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Published in: Seminars in Immunopathology 2/2012

01-03-2012 | Review

Exploring Staphylococcus aureus pathways to disease for vaccine development

Authors: Andrea DeDent, Hwan Keun Kim, Dominique Missiakas, Olaf Schneewind

Published in: Seminars in Immunopathology | Issue 2/2012

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Abstract

Staphylococcus aureus is a commensal of the human skin or nares and a pathogen that frequently causes skin and soft tissue infections as well as bacteremia and sepsis. Recent efforts in understanding the molecular mechanisms of pathogenesis revealed key virulence strategies of S. aureus in host tissues: bacterial scavenging of iron, induction of coagulation pathways to promote staphylococcal agglutination in the vasculature, and suppression of innate and adaptive immune responses. Advances in all three areas have been explored for opportunities in vaccine design in an effort to identify the critical protective antigens of S. aureus. Human clinical trials with specific subunit vaccines have failed, yet provide important insights for the design of future trials that must address the current epidemic of S. aureus infections with drug-resistant isolates (MRSA, methicillin-resistant S. aureus).
Literature
1.
go back to reference Peacock SJ, de Silva I, Lowy FD (2001) What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 9:605–610PubMedCrossRef Peacock SJ, de Silva I, Lowy FD (2001) What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 9:605–610PubMedCrossRef
3.
go back to reference Chambers HF, Deleo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7:629–641PubMedCrossRef Chambers HF, Deleo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7:629–641PubMedCrossRef
4.
go back to reference Chambers HF (2001) The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 7:178–182PubMedCrossRef Chambers HF (2001) The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 7:178–182PubMedCrossRef
5.
go back to reference Deleo FR, Otto M, Kreiswirth BN, HF Chambers Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375:1557–1568 Deleo FR, Otto M, Kreiswirth BN, HF Chambers Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375:1557–1568
6.
go back to reference Klevens RM, Edwards JR, Gaynes RP (2008) The impact of antimicrobial-resistant, health care-associated infections on mortality in the United States. Clin Infect Dis 47:927–930PubMedCrossRef Klevens RM, Edwards JR, Gaynes RP (2008) The impact of antimicrobial-resistant, health care-associated infections on mortality in the United States. Clin Infect Dis 47:927–930PubMedCrossRef
7.
go back to reference Projan SJ, Nesin M, Dunman PM (2006) Staphylococcal vaccines and immunotherapy: to dream the impossible dream? Curr Opin Pharmacol 6:473–479PubMedCrossRef Projan SJ, Nesin M, Dunman PM (2006) Staphylococcal vaccines and immunotherapy: to dream the impossible dream? Curr Opin Pharmacol 6:473–479PubMedCrossRef
9.
go back to reference Shinefield H, Black S, Fattom A, Horwith G, Rasgon S, Ordonez J, Yeoh H, Law D, Robbins JB, Schneerson R et al (2002) Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med 346:491–496PubMedCrossRef Shinefield H, Black S, Fattom A, Horwith G, Rasgon S, Ordonez J, Yeoh H, Law D, Robbins JB, Schneerson R et al (2002) Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med 346:491–496PubMedCrossRef
10.
go back to reference DeJonge M, Burchfield D, Bloom B, Duenas M, Walker W, Polak M, Jung E, Millard D, Schelonka R, Eyal F et al (2007) Clinical trial of safety and efficacy of INH-A21 for the prevention of nosocomial staphylococcal bloodstream infection in premature infants. J Pediatr 151:260–265, 265 e1PubMedCrossRef DeJonge M, Burchfield D, Bloom B, Duenas M, Walker W, Polak M, Jung E, Millard D, Schelonka R, Eyal F et al (2007) Clinical trial of safety and efficacy of INH-A21 for the prevention of nosocomial staphylococcal bloodstream infection in premature infants. J Pediatr 151:260–265, 265 e1PubMedCrossRef
11.
go back to reference Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, McNeely T, Noble L, Brown MJ, Zorman JK, Wang XM et al (2006) 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 74:2215–2223PubMedCrossRef Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, McNeely T, Noble L, Brown MJ, Zorman JK, Wang XM et al (2006) 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 74:2215–2223PubMedCrossRef
12.
go back to reference Fattom AI, Horwith G, Fuller S, Propst M, Naso R (2004) Development of StaphVAX, a polysaccharide conjugate vaccine against S. aureus infection: from the lab bench to phase III clinical trials. Vaccine 22:880–887PubMedCrossRef Fattom AI, Horwith G, Fuller S, Propst M, Naso R (2004) Development of StaphVAX, a polysaccharide conjugate vaccine against S. aureus infection: from the lab bench to phase III clinical trials. Vaccine 22:880–887PubMedCrossRef
14.
go back to reference Huff RL, Hennessy TG, Austin RE, Garcia JF, Roberts BM, Lawrence JH (1950) Plasma and red cell iron turnover in normal subjects and in patients having various hematopoietic disorders. J Clin Invest 29:1041–1052PubMedCrossRef Huff RL, Hennessy TG, Austin RE, Garcia JF, Roberts BM, Lawrence JH (1950) Plasma and red cell iron turnover in normal subjects and in patients having various hematopoietic disorders. J Clin Invest 29:1041–1052PubMedCrossRef
15.
go back to reference Morgan WT, Liem HH, Sutor RP, Muller-Ebergard U (1976) Transfer of heme from heme–albumin to hemopexin. Biochim Biophys Acta 444:435–445PubMedCrossRef Morgan WT, Liem HH, Sutor RP, Muller-Ebergard U (1976) Transfer of heme from heme–albumin to hemopexin. Biochim Biophys Acta 444:435–445PubMedCrossRef
16.
go back to reference Giblett ER (1968) Recent advances in heptoglobin and transferrin genetics. Bibl Haematol 29:10–20PubMed Giblett ER (1968) Recent advances in heptoglobin and transferrin genetics. Bibl Haematol 29:10–20PubMed
17.
go back to reference Kristiansen M, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, Law SK, Moestrup SK (2001) Identification of the haemoglobin scavenger receptor. Nature 409:198–201PubMedCrossRef Kristiansen M, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, Law SK, Moestrup SK (2001) Identification of the haemoglobin scavenger receptor. Nature 409:198–201PubMedCrossRef
18.
go back to reference Uchida T, Akitsuki T, Kimura H, Tanaka T, Matsuda S, Kariyone S (1983) Relationship among plasma iron, plasma iron turnover, and reticuloendothelial iron release. Blood 61:799–802PubMed Uchida T, Akitsuki T, Kimura H, Tanaka T, Matsuda S, Kariyone S (1983) Relationship among plasma iron, plasma iron turnover, and reticuloendothelial iron release. Blood 61:799–802PubMed
19.
