Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells

Molecular Microbiology

Volumn 46, Issue 4, 2002, Pages 933-946

  Unkmeir, Alexandra ^a   Latsch, Kirsten ^a   Dietrich, Guido ^a,c   Wintermeyer, Eva ^a   Schinke, Birgitta ^a   Schwender, Stefan ^a   Kim, Kwang Sik ^b   Eigenthaler, Martin ^a   Frosch, Matthias ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

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

^c Berna Biotech AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; INTEGRIN RECEPTOR; PROTEIN; PROTEIN SUBUNIT;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BLOOD ANALYSIS; BRAIN BLOOD VESSEL; BRAIN INFECTION; CHROMATOGRAPHY; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; INTERNALIZATION; MICROVASCULATURE; MUTAGENESIS; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SEPARATION TECHNIQUE;

ANTIBODIES, MONOCLONAL; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; BRAIN; CELLS, CULTURED; CULTURE MEDIA; ENDOTHELIUM, VASCULAR; FIBRONECTINS; GENE DELETION; HEPARIN; HUMANS; INTEGRIN ALPHA5BETA1; NEISSERIA MENINGITIDIS; OLIGOPEPTIDES; PEPTIDES;

BACTERIA (MICROORGANISMS); BOVINAE; NEGIBACTERIA; NEISSERIA; NEISSERIA MENINGITIDIS;

EID: 0036434984     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2002.03222.x     Document Type: Article

References (61)

