Staphylococcus aureus secretes coagulase and von willebrand factor binding protein to modify the coagulation cascade and establish host infections

Journal of Innate Immunity

Volumn 4, Issue 2, 2012, Pages 141-148

  McAdow, Molly ^a   Missiakas, Dominique M ^a   Schneewind, Olaf ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Coagulation; Host defense; Neutrophils; Proteinases; Sepsis; Staphylococcus aureus infection

Indexed keywords

BINDING PROTEIN; BLOOD CLOTTING FACTOR 7A; CALCIUM; COAGULASE; FIBRIN; FIBRINOGEN; FIBRINOPEPTIDE A; FIBRINOPEPTIDE B; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE; PHOSPHOLIPID; PLASMINOGEN; PROTHROMBIN; STAPHYLOCOCCUS PROTEIN A; THROMBIN; VON WILLEBRAND FACTOR;

ABSCESS; AUTOPSY; BACTERIAL ENDOCARDITIS; BACTERIAL VIRULENCE; BLOOD CLOTTING; ENZYME ACTIVITY; FIBRINOLYSIS; HISTOPATHOLOGY; HUMAN; INNATE IMMUNITY; MASTITIS; NONHUMAN; PATHOGENESIS; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; REVIEW; STAPHYLOCOCCAL BACTEREMIA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; STREPTOCOCCUS GORDONII; THROMBOCYTE ACTIVATION; THROMBOELASTOGRAPHY;

ANIMALS; BACTERIAL PROTEINS; BLOOD COAGULATION; COAGULASE; HUMANS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84857789311     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000333447     Document Type: Review

References (81)

