Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host

Future Microbiology

Volumn 4, Issue 10, 2009, Pages 1337-1352

  Speziale, Pietro ^a   Pietrocola, Giampiero ^a   Rindi, Simonetta ^a   Provenzano, Maria ^a   Provenza, Giulio ^a   Di Poto, Antonella ^a   Visai, Livia ^a,b   Arciola, Carla Renata ^c,d  

^a Department of Biochemistry ^*  (Italy)

^b Center for Tissue Engineering CIT   (Italy)

^c RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Adhesion; Extracellular matrix; MSCRAMM; Staphylococcus aureus; Vaccine

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; BONE SIALOPROTEIN; CLUMPING FACTOR A; CLUMPING FACTOR B; COLLAGEN; COLLAGEN BINDING PROTEIN; CYTOKERATIN 10; DNA VACCINE; FIBRINOGEN; FIBRONECTIN; FIBRONECTIN BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; IRON REGULATORY FACTOR; PROTEIN A; SCLEROPROTEIN; SERINE ASPARTATE DIPEPTIDE REPEAT PROTEIN; TEFIBAZUMAB; UNCLASSIFIED DRUG; VANCOMYCIN; VASCULAR CELL ADHESION MOLECULE 1;

BACTERIAL INFECTION; CELL ADHESION; CELL INVASION; CELL SURFACE; ENDOCARDITIS; EXTRACELLULAR MATRIX; HOST PATHOGEN INTERACTION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SEPSIS; STAPHYLOCOCCUS AUREUS;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 74749090539     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.09.102     Document Type: Review

References (128)

1. Verhoef J, Fluit Ad C, Schmitz F-J: Staphylococci and other micrococci. In: Infectious Disease. Cohen J, Powderly WG (Eds). Elsevier (Mosby), Amsterdam, The Netherlands, 2119-2132 (2004).
2. Projan J, Novick R: The molecular basis of pathogenicity. In: The Staphylococci in Human Disease. Grossley KB, Archer GL (Eds). Churchill Livingstone, NY, USA, 55-81 (1997).
3. Chambers HF, DeLeo FR: Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7(9), 629-641 (2009).
4. Deleo FR, Chambers HF: Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J. Clin. Invest. 119 (9), 2464-2474 (2009).
5. Lowy FD: Antimicrobial resistance: the example of Staphylococcus aureus. J. Clin. Invest. 111(9), 1265-1273 (2003).
6. Weigel LM, Clewell DB, Gill SR et al.: Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302(5650), 1569-1571 (2003).
7. von Eiff C, Becker K, Machka K, Stammer H, Peters GN: Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N. Engl. J. Med. 344(1), 11-16 (2001).
8. Wertheim HF, Vos MC, Ott A et al.: Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus noncarriers. Lancet 364 (9435), 703-705 (2004).
9. Patti JM, Allen BL, McGavin MJ, Höök M: MSCRAMM-mediated adherence of microrganisms to host tissues. Annu. Rev. Microbiol. 48, 585-617 (1994). ■ Provides an introspective and comprehensive overview of microbial surface component recognizing adhesive matrix molecules (MSCRAMMs).
10. Beckerle M: Cell Adhesion. Oxford University Press, Oxford, UK (2002).
11. Kreis T, Vale R: Guidebook to the Extracellular Matrix, Anchor, and Adhesion Proteins. Oxford University Press, Oxford, UK (1999).
12. Hynes RO: Integrins: bidirectional, allosteric signaling machines. Cell 110(6), 673-687 (2002). ■ Exemplifies how extracellular matrix proteins can be pivotal in several biological processes.
13. Luo BH, Springer TA: Integrin structures and conformational signaling. Curr. Opin. Cell Biol. 18(5), 579-586 (2006).
14. Rivas JM, Speziale P, Patti JM, Höök M: MSCRAMM-targeted vaccines and immunotherapy for staphylococcal infection. Curr. Opin. Drug Discov. Devel. 7(2), 223-227 (2004). ■ Provides an introspective and comprehensive overview of MSCRAMMs.