go back to reference Pigeon C, Ilyin G, Courselaud B, Leroyer P, Turlin B, Brissot P, Loreal O (2001) A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem 276:7811–7819PubMedCrossRef Pigeon C, Ilyin G, Courselaud B, Leroyer P, Turlin B, Brissot P, Loreal O (2001) A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem 276:7811–7819PubMedCrossRef
20.
go back to reference Park CH, Valore EV, Waring AJ, Ganz T (2001) Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem 276:7806–7810PubMedCrossRef Park CH, Valore EV, Waring AJ, Ganz T (2001) Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem 276:7806–7810PubMedCrossRef
21.
go back to reference Krause A, Neitz S, Magert HJ, Schulz A, Forssmann WG, Schulz-Knappe P, Adermann K (2000) LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity. FEBS Lett 480:147–150PubMedCrossRef Krause A, Neitz S, Magert HJ, Schulz A, Forssmann WG, Schulz-Knappe P, Adermann K (2000) LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity. FEBS Lett 480:147–150PubMedCrossRef
22.
go back to reference Nicolas G, Bennoun M, Devaux I, Beaumont C, Grandchamp B, Kahn A, Vaulont S (2001) Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci USA 98:8780–8785PubMedCrossRef Nicolas G, Bennoun M, Devaux I, Beaumont C, Grandchamp B, Kahn A, Vaulont S (2001) Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci USA 98:8780–8785PubMedCrossRef
23.
go back to reference Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306:2090–2093PubMedCrossRef Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306:2090–2093PubMedCrossRef
24.
go back to reference Knutson MD, Oukka M, Koss LM, Aydemir F, Wessling-Resnick M (2005) Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc Natl Acad Sci USA 102:1324–1328PubMedCrossRef Knutson MD, Oukka M, Koss LM, Aydemir F, Wessling-Resnick M (2005) Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc Natl Acad Sci USA 102:1324–1328PubMedCrossRef
25.
go back to reference Nicolas G, Chauvet C, Viatte L, Danan JL, Bigard X, Devaux I, Beaumont C, Kahn A, Vaulont S (2002) The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 110:1037–1044PubMed Nicolas G, Chauvet C, Viatte L, Danan JL, Bigard X, Devaux I, Beaumont C, Kahn A, Vaulont S (2002) The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 110:1037–1044PubMed
26.
go back to reference Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T (2003) Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 101:2461–2463PubMedCrossRef Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T (2003) Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 101:2461–2463PubMedCrossRef
27.
go back to reference Weinberg ED (1984) Iron withholding: a defense against infection and neoplasia. Physiol Rev 64:65–102PubMed Weinberg ED (1984) Iron withholding: a defense against infection and neoplasia. Physiol Rev 64:65–102PubMed
28.
go back to reference Rivera S, Nemeth E, Gabayan V, Lopez MA, Farshidi D, Ganz T (2005) Synthetic hepcidin causes rapid dose-dependent hypoferremia and is concentrated in ferroportin-containing organs. Blood 106:2196–2199PubMedCrossRef Rivera S, Nemeth E, Gabayan V, Lopez MA, Farshidi D, Ganz T (2005) Synthetic hepcidin causes rapid dose-dependent hypoferremia and is concentrated in ferroportin-containing organs. Blood 106:2196–2199PubMedCrossRef
29.
go back to reference Pietrangelo A (2006) Molecular insights into the pathogenesis of hereditary haemochromatosis. Gut 55:564–568PubMedCrossRef Pietrangelo A (2006) Molecular insights into the pathogenesis of hereditary haemochromatosis. Gut 55:564–568PubMedCrossRef
30.
go back to reference Van Snick JL, Masson PL, Heremans JF (1974) The involvement of lactoferrin in the hyposideremia of acute inflammation. J Exp Med 140:1068–1084PubMedCrossRef Van Snick JL, Masson PL, Heremans JF (1974) The involvement of lactoferrin in the hyposideremia of acute inflammation. J Exp Med 140:1068–1084PubMedCrossRef
31.
go back to reference van Snick JL, Markowetz B, Masson PL (1977) The ingestion and digestion of human lactoferrin by mouse peritoneal macrophages and the transfer of its iron into ferritin. J Exp Med 146:817–827PubMedCrossRef van Snick JL, Markowetz B, Masson PL (1977) The ingestion and digestion of human lactoferrin by mouse peritoneal macrophages and the transfer of its iron into ferritin. J Exp Med 146:817–827PubMedCrossRef
32.
go back to reference Fluckinger M, Haas H, Merschak P, Glasgow BJ, Redl B (2004) Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob Agents Chemother 48:3367–3372PubMedCrossRef Fluckinger M, Haas H, Merschak P, Glasgow BJ, Redl B (2004) Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob Agents Chemother 48:3367–3372PubMedCrossRef
33.
go back to reference Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, Strong RK, Akira S, Aderem A (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432:917–921PubMedCrossRef Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, Strong RK, Akira S, Aderem A (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432:917–921PubMedCrossRef
34.
go back to reference Ford FA, Mouratidou T, Wademan SE, Fraser RB (2009) Effect of the introduction of 'Healthy Start' on dietary behaviour during and after pregnancy: early results from the 'before and after' Sheffield study. Br J Nutr 101:1828–1836PubMedCrossRef Ford FA, Mouratidou T, Wademan SE, Fraser RB (2009) Effect of the introduction of 'Healthy Start' on dietary behaviour during and after pregnancy: early results from the 'before and after' Sheffield study. Br J Nutr 101:1828–1836PubMedCrossRef
35.
go back to reference Eaton JW, Brandt P, Mahoney JR, Lee JT Jr (1982) Haptoglobin: a natural bacteriostat. Science 215:691–693PubMedCrossRef Eaton JW, Brandt P, Mahoney JR, Lee JT Jr (1982) Haptoglobin: a natural bacteriostat. Science 215:691–693PubMedCrossRef
36.
go back to reference Moore DG, Earhart CF (1981) Specific inhibition of Escherichia coli ferrienterochelin uptake by a normal human serum immunoglobulin. Infect Immun 31:631–635PubMed Moore DG, Earhart CF (1981) Specific inhibition of Escherichia coli ferrienterochelin uptake by a normal human serum immunoglobulin. Infect Immun 31:631–635PubMed
37.
go back to reference Bullen JJ, Rogers HJ, Griffiths E (1978) Role of iron in bacterial infection. Curr Top Microbiol Immunol 80:1–35PubMedCrossRef Bullen JJ, Rogers HJ, Griffiths E (1978) Role of iron in bacterial infection. Curr Top Microbiol Immunol 80:1–35PubMedCrossRef
38.