1. Wang Z, Wilhelmsson C, Hyrsl P, Loof TG, Dobes P, Klupp M, Loseva O, Morgelin M, Ikle J, Cripps RM, Herwald H, Theopold U: Pathogen entrapment by transglutaminase -a conserved early innate immune mechanism. PLoS Pathog 2010; 6:e1000763.
2. Loof TG, Morgelin M, Johansson L, Oehmcke S, Olin AI, Dickneite G, Norrby-Teglund A, Theopold U, Herwald H: Coagulation, an ancestral serine protease cascade, exerts a novel function in early immune defense. Blood 2011; 118: 2589-2598.
3. Krarup A, Wallis R, Presanis JS, Gal P, Sim RB: Simultaneous activation of complement and coagulation by MBL-associated serine protease 2. PLoS One 2007; 2:e623.
4. Loeb L: The influence of certain bacteria on the coagulation of the blood. J Med Res 1903; 10: 407-419.
5. Lowy FD: Staphylococcus aureus infections. N Engl J Med 1998; 339: 520-532.
6. Boucher HW, Corey GR: Epidemiology of methicillin-resistant Staphylococcus aureus Clin Infect Dis 2008; 46(suppl 5):S344-S349. (Pubitemid 351717321)
7. Chu VH, Crosslin DR, Friedman JY, Reed SD, Cabell CH, Griffiths RI, Masselink LE, Kaye KS, Corey GR, Reller LB, Stryjewski ME, Schulman KA, Fowler VG Jr: Staphylococcus aureus bacteremia in patients with prosthetic devices: Costs and outcomes. Am J Med 2005; 118: 1416.
8. Kallen AJ, Brunkard J, Moore Z, Budge P, Arnold KE, Fosheim G, Finelli L, Beekmann SE, Polgreen PM, Gorwitz R, Hageman J: Staphylococcus aureus community-acquired pneumonia during the 2006 to 2007 influenza season. Ann Emerg Med 2009; 53: 358-365.
9. Cheng AG, McAdow M, Kim HK, Bae T, Missiakas DM, Schneewind O: Contribution of coagulases towards Staphylococcus aureus disease and protective immunity. PLoS Pathog 2010; 6:e1001036
10. Adams RL, Bird RJ: Coagulation cascade and therapeutics update: Relevance to nephrology. Part 1. Overview of coagulation, thrombophilias and history of anticoagulants. Nephrology 2009; 14: 462-470.
11. Gailani D, Renne T: Intrinsic pathway of coagulation and arterial thrombosis. Arterioscler Thromb Vasc Biol 2007; 27: 2507-2513. (Pubitemid 350158899)
12. Procyk R, Blomback B: Disulfide bond reduction in fibrinogen: Calcium protection and effect on clottability. Biochemistry 1990; 29: 1501-1507. (Pubitemid 20063381)
13. Kollman JM, Pandi L, Sawaya MR, Riley M, Doolittle RF: Crystal structure of human fibrinogen. Biochemistry 2009; 48: 3877-3886.
14. Blomback B, Hessel B, Hogg D, Therkildsen L: A two-step fibrinogen-fibrin transition in blood coagulation. Nature 1978; 275: 501-505. (Pubitemid 9020557)
15. Yang Z, Mochalkin I, Doolittle RF: A model of fibrin formation based on crystal structures of fibrinogen and fibrin fragments complexed with synthetic peptides. Proc Natl Acad Sci USA 2000; 97: 14156-14161. (Pubitemid 32016546)
16. Lorand L: Sol Sherry lecture in thrombosis: Research on clot stabilization provides clues for improving thrombolytic therapies. Arterioscler Thromb Vasc Biol 2000; 20: 2-9. (Pubitemid 30048340)
17. Delvaeye M, Conway EM: Coagulation and innate immune responses: Can we view them separately? Blood 2009; 114: 2367-2374.
18. Walker JB, Nesheim ME: The molecular weights, mass distribution, chain composition, and structure of soluble fibrin degradation products released from a fibrin clot perfused with plasmin. J Biol Chem 1999; 274: 5201-5212.
19. Rijken DC, Lijnen HR: New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost 2009; 7: 4-13.
20. Lord ST: Molecular mechanisms affecting fibrin structure and stability. Arterioscler Thromb Vasc Biol 2011; 31: 494-499.
21. Konings J, Govers-Riemslag JW, Philippou H, Mutch NJ, Borissoff JI, Allan P, Mohan S, Tans G, Ten Cate H, Ariens RA: Factor XIIa regulates the structure of the fibrin clot independently of thrombin generation through direct interaction with fibrin. Blood 2011, Epub ahead of print.
