Source: http://www.asmscience.org/content/book/10.1128/9781555816513.chap42
Timestamp: 2019-04-20 04:26:06+00:00

Document:
The pathogen Staphylococcus aureus causes a diversity of diseases that range from minor skin and soft tissue infections to life-threatening systemic infections. S. aureus-endothelial cell interactions have been the most extensively studied and are among the most important events in the pathogenesis of invasive systemic disease. While this chapter primarily focuses on S. aureus-endothelial cell interactions as a model of staphylococcal interaction with eukaryotic cells, reference is also made to more recent publications describing staphylococcal interactions with other cell types. S. aureus adherence to endothelial cells is the critical first step in the invasion process. It was demonstrated that staphylococci adhere to endovascular tissue and endothelial cells grown in tissue culture more avidly than do other bacterial species. In general, the bacterial species most commonly associated with acute bacterial endocarditis were also the most adherent. Variation in endothelial cell growth conditions altered adherence of staphylococci to endothelial cells. A variety of cellular changes occurs as a result of S. aureus invasion. Surface expression of proteins, such as Fc receptors and adhesion molecules, as well as secretion of cytokines, all occur in response to staphylococcal invasion. A prevailing concern regarding the in vitro observations of S. aureus invasion of eukaryotic cells has been the limited amount of supporting clinical and experimental in vivo data. S. aureus appears able to partially modulate the host cell-mediated immune response by eliciting or inhibiting its inflammatory response, which could account for differences in the outcomes of the infective process.
Model for S. aureus–endothelial cell interactions. Staphylococci adhere using fibronectin (Fn) as a bridging ligand to host cell integrin α5β1 and Hsp60. This process elicits endothelial cell-mediated phagocytosis of S. aureus and the subsequent phagolysosomal fusion. S. aureus escapes the endosome through the action of unidentified toxins. Staphylococci in the cytosol can induce host cell apoptosis via a variety of pathways involving among other components alphatoxin, host cell caspases and Jun amino-terminal kinase. S. aureus cells induce expression of a wide range of both secreted and host cell surface factors. Some of these molecules are in turn involved in pathogenetic processes that include recruitment of PMN leukocytes and monocytes to sites of infection with migration across the endovascular tissue and the ECM to sites of inflammation. S. aureus cells also elaborate a variety of proteolytic enzymes that facilitate their translocation across the ECM to adjacent tissues.
1. Agerer, F.,, A. Michel,, K. Ohlsen,, and C. R. Hauck. 2003. Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J. Biol. Chem. 278: 42524– 42531.
2. Ahmed, S.,, S. Meghji,, R. J. Williams,, B. Henderson,, J. H. Brock,, and S. P. Nair. 2001. Staphylococcus aureus fibronectin-binding proteins are essential for internalization by osteoblasts but do not account for differences in intracellular levels of bacteria. Infect. Immun. 69: 2872– 2877.
3. Alexander, E. H.,, J. L. Bento,, F. M. Hughes, Jr.,, I. Marriott,, M. C. Hudson,, and K. L. Bost. 2001. Staphylococcus aureus and Salmonella enterica serovar Dublin induce tumor necrosis factor-related apoptosis-inducing ligand expression by normal mouse and human osteoblasts. Infect. Immun. 69: 1581– 1586.
4. Alexander, E. H.,, and M. C. Hudson. 2001. Factors influencing the internalization of Staphylococcus aureus and impacts on the course of infections in humans. Appl. Microbiol. Biotechnol. 56: 361– 366.
5. Alexander, E. H.,, F. A. Rivera,, I. Marriott,, J. Anguita,, K. L. Bost,, and M. C. Hudson. 2003. Staphylococcus aureus-induced tumor necrosis factor-related apoptosisinducing ligand expression mediates apoptosis and caspase-8 activation in infected osteoblasts. BMC Microbiol. 3: 5.
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. Alston, W. K.,, D. A. Elliott,, M. E. Epstein,, V. B. Hatcher,, M. Tang,, and F. D. Lowy. 1997. Extracellular matrix heparan sulfate modulates endothelial cell susceptibility to Staphylococcus aureus. J. Cell Physiol. 173: 102– 109.
8. Balwit, J. M.,, P. van Langevelde,, J. M. Vann,, and R. A. Proctor. 1994. Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J. Infect. Dis. 170: 1033– 1037.