15. Rivera J, Vannakambadi G, Höök M, Speziale P: Fibrinogen-binding proteins of Gram-positive bacteria. Thromb. Haemost. 98(3), 503-511 (2007). ■ Provides a comprehensive overview of fibrinogen-binding MSCRAMMs.
16. Chavakis T, Wiechmann K, Preissner KT, Herrmann M: Staphylococcus aureus interactions with the endothelium: the role of bacterial "secretable expanded repertoire adhesive molecules" (SERAM) in disturbing host defense systems. Thromb. Haemost. 94(2), 278-285 (2005).
17. Roche FM, Massey R, Peacock SJ et al.: Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 149(Pt 3), 643-654 (2003).
18. DeDent A, Bae T, Missiakas DM, Schneewind O: Signal peptides direct surface proteins to distinct envelope location of Staphylococcus aureus. EMBO J. 2720, 2656-2668 (2008).
19. Marraffini LA, Dedent AC, Schneewind O: Sortases and the art of anchoring proteins to the envelopes of Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 70(1), 192-221 (2006).
20. Maresso AW, Schneewind O: Sortase as a target of anti-infective therapy. Pharmacol. Rev. 60(1), 128-141 (2008).
21. Meenan NA, Visai L, Valtulina V et al.: The tandem b-zipper model defines high affinity fibronectin-binding repeats within Staphylococcus aureus FnBPA. J. Biol. Chem. 282(35), 25893-25902 (2007).
22. Prabhakaran S, Liang X, Skare JT, Potts JR, Höök M: A novel fibronectin binding motif in MSCRAMMs targets F3 modules. PLoS ONE 4(4), e5412 (2009).
23. McDevitt D, Francois P, Vaudaux P, Foster TJ: Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol. Microbiol. 11(2), 237-248 (1994).
24. Deivanayagam CC, Wann ER, Chen W et al.: A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J. 21(24), 6660-6672 (2002).
25. Ponnuraj K, Bowden MG, Davis S et al.: A "dock, lock, and latch" structural model for a staphylococcal adhesin binding to fibrinogen. Cell 115(2), 217-228 (2003). ■■ Demonstrates the ostensibly sophisticated mechanism between bacterial MSCRAMMs and their host ligand.
26. Ganesh VK, Rivera JJ, Smeds E et al.: A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog. 4(11), e1000226 (2008). ■ Demonstrates the ostensibly sophisticated mechanism between bacterial MSCRAMMs and their host ligand.
27. Peacock SJ, Moore CE, Justice A et al.: Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect. Immun. 70(9), 4987-4996 (2002).
28. Saravia-Otten P, Müller HP, Arvidson S: Transcription of Staphylococcus aureus fibronectin binding protein genes is negatively regulated by agr and an agr-independent mechanism. J. Bacteriol. 179(17), 5259-5263 (1997).
29. Entenza JM, Moreillon P, Senn MM et al.: Role of sigmaB in the expression of Staphylococcus aureus cell wall adhesins ClfA and FnbA and contribution to infectivity in a rat model of experimental endocarditis. Infect. Immun. 73(2), 990-998(2005).
30. Josefsson E, Hartford O, O'Brien L, Patti JM, Foster TJ: Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J. Infect. Dis. 184(12), 1572-1580 (2001).
31. Que YA, Haefliger JA, Piroth L et al.: Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J. Exp. Med. 201(10), 1627-1635 (2005). ■■ Highlights the crucial role of FnBPA and ClfA in the pathogenesis of infective endocarditis.
32. Siboo IR, Cheung AL, Bayer AS, Sullam PM: Clumping factor A mediates binding of Staphylococcus aureus to human platelets. Infect. Immun. 69(5), 3120-3127 (2001).
33. Sullam PM, Bayer AS, Foss WM, Cheung AL: Diminished platelet binding in vitro by Staphylococcus aureus is associated with reduced virulence in a rabbit model of infective endocarditis. Infect. Immun. 64(12), 4915-4921 (1996).