22. Ariens RA, Philippou H, Nagaswami C, Weisel JW, Lane DA, Grant PJ: The factor XIII v34l polymorphism accelerates thrombin activation of factor XIII and affects cross-linked fibrin structure. Blood 2000; 96: 988-995. (Pubitemid 30616865)
23. Andersen MD, Kjalke M, Bang S, Lautrup-Larsen I, Becker P, Andersen AS, Olsen OH, Stennicke HR: Coagulation factor XIII variants with altered thrombin activation rates. Biol Chem 2009; 390: 1279-1283.
24. Wolberg AS: Plasma and cellular contributions to fibrin network formation, structure and stability. Haemophilia 2010; 16(suppl 3):7-12.
25. Mutch NJ, Engel R, Uitte de Willige S, Philippou H, Ariens RA: Polyphosphate modifies the fibrin network and down-regulates fibrinolysis by attenuating binding of tPA and plasminogen to fibrin. Blood 2010; 115: 3980-3988.
26. Friedrich R, Panizzi P, Fuentes-Prior P, Richter K, Verhamme I, Anderson PJ, Kawabata S, Huber R, Bode W, Bock PE: Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation. Nature 2003; 425: 535-539. (Pubitemid 37237051)
27. Kroh HK, Panizzi P, Bock PE: Von Willebrand factor-binding protein is a hysteretic conformational activator of prothrombin. Proc Natl Acad Sci USA 2009; 106: 7786-7791.
28. Watanabe S, Ito T, Takeuchi F, Endo M, Okuno E, Hiramatsu K: Structural comparison of ten serotypes of staphylocoagulases in Staphylococcus aureus J Bacteriol 2005; 187: 3698-3707. (Pubitemid 40705573)
29. Kawabata S, Morita T, Iwanaga S, Igarashi H: Staphylocoagulase-binding region in human prothrombin. J Biochem 1985; 97: 325-331. (Pubitemid 15158967)
30. Cheung AI, Projan SJ, Edelstein RE, Fischetti VA: Cloning, expression, and nucleotide sequence of a Staphylococcus aureus gene ( fbpA ) encoding a fibrinogen-binding protein. Infect Immun 1995; 63: 1914-1920.
31. Phonimdaeng P, O'Reilly M, O'Toole PW, Foster TJ: Molecular cloning and expression of the coagulase gene of Staphylococcus aureus 8325-4. J Gen Microbiol 1988; 134: 75-83. (Pubitemid 18031725)
32. Bjerketorp J, Jacobsson K, Frykberg L: The von Willebrand factor-binding protein (vWbp) of Staphylococcus aureus is a coagulase. FEMS Microbiol Lett 2004; 234: 309-314. (Pubitemid 38595648)
33. Bjerketorp J, Nilsson M, Ljungh A, Flock JI, Jacobsson K, Frykberg L: A novel von Willebrand factor binding protein expressed by Staphylococcus aureus Microbiology 2002; 148: 2037-2044. (Pubitemid 34785288)
34. Chapman GH, Berens C, Peters A, Curcio L: Coagulase and hemolysin tests as measures of the pathogenicity of staphylococci. J Bacteriol 1934; 28: 343-363.
35. Spink WW, Vivino JJ: The coagulase test for staphylococci and its correlation with the resistance of the organisms to the bactericidal action of human blood. J Clin Invest 1942; 21: 353-356.
36. Ekstedt RD, Yotis WW: Studies on staphylococci. II. Effect of coagulase on the virulence of coagulase negative strains. J Bacteriol 1960; 80: 496-500.
37. Phonimdaeng P, O'Reilly M, Nowlan P, Bramley AJ, Foster TJ: The coagulase of Staphylococcus aureus 8325-4. Sequence analysis and virulence of site-specific coagulase-deficient mutants. Mol Microbiol 1990; 4: 393-404.
38. Baddour LM, Tayidi MM, Walker E, McDevitt D, Foster TJ: Virulence of coagulase-deficient mutants of Staphylococcus aureus in experimental endocarditis. J Med Microbiol 1994; 41: 259-263. (Pubitemid 24333792)
39. Moreillon P, Entenza JM, Francioli P, McDevitt D, Foster TJ, Francois P, Vaudaux P: Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun 1995; 63: 4738-4743.
40. Stutzmann Meier P, Entenza JM, Vaudaux P, Francioli P, Glauser MP, Moreillon P: Study of Staphylococcus aureus pathogenic genes by transfer and expression in the less virulent organism Streptococcus gordonii Infect Immun 2001; 69: 657-664. (Pubitemid 32109523)