9. Baran, J.,, K. Guzik,, W. Hryniewicz,, M. Ernst,, H. D. Flad,, and J. Pryjma. 1996. Apoptosis of monocytes and prolonged survival of granulocytes as a result of phagocytosis of bacteria. Infect. Immun. 64: 4242– 4248.
10. 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.
11. 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.
12. Bengualid, V.,, V. B. Hatcher,, B. Diamond,, E. A. Blumberg,, and F. D. Lowy. 1990. Staphylococcus aureus infection of human endothelial cells potentiates Fc receptor expression. J. Immunol. 145: 4279– 4283.
13. Blumberg, E. A.,, V. B. Hatcher,, and F. D. Lowy. 1988. Acidic fibroblast growth factor modulates Staphylococcus aureus adherence to human endothelial cells. Infect. Immun. 56: 1470– 1474.
14. Bost, K. L.,, J. L. Bento,, J. K. Ellington,, I. Marriott,, and M. C. Hudson. 2000. Induction of colony-stimulating factor expression following Staphylococcus or Salmonella interaction with mouse or human osteoblasts. Infect. Immun. 68: 5075– 5083.
15. Bost, K. L.,, W. K. Ramp,, N. C. Nicholson,, J. L. Bento,, I. Marriott,, and M. C. Hudson. 1999. Staphylococcus aureus infection of mouse or human osteoblasts induces high levels of interleukin-6 and interleukin-12 production. J. Infect. Dis. 180: 1912– 1920.
16. Brouillette, E.,, B. G. Talbot,, and F. Malouin. 2003. The fibronectin-binding proteins of Staphylococcus aureus may promote mammary gland colonization in a lactating mouse model of mastitis. Infect. Immun. 71: 2292– 2295.
17. Chavakis, T.,, M. Hussain,, S. M. Kanse,, G. Peters,, R. G. Bretzel,, J. I. Flock,, M. Herrmann,, and K. T. Preissner. 2002. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat. Med. 8: 687– 693.
18. Cheung, A. L.,, and V. A. Fischetti. 1990. The role of fibrinogen in staphylococcal adherence to catheters in vitro. J. Infect. Dis. 161: 1177– 1186.
19. 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.
20. Cheung, A. L.,, J. M. Koomey,, S. Lee,, E. A. Jaffe,, and V. A. Fischetti. 1991. Recombinant human tumor necrosis factor-α promotes adherence of Staphylococcus aureus to cultured human endothelial cells. Infect. Immun. 59: 3827– 3831.
21. Craven, N.,, and J. C. Anderson. 1979. The location of Staphylococcus aureus in experimental chronic mastitis in the mouse and the effect on the action of sodium cloxacillin. Br. J. Exp. Pathol. 60: 453– 459.
22. Drake, T. A.,, and M. Pang. 1988. Staphylococcus aureus induces tissue factor expression in cultured human cardiac valve endothelium. J. Infect. Dis. 157: 749– 756.
23. Dziewanowska, K.,, A. R. Carson,, J. M. Patti,, C. F. Deobald,, K. W. Bayles,, and G. A. Bohach. 2000. Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins: role in internalization by epithelial cells. Infect. Immun. 68: 6321– 6328.
24. Dziewanowska, K.,, J. M. Patti,, C. F. Deobald,, K. W. Bayles,, W. R. Trumble,, and G. A. Bohach. 1999. Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect. Immun. 67: 4673– 4678.
25. Esen, M.,, B. Schreiner,, V. Jendrossek,, F. Lang,, K. Fassbender,, H. Grassme,, and E. Gulbins. 2001. Mechanisms of Staphylococcus aureus induced apoptosis of human endothelial cells. Apoptosis 6: 431– 439.
26. Gomez, M. I.,, A. Lee,, B. Reddy,, A. Muir,, G. Soong,, A. Pitt,, A. Cheung,, and A. Prince. 2004. Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat. Med. 10: 842– 848.
27. Gould, K.,, C. H. Ramirez-Ronda,, R. K. Holmes,, and J. P. Sanford. 1975. Adherence of bacteria to heart valves in vitro. J. Clin. Invest. 56: 1364– 1370.
28. Gresham, H. D.,, J. H. Lowrance,, T. E. Caver,, B. S. Wilson,, A. L. Cheung,, and F. P. Lindberg. 2000. Survival of Staphylococcus aureus inside neutrophils contributes to infection. J. Immunol. 164: 3713– 3722.