34. Que YA, François P, Haefliger JA, Entenza JM, Vaudaux P, Moreillon P: Reassessing the role of Staphylococcus aureus clumping factor and fibronectin-binding protein by expression in Lactococcus lactis. Infect. Immun. 69(10), 6296-6302 (2001).
35. Hair PS, Ward MD, Semmes OJ, Foster TJ, Cunnion KM: Staphylococcus aureus clumping factor A binds to complement regulator factor I and increases factor I cleavage of C3b. J. Infect. Dis. 198(1), 125-133 (2008).
36. Josefsson E, Higgins J, Foster TJ, Tarkowski A: Fibrinogen binding sites P336 and Y338 of clumping factor A are crucial for Staphylococcus aureus virulence. PLoS ONE 3(5), e2206 (2008).
37. Higgins J, Loughman A, van Kessel KP, van Strijp JA, Foster TJ: Clumping factor A of Staphylococcus aureus inhibits phagocytosis by human polymorphonuclear leucocytes. FEMS Microbiol. Lett. 258(2), 290-296 (2006).
38. Palmqvist N, Patti JM, Tarkowski A, Josefsson E: Expression of staphylococcal clumping factor A impedes macrophage phagocytosis. Microbes Infect. 6(2), 188-195 (2004).
39. Loughman A, Fitzgerald JR, Brennan MP et al.: Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol. Microbiol. 57(3), 804-818 (2005).
40. Ní Eidhin D, Perkins S, Francois P, Vaudaux P, Höök M, Foster TJ: Clumping factor B (ClfB), a new surface-located fibrinogen-binding adhesin of Staphylococcus aureus. Mol. Microbiol. 30(2), 245-257 (1998).
41. McDevitt D, Nanavaty T, House-Pompeo K, et al.: Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur. J. Biochem. 247(1), 416-424 (1997).
42. Walsh EJ, Miajlovic H, Gorkun OV, Foster TJ: Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the aC-domain of human fibrinogen. Microbiology 156 (Pt 2), 550-558 (2008).
43. O'Brien LM, Walsh EJ, Massey RC, Peacock SJ, Foster TJ: Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol. 4(11), 759-770 (2002).
44. Wertheim HF, Walsh E, Choudhurry R et al.: Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med. 5(1), e17 (2008).
45. Walsh EJ, O'Brien LM, Liang X, Höök M, Foster TJ: Clumping factor B, a fibrinogenbinding MSCRAMM (microbial surface components recognizing adhesive matrix molecules) adhesin of Staphylococcus aureus, also binds to the tail region of type I cytokeratin 10. J. Biol. Chem. 279(49), 50691-50699 (2004).
46. McAleese FM, Walsh EJ, Sieprawska M, Potempa J, Foster TJ: Loss of clumping factor B fibrinogen binding activity by Staphylococcus aureus involves cessation of transcription, shedding and cleavage by metalloprotease. J. Biol. Chem. 276(32), 29969-29978 (2001).
47. O'Brien LM, 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. 44(4), 1033-1044 (2002).
48. Miajlovic H, Loughman A, Brennan M, Cox D, Foster TJ: Both complement- and fibrinogen-dependent mechanisms contribute to platelet aggregation mediated by Staphylococcus aureus clumping factor B. Infect. Immun. 75(7), 3335-3343 (2007).
49. Tung H, Guss B, Hellman U, Persson L, Rubin K, Rjdén C: A bone sialoproteinbinding protein from Staphylococcus aureus: a member of the staphylococcal Sdr family. Biochem. J. 345(Pt 3), 611-619 (2000).
50. Wann ER, Gurusiddappa S, Höök M: The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J. Biol. Chem. 275(18), 13863-13871 (2000).
51. Casolini F, Visai L, Joh D et al.: Antibody response to fibronectin-binding adhesin FnbpA in patients with Staphylococcus aureus infections. Infect. Immun. 66(11), 5433-5442 (1998).
52. House-Pompeo K, Xu Y, Joh D, Speziale P, Höök M: Conformational changes in the fibronectin binding MSCRAMMs are induced by ligand binding. J. Biol. Chem. 271(3), 1379-1384 (1996).
