1887

Abstract

The binding of to fibronectin (Fn), a component of the extracellular matrix, is mediated by a 37 kDa outer-membrane protein termed CadF for hesion to ibronectin. The specificity of binding to Fn, via CadF, was demonstrated using antibodies reactive against Fn and CadF. More specifically, the anti-CadF antibody reduced the binding of two clinical isolates to immobilized Fn by greater than 50 %. Furthermore, a wild-type isolate, in contrast to the isogenic CadF mutant, was found to compete with another wild-type isolate for host cell receptors. Given the relationship between the pericellular Fn matrix and the cytoskeleton, the involvement of host cell cytoskeletal components in internalization was also examined. Cytochalasin D and mycalolide B microfilament depolymerizing agents resulted in a significant reduction in invasion. Studies targeting paxillin, a focal adhesion signalling molecule, identified an increased level of tyrosine phosphorylation upon infection of INT 407 cells. Collectively, these data suggest CadF promotes the binding of to Fn, which in turn stimulates a signal transduction pathway involving paxillin.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.25820-0
2003-01-01
2019-08-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/1/mic149_16.html?itemId=/content/journal/micro/10.1099/mic.0.25820-0&mimeType=html&fmt=ahah

References

  1. Allos, B. M. & Blaser, M. J. ( 1995; ). Campylobacter jejuni and the expanding spectrum of related infections. Clin Infect Dis 20, 1092–1099.[CrossRef]
    [Google Scholar]
  2. Alrutz, M. A. & Isberg, R. R. ( 1998; ). Involvement of focal adhesion kinase in invasin-mediated uptake. Proc Natl Acad Sci U S A 95, 13658–13663.[CrossRef]
    [Google Scholar]
  3. Bacon, D. J., Alm, R. A., Burr, D. H., Hu, L., Kopecko, D. J., Ewing, C. P., Trust, T. J. & Guerry, P. ( 2000; ). Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun 68, 4384–4390.[CrossRef]
    [Google Scholar]
  4. Badger, J. L., Stins, M. F. & Kim, K. S. ( 1999; ). Citrobacter freundii invades and replicates in human brain microvascular endothelial cells. Infect Immun 67, 4208–4215.
    [Google Scholar]
  5. Ballestrem, C., Wehrle-Haller, B., Hinz, B. & Imhof, B. A. ( 2000; ). Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration. Mol Biol Cell 11, 2999–3012.[CrossRef]
    [Google Scholar]
  6. Baloda, S. B., Faris, A., Fröman, G. & Waldström, T. ( 1985; ). Fibronectin binding to Salmonella strains. FEMS Microbiol Lett 28, 1–5.[CrossRef]
    [Google Scholar]
  7. Biswas, D., Itoh, K. & Sasakawa, C. ( 2000; ). Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol Med Microbiol 29, 203–211.[CrossRef]
    [Google Scholar]
  8. Bolla, J.-M., Loret, E., Zalewski, M. & Pagès, J.-M. ( 1995; ). Conformational analysis of the Campylobacter jejuni porin. J Bacteriol 177, 4266–4271.
    [Google Scholar]
  9. Clark, E. A. & Brugge, J. S. ( 1995; ). Integrins and signal transduction pathways: the road taken. Science 268, 233–239.[CrossRef]
    [Google Scholar]
  10. Cooper, J. A. ( 1987; ). Effects of cytochalasin and phalloidin on actin. J Cell Biol 105, 1473–1478.[CrossRef]
    [Google Scholar]
  11. Danen, E. H. & Yamada, K. M. ( 2001; ). Fibronectin, integrins, and growth control. J Cell Physiol 189, 1–13.[CrossRef]
    [Google Scholar]
  12. Dawson, J. R. & Ellen, R. P. ( 1990; ). Tip-oriented adherence of Treponema denticola to fibronectin. Infect Immun 58, 3924–3928.
    [Google Scholar]
  13. Dawson, J. R. & Ellen, R. P. ( 1994; ). Clustering of fibronectin adhesins toward Treponema denticola tips upon contact with immobilized fibronectin. Infect Immun 62, 2214–2221.
    [Google Scholar]
  14. De Melo, M. A. & Pechère, J.-C. ( 1990; ). Identification of Campylobacter jejuni surface proteins that bind to eucaryotic cells in vitro. Infect Immun 58, 1749–1756.