29. 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.
30. Hamill, R. J.,, J. M. Vann,, and R. A. Proctor. 1986. Phagocytosis of Staphylococcus aureus by cultured bovine aortic endothelial cells: model for postadherence events in endovascular infections. Infect. Immun. 54: 833– 836.
31. Harraghy, N.,, M. Hussain,, A. Haggar,, T. Chavakis,, B. Sinha,, M. Herrmann,, and J. I. Flock. 2003. The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology 149: 2701– 2707.
32. Haslinger, B.,, K. Strangfeld,, G. Peters,, K. Schulze-Osthoff,, and B. Sinha. 2003. Staphylococcus aureus-toxin induces apoptosis in peripheral blood mononuclear cells: role of endogenous tumour necrosis factor-α and the mitochondrial death pathway. Cell Microbiol. 5: 729– 741.
33. Heilmann, C.,, M. Herrmann,, B. E. Kehrel,, and G. Peters. 2002. Platelet-binding domains in 2 fibrinogen-binding proteins of Staphylococcus aureus identified by phage display. J. Infect. Dis. 186: 32– 39.
34. Heilmann, C.,, S. Niemann,, B. Sinha,, M. Herrmann,, B. E. Kehrel,, and G. Peters. 2004. Staphylococcus aureus fibronectin-binding protein (FnBP)-mediated adherence to platelets, and aggregation of platelets induced by FnBPA but not by FnBPB. J. Infect. Dis. 190: 321– 329.
35. Herrmann, M.,, Q. J. Lai,, R. M. Albrecht,, D. F. Mosher,, and R. A. Proctor. 1993. Adhesion of Staphylococcus aureus to surface-bound platelets: role of fibrinogen/fibrin and platelet integrins. J. Infect. Dis. 167: 312– 322.
36. Hess, D. J.,, M. J. Henry-Stanley,, E. A. Erickson,, and C. L. Wells. 2003. Intracellular survival of Staphylococcus aureus within cultured enterocytes. J. Surg. Res. 114: 42– 49.
37. Hudson, M. C.,, W. K. Ramp,, N. C. Nicholson,, A. S. Williams,, and M. T. Nousiainen. 1995. Internalization of Staphylococcus aureus by cultured osteoblasts. Microb. Pathog. 19: 409– 419.
38. Hussain, M.,, A. Haggar,, C. Heilmann,, G. Peters,, J. I. Flock,, and M. Herrmann. 2002. Insertional inactivation of Eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect. Immun. 70: 2933– 2940.
39. Ing, M. B.,, L. M. Baddour,, and A. S. Bayer,. 1997. Bacteremia, and infective endocarditis: pathogenesis, diagnosis, and complications, p. 331– 354. In K. B. Crossley, and G. L. Archer (ed.), The Staphylococci in Human Disease. Churchill Livingstone, New York, N.Y.
40. Johnson, C. M.,, G. A. Hancock,, and G. D. Goulin. 1988. Specific binding of Staphylococcus aureus to cultured porcine cardiac valvular endothelial cells. J. Lab. Clin. Med. 112: 16– 22.
41. Jung, K. Y.,, J. D. Cha,, S. H. Lee,, W. H. Woo,, D. S. Lim,, B. K. Choi,, and K. J. Kim. 2001. Involvement of staphylococcal protein A and cytoskeletal actin in Staphylococcus aureus invasion of cultured human oral epithelial cells. J. Med. Microbiol. 50: 35– 41.
42. Juuti, K. M.,, B. Sinha,, C. Werbick,, G. Peters,, and P. I. Kuusela. 2004. Reduced adherence and host cell invasion by methicillin-resistant Staphylococcus aureus expressing the surface protein Pls. J. Infect. Dis. 189: 1574– 1584.
43. Kahl, B. C.,, M. Goulian,, W. van Wamel,, M. Herrmann,, S. M. Simon,, G. Kaplan,, G. Peters,, and A. L. Cheung. 2000. Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line. Infect. Immun. 68: 5385– 5392.
44. Kielian, T.,, A. Cheung,, and W. F. Hickey. 2001. Diminished virulence of an α-toxin mutant of Staphylococcus aureus in experimental brain abscesses. Infect. Immun. 69: 6902– 6911.
