Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis

Journal of Experimental Medicine

Volumn 201, Issue 10, 2005, Pages 1627-1635

  Que, Yok Ai ^b   Haefliger, Jacques Antoine ^b   Piroth, Lionel ^a   François, Patrice ^c   Widmer, Eleonora ^a   Entenza, José M ^a,b   Sinha, Bhanu ^d   Herrmann, Mathias ^e   Francioli, Patrick ^b   Vaudaux, Pierre ^c   Moreillon, Philippe ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^e SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; CLUMPING FACTOR A; FIBRINOGEN; FIBRONECTIN; FIBRONECTIN BINDING PROTEIN; FIBRONECTIN BINDING PROTEIN A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL ENDOCARDITIS; BINDING AFFINITY; CELL INVASION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; INTRACELLULAR TRANSPORT; LACTOBACILLUS DELBRUECKII; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SPLEEN; STAPHYLOCOCCUS AUREUS; VALVULAR HEART DISEASE;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; COAGULASE; ENDOCARDITIS, BACTERIAL; ENDOTHELIUM, VASCULAR; FEMALE; FIBRINOGEN; FIBRONECTINS; HEART VALVES; LACTOCOCCUS LACTIS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, WISTAR; SEQUENCE DELETION; SPLEEN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 21144433633     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20050125     Document Type: Article

References (54)