53. Schwarz-Linek U, Werner JM, Pickford AR et al.: Pathogenic bacteria attach to human fibronectin through a tandem b-zipper. Nature 423(6936), 177-181(2003). ■ Demonstrates the ostensible sophisticated mechanism between bacterial MSCRAMMs and their host ligand.
54. Pilka ES, Werner JM, Schwarz-Linek U et al.: Structural insight into binding of Staphylococcus aureus to human fibronectin. FEBS Lett. 580(1), 273-277 (2006).
55. Bingham RJ, Rudiño-Piñera E, Meenan NA et al.: Crystal structures of fibronectinbinding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains. Proc. Natl Acad. Sci. USA 105(34), 12254-12258 (2008).
56. Roche FM, Downer R, Keane F, Speziale P, Park PW, Foster TJ: The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J. Biol. Chem. 279(37), 38433-38440 (2004).
57. Keane FM, Clarke AW, Foster TJ, Weiss AS: The N-terminal A domain of Staphylococcus aureus fibronectin-binding protein A binds to tropoelastin. Biochemistry 46(24), 7226-7232 (2007).
58. Keane FM, Loughman A, Valtulina V, Brennan M, Speziale P, Foster TJ: Fibrinogen and elastin bind to the same region within the A domain of fibronectin binding protein A, an MSCRAMM of Staphylococcus aureus. Mol. Microbiol. 63(3), 711-723 (2007).
59. Loughman A, Sweeney T, Keane FM, Pietrocola G, Speziale P, Foster TJ: Sequence diversity in the A domain of Staphylococcus aureus fibronectin-binding protein A. BMC Microbiol. 8, 74 (2008).
60. Fitzgerald JR, Loughman A, Keane F et al.: Fibronectin-binding proteins of Staphylococcus aureus mediate activation of human platelets via fibrinogen and fibronectin bridges to integrin GPIIb/IIIa and IgG binding to the FcgRIIa receptor. Mol. Microbiol. 59(1), 212-230 (2006).
61. Heying R, van de Gevel J, Que YA, Moreillon P, Beekhuizen H: Fibronectin-binding proteins and clumping factor A in Staphylococcus aureus experimental endocarditis: FnBPA is sufficient to activate human endothelial cells. Thromb. Haemost. 97(4), 617-626 (2007).
62. Piroth L, Que YA, Widmer E et al.: The fibrinogen- and fibronectin-binding domains of Staphylococcus aureus fibronectinbinding protein A synergistically promote endothelial invasion and experimental endocarditis. Infect. Immun. 76(8), 3824-3831 (2008).
63. Fowler T, Wann ER, Joh D, Johansson S, Foster TJ, Höök M: Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell b1 integrins. Eur. J. Cell Biol. 79(10), 672-679 (2000).
64. Sinha B, François PP, Nüsse O et al.: Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin a5b1. Cell Microbiol. 1(2), 101-117 (1999).
65. Massey RC, Kantzanou MN, Fowler T et al.: 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(12), 839-851 (2001).
66. Heying R, van de Gevel J, Que YA, Piroth L, Moreillon P, Beekhuizen H: Contribution of (sub)domains of Staphylococcus aureus fibronectin-binding protein to the proinflammatory and procoagulant response of human vascular endothelial cells. Thromb. Haemost. 101(3), 495-504 (2009).
67. O'Neill E, Pozzi C, Houston P et al.: A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectinbinding proteins, FnBPA and FnBPB. J. Bacteriol. 190(11), 3835-3850 (2008).
68. Switalski LM, Patti JM, Butcher W, Gristina AG, Speziale P, Höök M: A collagen receptor on Staphylococcus aureus strains isolated from patients with septic arthritis mediates adhesion to cartilage. Mol. Microbiol. 7(1), 99-107 (1993).
69. Patti JM, Boles JO, Höök M: Identification and biochemical characterization of the ligand binding domain of the collagen adhesin from Staphylococcus aureus. Biochemistry 32(42), 11428-11435 (1993).
70. Rich RL, Demeler B, Ashby K et al.: Domain structure of the Staphylococcus aureus collagen adhesin. Biochemistry 37(44), 15423-15433 (1998).