go back to reference Horsburgh MJ, Clements MO, Crossley H, Ingham E, Foster SJ (2001) PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect Immun 69:3744–3754PubMedCrossRef Horsburgh MJ, Clements MO, Crossley H, Ingham E, Foster SJ (2001) PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect Immun 69:3744–3754PubMedCrossRef
39.
go back to reference Horsburgh MJ, Wharton SJ, Cox AG, Ingham E, Peacock S, Foster SJ (2002) MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol Microbiol 44:1269–1286PubMedCrossRef Horsburgh MJ, Wharton SJ, Cox AG, Ingham E, Peacock S, Foster SJ (2002) MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol Microbiol 44:1269–1286PubMedCrossRef
40.
go back to reference Hill PJ, Cockayne A, Landers P, Morrissey JA, Sims CM, Williams P (1998) SirR, a novel iron-dependent repressor in Staphylococcus epidermidis. Infect Immun 66:4123–4129PubMed Hill PJ, Cockayne A, Landers P, Morrissey JA, Sims CM, Williams P (1998) SirR, a novel iron-dependent repressor in Staphylococcus epidermidis. Infect Immun 66:4123–4129PubMed
41.
go back to reference Xiong A, Singh VK, Cabrera G (2000) RK Jayaswal: Molecular characterization of the ferric-uptake regulator, fur, from Staphylococcus aureus. Microbiology 146(Pt 3):659–668PubMed Xiong A, Singh VK, Cabrera G (2000) RK Jayaswal: Molecular characterization of the ferric-uptake regulator, fur, from Staphylococcus aureus. Microbiology 146(Pt 3):659–668PubMed
42.
go back to reference Horsburgh MJ, Ingham E, Foster SJ (2001) In Staphylococcus aureus, fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol 183:468–475PubMedCrossRef Horsburgh MJ, Ingham E, Foster SJ (2001) In Staphylococcus aureus, fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol 183:468–475PubMedCrossRef
43.
go back to reference Torres VJ, Attia AS, Mason WJ, Hood MI, Corbin BD, Beasley FC, Anderson KL, Stauff DL, McDonald WH, Zimmerman LJ et al Staphylococcus aureus fur regulates the expression of virulence factors that contribute to the pathogenesis of pneumonia. Infect Immun 78:1618–1628 Torres VJ, Attia AS, Mason WJ, Hood MI, Corbin BD, Beasley FC, Anderson KL, Stauff DL, McDonald WH, Zimmerman LJ et al Staphylococcus aureus fur regulates the expression of virulence factors that contribute to the pathogenesis of pneumonia. Infect Immun 78:1618–1628
44.
go back to reference Stauff DL, Bagaley D, Torres VJ, Joyce R, Anderson KL, Kuechenmeister L, Dunman PM, Skaar EP (2008) Staphylococcus aureus HrtA is an ATPase required for protection against heme toxicity and prevention of a transcriptional heme stress response. J Bacteriol 190:3588–3596PubMedCrossRef Stauff DL, Bagaley D, Torres VJ, Joyce R, Anderson KL, Kuechenmeister L, Dunman PM, Skaar EP (2008) Staphylococcus aureus HrtA is an ATPase required for protection against heme toxicity and prevention of a transcriptional heme stress response. J Bacteriol 190:3588–3596PubMedCrossRef
45.
go back to reference Stauff DL, Torres VJ, Skaar EP (2007) Signaling and DNA-binding activities of the Staphylococcus aureus HssR-HssS two-component system required for heme sensing. J Biol Chem 282:26111–26121PubMedCrossRef Stauff DL, Torres VJ, Skaar EP (2007) Signaling and DNA-binding activities of the Staphylococcus aureus HssR-HssS two-component system required for heme sensing. J Biol Chem 282:26111–26121PubMedCrossRef
46.
go back to reference Torres VJ, Stauff DL, Pishchany G, Bezbradica JS, Gordy LE, Iturregui J, Anderson KL, Dunman PM, Joyce S, Skaar EP (2007) A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1:109–119PubMedCrossRef Torres VJ, Stauff DL, Pishchany G, Bezbradica JS, Gordy LE, Iturregui J, Anderson KL, Dunman PM, Joyce S, Skaar EP (2007) A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1:109–119PubMedCrossRef
47.
go back to reference Attia AS, Benson MA, Stauff DL, Torres VJ, Skaar EP Membrane damage elicits an immunomodulatory program in Staphylococcus aureus. PLoS Pathog 6:e1000802 Attia AS, Benson MA, Stauff DL, Torres VJ, Skaar EP Membrane damage elicits an immunomodulatory program in Staphylococcus aureus. PLoS Pathog 6:e1000802
48.
go back to reference Crosa JH, Walsh CT (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223–249PubMedCrossRef Crosa JH, Walsh CT (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223–249PubMedCrossRef
49.
go back to reference Challis GL (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. Chembiochem 6:601–611PubMedCrossRef Challis GL (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. Chembiochem 6:601–611PubMedCrossRef
50.
go back to reference Cotton JL, Tao J, Balibar CJ (2009) Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry 48:1025–1035PubMedCrossRef Cotton JL, Tao J, Balibar CJ (2009) Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry 48:1025–1035PubMedCrossRef
51.
go back to reference Dale SE, Doherty-Kirby A, Lajoie G, Heinrichs DE (2004) Role of siderophore biosynthesis in virulence of Staphylococcus aureus: identification and characterization of genes involved in production of a siderophore. Infect Immun 72:29–37PubMedCrossRef Dale SE, Doherty-Kirby A, Lajoie G, Heinrichs DE (2004) Role of siderophore biosynthesis in virulence of Staphylococcus aureus: identification and characterization of genes involved in production of a siderophore. Infect Immun 72:29–37PubMedCrossRef
52.
go back to reference Modun B, Evans RW, Joannou CL, Williams P (1998) Receptor-mediated recognition and uptake of iron from human transferrin by Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 66:3591–3596PubMed Modun B, Evans RW, Joannou CL, Williams P (1998) Receptor-mediated recognition and uptake of iron from human transferrin by Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 66:3591–3596PubMed
53.
go back to reference Beasley FC, Vines ED, Grigg JC, Zheng Q, Liu S, Lajoie GA, Murphy ME, Heinrichs DE (2009) Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol Microbiol 72:947–963PubMedCrossRef Beasley FC, Vines ED, Grigg JC, Zheng Q, Liu S, Lajoie GA, Murphy ME, Heinrichs DE (2009) Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol Microbiol 72:947–963PubMedCrossRef
54.