1. Lowy, F.D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
2. Foster, T.J., and M. Hook, 1998. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 6:484-488.
3. Dinges, M.M., P.M. Orwin, and P.M. Schlievert. 2000. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13:16-34.
4. Arvidson, S. 2000. Extracellular enzymes. In Gram-positive Pathogens. V.A. Fischetti, R.P. Novick, J.J. Ferretti, D.A. Portnoy, and J.I. Rood, editors. American Society for Microbiology, Washington, DC. 379-385.
5. Kintarak, S., S.A. Whawell, P.M. Speight, S. Packer, and S.P. Nair. 2004. Internalization of Staphylocuccus aureus by human keratinocytes. Infect. Immun. 72:5668-5675.
6. Almeida, R.A., K.R. Matthews, E. Cifrian, A.J. Guidry, and S.P. Oliver. 1996. Staphylococcus aureus invasion of bovine mammary epithelial cells. J. Dairy Sci. 79:1021-1026.
7. Bayles, K.W., C.A. Wesson, L.E. Liou, L.K. Fox, G.A. Bohach, and W.R. Trumble. 1998. Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect. Immun. 66:336-342.
8. 1. Cell. Microbiol. 1:101-117.
9. Jevon, M., C. Guo, B. Ma, N. Mordan, S.P. Nair, M. Harris, B. Henderson, G. Bentley, and S. Meghji, 1999. Mechanisms of internalization of Staphylococcus aureus by cultured human osteoblasts. Infect. Immun. 67:2677-2681.
10. Vann, J.M., R.J. Hamill, R.M. Albrecht, D.F. Mosher, and R.A. Proctor. 1989. Immunoelectron microscopic localization of fibronectin in adherence of Staphylococcus aureus to cultured bovine endothelial cells. J. Infect. Dis. 160:538-542.
11. Peacock, S.J., T.J. Foster, B.J. Cameron, and A.R. Berendt. 1999. Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology. 145:3477-3486.
12. Beekhuizen, H., J.S. van de Gevel, B. Olsson, I.J. van Benten, and R. van Furth. 1997. Infection of human vascular endothelial cells with Staphylococcus aureus induces hyperadhesiveness for human monocytes and granulocytes. J. Immunol. 158:774-782.
13. Moreillon, P., and Y.A. Que. 2004. Infective endocarditis. Lancet. 363: 139-149.
14. Novick, R.P., H.F. Ross, S.J. Projan, J. Kornblum, B. Kreiswirth, and S. Moghazeh. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12:3967-3975.
15. Cheung, A.L., J.M. Koomey, C.A. Butler, S.J. Projan, and V.A. Fischetti. 1992. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. Proc. Natl. Acad. Sci. USA. 89: 6462-6466.
16. Wu, S., H. de Lencastre, and A. Tomasz. 1996. Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing. J. Bacteriol. 178: 6036-6042.
17. Niebuhr, K., and P.J. Sansonetti. 2000. Invasion of epithelial cells by bacterial pathogens the paradigm of Shigella. Subcell. Biochem. 33:251-287.
18. Que, Y.A., P. François, J.A. Haefliger, J.M. Entenza, P. Vaudaux, and P. Moreillon. 2001. Reassessing the role of Staphylococcus aureus clumping-factor and fibronectin-binding protein by expression in Lactococcus lactis. Infect. Immun. 69:6296-6302.
19. McDevitt, D., P. Francois, P. Vaudaux, and T.J. Foster. 1994. Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol. Microbiol. 11:237-248.
20. Signas, C., G. Raucci, K. Jonsson, P.E. Lindgren, G.M. Anantharamaiah, M. Hook, and M. Lindberg. 1989. Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc. Natl. Acad. Sci. USA. 86:699-703.
21. Wann, E.R., S. Gurusiddappa, and M. Hook. 2000. The fibronectin-binding MSCRAMM FnBPA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J. Biol. Chem. 275:13863-13871.
22. Moreillon, P., J.M. Entenza, P. Francioli, D. McDevitt, T.J. Foster, P. Francois, and P. Vaudaux. 1995. Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect. Immun. 63:4738-4743.
23. Moreillon, P., P. Francioli, D. Overholser, P. Meylan, and M. Glauser. 1986. Mechanisms of successful amoxicillin prophylaxis of experimental endocarditis due to Streptococcus intermedius. J. Infect. Dis. 154:801-807.
24. Entenza, J.M., T.J. Foster, D. Ni Eidhin, P. Vaudaux, P. Francioli, and P. Moreillon. 2000. Contribution of clumping factor B to pathogenesis of experimental endocarditis due to Staphylococcus aureus. Infect. Immun. 68:5443-5446.
25. Stutzmann, P., J.M. Entenza, P. Vaudaux, P. Francioli, M.P. Glauser, and P. Moreillon. 2001. Study of Staphylococcus aureus pathogenic genes by transfer and expression in the less virulent organism Streptococcus gordonii. Infect. Immun. 69:657-664.
26. Durack, D.T., and P.B. Beeson. 1972. Experimental bacterial endocarditis. II. Survival of bacteria in endocardial vegetations. Br. J. Exp. Pathol. 53:50-53.
27. Durack, D.T. 1975. Experimental bacterial endocarditis. IV. Structure and evolution of very early lesions. J. Pathol. 115:81-89.
28. Dankert, J., J. Van den Werff, S.A.J. Zaat, W. Joldersma, D. Klein, and J. Hess. 1995. Involvement of bactericidal factors from thrombin-stimulated platelets in clearance of adherent viridans streptococci in experimental infective endocarditis. Infect. Immun. 63:663-671.
