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Thromb Haemost 2005; 94(02): 278-285
DOI: 10.1160/TH05-05-0306
Theme Issue Article
Schattauer GmbH

Staphylococcus aureus interactions with the endothelium

The role of bacterial “Secretable Expanded Repertoire Adhesive Molecules” (SERAM) in disturbing host defense systems
Triantafyllos Chavakis
1   Experimental Immunology Branch, NCI, NIH, Bethesda, Maryland, USA
,
Klaus Wiechmann
2   Institute for Biochemistry, Justus-Liebig-University Giessen, Giessen, Germany
,
Klaus T. Preissner
2   Institute for Biochemistry, Justus-Liebig-University Giessen, Giessen, Germany
,
Mathias Herrmann
3   Institute of Medical Microbiology and Hygiene, University of Saarland Hospital, Homburg/Saar, Germany
› Author Affiliations
Further Information

Publication History

Received: 04 May 2005

Accepted after major revision: 24 June 2005

Publication Date:
05 December 2017 (online)

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Summary

The intravascular maof nifestation Staphylococcus aureus infection is often associated with a severe, and sometimes catastrophic disease. Many host factors contribute to endothelial tropism of S.aureus including subendothelial matrix proteins,endothelial cell receptors, and platelets that are engaged together with S. aureus cell wall adhesins such as the fibronectin binding proteins. Recently, the role of secreted staphylococcal factors that were initially identified by virtue of their binding function with host proteins and ligands, has been reappraised in this regard. Among these, bacterial proteins without significant homology among each other, coagulase (Coa), the extracellular fibrinogen binding protein (Efb), the extracellular matrix binding protein (Emp), or the extracellular adhesive protein (Eap), are the most prominent ones to be associated with endovascular disease. Newly discovered interactions with host components may account for profound effects on immunmodulation and wound healing which are summarized in this short review and which ascribe an important role of these molecules in acute and chronic endo- and extravascular staphylococcal disease. Further research in the complex functional role of these "secretable expanded repertoire adhesive molecules" (SERAM) may not only help to increase our understanding in the pathogenesis of S. aureus infection but can specify novel targets for preventive or therapeutic strategies.

Keywords

Staphylococcus aureus - endothelium - extracellular adhesive protein - endovascular infection
 