71. Xu Y, Rivas JM, Brown EL, Liang X, Höök MJ: Virulence potential of the staphylococcal adhesin CNA in experimental arthritis is determined by its affinity for collagen. J. Infect. Dis. 189(12), 2323-2333 (2004).
72. Zong Y, Xu Y, Liang X et al.: A 'collagen hug' model for Staphylococcus aureus CNA binding to collagen. EMBO J. 24(24), 4224-4236 (2005). ■ Demonstrates the ostensibly sophisticated mechanism between bacterial MSCRAMMs and their host ligand.
73. Liotta LA, Triggvason K, Garbisa S et al.: Metastatic potential correlates with enzimatic degradation of basement membrane collagen. Nature 284(5751), 67-68 (1980).
74. Kehrel B: Platelet-collagen interactions. Semin. Thromb. Hemost. 21(2), 123-129 (1995).
75. Hartford O, McDevitt D, Foster TJ: Matrix-binding proteins of Staphylococcus aureus: functional analysis of mutant and hybrid molecules. Microbiology 145(Pt 9), 2497-2505 (1999).
76. Gillaspy AF, Patti JM, Smeltzer MS: Transcriptional regulation of the Staphylococcus aureus collagen adhesion gene, cna. Infect. Immun. 65(4), 1536-1540 (1997).
77. Blevins JS, Gillaspy AF, Rechtin TM, Hurlburt BK, Smeltzer MS: The staphylococcal accessory regulator (sar) represses transcription of the Staphylococcus aureus collagen adhesin gene (cna) in an agr-independent manner. Mol. Microbiol. 33(2), 317-326 (1999).
78. Hienz SA, Schennings T, Heimdahl A, Flock JI: Collagen binding of Staphylococcus aureus is a virulence factor in experimental endocarditis. J. Infect. Dis. 174(1), 83-88 (1996).
79. Elasri MO, Thomas JR, Skinner RA et al.: Staphylococcus aureus collagen adhesin contributes to the pathogenesis of osteomyelitis. Bone 30(1), 275-280 (2002).
80. Rhem MN, Lech EM, Patti JM et al.: The collagen-binding adhesin is a virulence factor in Staphylococcus aureus keratitis. Infect. Immun. 68(6), 3776-3779 (2000).
81. Mascari LM, Ross JM: Quantification of staphylococcal-collagen binding interactions in whole blood by use of a confocal microscopy shear-adhesion assay. J. Infect. Dis. 188(1), 98-107 (2003).
82. Langone JJ: Protein A of Staphylococcus aureus and related immunoglobulin receptors produced by streptococci and pneumonococci. Adv. Immunol. 32, 157-252 (1982).
83. Uhlén M, Guss B, Nilsson B, Gatenbeck S, Philipson L, Lindberg M: Complete sequence of the staphylococcal gene encoding protein A. A gene evolved through multiple duplications. J. Biol. Chem. 259(3), 1695-1702 (1984).
84. Moks T, Abrahmsén L, Nilsson B, Hellman U, Sjöquist J, Uhlén M: Staphylococcal protein A consists of five IgG-binding domains. Eur. J. Biochem. 156(3), 637-643 (1986).
85. Roben PW, Salem AN, Silverman GJ: VH3 family antibodies bind domain D of staphylococcal protein A. J. Immunol. 154(12), 6437-6445 (1995).
86. Deisenhofer J: Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-Å resolution. Biochemistry 20(9), 2361-2370 (1981).
87. Starovasnik MA, Skelton NJ, O'Connell MP, Kelley RF, Reilly D, Fairbrother WJ: Solution structure of the E-domain of staphylococcal protein A. Biochemistry 35(48), 15558-15569 (1996).
88. Graille M, Stura EA, Corper AL et al.: Crystal structure of a Staphylococcus aureus protein A domain complexed with the Fab fragment of a human IgM antibody: structural basis for recognition of B-cell receptors and superantigen activity. Proc. Natl Acad. Sci. USA 97(10), 5399-5404 (2000).