1. Achtman, M. (1995a) Global epidemiology of meningococcal disease. In Meningococcal Disease. Cartwright, K. (ed.). Chichester: John Wiley and Sons, pp. 159-175.
2. Achtman, M. (1995b) Epidemic spread and antigenic variability of Neisseria meningitidis. Trends Microbiol 3: 186-192.
3. Achtman, M., Neibert, M., Crowe, B.A., Strittmatter, W., Kusecek, B., Weyse, E.,et al. (1988) Purification and characterization of eight class 5 outer membrane protein variants from a clone of Neisseria meningitidis serogroup A. J Exp Med 168: 507-525.
4. Ashton, F.E., Ryan, J.A., Borczyk, A., Caugant, D.A., Mancino, L., and Huang, D. (1991) Emergence of a virulent clone of Neisseria meningitidis serotype 2a that is associated with meningococcal group C disease in Canada. J Clin Microbiol 29: 2489-2493.
5. Badger, J.L., Wass, W.A., and Kim, K.S. (2000) Identification of Escherichia coli K1 genes contributing to human brain microvascular endothelial cell invasion by differential fluorescence induction. Mol Microbiol 36: 174-182.
6. Deghmane, A.E., Petit, S., Topilko, A., Pereira, Y., Giorgini, D., Larribe, M., and Taha, M.K. (2000) Intimate adhesion of Neisseria meningitidis to human epithelial cells is under the control of the crgA gene, a novel LysR-type transcriptional regulator. EMBO J 19: 1068-1078.
7. Deghmane, A.E., Giorgini, D., Larribe, M., Alonso, J.M., and Taha, M.K. (2002) Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol Microbiol 43: 1555-1564.
8. Dejana, E. (1991) Endothelial cell integrin receptors. In Vascular Endothelium: Interaction with Circulating Cells. Gordon, J.L. (ed.). Oxford: Elsevier Science Publishers, pp. 31-44.
9. Duensing, T.D., and van Putten, J.P. (1997) Vitronectin mediates internalisation of Neisseria gonorrhoeae by Chinese hamster ovary cells. Infect Immun 65: 964-970.
10. Dziewanowska, K., Patti, J.M., Deobald, C.F., Bayles, K.W., Trumble, W.R., and Bohach, G.A. (1999) Fibronectin binding protein and host cell tyrosine kinase are required for internalisation of Staphylococcus aureus by epithelial cells. Infect Immun 67: 4673-4678.
11. Eberhard, T., Virkola, R., Korhonen, T., Kronvall, G., and Ullberg, M. (1998) Binding to human extracellular matrix by Neisseria meningitidis. Infect Immun 66: 1791-1794.
12. van der Flier, F.M., Chhun, N., Wizemann, T.M., Min, J., McCarthy, J.B., and Tuomanen, E.I. (1995) Adherence of Streptococcus pneumoniae to immobilized. Infect Immun 63: 4317-4322.
13. Frosch, M., Gorgen, I., Boulnois, G.J., Timmis, K.N., and Bitter-Suermann, D. (1985) NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: Isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc Natl Acad Sci USA 82: 1194-1198.
14. Gomez-Duarte, O.G., Dehio, M., Guzman, C.A., Chhatwal, G.S., Dehio, C., and Meyer, T.F. (1997) Binding of vitronectin to opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect Immun 65: 3857-3866.
15. Greiffenberg, L., Goebel, W., Kim, K.S., Weiglein, I., Bubert, A., Engelbrecht, F., et al. (1998) Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: IntB-dependent invasion, long-term intracellular growth, and spread from macrophages to endothelial cells. Infect Immun 66: 5260-5267.
16. Guckenberger, M., Kurz, S., Aepinus, C., Theiss, S., Haller, S., Leimbach, T., et al. (2002) Analysis of the heat shock response of Neisseria meningitidis with cDNA- and oligonucleotide-based DNA microarrays. J Bacteriol 184: 2546-2551.
17. Hammerschmidt, S., Hilse, R., van Putten, J.P., Gerardy-Schahn, R., Unkmeir, A., and Frosch, M. (1996a) Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J 15: 192-198.
18. Hammerschmidt, S., Muller, A., Sillmann, H., Muhlenhoff, M., Borrow, R., Fox, A., et al. (1996b) Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): Correlation with bacterial invasion and the outbreak of meningococcal disease. Mol Microbiol 20: 1211-1220.
19. Hardy, S.J., Christodoulides, M., Weller, R.O., and Heckels, J.E. (2000) Interactions of Neisseria meningitidis with cells of the human meninges. Mol Microbiol 36: 817-829.
20. Horton, M. (1990) Vitronectin receptor: Tissue specific expression or adaptation to culture? Int J Exp Pathol 71: 741-759.
21. Isogai, C., Laug, W.E., Shimada, H., Declerck, P.J., Stins, M., Durden, D.L., et al. (2001) Plasminogen activator inhibitor-1 promotes angiogenesis by stimulating endothelial cell migration toward fibronectin. Cancer Res 61: 5587-5594.
22. Johnston, D.M., and Cannon, J.G. (1999) Construction of mutant strains of Neisseria gonorrhoeae lacking new antibiotic resistance markers using a two gene cassette with positive and negative selection. Gene 236: 179-184.
23. Jonsson, A.B., Nyberg, G., and Normark, S. (1991) Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J 10: 477-488.
24. Kriz, P., Vlckova, J., and Bobak, M. (1995) Targeted vaccination with meningococcal polysaccharide vaccine in one district of the Czech Republic. Epidemiol Infect 115: 411-418.
25. Kriz, P., Musilek, M., Skoczynska, A., and Hryniewicz, W. (2000) Genetic and antigenetic characteristics of Neisseria meningitidis strains isolated in the Czech Republic in 1997-98. Eur J Clin Microbiol Infect Dis 19: 452-459.
26. Kuusela, P. (1978) Fibronectin binds to Staphylococcus aureus. Nature 276: 718-720.
27. Levine, S. (1987) Choroid plexus: Target for systemic disease and pathway to the brain. Lab Invest 56: 231-233.
28. Lowrance, J.H., Hasty, D.L., and Simpson, W.A. (1988) Adherence of Streptococcus sanguis to conformationally specific determinants in fibronectin. Infect Immun 56: 2279-2285.
29. McNeil, G., and Virji, M. (1997) Phenotypic variants of meningococci and their potential in phagocytic interactions: The influence of opacity proteins, pili, PilC and surface sialic acids. Microb Pathog 22: 295-304.