    [Google Scholar]
  15. Fauchère, J. L., Rosenau, A., Véron, M., Moyen, E. N., Richard, S. & Pfister, A. ( 1986; ). Association with HeLa cells of Campylobacter jejuni and Campylobacter coli isolated from human feces. Infect Immun 54, 283–287.
    [Google Scholar]
  16. Fauchère, J.-L., Kervella, M., Rosenau, A., Mohanna, K. & Véron, M. ( 1989; ). Adhesion to HeLa cells of Campylobacter jejuni and C. coli outer membrane components. Res Microbiol 140, 379–392.[CrossRef]
    [Google Scholar]
  17. Finlay, B. B., Ruschkowski, S. & Dedhar, S. ( 1991; ). Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J Cell Sci 99, 283–296.
    [Google Scholar]
  18. Francis, C. L., Starnbach, M. N. & Falkow, S. ( 1992; ). Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella typhimurium grown under low-oxygen conditions. Mol Microbiol 6, 3077–3087.[CrossRef]
    [Google Scholar]
  19. Francis, C. L., Ryan, T. A., Jones, B. D., Smith, S. J. & Falkow, S. ( 1993; ). Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364, 639–642.[CrossRef]
    [Google Scholar]
  20. Fröman, G., Switalski, L. M., Faris, A., Wadström, T. & Höök, M. ( 1984; ). Binding of Escherichia coli to fibronectin. J Biol Chem 259, 14899–14905.
    [Google Scholar]
  21. Goode, B. L., Drubin, D. G. & Barnes, G. ( 2000; ). Functional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12, 63–71.[CrossRef]
    [Google Scholar]
  22. Gumbiner, B. M. ( 1996; ). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345–357.[CrossRef]
    [Google Scholar]
  23. Hu, L. & Kopecko, D. J. ( 1999; ). Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect Immun 67, 4171–4182.
    [Google Scholar]
  24. Hu, L. & Kopecko, D. J. ( 2000; ). Interactions of Campylobacter with eukaryotic cells: gut luminal colonization and mucosal invasion mechanisms. In Campylobacter, 2nd edn, pp. 191–215. Edited by I. Nachamkin & M. J. Blaser. Washington, DC: American Society for Microbiology.
  25. Humason, G. L. ( 1979; ). Animal Tissue Techniques. San Francisco, CA: W. H. Freeman.
  26. Hynes, R. O. ( 1992; ). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11–25.[CrossRef]
    [Google Scholar]
  27. Isberg, R. R. & Tran Van Nhieu, G. ( 1994; ). Two mammalian cell internalization strategies used by pathogenic bacteria. Annu Rev Genet 28, 395–422.[CrossRef]
    [Google Scholar]
  28. Jaffe, J., Natanson-Yaron, S., Caparon, M. G. & Hanski, E. ( 1996; ). Protein F2, a novel fibronectin-binding protein from Streptococcus pyogenes, possesses two binding domains. Mol Microbiol 21, 373–384.[CrossRef]
    [Google Scholar]
  29. Jin, S., Joe, A., Lynett, J., Hani, E. K., Sherman, P. & Chan, V. L. ( 2001; ). JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol Microbiol 39, 1225–1236.[CrossRef]
    [Google Scholar]
  30. Kelle, K., Pagès, J.-M. & Bolla, J.-M. ( 1998; ). A putative adhesin gene cloned from Campylobacter jejuni. Res Microbiol 149, 723–733.[CrossRef]
    [Google Scholar]
  31. Kervella, M., Pagès, J.-M., Pei, Z., Grollier, G., Blaser, M. J. & Fauchère, J.-L. ( 1993; ). Isolation and characterization of two Campylobacter glycine-extracted proteins that bind to HeLa cell membranes. Infect Immun 61, 3440–3448.
    [Google Scholar]
  32. Konkel, M. E., Mead, D. J. & Cieplak, W., Jr ( 1993; ). Kinetic and antigenic characterization of altered protein synthesis by Campylobacter jejuni during cultivation with human epithelial cells. J Infect Dis 168, 948–954.[CrossRef]
    [Google Scholar]
  33. Konkel, M. E., Garvis, S. G., Tipton, S. L., Anderson, D. E., Jr & Cieplak, W., Jr ( 1997; ). Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni. Mol Microbiol 24, 953–963.[CrossRef]
    [Google Scholar]
  34. Konkel, M. E., Gray, S. A., Kim, B. J., Garvis, S. G. & Yoon, J. ( 1999; ). Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J Clin Microbiol 37, 510–517.