  • References

  • 1 Lowy FD. Medical progress – Staphylococcus aureus infections. N Engl J Med 1998; 339: 520-32.
    CrossrefPubMedGoogle Scholar
  • 2 Petti CA, Fowler VG. Staphylococcus aureus bacteremia and endocarditis. Infect Dis Clin North Am 2002; 16: 413-35.
    CrossrefPubMedGoogle Scholar
  • 3 Fowler VG, Justice A, Moore C. et al. Risk factors for hematogenous complications of intravscular catheter- associated Staphylococcus aureus bacteremia. Clin Infect Dis 2005; 40: 695-703.
    CrossrefPubMedGoogle Scholar
  • 4 Grady M, Cullen JJ. Preventing postoperative Staphylococcus infections: an update. Surg Technol Int 2003; 11: 57-60.
    PubMedGoogle Scholar
  • 5 Edwards R, Harding KG. Bacteria and wound healing. Curr Opin Infect Dis 2004; 17: 91-6.
    CrossrefPubMedGoogle Scholar
  • 6 Farrington M, Redpath C, Trundle C. et al. Winning the battle but losing the war: methicillin-resistant Staphylococcus aureus (MRSA) infection at a teaching hospital. Q J Med 998 (91) 539-48.
    PubMedGoogle Scholar
  • 7 Carleton HA, Diep BA, Charlebois ED. et al. Community- adapated methicillin-resistant Staphylococcus aureus (MRSA): population dynamics of an expanding community reservoir of MRSA. Clin Infect Dis 2004; 15: 1730-8.
    PubMedGoogle Scholar
  • 8 Vancomycin-resistant Staphylococcus aureus – New York, 2004. MMWR 2004; 53: 322-3.
    PubMedGoogle Scholar
  • 9 Foster TJ, Höök M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 1998; 6: 484-8.
    CrossrefPubMedGoogle Scholar
  • 10 Wann ER, Gurusiddappa S, Hook M. The fibronectin- binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 2000; 275: 13863-71.
    CrossrefPubMedGoogle Scholar
  • 11 McDevitt D, Francois P, Vaudaux P. et al. Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol 1994; 11: 237-48.
    CrossrefPubMedGoogle Scholar
  • 12 Ni Eidhin D, Perkins S, Francois P. et al. Clumping factor B (ClfB), a new surface-located fibrinogenbinding adhesin of Staphylcoccus aureus. Mol Microbiol 1998; 30: 245-57.
    CrossrefPubMedGoogle Scholar
  • 13 Navarre WW, Ton-That H, Faull KF. et al. Anchor structure of staphylococcal surface proteins II. COOHterminal structure of muramidase and amidase-solubilized surface protein. J Biol Chem 1998; 273: 29135-42.
    CrossrefPubMedGoogle Scholar
  • 14 Mazmanian SK, Liu G, Jensen ER. et al. Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc Natl Acad Sci USA 2000; 97: 5510-5.
    CrossrefPubMedGoogle Scholar
  • 15 Roche FM, Massey R, Peacock SJ. et al. Characterization of novel LPXTG-containing proteins of Staphylococcus lococcus aureus identified from genome sequences. Microbiology 2003; 149: 643-54.
    CrossrefPubMedGoogle Scholar
  • 16 Tompkins DC, Hatcher VB, Patel D. et al. A human endothelial cell membrane protein that binds Staphylococcus aureus in vitro. J Clin Invest 1990; 85: 1248-54.
    CrossrefPubMedGoogle Scholar
  • 17 Tompkins DC, Blackwell LJ, Hatcher VB. et al. Staphylococcus aureus proteins that bind to human endothelial cells. Infect Immun 1992; 60: 965-9.
    CrossrefPubMedGoogle Scholar
  • 18 Que YA, Francois P, Haefliger JA. et al. Reassessing the role of Staphylococcus aureus clumping factor and fibronectin-binding protein by expression in Lactococcus lactis. Infect Immun 2001; 69: 6296-302.
    CrossrefPubMedGoogle Scholar
  • 19 Stewart BF, Siscovick D, Lind BK. et al. Clinical factors associated with calcific aortic valve disease. Cardiovascular Health Study. J Am Coll Cardiol 1997; 29: 630-4.
    CrossrefPubMedGoogle Scholar
  • 20 Herrmann M, Hartleib J, Kehrel B. et al. Interaction of von Willebrand factor with Staphylococcus aureus. J Infect Dis 1997; 176: 984-91.
    CrossrefPubMedGoogle Scholar
  • 21 Hartleib J, Köhler N, Dickinson RB. et al. Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood 2000; 96: 2149-56.
    PubMedGoogle Scholar