45. Kluytmans, J.,, A. van Belkum,, and H. Verbrugh. 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10: 505– 520.
46. Kreikemeyer, B.,, D. McDevitt,, and A. Podbielski. 2002. The role of the map protein in Staphylococcus aureus matrix protein and eukaryotic cell adherence. Int. J. Med. Microbiol. 292: 283– 295.
47. Kupferwasser, L. I.,, M. R. Yeaman,, S. M. Shapiro,, C. C. Nast,, and A. S. Bayer. 2002. In vitro susceptibility to thrombin-induced platelet microbicidal protein is associated with reduced disease progression and complication rates in experimental Staphylococcus aureus endocarditis: microbiological, histopathologic, and echocardiographic analyses. Circulation 105: 746– 752.
48. Lee, L. Y.,, Y. J. Miyamoto,, B. W. McIntyre,, M. Hook,, K. W. McCrea,, D. McDevitt,, and E. L. Brown. 2002. The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J. Clin. Invest. 110: 1461– 1471.
49. Lee, M. S.,, S. W. Ueng,, C. H. Shih,, and C. C. Chao. 2001. Primary cultures of human chondrocytes are susceptible to low inocula of Staphylococcus aureus infection and undergo apoptosis. Scand. J. Infect. Dis. 33: 47– 50.
50. Lowy, F. D. 2000. Is Staphylococcus aureus an intracellular pathogen? Trends Microbiol. 8: 341– 343.
51. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520– 532.
52. Lowy, F. D.,, J. Fant,, L. L. Higgins,, S. K. Ogawa,, and V. B. Hatcher. 1988. Staphylococcus aureus—human endothelial cell interactions. J. Ultrastruct. Mol. Struct. Res. 98: 137– 146.
53. Lundqvist-Gustafsson, H.,, S. Norrman,, J. Nilsson,, and A. Wilsson. 2001. Involvement of p38-mitogen-activated protein kinase in Staphylococcus aureus-induced neutrophil apoptosis. J. Leukoc. Biol. 70: 642– 648.
54. Marriott, I.,, D. L. Gray,, S. L. Tranguch,, V. G. Fowler, Jr.,, M. Stryjewski,, L. Scott Levin,, M. C. Hudson,, and K. L. Bost. 2004. Osteoblasts express the inflammatory cytokine interleukin-6 in a murine model of Staphylococcus aureus osteomyelitis and infected human bone tissue. Am. J. Pathol. 164: 1399– 1406.
55. 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.
56. Menzies, B. E.,, and I. Kourteva. 1998. Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect. Immun. 66: 5994– 5998.
57. Menzies, B. E.,, and I. Kourteva. 2000. Staphylococcus aureus α-toxin induces apoptosis in endothelial cells. FEMS Immunol. Med. Microbiol. 29: 39– 45.
58. Molinari, G.,, and G. S. Chhatwal. 1999. Streptococcal invasion. Curr. Opin. Microbiol. 2: 56– 61.
59. Moreillon, P.,, Y. A. Que,, and A. S. Bayer. 2002. Pathogenesis of streptococcal and staphylococcal endocarditis. Infect. Dis. Clin. North Am. 16: 297– 318.
60. Moreland, J. G.,, G. Bailey,, W. M. Nauseef,, and J. P. Weiss. 2004. Organism-specific neutrophil-endothelial cell interactions in response to Escherichia coli, Streptococcus pneumoniae, and Staphylococcus aureus. J. Immunol. 172: 426– 432.
61. Murai, M.,, J. Sakurada,, K. Seki,, H. Shinji,, Y. Hirota,, and S. Masuda. 1999. Apoptosis observed in BALB/3T3 cells having ingested Staphylococcus aureus. Microbiol. Immunol. 43: 653– 661.
62. Nguyen, T.,, B. Ghebrehiwet,, and E. I. Peerschke. 2000. Staphylococcus aureus protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infect. Immun. 68: 2061– 2068.
63. Nilsdotter-Augustinsson, A.,, A. Wilsson,, J. Larsson,, O. Stendahl,, L. Ohman,, and H. Lundqvist-Gustafsson. 2004. Staphylococcus aureus, but not Staphylococcus epidermidis, modulates the oxidative response and induces apoptosis in human neutrophils. APMIS 112: 109– 118.
64. Nuzzo, I.,, M. R. Sanges,, A. Folgore,, and C. R. Carratelli. 2000. Apoptosis of human keratinocytes after bacterial invasion. FEMS Immunol. Med. Microbiol. 27: 235– 240.