    [Google Scholar]
  35. Kopecko, D. J., Hu, L. & Zaal, K. J. ( 2001; ). Campylobacter jejuni – microtubule-dependent invasion. Trends Microbiol 9, 389–396.[CrossRef]
    [Google Scholar]
  36. Kuusela, P. ( 1978; ). Fibronectin binds to Staphylococcus aureus. Nature 276, 718–720.[CrossRef]
    [Google Scholar]
  37. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  38. Lyngstadaas, A., Lobner-Olesen, A., Grelland, E. & Boye, E. ( 1999; ). The gene for 2-phosphoglycolate phosphatase (gph) in Escherichia coli is located in the same operon as dam and at least five other diverse genes. Biochim Biophys Acta 1472, 376–384.[CrossRef]
    [Google Scholar]
  39. McSweegan, E. & Walker, R. I. ( 1986; ). Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect Immun 53, 141–148.
    [Google Scholar]
  40. Mejillano, M. R., Shivanna, B. D. & Himes, R. H. ( 1996; ). Studies on the nocodazole-induced GTPase activity of tubulin. Arch Biochem Biophys 336, 130–138.[CrossRef]
    [Google Scholar]
  41. Miyamoto, S., Katz, B.-Z., LaFrenie, R. M. & Yamada, K. M. ( 1998; ). Fibronectin and integrins in cell adhesion, signaling, and morphogenesis. Ann N Y Acad Sci 857, 119–129.[CrossRef]
    [Google Scholar]
  42. Moser, I. & Schröder, W. ( 1995; ). Binding of outer membrane preparations of Campylobacter jejuni to INT 457 cell membranes and extracellular matrix proteins. Med Microbiol Immunol 184, 147–153.
    [Google Scholar]
  43. Moser, I., Schröder, W. F. & Hellmann, E. ( 1992; ). In vitro binding of Campylobacter jejuni/coli outer membrane preparations to INT 407 cell membranes. Med Microbiol Immunol 180, 289–303.
    [Google Scholar]
  44. Moser, I., Schröder, W. & Salnikow, J. ( 1997; ). Campylobacter jejuni major outer membrane protein and a 59-kDa protein are involved in binding to fibronectin and INT 407 cell membranes. FEMS Microbiol Lett 157, 233–238.
    [Google Scholar]
  45. Myhre, E. B. & Kuusela, P. ( 1983; ). Binding of human fibronectin to group A, C, and G Streptococci. Infect Immun 40, 29–34.
    [Google Scholar]
  46. Oelschlaeger, T. A., Guerry, P. & Kopecko, D. J. ( 1993; ). Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc Natl Acad Sci U S A 90, 6884–6888.[CrossRef]
    [Google Scholar]
  47. Parkhill, J., Wren, B. W., Mungall, K. & 18 other authors ( 2000; ). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668.[CrossRef]
    [Google Scholar]
  48. Pei, Z. & Blaser, M. J. ( 1993; ). PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in Gram-negative nutrient transport systems. J Biol Chem 268, 18717–18725.
    [Google Scholar]
  49. Pei, Z., Burucoa, C., Grignon, B., Baqar, S., Huang, X.-Z., Kopecko, D. J., Bourgeois, A. L., Fauchere, J.-L. & Blaser, M. J. ( 1998; ). Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect Immun 66, 938–943.
    [Google Scholar]
  50. Quaroni, A., Isselbacher, K. J. & Ruoslahti, E. ( 1978; ). Fibronectin synthesis by epithelial crypt cells of rat small intestine. Proc Natl Acad Sci U S A 75, 5548–5552.[CrossRef]
    [Google Scholar]
  51. Roberts, D. D. ( 1990; ). Interactions of respiratory pathogens with host cell surface and extracellular matrix components. Am J Respir Cell Mol Biol 3, 181–186.[CrossRef]
    [Google Scholar]
  52. Rydén, C., Rubin, K., Speziale, P., Höök, M., Lindberg, M. & Wadström, T. ( 1983; ). Fibronectin receptors from Staphylococcus aureus. J Biol Chem 258, 3396–3401.