89. Starovasnik MA, O'Connell MP, Fairbrother WJ, Kelley RF: Antibody variable region binding by staphylococcal protein A: thermodynamic analysis and location of the Fv binding site on E-domain. Protein Sci. 8(7), 1423-1431 (1999).
90. Gemmell CG: Changes in expression of bacterial surface antigens induced by antibiotics and their influence on host defenses. Pathol. Biol. (Paris) 35(10 Pt 2), 1377-1381 (1987).
91. Gemmell C, Tree R, Patel A, O'Reilly M, Foster TJ: Susceptibility to opsonophagocytosis of protein A, a-haemolysin and b-toxin deficient mutants of Staphylococcus aureus isolated by allelereplacement. Zentralbl. Bakteriol. 21(Suppl.), 273-277 (1991)
92. Palmqvist N, Foster T, Tarkowski A, Josefsson E: Protein A is a virulence factor in Staphylococcus aureus arthritis and septic death. Microb. Pathog. 33(5), 239-249 (2002).
93. Goodyear CS, Silverman GJ: Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes. Proc. Natl Acad. Sci. USA 101(31), 11392-11397 (2004).
94. Viau M, Longo NS, Lipsky PE, Zouali M: Staphylococcal protein A deletes B-1a and marginal zone B lymphocytes expressing human immunoglobulins: an immune evasion mechanism. J. Immunol. 175(11), 7719-7727 (2005).
95. Hartleib J, Köhler N, Dickinson RB et al.: Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood 96(6), 2149-2156 (2000).
96. Pawar P, Shin PK, Mousa SA, Ross JM, Konstantopoulos KJ: Fluid shear regulates the kinetics and receptor specificity of Staphylococcus aureus binding to activated platelets. J. Immunol. 173(2), 1258-1265 (2004).
97. O'Seaghdha M, van Schooten CJ, Kerrigan SW et al.: Staphylococcus aureus protein A binding to von Willebrand factor A1 domain is mediated by conserved IgG binding regions. FEBS J. 273(21), 4831-4841 (2006).
98. Nguyen T, Ghebrehiwet B, Peerschke EI: Staphylococcus aureus protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infect. Immun. 68(4), 2061-2068 (2000).
99. Gómez MI, Lee A, Reddy B et al.: Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat. Med. 8(10), 842-848 (2004).
100. Gómez MI, O'Seaghdha M, Magargee M, Foster TJ, Prince AS: Staphylococcus aureus protein A activates TNFR1 signaling through conserved IgG binding domains. J. Biol. Chem. 281(29), 20190-20196 (2006).
101. Gómez MI, Seaghdha MO, Prince AS: Staphylococcus aureus protein A activates TACE through EGFR-dependent signaling. EMBO J. 26(3), 701-709 (2007).
102. Martin FJ, Gomez MI, Wetzel DM et al.: Staphylococcus aureus activates type I IFN signaling in mice and humans through the Xr repeated sequences of protein A. J. Clin. Invest. 119(7), 1931-1939 (2009).
103. Merino N, Toledo-Arana A, Vergara-Irigaray M et al.: Protein A-mediated multicellular behavior in Staphylococcus aureus. J. Bacteriol. 191(3), 832-843 (2009).
104. Mazmanian SK, Ton-That H, Su K, Schneewind O: An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc. Natl Acad. Sci. USA 99(4), 2293-2298 (2002)
105. Clarke SR, Wiltshire MD, Foster SJ: IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol. Microbiol. 51(5), 1509-1519 (2004).
106. Clarke SR, Andre G, Walsh EJ, Dufrêne YF, Foster TJ, Foster SJ: Iron-regulated surface determinant protein A (IsdA) mediates adhesion of Staphylococcus aureus to human corneocyte enevelope proteins. Infect. Immun. 77(6), 2408-2416 (2009).
107. Clarke SR, Mohamed R, Bian L et al.: The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1(3), 199-212 (2007).
108. Clarke SR, Foster SJ: IsdA protects Staphylococcus aureus against the bactericidal protease activity of apolactoferrin. Infect. Immun. 76(4), 1518-1526 (2008).