65. O’Brien, L. M.,, E. J. Walsh,, R. C. Massey,, S. J. Peacock,, and T. J. Foster. 2002. Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol. 4: 759– 770.
66. Ogawa, S. K.,, E. R. Yurberg,, V. B. Hatcher,, M. A. Levitt,, and F. D. Lowy. 1985. Bacterial adherence to human endothelial cells in vitro. Infect. Immun. 50: 218– 224.
67. Patti, J. M.,, B. L. Allen,, M. J. McGavin,, and M. Hook. 1994. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48: 585– 617.
68. Pawar, P.,, P. K. Shin,, S. A. Mousa,, J. M. Ross,, and K. Konstantopoulos. 2004. Fluid shear regulates the kinetics and receptor specificity of Staphylococcus aureus binding to activated platelets. J. Immunol. 173: 1258– 1265.
69. Peacock, S. J.,, I. de Silva,, and F. D. Lowy. 2001. What determines nasal carriage of Staphylococcus aureus? Trends Microbiol. 9: 605– 610.
70. 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.
71. Peng, H. L.,, R. P. Novick,, B. Kreiswirth,, J. Kornblum,, and P. Schlievert. 1988. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170: 4365– 4372.
72. Pohlmann-Dietze, P.,, M. Ulrich,, K. B. Kiser,, G. Doring,, J. C. Lee,, J. M. Fournier,, K. Botzenhart,, and C. Wolz. 2000. Adherence of Staphylococcus aureus to endothelial cells: influence of capsular polysaccharide, global regulator agr, and bacterial growth phase. Infect. Immun. 68: 4865– 4871.
73. Proctor, R. A.,, P. van Langevelde,, M. Kristjansson,, J. N. Maslow,, and R. D. Arbeit. 1995. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20: 95– 102.
74. Qamer, S.,, J. A. Sandoe,, and K. G. Kerr. 2003. Use of colony morphology to distinguish different enterococcal strains and species in mixed culture from clinical specimens. J. Clin. Microbiol. 41: 2644– 2646.
75. Reddy, K.,, and J. M. Ross. 2001. Shear stress prevents fibronectin binding protein-mediated Staphylococcus aureus adhesion to resting endothelial cells. Infect. Immun. 69: 3472– 3475.
76. Reilly, S. S.,, M. C. Hudson,, J. F. Kellam,, and W. K. Ramp. 2000. In vivo internalization of Staphylococcus aureus by embryonic chick osteoblasts. Bone 26: 63– 70.
77. Roche, F. M.,, M. Meehan,, and T. J. Foster. 2003. The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 149: 2759– 2767.
78. Ruoslahti, E. 1996. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12: 697– 715.
79. Shenkman, B.,, E. Rubinstein,, A. L. Cheung,, G. E. Brill,, R. Dardik,, I. Tamarin,, N. Savion,, and D. Varon. 2001. Adherence properties of Staphylococcus aureus under static and flow conditions: roles of agr and sar loci, platelets, and plasma ligands. Infect. Immun. 69: 4473– 4478.
80. Shenkman, B.,, E. Rubinstein,, I. Tamarin,, R. Dardik,, N. Savion,, and D. Varon. 2000. Staphylococcus aureus adherence to thrombin-treated endothelial cells is mediated by fibrinogen but not by platelets. J. Lab. Clin. Med. 135: 43– 51.
81. Shenkman, B.,, D. Varon,, I. Tamarin,, R. Dardik,, M. Peisachov,, N. Savion,, and E. Rubinstein. 2002. Role of agr (RNAIII) in Staphylococcus aureus adherence to fibrinogen, fibronectin, platelets and endothelial cells under static and flow conditions. J. Med. Microbiol. 51: 747– 754.
82. Shompole, S.,, K. T. Henon,, L. E. Liou,, K. Dziewanowska,, G. A. Bohach,, and K. W. Bayles. 2003. Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agr-mediated diffusion sensing. Mol. Microbiol. 49: 919– 927.
83. Sinha, B.,, P. Francois,, Y. A. Que,, M. Hussain,, C. Heilmann,, P. Moreillon,, D. Lew,, K. H. Krause,, G. Peters,, and M. Herrmann. 2000. Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect. Immun. 68: 6871– 6878.