    [Google Scholar]
  53. Saito, S., Watabe, S., Ozaki, H., Fusetani, N. & Karaki, H. ( 1994; ). Mycalolide B, a novel actin depolymerizing agent. J Biol Chem 269, 29710–29714.
    [Google Scholar]
  54. Saito, S. Y., Watabe, S., Ozaki, H., Kobayashi, M., Suzuki, T., Kobayashi, H., Fusetani, N. & Karaki, H. ( 1998; ). Actin-depolymerizing effect of dimeric macrolides, bistheonellide A and swinholide A1. J Biochem 123, 571–578.[CrossRef]
    [Google Scholar]
  55. Sarkar, S. ( 1999; ). Focal adhesions. Curr Biol 9, R428.[CrossRef]
    [Google Scholar]
  56. Sastry, S. K. & Burridge, K. ( 2000; ). Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics. Exp Cell Res 261, 25–36.[CrossRef]
    [Google Scholar]
  57. Schlaepfer, D. D., Hauck, C. R. & Sieg, D. J. ( 1999; ). Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71, 435–478.[CrossRef]
    [Google Scholar]
  58. Schorey, J. S., Holsti, M. A., Ratliff, T. L., Allen, P. M. & Brown, E. J. ( 1996; ). Characterization of the fibronectin-attachment protein of Mycobacterium avium reveals a fibronectin-binding motif conserved among mycobacteria. Mol Microbiol 21, 321–329.[CrossRef]
    [Google Scholar]
  59. Schröder, W. & Moser, I. ( 1997; ). Primary structure analysis and adhesion studies on the major outer membrane protein of Campylobacter jejuni. FEMS Microbiol Lett 150, 141–147.[CrossRef]
    [Google Scholar]
  60. Tachibana, K., Sato, T., D′Avirro, N. & Morimoto, C. ( 1995; ). Direct association of pp125FAK with paxillin, the focal adhesion-targeting mechanism of pp125FAK. J Exp Med 182, 1089–1100.[CrossRef]
    [Google Scholar]
  61. Thomas, D. D., Baseman, J. B. & Alderete, J. F. ( 1985; ). Fibronectin mediates Treponema pallidum cytadherence through recognition of fibronectin cell-binding domain. J Exp Med 161, 514–525.[CrossRef]
    [Google Scholar]
  62. van der Flier, A. & Sonnenberg, A. ( 2001; ). Function and interactions of integrins. Cell Tissue Res 305, 285–298.[CrossRef]
    [Google Scholar]
  63. van Putten, J. P., Duensing, T. D. & 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.[CrossRef]
    [Google Scholar]
  64. Visai, L., Bozzini, S., Petersen, T. E., Speciale, L. & Speziale, P. ( 1991; ). Binding sites in fibronectin for an enterotoxigenic strain of E. coli B342289c. FEBS Lett 290, 111–114.[CrossRef]
    [Google Scholar]
  65. Vuori, K. ( 1998; ). Integrin signaling: tyrosine phosphorylation events in focal adhesions. J Membr Biol 165, 191–199.[CrossRef]
    [Google Scholar]
  66. Wada, S., Matsunaga, S., Saito, S., Fusetani, N. & Watabe, S. ( 1998; ). Actin-binding specificity of marine macrolide toxins, mycalolide B and kabiramide D. J Biochem 123, 946–952.[CrossRef]
    [Google Scholar]
  67. Wassenaar, T. M. & Blaser, M. J. ( 1999; ). Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1, 1023–1033.[CrossRef]
    [Google Scholar]
  68. Watarai, M., Funato, S. & Sasakawa, C. ( 1996; ). Interaction of Ipa proteins of Shigella flexneri with α5β1 integrin promotes entry of the bacteria into mammalian cells. J Exp Med 183, 991–999.[CrossRef]
    [Google Scholar]
  69. Wooldridge, K. G., Williams, P. H. & Ketley, J. M. ( 1996; ). Host signal transduction and endocytosis of Campylobacter jejuni. Microb Pathog 21, 299–305.[CrossRef]
    [Google Scholar]
  70. Ziprin, R. L., Young, C. R., Hume, M. E. & Konkel, M. E. ( 1999; ). The absence of cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin-binding protein. Avian Dis 43, 586–589.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.25820-0
Loading
/content/journal/micro/10.1099/mic.0.25820-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error