go back to reference Dale SE, Sebulsky MT, Heinrichs DE (2004) Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J Bacteriol 186:8356–8362PubMedCrossRef Dale SE, Sebulsky MT, Heinrichs DE (2004) Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J Bacteriol 186:8356–8362PubMedCrossRef
55.
go back to reference Grigg JC, Cheung J, Heinrichs DE, Murphy ME Specificity of Staphyloferrin B recognition by the SirA receptor from Staphylococcus aureus. J Biol Chem 285:34579–34588 Grigg JC, Cheung J, Heinrichs DE, Murphy ME Specificity of Staphyloferrin B recognition by the SirA receptor from Staphylococcus aureus. J Biol Chem 285:34579–34588
56.
go back to reference Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O (2004) Iron-source preference of Staphylococcus aureus infections. Science 305:1626–1628PubMedCrossRef Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O (2004) Iron-source preference of Staphylococcus aureus infections. Science 305:1626–1628PubMedCrossRef
57.
go back to reference Sebulsky MT, Hohnstein D, Hunter MD, Heinrichs DE (2000) Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J Bacteriol 182:4394–4400PubMedCrossRef Sebulsky MT, Hohnstein D, Hunter MD, Heinrichs DE (2000) Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J Bacteriol 182:4394–4400PubMedCrossRef
58.
go back to reference Sebulsky MT, Heinrichs DE (2001) Identification and characterization of fhuD1 and fhuD2, two genes involved in iron-hydroxamate uptake in Staphylococcus aureus. J Bacteriol 183:4994–5000PubMedCrossRef Sebulsky MT, Heinrichs DE (2001) Identification and characterization of fhuD1 and fhuD2, two genes involved in iron-hydroxamate uptake in Staphylococcus aureus. J Bacteriol 183:4994–5000PubMedCrossRef
59.
go back to reference Beasley FC, Marolda CL, Cheung J, Buac S, Heinrichs DE Staphylococcus aureus transporters Hts, Sir, and Sst capture iron liberated from human transferrin by Staphyloferrin A, Staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79:2345–2355 Beasley FC, Marolda CL, Cheung J, Buac S, Heinrichs DE Staphylococcus aureus transporters Hts, Sir, and Sst capture iron liberated from human transferrin by Staphyloferrin A, Staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79:2345–2355
60.
go back to reference Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, Joachmiak A, Missiakas DM, Schneewind O (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299:906–909PubMedCrossRef Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, Joachmiak A, Missiakas DM, Schneewind O (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299:906–909PubMedCrossRef
61.
go back to reference Mazmanian SK, Ton-That H, Su K, Schneewind O (2002) An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc Natl Acad Sci USA 99:2293–2298PubMedCrossRef Mazmanian SK, Ton-That H, Su K, Schneewind O (2002) An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc Natl Acad Sci USA 99:2293–2298PubMedCrossRef
62.
go back to reference Torres VJ, Pishchany G, Humayun M, Schneewind O, Skaar EP (2006) Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J Bacteriol 188:8421–8429PubMedCrossRef Torres VJ, Pishchany G, Humayun M, Schneewind O, Skaar EP (2006) Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J Bacteriol 188:8421–8429PubMedCrossRef
63.
go back to reference Dryla A, Gelbmann D, von Gabain A, Nagy E (2003) Identification of a novel iron regulated staphylococcal surface protein with haptoglobin-haemoglobin binding activity. Mol Microbiol 49:37–53PubMedCrossRef Dryla A, Gelbmann D, von Gabain A, Nagy E (2003) Identification of a novel iron regulated staphylococcal surface protein with haptoglobin-haemoglobin binding activity. Mol Microbiol 49:37–53PubMedCrossRef
64.
go back to reference Pishchany G, Dickey SE, Skaar EP (2009) Subcellular localization of the Staphylococcus aureus heme iron transport components IsdA and IsdB. Infect Immun 77:2624–2634PubMedCrossRef Pishchany G, Dickey SE, Skaar EP (2009) Subcellular localization of the Staphylococcus aureus heme iron transport components IsdA and IsdB. Infect Immun 77:2624–2634PubMedCrossRef
65.
go back to reference Muryoi N, Tiedemann MT, Pluym M, Cheung J, Heinrichs DE, Stillman MJ (2008) Demonstration of the iron-regulated surface determinant (Isd) heme transfer pathway in Staphylococcus aureus. J Biol Chem 283:28125–28136PubMedCrossRef Muryoi N, Tiedemann MT, Pluym M, Cheung J, Heinrichs DE, Stillman MJ (2008) Demonstration of the iron-regulated surface determinant (Isd) heme transfer pathway in Staphylococcus aureus. J Biol Chem 283:28125–28136PubMedCrossRef
66.
go back to reference Liu M, Tanaka WN, Zhu H, Xie G, Dooley DM, Lei B (2008) Direct hemin transfer from IsdA to IsdC in the iron-regulated surface determinant (Isd) heme acquisition system of Staphylococcus aureus. J Biol Chem 283:6668–6676PubMedCrossRef Liu M, Tanaka WN, Zhu H, Xie G, Dooley DM, Lei B (2008) Direct hemin transfer from IsdA to IsdC in the iron-regulated surface determinant (Isd) heme acquisition system of Staphylococcus aureus. J Biol Chem 283:6668–6676PubMedCrossRef
67.
go back to reference Tiedemann MT, Muryoi N, Heinrichs DE, Stillman MJ (2008) Iron acquisition by the haem-binding Isd proteins in Staphylococcus aureus: studies of the mechanism using magnetic circular dichroism. Biochem Soc Trans 36:1138–1143PubMedCrossRef Tiedemann MT, Muryoi N, Heinrichs DE, Stillman MJ (2008) Iron acquisition by the haem-binding Isd proteins in Staphylococcus aureus: studies of the mechanism using magnetic circular dichroism. Biochem Soc Trans 36:1138–1143PubMedCrossRef
68.
go back to reference Pluym M, Vermeiren CL, Mack J, Heinrichs DE, Stillman MJ (2007) Heme binding properties of Staphylococcus aureus IsdE. Biochemistry 46:12777–12787PubMedCrossRef Pluym M, Vermeiren CL, Mack J, Heinrichs DE, Stillman MJ (2007) Heme binding properties of Staphylococcus aureus IsdE. Biochemistry 46:12777–12787PubMedCrossRef
69.
go back to reference Mack J, Vermeiren C, Heinrichs DE, Stillman MJ (2004) In vivo heme scavenging by Staphylococcus aureus IsdC and IsdE proteins. Biochem Biophys Res Commun 320:781–788PubMedCrossRef Mack J, Vermeiren C, Heinrichs DE, Stillman MJ (2004) In vivo heme scavenging by Staphylococcus aureus IsdC and IsdE proteins. Biochem Biophys Res Commun 320:781–788PubMedCrossRef
70.