84. Sinha, B.,, P. P. Francois,, O. Nusse,, M. Foti,, O. M. Hartford,, P. Vaudaux,, T. J. Foster,, D. P. Lew,, M. Herrmann,, and K. H. Krause. 1999. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin a5b1. Cell Microbiol. 1: 101– 117.
85. Soderquist, B.,, J. Kallman,, H. Holmberg,, T. Vikerfors,, and E. Kihlstrom. 1998. Secretion of IL-6, IL-8 and G-CSF by human endothelial cells in vitro in response to Staphylococcus aureus and staphylococcal exotoxins. APMIS 106: 1157– 1164.
86. Sullam, P. M.,, A. S. Bayer,, W. M. Foss,, and A. L. Cheung. 1996. Diminished platelet binding in vitro by Staphylococcus aureus is associated with reduced virulence in a rabbit model of infective endocarditis. Infect. Immun. 64: 4915– 4921.
87. Tekstra, J.,, H. Beekhuizen,, J. S. Van De Gevel,, I. J. Van Benten,, C. W. Tuk,, and R. H. Beelen. 1999. Infection of human endothelial cells with Staphylococcus aureus induces the production of monocyte chemotactic protein-1 (MCP-1) and monocyte chemotaxis. Clin. Exp. Immunol. 117: 489– 495.
88. Tompkins, D. C.,, L. J. Blackwell,, V. B. Hatcher,, D. A. Elliott,, C. O’Hagan-Sotsky,, and F. D. Lowy. 1992. Staphylococcus aureus proteins that bind to human endothelial cells. Infect. Immun. 60: 965– 969.
89. Tucker, K. A.,, S. S. Reilly,, C. S. Leslie,, and M. C. Hudson. 2000. Intracellular Staphylococcus aureus induces apoptosis in mouse osteoblasts. FEMS Microbiol. Lett. 186: 151– 156.
90. van Langevelde, P.,, E. Ravensbergen,, P. Grashoff,, H. Beekhuizen,, P. H. Groeneveld,, and J. T. van Dissel. 1999. Antibiotic-induced cell wall fragments of Staphylococcus aureus increase endothelial chemokine secretion and adhesiveness for granulocytes. Antimicrob. Agents Chemother. 43: 2984– 2989.
91. Vann, J. M.,, and R. A. Proctor. 1988. Cytotoxic effects of ingested Staphylococcus aureus on bovine endothelial cells: role of S. aureus alpha-hemolysin. Microb. Pathog. 4: 443– 453.
92. Vercellotti, G. M.,, D. Lussenhop,, P. K. Peterson,, L. T. Furcht,, J. B. McCarthy,, H. S. Jacob,, and C. F. Moldow. 1984. Bacterial adherence to fibronectin and endothelial cells: a possible mechanism for bacterial tissue tropism. J. Lab. Clin. Med. 103: 34– 43.
93. Weglarczyk, K.,, J. Baran,, M. Zembala,, and J. Pryjma. 2004. Caspase-8 activation precedes alterations of mitochondrial membrane potential during monocyte apoptosis induced by phagocytosis and killing of Staphylococcus aureus. Infect. Immun. 72: 2590– 2597.
94. Weidenmaier, C.,, J. F. Kokai-Kun,, S. A. Kristian,, T. Chanturiya,, H. Kalbacher,, M. Gross,, G. Nicholson,, B. Neumeister,, J. J. Mond,, and A. Peschel. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10: 243– 245.
95. Wesson, C. A.,, J. Deringer,, L. E. Liou,, K. W. Bayles,, G. A. Bohach,, and W. R. Trumble. 2000. Apoptosis induced by Staphylococcus aureus in epithelial cells utilizes a mechanism involving caspases 8 and 3. Infect. Immun. 68: 2998– 3001.
96. Yao, L.,, V. Bengualid,, F. D. Lowy,, J. J. Gibbons,, V. B. Hatcher,, and J. W. Berman. 1995. Internalization of Staphylococcus aureus by endothelial cells induces cytokine gene expression. Infect. Immun. 63: 1835– 1839.
97. Yao, L.,, F. D. Lowy,, and J. W. Berman. 1996. Interleukin-8 gene expression in Staphylococcus aureus-infected endothelial cells. Infect. Immun. 64: 3407– 3409.
98. Yeaman, M. R. 1997. The role of platelets in antimicrobial host defense. Clin. Infect. Dis. 25: 951– 968; quiz 969-970.

References: V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V.