Staphylococcus aureus protein A binding to von Willebrand factor A1 domain is mediated by conserved IgG binding regions

FEBS Journal

Volumn 273, Issue 21, 2006, Pages 4831-4841

  O'Seaghdha, Maghnus ^a   Van Schooten, Carina J ^b   Kerrigan, Steven W ^c   Emsley, Jonas ^d   Silverman, Gregg J ^e   Cox, Dermot ^c   Lenting, Peter J ^b   Foster, Timothy J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Immunoglobulin G; Protein A; Staphylococcus aureus; Von Willebrand factor

Indexed keywords

GLUTATHIONE TRANSFERASE; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; PROTEIN A; RECOMBINANT PROTEIN; VON WILLEBRAND FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM ADHERENCE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HEAVY CHAIN; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SHEAR STRESS; SITE DIRECTED MUTAGENESIS; STAPHYLOCOCCUS AUREUS; THROMBOCYTE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; EXTRACELLULAR MATRIX PROTEINS; GLUTATHIONE TRANSFERASE; HUMANS; IMMUNOGLOBULIN G; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; STAPHYLOCOCCAL PROTEIN A;

STAPHYLOCOCCUS AUREUS;

EID: 33750054371     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05482.x     Document Type: Article

References (51)

1. Peacock SJ, de Silva I & Lowy FD (2001) What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 9, 605-610.
2. Moreillon P & Que YA (2004) Infective endocarditis. Lancet 363, 139-149.
3. Foster TJ & Hook M (1998) Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6, 484-488.
4. Fitzgerald JR, Loughman A, Keane F, Brennan M, Knobel M, Higgins J, Visai L, Speziale P, Cox D & Foster TJ (2006) 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 FcgammaRIIa receptor. Mol Microbiol 59, 212-230.
5. Foster TJ (2005) Immune evasion by staphylococci. Nat Rev Microbiol 3, 948-958.
6. O'Brien L, Kerrigan SW, Kaw G, Hogan M, Penades J, Litt D, Fitzgerald DJ, Foster TJ & Cox D (2002) 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, 1033-1044.
7. Sullam PM, Bayer AS, Foss WM & Cheung AL (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.
8. Loughman A, Fitzgerald JR, Brennan MP, Higgins J, Downer R, Cox D & Foster TJ (2005) Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol Microbiol 57, 804-818.
9. Palmqvist N, Foster T, Fitzgerald JR, Josefsson E & Tarkowski A (2005) Fibronectin-binding proteins and fibrinogen-binding clumping factors play distinct roles in staphylococcal arthritis and systemic inflammation. J Infect Dis 191, 791-798.
10. Uhlen M, Guss B, Nilsson B, Gatenbeck S, Philipson L & Lindberg M (1984) Complete sequence of the staphylococcal gene encoding protein A. A gene evolved through multiple duplications. J Biol Chem 259, 1695-1702.
11. Moks T, Abrahmsen L, Nilsson B, Hellman U, Sjoquist J & Uhlen M (1986) Staphylococcal protein A consists of five IgG-binding domains. Eur J Biochem 156, 637-643.
12. Graille M, Stura EA, Corper AL, Sutton BJ, Taussig MJ, Charbonnier JB & Silverman GJ (2000) 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, 5399-5404.
13. Roben PW, Salem AN & Silverman GJ (1995) VH3 family antibodies bind domain D of staphylococcal protein A. J Immunol 154, 6437-6445.
14. Starovasnik MA, O'Connell MP, Fairbrother WJ & Kelley RF (1999) Antibody variable region binding by Staphylococcal protein A: thermodynamic analysis and location of the Fv binding site on E-domain. Protein Sci 8, 1423-1431.
15. Hartleib J, Kohler N, Dickinson RB, Chhatwal GS, Sixma JJ, Hartford OM, Foster TJ, Peters G, Kehrel BE & Herrmann M (2000) Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood 96, 2149-2156.
16. Sadler JE (1998) Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 67, 395-424.
17. Emsley J, Cruz M, Handin R & Liddington R (1998) Crystal structure of the von Willebrand Factor A1 domain and implications for the binding of platelet glycoprotein Ib. J Biol Chem 273, 10396-10401.
18. Huizinga EG, Tsuji S, Romijn RA, Schiphorst ME, de Groot PG, Sixma JJ & Gros P (2002) Structures of glycoprotein Ibalpha and its complex with von Willebrand factor A1 domain. Science 297, 1176-1179.
19. Uff S, Clemetson JM, Harrison T, Clemetson KJ & Emsley J (2002) Crystal structure of the platelet glycoprotein Ib (alpha) N-terminal domain reveals an unmasking mechanism for receptor activation. J Biol Chem 277, 35657-35663.
20. Siedlecki CA, Lestini BJ, Kottke-Marchant KK, Eppell SJ, Wilson DL & Marchant RE (1996) Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood 88, 2939-2950.
21. Novak L, Deckmyn H, Damjanovich S & Harsfalvi J (2002) Shear-dependent morphology of von Willebrand factor bound to immobilized collagen. Blood 99, 2070-2076.
22. Hulstein JJ, de Groot PG, Silence K, Veyradier A, Fijnheer R & Lenting PJ (2005) A novel nanobody that detects the gain-of-function phenotype of Von Willebrand factor in adamts13 deficiency and Von Willebrand disease type 2B. Blood 106, 3035-3042.
23. Kroll MH, Hellums JD, McIntire LV, Schafer AI & Moake JL (1996) Platelets and shear stress. Blood 88, 1525-1541.
24. Xiong JP, Stehle T, Goodman SL & Arnaout MA (2003) New insights into the structural basis of integrin activation. Blood 102, 1155-1159.