go back to reference Wu R, Skaar EP, Zhang R, Joachimiak G, Gornicki P, Schneewind O, Joachimiak A (2005) Staphylococcus aureus IsdG and IsdI, heme-degrading enzymes with structural similarity to monooxygenases. J Biol Chem 280:2840–2846PubMedCrossRef Wu R, Skaar EP, Zhang R, Joachimiak G, Gornicki P, Schneewind O, Joachimiak A (2005) Staphylococcus aureus IsdG and IsdI, heme-degrading enzymes with structural similarity to monooxygenases. J Biol Chem 280:2840–2846PubMedCrossRef
71.
go back to reference Skaar EP, Gaspar AH, Schneewind O (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 279:436–443PubMedCrossRef Skaar EP, Gaspar AH, Schneewind O (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 279:436–443PubMedCrossRef
72.
go back to reference Kim HK, DeDent A, Cheng AG, McAdow M, Bagnoli F, Missiakas DM, Schneewind O IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 28:6382–6392 Kim HK, DeDent A, Cheng AG, McAdow M, Bagnoli F, Missiakas DM, Schneewind O IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 28:6382–6392
73.
go back to reference Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, Missiakas DM (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23:3393–3404PubMedCrossRef Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, Missiakas DM (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23:3393–3404PubMedCrossRef
74.
go back to reference Clarke SR, Brummell KJ, Horsburgh MJ, McDowell PW, Mohamad SA, Stapleton MR, Acevedo J, Read RC, Day NP, Peacock SJ et al (2006) Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis 193:1098–1108PubMedCrossRef Clarke SR, Brummell KJ, Horsburgh MJ, McDowell PW, Mohamad SA, Stapleton MR, Acevedo J, Read RC, Day NP, Peacock SJ et al (2006) Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis 193:1098–1108PubMedCrossRef
75.
go back to reference Etz H, Minh DB, Henics T, Dryla A, Winkler B, Triska C, Boyd AP, Sollner J, Schmidt W, von Ahsen U et al (2002) Identification of in vivo expressed vaccine candidate antigens from Staphylococcus aureus. Proc Natl Acad Sci USA 99:6573–6578PubMedCrossRef Etz H, Minh DB, Henics T, Dryla A, Winkler B, Triska C, Boyd AP, Sollner J, Schmidt W, von Ahsen U et al (2002) Identification of in vivo expressed vaccine candidate antigens from Staphylococcus aureus. Proc Natl Acad Sci USA 99:6573–6578PubMedCrossRef
76.
go back to reference Stranger-Jones YK, Bae T, Schneewind O (2006) Vaccine assembly from surface proteins of Staphylococcus aureus. Proc Natl Acad Sci USA 103:16942–16947PubMedCrossRef Stranger-Jones YK, Bae T, Schneewind O (2006) Vaccine assembly from surface proteins of Staphylococcus aureus. Proc Natl Acad Sci USA 103:16942–16947PubMedCrossRef
77.
go back to reference Raedler MD, Heyne S, Wagner E, Shalkowski SK, Secore S, Anderson AS, Cook J, Cope L, McNeely T, Retzlaff M et al (2009) Serologic assay to quantify human immunoglobulin G antibodies to the Staphylococcus aureus iron surface determinant B antigen. Clin Vaccine Immunol 16:739–748PubMedCrossRef Raedler MD, Heyne S, Wagner E, Shalkowski SK, Secore S, Anderson AS, Cook J, Cope L, McNeely T, Retzlaff M et al (2009) Serologic assay to quantify human immunoglobulin G antibodies to the Staphylococcus aureus iron surface determinant B antigen. Clin Vaccine Immunol 16:739–748PubMedCrossRef
78.
go back to reference Brown M, Kowalski R, Zorman J, Wang XM, Towne V, Zhao Q, Secore S, Finnefrock AC, Ebert T, Pancari G et al (2009) Selection and characterization of murine monoclonal antibodies to Staphylococcus aureus iron-regulated surface determinant B with functional activity in vitro and in vivo. Clin Vaccine Immunol 16:1095–1104PubMedCrossRef Brown M, Kowalski R, Zorman J, Wang XM, Towne V, Zhao Q, Secore S, Finnefrock AC, Ebert T, Pancari G et al (2009) Selection and characterization of murine monoclonal antibodies to Staphylococcus aureus iron-regulated surface determinant B with functional activity in vitro and in vivo. Clin Vaccine Immunol 16:1095–1104PubMedCrossRef
79.
go back to reference Ebert T, Smith S, Pancari G, Clark D, Hampton R, Secore S, Towne V, Fan H, Wang XM, Wu X, et al A fully human monoclonal antibody to Staphylococcus aureus iron regulated surface determinant B (IsdB) with functional activity in vitro and in vivo. Hum Antibodies 19:113–128 Ebert T, Smith S, Pancari G, Clark D, Hampton R, Secore S, Towne V, Fan H, Wang XM, Wu X, et al A fully human monoclonal antibody to Staphylococcus aureus iron regulated surface determinant B (IsdB) with functional activity in vitro and in vivo. Hum Antibodies 19:113–128
80.
go back to reference Smith JF, Kowalski R, Esser MT, Brown MJ, Bryan JT (2008) Evolution of type-specific immunoassays to evaluate the functional immune response to Gardasil: a vaccine for human papillomavirus types 16, 18, 6 and 11. Hum Vaccin 4:134–142PubMedCrossRef Smith JF, Kowalski R, Esser MT, Brown MJ, Bryan JT (2008) Evolution of type-specific immunoassays to evaluate the functional immune response to Gardasil: a vaccine for human papillomavirus types 16, 18, 6 and 11. Hum Vaccin 4:134–142PubMedCrossRef
81.
go back to reference Khan FA, Fisher MA, Khakoo RA (2007) Association of hemochromatosis with infectious diseases: expanding spectrum. Int J Infect Dis 11:482–487PubMedCrossRef Khan FA, Fisher MA, Khakoo RA (2007) Association of hemochromatosis with infectious diseases: expanding spectrum. Int J Infect Dis 11:482–487PubMedCrossRef
82.
go back to reference Kumar V, Abbas AK, Fausto N, Aster JC (eds) (2010) Robbins and Cotran pathologic basis of disease, 8th edn. Saunders Elsevier, Philadelphia Kumar V, Abbas AK, Fausto N, Aster JC (eds) (2010) Robbins and Cotran pathologic basis of disease, 8th edn. Saunders Elsevier, Philadelphia
83.