30. Nizet, V., Kim, K.S., Stins, M., Jonas, M., Chi, E.Y., Nguyen, D., and Rubens, C.E. (1997) Invasion of brain microvascular endothelial cells by group B streptococci. Infect Immun 65: 5074-5081.
31. Ozeri, V., Rosenshine, I., Mosher, D.F., Fassler, R., and Hanski, E. (1998) Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol Microbiol 3: 625-637.
32. Panetti, T.S., and McKeown-Longo, P.J. (1993) The alpha v beta 5 integrin receptor regulates receptor-mediated endocytosis of vitronectin. J Biol Chem 268: 11492-11495.
33. Panetti, T.S., Wilcox, S.A., Horzempa, C., and McKeown-Longo, P.J. (1995) Alpha v beta 5 integrin receptor-mediated endocytosis of vitronectin is protein kinase C-dependent. J Biol Chem 270: 18593-18597.
34. Pierschbacher, M.D., and Ruoslahti, E. (1987) Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J Biol Chem 262: 17294-17298.
35. Pinner, R.W., Spellman, P.A., and Stephens, D.S. (1991) Evidence for functionally distinct pili expressed by Neisseria meningitidis. Infect Immun 59: 3169-3175.
36. Prasadaro, 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 human brain microvascular endothelial cell. Infect Immun 67: 1131-1138.
37. Pron, B., Taha, M.K., Rambaud, C., Fournet, J.C., Pattey, N., Monnet, J.P.,et al. (1997) Interaction of Neisseria meningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC. J Infect Dis 176: 1285-1292.
38. van Putten, J.P., Duensing, T.D., and Cole, R.L. (1998) Entry of OpaA+ gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol Microbiol 29: 369-379.
39. Ram, S., Sharma, A.K., Simpson, S.D., Gulati, S., McQuillen, D.P., Pangburn, M.K., and Rice, P.A. (1998) A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J Exp Med 187: 743-752.
40. Rubin, L.L., Hall, D.E., Porter, S., Barbu, K., Cannon, C., Horner, H.C., et al. (1991) A cell culture model of the blood-brain barrier. J Cell Biol 115: 1725-1735.
41. Rudel, T., van Putten, J.P., Gibbs, C.P., Haas, R., and Meyer, T.F. (1992) Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol Microbiol 6: 3439-3450.
42. Sarkari, J., Pandit, N., Moxon, E.R., and Achtman, M. (1994) Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing polycytidine. Mol Microbiol 13: 207-217.
43. Schulze-Koops, H., Burkhardt, H., Heesemann, J., Kirsch, T., Swoboda, B., Bull, C., et al. (1993) Outer membrane protein YadA of enteropathogenic yersiniae mediates specific binding to cellular but not plasma fibronectin. Infect Immun 61: 2513-2519.
44. Seiler, A., Reinhardt, R., Sarkari, J., Caugant, D.A., and Achtman, M. (1996) Allelic polymorphism and site-specific recombination in the opc locus of Neisseria meningitidis. Mol Microbiol 19: 841-856.
45. Simonson, C., Brener, D., and DeVoe, I.W. (1982) Expression of a high-affinity mechanism for acquisition of transferrin iron by Neisseria meningitidis. Infect Immun 36: 107-113.
46. 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.
47. Stins, M.F., Badger, J., and Kim, K.S. (2001) Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathog 30: 19-28.
48. Struncova, V., Kasal, E., Sedlack, D., Subert, I., Matouska, D., Krizova, P., and Taborska, J. (1998) Clinical course and sequelae of invasive meningococcal disease. In Abstracts of the Eleventh International Pathogenic Neisseria Conference. Nassif, X., Quentin-Millet, M.-J., and Taha, M.K. (eds), p. 88. International congress, Nice, France.
49. Tamura, G.S., and Rubens, C.E. (1995) Group B streptococci adhere to a variant of fibronectin attached to a solid phase. Mol Microbiol 15: 581-589.
50. Virji, M., and Everson, J.S. (1981) Comparative virulence of opacity variants of Neisseria gonorrhoeae strain P9. Infect Immun 31: 965-970.
51. Virji, M., Kayhty, H., Ferguson, D.J., Alexandrescu, C., Heckels, J.E., and Moxon, E.R. (1991) The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5: 1831-1841.
52. Virji, M., Makepeace, K., Ferguson, D.J., Achtman, M., Sarkari, J., and Moxon, E.R. (1992) Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol 6: 2785-2795.
53. Virji, M., Makepeace, K., Ferguson, D.J., Achtman, M., and Moxon, E.R. (1993) Meningococcal Opa and Opc proteins: Their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10: 499-510.
54. Virji, M., Makepeace, K., and Moxon, E.R. (1994) Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol Microbiol 14: 173-184.
55. Virji, M., Makepeace, K., Peak, I.R., Ferguson, D.J., Jennings, M.P., and Moxon, E.R. (1995) Opc- and pilus-dependent interactions of meningococci with human endothelial cells: Molecular mechanisms and modulation by surface polysaccharides. Mol Microbiol 18: 741-754.
56. Vogel, U., and Frosch, M. (1999) Mechanism of neisserial serum resistance. Mol Microbiol 32: 1133-1139.
57. de Vries, F.P., Cole, R., Dankert, J., Frosch, M., and van Putten, J.P. (1998) Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 27: 1203-1212.
58. Waage, A., Brandtzaeg, P., Halstensen, A., Kierulf, P., and Espevik, T. (1989) The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J Exp Med 169: 333-338.
59. Whalen, C.M., Hockin, J.C., Ryan, A., and Ashton, F. (1995) The changing epidemiology of invasive meningococcal disease in Canada, 1985 through 1992. Emergence of a virulent clone of Neisseria meningitidis. J Am Med Assoc 273: 390-394.
60. Woods, J.P., and Cannon, J.G. (1990) Variation in expression of class 1 and class 5 outer membrane proteins during nasopharyngeal carriage of Neisseria meningitidis. Infect Immun 58: 569-572.
61. Yamada, K.M., and Kennedy, D.W. (1984) Dualistic nature of adhesive protein function: Fibronectin and its biologically active peptide fragments can autoinhibit fibronectin function. J Cell Biol 99: 29-36.