  • 22 Preissner KT, Chhatwal GS. Extracellular matrix and host cell surfaces: potential sites of pathogen interaction. Cossart P, Boquet P, Normark S, Rappuoli R. Cellular Microbiology. ASM-Press; Washington D. C.: 2005: 87-104.
    Google Scholar
  • 23 Weidenmaier C, Peschel A, Xiong YQ. et al. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 2005; 191: 1771-7.
    CrossrefPubMedGoogle Scholar
  • 24 Laschke MW, Kerdudou S, Herrmann M. et al. Intravital fluorescence microscopy: a novel tool for the study of the interaction of Staphylococcus aureus with the microvascular endothelium in vivo. J Infect Dis 2005; 191: 435-43.
    CrossrefPubMedGoogle Scholar
  • 25 Clawson CC, White JG. Platelet interaction with bacteria. I. Reaction phases and effects of inhibitors. Am J Pathol 1971; 65: 367-80.
    PubMedGoogle Scholar
  • 26 Herrmann M, Lai QJ, Albrecht RM. et al. Adhesion of Staphylococcus aureus to surface-bound platelets: Role of fibrinogen/fibrin and platelet integrins. J Infect Dis 1993; 167: 312-22.
    CrossrefPubMedGoogle Scholar
  • 27 Siboo IR, Cheung AL, Bayer AS. et al. Clumping factor A mediates binding of Staphylococcus aureus to human platelets. Infect Immun 2001; 69: 3120-7.
    CrossrefPubMedGoogle Scholar
  • 28 Nguyen T, Ghebrehiwet B, Peerschke EI. Staphylococcus aureus protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal in teractions with platelets. Infect Immun 2000; 68: 2061-8.
    CrossrefPubMedGoogle Scholar
  • 29 Heilmann C, Herrmann M, Kehrel BE. et al. Platelet- binding domains in 2 fibrinogen-binding proteins of Staphylococcus aureus identified by phage display. J Infect Dis 2002; 186: 32-9.
    CrossrefPubMedGoogle Scholar
  • 30 Heilmann C, Niemann S, Sinha B. et al. Staphylococcus aureus fibronectin-binding protein (FnBP) mediates adherence to platelets and platelet aggregation. J Infect Dis 2004; 190: 321-9.
    CrossrefPubMedGoogle Scholar
  • 31 Bayer AS, Sullam PM, Ramos M. et al. Staphylococcus aureus induces platelet aggregation via a fibrinogen-dependent mechanism which is independent of principal platelet glycoprotein IIb/IIIa fibrinogen- binding domains. Infect Immun 1995; 63: 3634-41.
    CrossrefPubMedGoogle Scholar
  • 32 O’Brien L, Kerrigan SW, Kaw G. et al. Multiple mechanisms for the activation of human platelet aggregation by Staphylococcus aureus: roles for the clumping factors ClfA and ClfB, the serine-aspartate repeat protein SdrE and protein A. Mol Microbiol 2002; 44: 1033-44.
    CrossrefPubMedGoogle Scholar
  • 33 Niemann S, Spehr N, Van Aken H. et al. Soluble fibrin is the main mediator of S. aureus adhesion to platelets. Circulation 2004; 110: 193-200.
    CrossrefPubMedGoogle Scholar
  • 34 Dhawan VK, Yeaman MR, Cheung AL. et al. Phenotypic resistance to thrombin-induced platelet microbicidal protein in vitro is correlated with enhanced virulence in experimental endocarditis due to Staphylococcus aureus. Infect Immun 1997; 65: 3293-9.
    CrossrefPubMedGoogle Scholar
  • 35 Fowler VG, Sakoulas G, McIntyre LM. et al. Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombininduced platelet microbicidal protein. J Infect Dis 2004; 190: 1140-9.
    CrossrefPubMedGoogle Scholar
  • 36 Sinha B, Herrmann M. Mechanism and consequences of invasion of endothelial cells by Staphylococcus aureus. Thromb Haemost 2005; 94: 266-77.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 37 Grundmeier M, Hussain M, Becker P. et al. 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 2004; 72: 7155-63.
    CrossrefPubMedGoogle Scholar
  • 38 Vesga O, Groeschel MC, Otten MF. et al. Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J Infect Dis 1996; 173: 739-42.
    CrossrefPubMedGoogle Scholar
  • 39 Vann JM, Proctor RA. Ingestion of Staphylococcus aureus by bovine endothelial cells results in time- and inoculum-dependent damage to endothelial cell monolayers. Infect Immun 1987; 55: 2155-63.