25. Pawar P, Shin PK, Mousa SA, Ross JM & Konstantopoulos K (2004) Fluid shear regulates the kinetics and receptor specificity of Staphylococcus aureus binding to activated platelets. J Immunol 173, 1258-1265.
26. Mascari LM & Ross JM (2003) Quantification of staphylococcal-collagen binding interactions in whole blood by use of a confocal microscopy shear-adhesion assay. J Infect Dis 188, 98-107.
27. Jansson B, Uhlen M & Nygren PA (1998) All individual domains of staphylococcal protein A show Fab binding. FEMS Immunol Med Microbiol 20, 69-78.
28. Deisenhofer J (1981) 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-A resolution. Biochemistry 20, 2361-2370.
29. Palmqvist N, Foster T, Tarkowski A & Josefsson E (2002) Protein A is a virulence factor in Staphylococcus aureus arthritis and septic death. Microb Pathog 33, 239-249.
30. Patel AH, Nowlan P, Weavers ED & Foster T (1987) Virulence of protein A-deficient and alpha-toxin-deficient mutants of Staphylococcus aureus isolated by allele replacement. Infect Immun 55, 3103-3110.
31. Gomez MI, Lee A, Reddy B, Muir A, Soong G, Pitt A, Cheung A & Prince A (2004) Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 10, 842-848.
32. Goodyear CS & Silverman GJ (2004) Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes. Proc Natl Acad Sci USA 101, 11392-11397.
33. Vlot AJ, Koppelman SJ, Meijers JC, Dama C, van den Berg HM, Bouma BN, Sixma JJ & Willems GM (1996) Kinetics of factor VIII-von Willebrand factor association. Blood 87, 1809-1816.
34. Vlot AJ, Koppelman SJ, van den Berg MH, Bouma BN & Sixma JJ (1995) The affinity and stoichiometry of binding of human factor VIII to von Willebrand factor. Blood 85, 3150-3157.
35. Slayter H, Loscalzo J, Bockenstedt P & Handin RI (1985) Native conformation of human von Willebrand protein. Analysis by electron microscopy and quasi-elastic light scattering. J Biol Chem 260, 8559-8563.
36. Fowler WE, Fretto LJ, Hamilton KK, Erickson HP & McKee PA (1985) Substructure of human von Willebrand factor. J Clin Invest 76, 1491-1500.
37. Alonso DO & Daggett V (2000) Staphylococcal protein A: unfolding pathways, unfolded states, and differences between the B and E domains. Proc Natl Acad Sci USA 97, 133-138.
38. Olszewski KA, Kolinski A & Skolnick J (1996) Folding simulations and computer redesign of protein A threehelix bundle motifs. Proteins 25, 286-299.
39. Linhult M, Gulich S, Graslund T, Simon A, Karlsson M, Sjoberg A, Nord K & Hober S (2004) Improving the tolerance of a protein a analogue to repeated alkaline exposures using a bypass mutagenesis approach. Proteins 55, 407-416.
40. Cedergren L, Andersson R, Jansson B, Uhlen M & Nilsson B (1993) Mutational analysis of the interaction between staphylococcal protein A and human IgG1. Protein Eng 6, 441-448.
41. Jendeberg L, Persson B, Andersson R, Karlsson R, Uhlen M & Nilsson B (1995) Kinetic analysis of the interaction between protein A domain variants and human Fc using plasmon resonance detection. J Mol Recognit 8, 270-278.
42. Huston JS, Cohen C, Maratea D, Fields F, Tai MS, Cabral-Denison N, Juffras R, Rueger DC, Ridge RJ, Oppermann H, et al. (1992) Multisite association by recombinant proteins can enhance binding selectivity. Preferential removal of immune complexes from serum by immobilized truncated FB analogues of the B domain from staphylococcal protein A. Biophys J 62, 87-91.
43. Langone JJ (1982) Protein A of Staphylococcus aureus and related immunoglobulin receptors produced by streptococci and pneumonococci. Adv Immunol 32, 157-252.
44. Lausch R, Reif OW, Riechel P & Scheper T (1995) Analysis of immunoglobulin G using a capillary electrophoretic affinity assay with protein A and laser-induced fluorescence detection. Electrophoresis 16, 636-641.
45. Patel AH, Kornblum J, Kreiswirth B, Novick R & Foster TJ (1992) Regulation of the protein A-encoding gene in Staphylococcus aureus. Gene 114, 25-34.
46. Sasano M, Burton DR & Silverman GJ (1993) Molecular selection of human antibodies with an unconventional bacterial B cell antigen. J Immunol 151, 5822-5839.
47. Cary S, Krishnan M, Marion TN & Silverman GJ (1999) The murine clan V(H)III related 7183, J606 and S107 and DNA4 families commonly encode for binding to a bacterial B cell superantigen. Mol Immunol 36, 769-776.
48. Lenting PJ, Westein E, Terraube V, Ribba AS, Huizinga EG, Meyer D, de Groot PG & Denis CV (2004) An experimental model to study the in vivo survival of von Willebrand factor. Basic aspects and application to the R1205H mutation. J Biol Chem 279, 12102-12109.
49. Huizinga EG, Martijn van der Plas R, Kroon J, Sixma JJ & Gros P (1997) Crystal structure of the A3 domain of human von Willebrand factor: implications for collagen binding. Structure 5, 1147-1156.
50. Cruz MA, Handin RI & Wise RJ (1993) The interaction of the von Willebrand factor-A1 domain with platelet glycoprotein Ib/IX. The role of glycosylation and disul-fide bonding in a monomeric recombinant A1 domain protein. J Biol Chem 268, 21238-21245.
51. Ansorge W (1985) Fast and sensitive detection of protein and DNA bands by treatment with potassium permanganate. J Biochem Biophys Methods 11, 13-20.