109. Corrigan RM, Miajlovic H, Foster TJ: Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol. 9, 22 (2009).
110. Clarke SR, Brummell KJ, Horsburgh MJ et al.: Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J. Infect. Dis. 193(8), 1098-1108 (2006).
111. Nilsson IM, Patti JM, Bremell T, Höök M, Tarkowski A: Vaccination with a recombinant fragment of collagen adhesin provides protection against Staphylococcus aureus-mediated septic death. J. Clin. Invest. 101(12), 2640-2649 (1998).
112. Visai L, Xu Y, Casolini F, Rindi S, Höök M, Speziale P: Monoclonal antibodies to CNA, a collagen-binding microbial surface component recognizing adhesive matrix molecules, detach Staphylococcus aureus from a collagen substrate. J. Biol. Chem. 275(51), 39837-39845 (2000).
113. Hall AE, Domanski PJ, Patel PR et al.: Characterization of a protective monoclonal antibody recognizing Staphylococcus aureus MSCRAMM protein clumping factor A. Infect. Immun. 71(12), 6864-6870 (2003).
114. Patti JM: A humanized monoclonal antibody targeting Staphylococcus aureus. Vaccine. 22(Suppl. 1), S39-S43 (2004).
115. Bloom B, Schelonka R, Kueser T et al.: Multicenter study to assess safety and efficacy of INH-A21, a donor-selected human staphylococcal immunoglobulin, for prevention of nosocomial infections in very low birth weight infants. Pediatr. Infect. Dis. J. 24(10), 858-866 (2005).
116. Vernachio JH, Bayer AS, Ames B et al.: Human immunoglobulin G recognizing fibrinogenbinding surface proteins is protective against both Staphylococcus aureus and Staphylococcus epidermidis infections in vivo. Antimicrob. Agents Chemother. 50(2), 511-518 (2006).
117. Schaffer AC, Solinga RM, Cocchiaro J et al.: Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model. Infect. Immun. 74(4), 2145-2153 (2006).
118. Domanski PJ, Patel PR, Bayer AS et al.: Characterization of a humanized monoclonal antibody recognizing clumping factor A expressed by Staphylococcus aureus. Infect. Immun. 73(8), 5229-5232 (2005).
119. Wertheim HF, Walsh E, Choudhurry R et al.: Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med. 5(1), e17 (2008).
120. Kuklin NA, Clark DJ, Secore S et al.: A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun. 74(4), 2215-2223 (2006).
121. Arrecubieta C, Matsunaga I, Asai T, Naka Y, Deng MC, Lowy FD: Vaccination with clumping factor A and fibronectin binding protein A to prevent Staphylococcus aureus infection of an aortic patch in mice. J. Infect. Dis. 198(4), 571-575 (2008).
122. Stranger-Jones YK, Bae T, Schneewind O: Vaccine assembly from surface proteins of Staphylococcus aureus. Proc. Natl Acad. Sci. USA 103(45), 16942-16947 (2006).
123. Gaudreau MC, Lacasse P, Talbot BG: Protective immune responses to a multi-gene DNA vaccine against Staphylococcus aureus. Vaccine 25(5), 814-824 (2007).
124. Castagliuolo I, Piccinini R, Beggiao E et al.: Mucosal genetic immunization against four adhesins protects against Staphylococcus aureus-induced mastitis in mice. Vaccine 24(20), 4393-4402 (2006).
125. Koziel J, Maciag-Gudowska A, Mikolajczyk T et al.: Phagocytosis of Staphylococcus aureus by macrophages exerts cytoprotective effects manifested by the upregulation of antiapoptotic factors. PLoS ONE 4(4), e5210 (2009).
126. Garzoni C, Francois P, Huyghe A et al.: A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells. BMC Genomics 8, 171 (2007).
127. Petsko GA, Ringe D: Protein Structure and Function. New Science Press, Oxford, UK (2004).
128. Herrick S, Blanc-Brude O, Gray A, Laurent G: Fibrinogen. Int. J. Biochem. Cell Biol. 31(7), 741-746 (1999).