    CrossrefPubMedGoogle Scholar
  • 40 Martin P. Wound healing—aiming for perfect skin regeneration. Science 1997; 276: 75-81.
    CrossrefPubMedGoogle Scholar
  • 41 Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med 1999; 341: 738-46.
    CrossrefPubMedGoogle Scholar
  • 42 Keane MP, Strieter RM. The role of CXC chemokines in the regulation of angiogenesis. Chem Immunol 1999; 72: 86-101.
    PubMedGoogle Scholar
  • 43 Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000; 18: 217-42.
    CrossrefPubMedGoogle Scholar
  • 44 Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 1994; 76: 301-14.
    CrossrefPubMedGoogle Scholar
  • 45 Gahmberg CG. Leukocyte adhesion. CD11/CD18 integrins and intercellular adhesion molecules. Curr Opin Cell Biol. 1997; 9: 643-50.
    CrossrefPubMedGoogle Scholar
  • 46 Plow EF, Haas TA, Zhang L. et al. Ligand binding to integrins. J Biol Chem 2000; 275: 21785-8.
    CrossrefPubMedGoogle Scholar
  • 47 Chavakis T, Preissner KT, Santoso S. Leukocyte trans-endothelial migration: JAMs add new pieces to the puzzle. Thromb Haemost 2003; 89: 13-7.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 48 Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecules. Blood 1994; 84: 2068-101.
    CrossrefPubMedGoogle Scholar
  • 49 Verdrengh M, Springer TA, Gutierrez-Ramos JC. et al. Role of intercellular adhesion molecule 1 in pathogenesis of staphylococcal arthritis and in host defense against staphylococcal bacteremia. Infect Immun 1996; 64: 2804-7.
    CrossrefPubMedGoogle Scholar
  • 50 Schlievert PM. Role of superantigens in human disease. J Infect Dis 1993; 167: 997-1002.
    CrossrefPubMedGoogle Scholar
  • 51 Kim J, Urban RG, Strominger JL. et al. Toxic shock syndrome toxin-1 complexed with a class II major histocompatibility molecule HLA-DR1. Science 1994; 266: 1870-4.
    CrossrefPubMedGoogle Scholar
  • 52 Madsen SM, Westh H, Danielsen L. et al. Bacterial colonization and healing of venous leg ulcers. APMIS 1996; 104: 895-9.
    CrossrefPubMedGoogle Scholar
  • 53 Grimble SA, Magee TR, Galland RB. Methicillin resistant Staphylococcus aureus in patients undergoing major amputation. Eur J Vasc Endovasc Surg 2001; 22: 215-8.
    CrossrefPubMedGoogle Scholar
  • 54 McDevitt D, Vaudaux PE, Foster TJ. Genetic evidence that bound coagulase of Staphylococcus aureus is not clumping factor. Infect Immun 1992; 60: 1514-23.
    CrossrefPubMedGoogle Scholar
  • 55 Stutzmann Meier P, Entenza JM, Vaudaux P. et al. Study of Staphylococcus aureus pathogenic genes by transfer and expression in the less virulent organism Streptococcus gordonii. Infect Immun 2001; 69: 657-64.
    CrossrefPubMedGoogle Scholar
  • 56 Cheung AL, Projan SJ, Edelstein RE, Fischetti VA. Cloning, expression, and nucleotide sequence of Staphylococcus aureus gene (fbpA) encoding a fibrinogen- binding protein. Infect Immun 1995; 63: 1914-20.
    CrossrefPubMedGoogle Scholar
  • 57 Watanabe S, Ito T, Takeuchi F. et al. Structural comparison of ten serotypes of staphylocoagulases in Staphylococcus aureus. J Bacteriol 2005; 187: 3698-707.
    CrossrefPubMedGoogle Scholar
  • 58 Bjerketorp J, Nilsson M, Ljungh A. et al. A novel von Willebrand factor binding protein expressed by Staphylococcus aureus. Microbiology 2002; 148: 2037-44.
    CrossrefPubMedGoogle Scholar
  • 59 Bjerketorp J, Jacobsson K, Frykberg L. The von Willebrand factor-binding protein (vWbp) of Staphylococcus aureus is a coagulase. FEMS Microbiol Lett 2004; 234: 309-14.
    CrossrefPubMedGoogle Scholar
  • 60 Boden Wastfelt MK, Flock JI. Incidence of the highly conserved fib gene and expression of the fibrinogen- binding (Fib) protein among clinical isolates of Staphylococcus aureus. J Clin Microbiol 1995; 33: 2347-52.
    CrossrefPubMedGoogle Scholar