41. Sawai T, Tomono K, Yanagihara K, Yamamoto Y, Kaku M, Hirakata Y, Koga H, Tashiro T, Kohno S: Role of coagulase in a murine model of hematogenous pulmonary infection induced by intravenous injection of Staphylococcus aureus enmeshed in agar beads. Infect Immun 1997; 65: 466-471. (Pubitemid 27053210)
42. Haraldsson I, Jonsson P: Histopathology and pathogenesis of mouse mastitis induced with Staphylococcus aureus mutants. J Comp Pathol 1984; 94: 183-196. (Pubitemid 15060846)
43. Jonsson P, Lindberg M, Haraldsson I, Wadstrom T: Virulence of Staphylococcus aureus in a mouse mastitis model: Studies of alpha hemolysin, coagulase, and protein A as possible virulence determinants with protoplast fusion and gene cloning. Infect Immun 1985; 49: 765-769. (Pubitemid 15021542)
44. Seki K, Ogasawara M, Sakurada J, Murai M, Masuda S: Altered virulence of a pleiotropic Staphylococcus aureus mutant with a low producibility of coagulase and other factors in mice. Microbiol Immunol 1989; 33: 981-990. (Pubitemid 20082964)
45. Johnstone JM, Smith DD: Coagulase activity in vivo. Nature 1956; 178: 982-983.
46. Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, Missiakas DM: Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 2009; 23: 3393-3404.
47. Lam GT, Sweeney FJ Jr, Witmer CM, Wise RI: Abscess-forming factor(s) produced by Staphylococcus aureus. I. Collodion bag implantation technique. J Bacteriol 1963; 86: 611-615.
48. Lam GT, Sweeney FJ Jr, Witmer CM, Wise RI: Abscess-forming factor(s) produced by Staphylococcus aureus II. Abscess formation and immunity by a staphylococcus and its mutants. J Bacteriol 1963; 86: 87-91.
49. Cawdery M, Foster WD, Hawgood BC, Taylor C: The role of coagulase in the defence of Staphylococcus aureus against phagocytosis. Br J Exp Pathol 1969; 50: 408-412.
50. Kapral FA: Clumping of Staphylococcus aureus in the peritoneal cavity of mice. J Bacteriol 1966; 92: 1188-1195.
51. Yeaman MR, Norman DC, Bayer AS: Platelet microbicidal protein enhances antibiotic-induced killing of and postantibiotic effect in Staphylococcus aureus Antimicrob Agents Chemother 1992; 36: 1665-1670.
52. Fitzgerald JR, Foster TJ, Cox D: The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006; 4: 445-457. (Pubitemid 43771864)
53. Ni Eidhin D, Perkins S, Francois P, Vaudaux P, Hook M, Foster TJ: Clumping factor B ( clfB ), a new surface-located fibrinogenbinding adhesin of Staphylococcus aureus Mol Microbiol 1998; 30: 245-257. (Pubitemid 28480176)
54. O'Brien L, Kerrigan SW, Kaw G, Hogan M, Penades J, Litt D, Fitzgerald DJ, Foster TJ, Cox D: 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: 1033-1044. (Pubitemid 34535538)
55. Niemann S, Spehr N, Van Aken H, Morgenstern E, Peters G, Herrmann M, Kehrel BE: Soluble fibrin is the main mediator of Staphylococcus aureus adhesion to platelets. Circulation 2004; 110: 193-200. (Pubitemid 38924588)
56. Much H: Über eine Vorstufe des Fibrinfermentes in Kulturen von Staphylococcus aureus Biochem Z 1908; 14: 143-155.
57. Birch-Hirschfeld L: Über die Agglutination von Staphylokokken durch Bestandteile des Säugetierblutplasmas. Klin Wochenschr 1934; 13: 331.
58. Cadness-Graves B, Williams R, Harper GJ, Miles AA: Slide test for coagulase-positive staphylococci. Lancet 1943; 2: 736-738.
59. Berger F: Clumping of pathogenic staphylococci in plasma. J Pathol Bacteriol 1943; 55.
60. Duthie ES: Evidence for two forms of staphylococcal coagulase. J Gen Microbiol 1954; 10: 427-436.
61. McDevitt D, Francois P, Vaudaux P, Foster TJ: Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus Mol Microbiol 1994; 11: 237-248. (Pubitemid 24201596)
62. Que YA, Haefliger JA, Francioli P, Moreillon P: Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis ssp cremoris using a new shuttle vector. Infect Immun 2000; 68: 3516-3522. (Pubitemid 30340452)