29. Gaillard, J.L., P. Berche, C. Frehel, E. Gouin, and P. Cossart. 1991. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 65:1127-1141.
30. Jett, B.D., and M.S. Gilmore. 2002. Internalization of Staphylococcus aureus by human corneal epithelial cells: role of bacterial fibronectin-binding protein and host cell factors. Infect. Immun. 70:4697-4700.
31. Haggar, A., M. Hussain, H. Lonnies, M. Herrmann, A. Norrby-Teglund, and J.I. Flock. 2003. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect. Immun. 71:2310-2317.
32. Shinji, H., K. Seki, A. Tajima, A. Uchida, and S. Masuda. 2003. Fibronectin bound to the surface of Staphyhcoccus aureus induces association of very late antigen 5 and intracellular signaling factors with macrophage cytoskeleton. Infect. Immun. 71:140-146.
33. Novick, R.P., and T.W. Muir. 1999. Virulence gene regulation by peptides in staphylococci and other Gram-positive bacteria. Curr. Opin. Microbiol. 2:40-45.
34. Moreillon, P., Y.A. Que, and A.S. Bayer. 2002. Pathogenesis of streptococcal and staphylococcal endocarditis. Infect. Dis. Clin. North Am. 16:297-318.
35. Massey, R.C., M.N. Kantzanou, T. Fowler, N.P. Day, K. Schofield, E.R. Wann, A.R. Berendt, M. Hook, and S.J. Peacock. 2001. Fibronectin-binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell Microbiol. 3:839-851.
36. Joh, D., P. Speziale, S. Gurusiddappa, J. Manor, and M. Hook. 1998. Multiple specificities of the staphylococcal and streptococcal fibronectin-binding microbial surface components recognizing adhesive matrix molecules. Eur. J. Biochem. 258:897-905.
37. McGavin, M.J., G. Raucci, S. Gurusiddappa, and M. Hook. 1991. Fibronectin binding determinants of the Staphylococcus aureus fibronectin receptor. J. Biol. Chem. 266:8343-8347.
38. Roche, P.M., R. Downer, F. Keane, P. Speziale, P.W. Park, and T.J. Foster. 2004. The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J. Biol. Chem. 279:38433-38440.
39. Schwarz-Linek, U., J.M. Werner, A.R. Pickford, S. Gurusiddappa, J.H. Kim, E.S. Pilka, J.A. Briggs, T.S. Gough, M. Hook, I.D. Campbell, and J.R. Potts. 2003. Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature. 423:177-181.
40. Veltrop, M.H., H. Beekhuizen, and J. Thompson. 1999. Bacterial species- and strain-dependent induction of tissue factor in human vascular endothelial cells. Infect. Immun. 67:6130-6138.
41. Menzies, B.E., and I. Kourteva. 1998. Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect. Immun. 66:5994-5998.
42. Ingham, K.C., S. Brew, D. Vaz, D.N. Sauder, and M.J. McGavin. 2004. Interaction of Staphylococcus aureus fibronectin-binding protein with fibronectin: affinity, stoichiometry, and modular requirements. J. Biol. Chem. 279:42945-42953.
43. House-Pompeo, K., Y. Xu, D. Joh, P. Speziale, and M. Hook. 1996. Conformational changes in the fibronectin binding MSCRAMMs are induced by ligand binding. J. Biol. Chem. 271:1379-1384.
44. Penkett, C.J., C. Redfield, J.A. Jones, I. Dodd, J. Hubbard, R.A. Smith, L.J. Smith, and C.M. Dobson. 1998. Structural and dynamical characterization of a biologically active unfolded fibronectin-binding protein from Staphylococcus aureus. Biochemistry. 37:17054-17067.
45. Roche, F.M., R. Massey, S.J. Peacock, N.P. Day, L. Visai, P. Speziale, A. Lam, M. Pallen, and T.J. Foster. 2003. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology. 149:643-654.
46. Terzaghi, B.E., and W.E. Sandine. 1975. Improved medium for lactic streptococci and their bacteriophages. Appl. Microbiol. 29:807-813.
47. Que, Y., J. Haefliger, P. Francioli, and P. Moreillon. 2000. Expression of Staphylococcus aureus dumping-factor A in Lactococcus lactis cremoris using a new shuttle vector. Infect. Immun. 68:3516-3522.
48. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Preparation and transformation of competent E. coli. In Molecular Cloning: A Laboratory Manual. Second edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 1.74-1.84.
49. Heraief, E., M.P. Glauser, and L.R. Freedman. 1982. Natural history of aortic valve endocarditis in rats. Infect. Immun. 37:127-131.
50. Elsinghorst, E.A. 1994. Measurement of invasion by gentamicin resistance. Methods Enzymol. 236:405-420.
51. Grundmeier, M., M. Hussain, P. Becker, C. Heilmann, G. Peters, and B. Sinha. 2004. Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect. Immun. 72:7155-7163.
52. Simon, D., and A. Chopin. 1988. Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis. Biochimie. 70:559-566.
53. Novick, R. 1967. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology. 33:155-166.
54. Greene, C., D. McDevitt, P. Francois, P.E. Vaudaux, D.P. Lew, and T.J. Foster. 1995. Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol. Microbiol. 17:1143-1152.