  • 61 Palma M, Shannon O, Quezada HC. et al. Extracellular fibrinogen binding protein, Efb, from Staphy lococcus aureus blocks platelet aggregation due to its binding to the α-chain. J Biol Chem 2001; 276: 31691-7.
    CrossrefPubMedGoogle Scholar
  • 62 Wade D, Palma M, Löfving-Arvholm I. et al. Identification of functional domains in Efb, a fibrinogen binding protein of Staphylococcus aureus. Biochem Biophys Res Commun 1998; 248: 690-5.
    CrossrefPubMedGoogle Scholar
  • 63 Palma M, Wade D, Flock M. et al. Multiple binding sites in the interaction between an extracellular fibrinogen- binding protein from Staphylococcus aureus and fibrinogen. J Biol Chem 1998; 273: 13177-81.
    CrossrefPubMedGoogle Scholar
  • 64 Colque-Navarro P, Palma M, Soderquist B. et al. Antibody responses in patients with staphylococcal septicemia against two Staphylococcus aureus fibrinogen binding proteins: clumping factor and an extracellular fibrinogen binding protein. Clin Diagn Lab Immunol 2000; 7: 14-20.
    CrossrefPubMedGoogle Scholar
  • 65 Palma M, Nozohoor S, Schennings T. et al. Lack of the extracellular 19-kilodalton fibrinogen-binding protein from Staphylococcus aureus decreases virulence in experimental wound infection. Infect Immun 1996; 64: 5284-9.
    CrossrefPubMedGoogle Scholar
  • 66 Shannon O, Flock JL. Extracellular fibrinogen binding protein, Efb, from Staphylococcus aureus binds to platelets and inhibits platelet aggregation. Thromb Haemost 2004; 91: 779-89.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 67 Lee LY, Liang X, Hook M. et al. Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen binding protein (Efb). J Biol Chem 2004; 279: 50710-6.
    CrossrefPubMedGoogle Scholar
  • 68 Lee LY, Hook M, Haviland D. et al. Inhibition of complement activation by a secreted Staphylococcus aureus protein. J Infect Dis 2004; 190: 571-9.
    CrossrefPubMedGoogle Scholar
  • 69 Hussain M, Becker K, von Eiff C. et al. Identification and characterization of a novel 38,5-kilodalton secretory protein of Staphylococcus aureus with extended- spectrum binding activitiy for extracellular matrix and plasma. J Bacteriol 2001; 183: 6778-86.
    CrossrefPubMedGoogle Scholar
  • 70 McGavin MH, Krajewska Pietrasik D, Rydén C. et al. Identification of a Staphylococcus aureus extracellular matrix- binding protein with broad specificity. Infect Immun 1993; 61: 2479-85.
    CrossrefPubMedGoogle Scholar
  • 71 Jönsson K, McDevitt D, McGavin MH. et al. Staphylococcus aureus expresses a major histocompatibility complex class II analog. J Biol Chem 1995; 270: 21457-60.
    CrossrefPubMedGoogle Scholar
  • 72 Harraghy N, Hussain M, Haggar A. et al. The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology 2003; 149: 2701-7.
    CrossrefPubMedGoogle Scholar
  • 73 Palma M, Haggar A, Flock JI. Adherence of Staphylococcus aureus is enhanced by an endogenous secreted protein with broad binding activity. J Bacteriol 1999; 181: 2840-5.
    CrossrefPubMedGoogle Scholar
  • 74 Hussain M, Becker K, von Eiff C. et al. Analogs of the extracellular adherence protein (Eap) are conserved and prevalent in clinical Staphylococcus aureus isolates. Clin Diagn Lab Immunol 2001; 8: 1271-6.
    CrossrefPubMedGoogle Scholar
  • 75 Hussain M, Haggar A, Heilmann C. et al. Insertional inactivation of Eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect Immun 2002; 70: 2933-40.
    CrossrefPubMedGoogle Scholar
  • 76 Haggar A, Hussain M, Lonnies H. et al. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect Immun 2003; 71: 2310-7.
    CrossrefPubMedGoogle Scholar
  • 77 Kreikemeyer B, McDevitt D, Podbielski A. The role of the map protein in Staphylococcus aureus matrix protein and eukaryotic cell adherence. Int J Med Microbiol 2002; 292: 283-95.
    CrossrefPubMedGoogle Scholar