63. McAdow M, Kim HK, Dedent A, Hendrickx A, Missiakas DM, Schneewind O: Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog 2011; 10: 3e1002307.
64. Umeda A, Ikebuchi T, Amako K: Localization of bacteriophage receptor, clumping factor, and protein A on the cell surface of Staphylococcus aureus J Bacteriol 1980; 141: 838-844. (Pubitemid 10106290)
65. Jensen K: A normally occurring staphylococcus antibody in human serum. Acta Path Microbiol Scand 1958; 44: 421-428.
66. Deisenhofer J, Jones TA, Huber R, Sjodahl J, Sjoquist J: Crystallization, crystal structure analysis and atomic model of the complex formed by a human Fc fragment and fragment B of protein A from Staphylococcus aureus Hoppe Seylers Z Physiol Chem 1978; 359: 975-985. (Pubitemid 9060557)
67. Graille M, Stura EA, Corper AL, Sutton BJ, Taussig MJ, Charbonnier JB, Silverman GJ: 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 2000; 97: 5399-5404. (Pubitemid 30313730)
68. Hartleib J, Kohler N, Dickinson RB, Chhatwal GS, Sixma JJ, Hartford OM, Foster TJ, Peters G, Kehrel BE, Herrmann M: Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood 2000; 96: 2149-2156.
69. O'Seaghdha M, van Schooten CJ, Kerrigan SW, Emsley J, Silverman GJ, Cox D, Lenting PJ, Foster TJ: S taphylococcus aureus protein A binding to von Willebrand factor A1 domain is mediated by conserved IgG binding regions. FEBS J 2006; 273: 4831-4841. (Pubitemid 44583508)
70. Zajdel M, Wagrzynowicz Z, Jeljaszewicz J: Action of staphylothrombin on bovine fibrinogen. Thromb Res 1975; 6: 501-510.
71. Soulier JP, Prou-Wartelle O: Study of thrombin-coagulase. Thromb Diath Haemorrh 1967; 17: 321-334.
72. Kawabata S, Morita T, Iwanaga S, Igarashi H: Difference in enzymatic properties between alpha-thrombin-staphylocoagulase complex and free alpha-thrombin. J Biochem 1985; 97: 1073-1078. (Pubitemid 15097917)
73. Kawabata S, Morita T, Iwanaga S, Igarashi H: Enzymatic properties of staphylothrombin, an active molecular complex formed between staphylocoagulase and human prothrombin. J Biochem 1985; 98: 1603-1614. (Pubitemid 16169195)
74. Hendrix H, Lindhout T, Mertens K, Engels W, Hemker HC: Activation of human prothrombin by stoichiometric levels of staphylocoagulase. J Biol Chem 1983; 258: 3637-3644. (Pubitemid 13055779)
75. Kopec M, Wegrzynowicz Z, Budzynski AZ, Jeljaszewicz J, Latallo ZS, Lipinski B, Kowalski E: Formation and properties of fibrin clots resulting from staphylocoagulase (sc) action. Thromb Diath Haemorrh 1967; 18: 475-486.
76. Crawley JT, Zanardelli S, Chion CK, Lane DA: The central role of thrombin in hemostasis. J Thromb Haemost 2007; 5(suppl 1):95-101. (Pubitemid 46958822)
77. Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, Lambris JD, Warner RL, Flierl MA, Hoesel LM, Gebhard F, Younger JG, Drouin SM, Wetsel RA, Ward PA: Generation of C5a in the absence of C3: A new complement activation pathway. Nat Med 2006; 12: 682-687. (Pubitemid 43865238)
78. Lack CH: Staphylokinase: An activator of plasma protease. Nature 1948; 161: 559.
79. Sakharov DV, Lijnen HR, Rijken DC: Interactions between staphylokinase, plasmin (o gen), and fibrin. Staphylokinase discriminates between free plasminogen and plasminogen bound to partially degraded fibrin. J Biol Chem 1996; 271: 27912-27918. (Pubitemid 26367369)
80. Kwiecinski J, Josefsson E, Mitchell J, Higgins J, Magnusson M, Foster T, Jin T, Bokarewa M: Activation of plasminogen by staphylokinase reduces the severity of Staphylococcus aureus systemic infection. J Infect Dis 2010; 202: 1041-1049.
81. Vanassche T, Verhaegen J, Peetermans WE, Hoylaerts MF, Verhamme P: Dabigatran inhibits Staphylococcus aureus coagulase activity. J Clin Microbiol 2010; 48: 4248-4250.