go back to reference Foster TJ (2009) Colonization and infection of the human host by staphylococci: adhesion, survival and immune evasion. Vet Dermatol 20:456–470PubMedCrossRef Foster TJ (2009) Colonization and infection of the human host by staphylococci: adhesion, survival and immune evasion. Vet Dermatol 20:456–470PubMedCrossRef
84.
go back to reference Palazzolo-Ballance AM, Reniere ML, Braughton KR, Sturdevant DE, Otto M, Kreiswirth BN, Skaar EP, DeLeo FR (2008) Neutrophil microbicides induce a pathogen survival response in community-associated methicillin-resistant Staphylococcus aureus. J Immunol 180:500–509PubMed Palazzolo-Ballance AM, Reniere ML, Braughton KR, Sturdevant DE, Otto M, Kreiswirth BN, Skaar EP, DeLeo FR (2008) Neutrophil microbicides induce a pathogen survival response in community-associated methicillin-resistant Staphylococcus aureus. J Immunol 180:500–509PubMed
85.
go back to reference Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, Foster TJ Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 156:920–928 Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, Foster TJ Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 156:920–928
86.
go back to reference Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T (1988) A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332:411–415PubMedCrossRef Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T (1988) A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332:411–415PubMedCrossRef
87.
go back to reference Coller BS, Peerschke EI, Scudder LE, Sullivan CA (1983) Studies with a murine monoclonal antibody that abolishes ristocetin-induced binding of von Willebrand factor to platelets: additional evidence in support of GPIb as a platelet receptor for von Willebrand factor. Blood 61:99–110PubMed Coller BS, Peerschke EI, Scudder LE, Sullivan CA (1983) Studies with a murine monoclonal antibody that abolishes ristocetin-induced binding of von Willebrand factor to platelets: additional evidence in support of GPIb as a platelet receptor for von Willebrand factor. Blood 61:99–110PubMed
88.
go back to reference Bennett JS, Shattil SJ, Power JW, Gartner TK (1988) Interaction of fibrinogen with its platelet receptor. Differential effects of alpha and gamma chain fibrinogen peptides on the glycoprotein IIb–IIIa complex. J Biol Chem 263:12948–12953PubMed Bennett JS, Shattil SJ, Power JW, Gartner TK (1988) Interaction of fibrinogen with its platelet receptor. Differential effects of alpha and gamma chain fibrinogen peptides on the glycoprotein IIb–IIIa complex. J Biol Chem 263:12948–12953PubMed
89.
go back to reference Cook JJ, Trybulec M, Lasz EC, Khan S, Niewiarowski S (1992) Binding of glycoprotein IIIa-derived peptide 217–231 to fibrinogen and von Willebrand factors and its inhibition by platelet glycoprotein IIb/IIIa complex. Biochim Biophys Acta 1119:312–321PubMedCrossRef Cook JJ, Trybulec M, Lasz EC, Khan S, Niewiarowski S (1992) Binding of glycoprotein IIIa-derived peptide 217–231 to fibrinogen and von Willebrand factors and its inhibition by platelet glycoprotein IIb/IIIa complex. Biochim Biophys Acta 1119:312–321PubMedCrossRef
90.
go back to reference Adams RL, Bird RJ (2009) Review article: Coagulation cascade and therapeutics update: relevance to nephrology. Part 1: overview of coagulation, thrombophilias and history of anticoagulants. Nephrology (Carlton) 14:462–470CrossRef Adams RL, Bird RJ (2009) Review article: Coagulation cascade and therapeutics update: relevance to nephrology. Part 1: overview of coagulation, thrombophilias and history of anticoagulants. Nephrology (Carlton) 14:462–470CrossRef
91.
go back to reference Giesen PL, Rauch U, Bohrmann B, Kling D, Roque M, Fallon JT, Badimon JJ, Himber J, Riederer MA, Nemerson Y (1999) Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 96:2311–2315PubMedCrossRef Giesen PL, Rauch U, Bohrmann B, Kling D, Roque M, Fallon JT, Badimon JJ, Himber J, Riederer MA, Nemerson Y (1999) Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 96:2311–2315PubMedCrossRef
92.
93.
go back to reference Lutz BR, Fulton GP, Akers RP (1951) White thromboembolism in the hamster cheek pouch after trauma, infection and neoplasia. Circulation 3:339–351PubMed Lutz BR, Fulton GP, Akers RP (1951) White thromboembolism in the hamster cheek pouch after trauma, infection and neoplasia. Circulation 3:339–351PubMed
94.
go back to reference Nemerson Y, Esnouf MP (1973) Activation of a proteolytic system by a membrane lipoprotein: mechanism of action of tissue factor. Proc Natl Acad Sci USA 70:310–314PubMedCrossRef Nemerson Y, Esnouf MP (1973) Activation of a proteolytic system by a membrane lipoprotein: mechanism of action of tissue factor. Proc Natl Acad Sci USA 70:310–314PubMedCrossRef
95.
go back to reference Davie EW, Ratnoff OD (1964) Waterfall sequence for intrinsic blood clotting. Science 145:1310–1312PubMedCrossRef Davie EW, Ratnoff OD (1964) Waterfall sequence for intrinsic blood clotting. Science 145:1310–1312PubMedCrossRef
96.
go back to reference Macfarlane RG (1964) An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature 202:498–499PubMedCrossRef Macfarlane RG (1964) An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature 202:498–499PubMedCrossRef
97.
go back to reference Senior RM, Skogen WF, Griffin GL, Wilner GD (1986) Effects of fibrinogen derivatives upon the inflammatory response. Studies with human fibrinopeptide B. J Clin Invest 77:1014–1019PubMedCrossRef Senior RM, Skogen WF, Griffin GL, Wilner GD (1986) Effects of fibrinogen derivatives upon the inflammatory response. Studies with human fibrinopeptide B. J Clin Invest 77:1014–1019PubMedCrossRef
98.
go back to reference Zimmerman GA, McIntyre TM, Prescott SM (1985) Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro. J Clin Invest 76:2235–2246PubMedCrossRef Zimmerman GA, McIntyre TM, Prescott SM (1985) Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro. J Clin Invest 76:2235–2246PubMedCrossRef
99.
go back to reference Cooper JA, Solano SJ, Bizios R, Kaplan JE, Malik AB (1984) Pulmonary neutrophil kinetics after thrombin-induced intravascular coagulation. J Appl Physiol 57:826–832PubMed Cooper JA, Solano SJ, Bizios R, Kaplan JE, Malik AB (1984) Pulmonary neutrophil kinetics after thrombin-induced intravascular coagulation. J Appl Physiol 57:826–832PubMed
100.
go back to reference Pisano JJ, Finlayson JS, Peyton MP (1968) Cross-link in fibrin polymerized by factor 13: epsilon-(gamma-glutamyl)lysine. Science 160:892–893PubMedCrossRef Pisano JJ, Finlayson JS, Peyton MP (1968) Cross-link in fibrin polymerized by factor 13: epsilon-(gamma-glutamyl)lysine. Science 160:892–893PubMedCrossRef
101.