  • 78 Chavakis T, Hussain M, Kanse SM. et al. Staphylococcus aureus extracellular adherence protein serves as anti- inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med 2002; 8: 687-93.
    CrossrefPubMedGoogle Scholar
  • 79 Lee LY, Miyamoto YJ, McIntyre BW. et al. The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J Clin Invest 2002; 110: 1461-71.
    CrossrefPubMedGoogle Scholar
  • 80 Harraghy N, Kormanec J, Wolz C. et al. Sae is essential for expression of the staphylococcal adhesins Eap and Emp. Microbiology 2005; 151: 1789-800.
    CrossrefPubMedGoogle Scholar
  • 81 Steinhuber A, Goerke C, Bayer MG. et al. Molecular architecture of the regulatory locus sae of Staphylococcus aureus and its impact on expression of virulence factors. J Bacteriol 2003; 185: 1439-47.
    CrossrefPubMedGoogle Scholar
  • 82 Novick RP, Jiang D. The staphyloccal saeRS system coordinates environmental signals with agr quorum sensing. Microbiology 2003; 149: 2709-17.
    CrossrefPubMedGoogle Scholar
  • 83 Geisbrecht BV, Hamaoka BY, Perman B. et al. The crystal structures of EAP domains from Staphylococcus aureus reveal an unexpected homology to bacterial superantigens. J Biol Chem 2005; 280: 17243-50.
    CrossrefPubMedGoogle Scholar
  • 84 Flock M, Flock JI. Rebinding of extracellular adherence protein eap to Staphylococcus aureus can occur through a surface-bound neutral phosphatase. J Bacteriol 2001; 183: 3999-4003.
    CrossrefPubMedGoogle Scholar
  • 85 Vuong C, Keller D, Peschel A. et al. Binding of the Map protein of Staphylococcus aureus Newman to the cell wall is dependent on the D-alanylation of teichoic acids. 10th International Symposium on Staphylococci and Staphylococcal Infections. 2002 ISSSI 102-abstract 01.
    PubMedGoogle Scholar
  • 86 Jahreis A, Yousif Y, Rump JA. et al. Two novel cationic staphylococcal proteins induce IL-2 secretion, proliferation and immunoglobulin synthesis in peripheral blood mononuclear cells (PBMC) of both healthy controls and patients with common variable immunodeficiency (CVID). Clin Exp Immunol 1995; 100: 406-11.
    CrossrefPubMedGoogle Scholar
  • 87 Jahreis A, Beckheinrich P, Haustein UF. Effects of two novel cationic staphylococcal proteins (NP-tase and p70)and enterotoxin B on IgE synthesis and interleukin- 4 and interferon-gamma production in patients with atopic dermatitis. Br J Dermatol 2000; 142: 680-7.
    CrossrefPubMedGoogle Scholar
  • 88 de Haas CJC, Veldkamp KE, Peschel A. et al. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 2004; 199: 687-95.
    CrossrefPubMedGoogle Scholar
  • 89 Postma B, Poppelier MJ, van Galen JC. et al. Chemotaxis inhibitory protein of Staphylococcus aureus binds specifically to the C5a and formylated peptide receptor. J Immunol 2004; 172: 6994-7001.
    CrossrefPubMedGoogle Scholar
  • 90 Lee S, Zheng M, Kim B. et al. Role of matrix metalloproteinase- 9 in angiogenesis caused by ocular infection with herpes simplex virus. J Clin Invest 2002; 110: 1105-11.
    CrossrefPubMedGoogle Scholar
  • 91 Webb NJ, Myers CR, Watson CJ. et al. Activated human neutrophils express vascular endothelial growth factor (VEGF). Cytokine 1998; 10: 254-7.
    CrossrefPubMedGoogle Scholar
  • 92 Rhee JS, Black M, Schubert U. et al. The functional role of blood platelet components in angiogenesis. Thromb Haemost 2004; 92: 394-402.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 93 Melles DC, Gorkink RF, Boelens HA. et al. Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. J Clin Invest 2004; 114: 1732-40.
    CrossrefPubMedGoogle Scholar
  • 94 Foster TJ. The Staphylococcus aureus ‘‘superbug’’. J Clin Invest 2004; 114: 1693-6.
    CrossrefPubMedGoogle Scholar
  • 95 Rivas JM, Speziale P, Patti JM. et al. MSCRAMM– targeted vaccines and immunotherapy for staphylococcal infection. Curr Opin Drug Discov Devel 2004; 7: 223-7.
    PubMedGoogle Scholar