Chapter 42 : —Eukaryotic Cell Interactions

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

—Eukaryotic Cell Interactions, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816513/9781555813437_Chap42-1.gif /docserver/preview/fulltext/10.1128/9781555816513/9781555813437_Chap42-2.gif


The pathogen causes a diversity of diseases that range from minor skin and soft tissue infections to life-threatening systemic infections. -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 -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. 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 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 invasion of eukaryotic cells has been the limited amount of supporting clinical and experimental in vivo data. 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.

Citation: Arrecubieta C, Lowy F. 2006. —Eukaryotic Cell Interactions, p 517-525. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch42
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Demonstration of endothelial cell phagocytosis of in vitro. (Left) Staphylococci incubated with human umbilical vein endothelial cells in tissue culture (30 min). The bacteria are phagocytized, enclosed within a membrane-bound vacuole, and transported into the cell. Bar, 0.5 μm. (Right) Section of rabbit aorta incubated with staphylococci (bacteria incubated with tissue for 30 min, then replaced with medium for a 5.5-h incubation). The endothelial cell contains a large number of bacteria enclosed within vacuoles. The cell has ruptured, releasing bacteria into the medium. Bar, 1.0 μm. (Reprinted from the [ ] with the permission of Academic Press.)

Citation: Arrecubieta C, Lowy F. 2006. —Eukaryotic Cell Interactions, p 517-525. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch42
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Model for –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 and the subsequent phagolysosomal fusion. 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. 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. cells also elaborate a variety of proteolytic enzymes that facilitate their translocation across the ECM to adjacent tissues.

Citation: Arrecubieta C, Lowy F. 2006. —Eukaryotic Cell Interactions, p 517-525. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch42
Permissions and Reprints Request Permissions
Download as Powerpoint


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.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error