102.
go back to reference Bakker WW, Willink EJ, Donga J, Hulstaert CE, Hardonk MJ (1987) Antithrombotic activity of glomerular adenosine diphosphatase in the glomerular basement membrane of the rat kidney. J Lab Clin Med 109:171–177PubMed Bakker WW, Willink EJ, Donga J, Hulstaert CE, Hardonk MJ (1987) Antithrombotic activity of glomerular adenosine diphosphatase in the glomerular basement membrane of the rat kidney. J Lab Clin Med 109:171–177PubMed
103.
go back to reference Nieuwenhuizen W, Vermond A, Voskuilen M, Traas DW, Verheijen JH (1983) Identification of a site in fibrin(ogen) which is involved in the acceleration of plasminogen activation by tissue-type plasminogen activator. Biochim Biophys Acta 748:86–92PubMedCrossRef Nieuwenhuizen W, Vermond A, Voskuilen M, Traas DW, Verheijen JH (1983) Identification of a site in fibrin(ogen) which is involved in the acceleration of plasminogen activation by tissue-type plasminogen activator. Biochim Biophys Acta 748:86–92PubMedCrossRef
104.
go back to reference Loeb L (1903) The influence of certain bacteria on the coagulation of the blood. J Med Res 10:407–419PubMed Loeb L (1903) The influence of certain bacteria on the coagulation of the blood. J Med Res 10:407–419PubMed
105.
go back to reference Kolle W, Otto R (1902) Die Differenzierung der Staphylokokken mittelst der Agglutination. Z Hyg 41:369–379 Kolle W, Otto R (1902) Die Differenzierung der Staphylokokken mittelst der Agglutination. Z Hyg 41:369–379
106.
go back to reference Birch-Hirschfeld L (1934) Über die Agglutination von Staphylokokken durch Bestandteile des Säugetierblutplasmas. Klinische Woschenschrift 13 Birch-Hirschfeld L (1934) Über die Agglutination von Staphylokokken durch Bestandteile des Säugetierblutplasmas. Klinische Woschenschrift 13
107.
go back to reference Hawiger J, Timmons S, Strong DD, Cottrell BA, Riley M, Doolittle RF (1982) Identification of a region of human fibrinogen interacting with staphylococcal clumping factor. Biochemistry 21:1407–1413PubMedCrossRef Hawiger J, Timmons S, Strong DD, Cottrell BA, Riley M, Doolittle RF (1982) Identification of a region of human fibrinogen interacting with staphylococcal clumping factor. Biochemistry 21:1407–1413PubMedCrossRef
108.
go back to reference Friedrich R, Panizzi P, Fuentes-Prior P, Richter K, Verhamme I, Anderson PJ, Kawabata S, Huber R, Bode W, Bock PE (2003) Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation. Nature 425:535–539PubMedCrossRef Friedrich R, Panizzi P, Fuentes-Prior P, Richter K, Verhamme I, Anderson PJ, Kawabata S, Huber R, Bode W, Bock PE (2003) Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation. Nature 425:535–539PubMedCrossRef
109.
go back to reference Kroh HK, Panizzi P, Bock PE (2009) Von Willebrand factor-binding protein is a hysteretic conformational activator of prothrombin. Proc Natl Acad Sci USA 106:7786–7791PubMedCrossRef Kroh HK, Panizzi P, Bock PE (2009) Von Willebrand factor-binding protein is a hysteretic conformational activator of prothrombin. Proc Natl Acad Sci USA 106:7786–7791PubMedCrossRef
110.
go back to reference McDevitt D, Francois P, Vaudaux P, Foster TJ (1994) Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol 11:237–248PubMedCrossRef McDevitt D, Francois P, Vaudaux P, Foster TJ (1994) Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol 11:237–248PubMedCrossRef
111.
go back to reference Strong DD, Laudano AP, Hawiger J, Doolittle RF (1982) Isolation, characterization, and synthesis of peptides from human fibrinogen that block the staphylococcal clumping reaction and construction of a synthetic clumping particle. Biochemistry 21:1414–1420PubMedCrossRef Strong DD, Laudano AP, Hawiger J, Doolittle RF (1982) Isolation, characterization, and synthesis of peptides from human fibrinogen that block the staphylococcal clumping reaction and construction of a synthetic clumping particle. Biochemistry 21:1414–1420PubMedCrossRef
112.
go back to reference Smith W, Hale JH, Smith MM (1947) The role of coagulase in staphylococcal infections. Br J Exp Pathol 28:57–67PubMed Smith W, Hale JH, Smith MM (1947) The role of coagulase in staphylococcal infections. Br J Exp Pathol 28:57–67PubMed
113.
go back to reference Ekstedt RD, Yotis WW (1960) Studies on staphylococci. II. Effect of coagulase on the virulence of coagulase negative strains. J Bacteriol 80:496–500PubMed Ekstedt RD, Yotis WW (1960) Studies on staphylococci. II. Effect of coagulase on the virulence of coagulase negative strains. J Bacteriol 80:496–500PubMed
114.
go back to reference Duthie ES, Lorenz LL (1952) Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol 6:95–107PubMed Duthie ES, Lorenz LL (1952) Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol 6:95–107PubMed
115.
go back to reference Hemker HC, Bas BM, Muller AD (1975) Activation of a pro-enzyme by a stoichiometric reaction with another protein. The reaction between prothrombin and staphylocoagulase. Biochim Biophys Acta 379:180–188PubMed Hemker HC, Bas BM, Muller AD (1975) Activation of a pro-enzyme by a stoichiometric reaction with another protein. The reaction between prothrombin and staphylocoagulase. Biochim Biophys Acta 379:180–188PubMed
116.
go back to reference Kaida S, Miyata T, Yoshizawa Y, Kawabata S, Morita T, Igarashi H, Iwanaga S (1987) Nucleotide sequence of the staphylocoagulase gene: its unique COOH-terminal 8 tandem repeats. J Biochem 102:1177–1186PubMed Kaida S, Miyata T, Yoshizawa Y, Kawabata S, Morita T, Igarashi H, Iwanaga S (1987) Nucleotide sequence of the staphylocoagulase gene: its unique COOH-terminal 8 tandem repeats. J Biochem 102:1177–1186PubMed
117.
