulocyte membrane glycoprotein, to Escherichia coli expressing type 1 fimbriae. Infect Immun 59: 2485-2493.
32. Schembri, M.A., and Klemm, P. (2001) Biofilm formation in a hydrodynamic environment by novel fimh variants and ramifications for virulence. Infect Immun 69: 1322-1328.
33. Schembri, M.A., Hasman, H., and Klemm, P. (2000) Expression and purification of the mannose recognition domain of the FimH adhesin. FEMS Microbiol Lett 188: 147-151.
34. Scott, C., Iyasu, S., Pawley, D., and Atrash, H. (1998) Postnatal Mortality Surveillance -United States, 1980-1994. MMWR Morb Mortal Wkly Rep 47 (SS-2): 15-28.
35. Shin, J.S., and Abraham, S.N. (2001) Glycosylphosphatidylinositol-anchored receptor-mediated bacterial endocytosis. FEMS Microbiol Lett 197: 131-138.
36. Shin, J.S., Gao, Z., and Abraham, S.N. (1999) Bacteria-host cell interaction mediated by cellular cholesterol/glycolipid-enriched microdomains. Biosci Rep 19: 421-432.
37. Shin, J.S., Gao, Z., and Abraham, S.N. (2000) Involvement of cellular caveolae in bacterial entry into mast cells. Science 289: 785-788.
38. Staunton, D.E., and Thorley-Lawson, D.A. (1987) Molecular cloning of the lymphocyte activation marker Blast-1. EMBO J 6: 3695-3701.
39. Stins, M.F., Gilles, F., and Kim, K.S. (1997) Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76: 81-90.
40. Teng, C.H., Cai, M., Shin, S., Xie, Y., Kim, K.J., Khan, N.A, et.al. (2005) Escherichia coli K1 RS218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state. Infect Immun 73: 2923-2931.
41. 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.
42. 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 Escherichia 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.
43. TranVan Nhieu, G., Clair, C., Grompone, G., and Sansonetti, P. (2004) Calcium signalling during cell interactions with bacterial pathogens. Biol Cell 96: 93-101.
44. Unhanand, M., Mustafa, M.M., McCracken, G.H., Jr, and Nelson, J.D. (1993) Gram-negative enteric bacillary meningitis: A twenty-one-year experience. J Pediatr 122: 15-21.
45. Vouret-Craviari, V., Grall, D., Flatau, G., Pouyssegur, J., Boquet, P., and Van Obberghen-Schilling, E. (1999) Effects of cytotoxic necrotizing factor 1 and lethal toxin on actin cytoskeleton and VE-cadherin localization in human endothelial cell monolayers. Infect Immun 67: 3002-3008.
46. 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.
47. Yokoyama, S., Staunton, D., Fisher, R., Amiot, M., Fortin, J.J., and Thorley-Lawson, D.A. (1991) Expression of the Blast-1 activation/ adhesion molecule and its identification as CD48. J Immunol 146: 2192-2200.
48. Zhou, G., Mo, W.J., Sebbel, P., Min, G., Neubert, T.A., Glockshuber, R., et.al. (2001) Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: Evidence from in vitro FimH binding. J Cell Sci 114: 4095-4103.