go back to reference Phonimdaeng P, O'Reilly M, Nowlan P, Bramley AJ, Foster TJ (1990) The coagulase of Staphylococcus aureus 8325–4. Sequence analysis and virulence of site-specific coagulase-deficient mutants. Mol Microbiol 4:393–404PubMedCrossRef Phonimdaeng P, O'Reilly M, Nowlan P, Bramley AJ, Foster TJ (1990) The coagulase of Staphylococcus aureus 8325–4. Sequence analysis and virulence of site-specific coagulase-deficient mutants. Mol Microbiol 4:393–404PubMedCrossRef
118.
go back to reference Phonimdaeng P, O'Reilly M, O'Toole PW, Foster TJ (1988) Molecular cloning and expression of the coagulase gene of Staphylococcus aureus 8325–4. J Gen Microbiol 134:75–83PubMed Phonimdaeng P, O'Reilly M, O'Toole PW, Foster TJ (1988) Molecular cloning and expression of the coagulase gene of Staphylococcus aureus 8325–4. J Gen Microbiol 134:75–83PubMed
119.
go back to reference Bjerketorp J, Jacobsson K, Frykberg L (2004) The von Willebrand factor-binding protein (vWbp) of Staphylococcus aureus is a coagulase. FEMS Microbiol Lett 234:309–314PubMedCrossRef Bjerketorp J, Jacobsson K, Frykberg L (2004) The von Willebrand factor-binding protein (vWbp) of Staphylococcus aureus is a coagulase. FEMS Microbiol Lett 234:309–314PubMedCrossRef
120.
go back to reference Bjerketorp J, Nilsson M, Ljungh A, Flock JI, Jacobsson K, Frykberg L (2002) A novel von Willebrand factor binding protein expressed by Staphylococcus aureus. Microbiology 148:2037–2044PubMed Bjerketorp J, Nilsson M, Ljungh A, Flock JI, Jacobsson K, Frykberg L (2002) A novel von Willebrand factor binding protein expressed by Staphylococcus aureus. Microbiology 148:2037–2044PubMed
121.
go back to reference Panizzi P, Friedrich R, Fuentes-Prior P, Richter K, Bock PE, Bode W (2006) Fibrinogen substrate recognition by staphylocoagulase. (pro)thrombin complexes. J Biol Chem 281:1179–1187PubMedCrossRef Panizzi P, Friedrich R, Fuentes-Prior P, Richter K, Bock PE, Bode W (2006) Fibrinogen substrate recognition by staphylocoagulase. (pro)thrombin complexes. J Biol Chem 281:1179–1187PubMedCrossRef
123.
go back to reference Di Nisio M, Middeldorp S, Buller HR (2005) Direct thrombin inhibitors. N Engl J Med 353:1028–1040PubMedCrossRef Di Nisio M, Middeldorp S, Buller HR (2005) Direct thrombin inhibitors. N Engl J Med 353:1028–1040PubMedCrossRef
124.
go back to reference Vanassche T, Verhaegen J, Peetermans WE, Hoylaerts MF, Verhamme P Dabigatran inhibits Staphylococcus aureus coagulase activity. J Clin Microbiol 48:4248–50 Vanassche T, Verhaegen J, Peetermans WE, Hoylaerts MF, Verhamme P Dabigatran inhibits Staphylococcus aureus coagulase activity. J Clin Microbiol 48:4248–50
125.
go back to reference Panizzi P, Friedrich R, Fuentes-Prior P, Kroh HK, Briggs J, Tans G, Bode W, Bock PE (2006) Novel fluorescent prothrombin analogs as probes of staphylocoagulase–prothrombin interactions. J Biol Chem 281:1169–1178PubMedCrossRef Panizzi P, Friedrich R, Fuentes-Prior P, Kroh HK, Briggs J, Tans G, Bode W, Bock PE (2006) Novel fluorescent prothrombin analogs as probes of staphylocoagulase–prothrombin interactions. J Biol Chem 281:1169–1178PubMedCrossRef
126.
go back to reference Baddour LM, Tayidi MM, Walker E, McDevitt D, Foster TJ (1994) Virulence of coagulase-deficient mutants of Staphylococcus aureus in experimental endocarditis. J Med Microbiol 41:259–263PubMedCrossRef Baddour LM, Tayidi MM, Walker E, McDevitt D, Foster TJ (1994) Virulence of coagulase-deficient mutants of Staphylococcus aureus in experimental endocarditis. J Med Microbiol 41:259–263PubMedCrossRef
127.
go back to reference Hasegawa N, Kondo I, Hoshina S, Kurosaka K, Igarashi H (1983) Effect of highly purified coagulase and culture filtrate on virulence and immunity of a coagulase-negative mutant of Staphylococcus aureus BB. Infect Immun 39:1236–1242PubMed Hasegawa N, Kondo I, Hoshina S, Kurosaka K, Igarashi H (1983) Effect of highly purified coagulase and culture filtrate on virulence and immunity of a coagulase-negative mutant of Staphylococcus aureus BB. Infect Immun 39:1236–1242PubMed
128.
go back to reference Jonsson P, Lindberg M, Haraldsson I, Wadstrom T (1985) 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 49:765–769PubMed Jonsson P, Lindberg M, Haraldsson I, Wadstrom T (1985) 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 49:765–769PubMed
129.
go back to reference Seki K, Ogasawara M, Sakurada J, Murai M, Masuda S (1989) Altered virulence of a pleiotropic Staphylococcus aureus mutant with a low producibility of coagulase and other factors in mice. Microbiol Immunol 33:981–990PubMed Seki K, Ogasawara M, Sakurada J, Murai M, Masuda S (1989) Altered virulence of a pleiotropic Staphylococcus aureus mutant with a low producibility of coagulase and other factors in mice. Microbiol Immunol 33:981–990PubMed
130.
go back to reference Moreillon P, Entenza JM, Francioli P, McDevitt D, Foster TJ, Francois P, Vaudaux P (1995) Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun 63:4738–4743PubMed Moreillon P, Entenza JM, Francioli P, McDevitt D, Foster TJ, Francois P, Vaudaux P (1995) Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun 63:4738–4743PubMed
131.
go back to reference Sawai T, Tomono K, Yanagihara K, Yamamoto Y, Kaku M, Hirakata Y, Koga H, Tashiro T, Kohno S (1997) Role of coagulase in a murine model of hematogenous pulmonary infection induced by intravenous injection of Staphylococcus aureus enmeshed in agar beads. Infect Immun 65:466–471PubMed Sawai T, Tomono K, Yanagihara K, Yamamoto Y, Kaku M, Hirakata Y, Koga H, Tashiro T, Kohno S (1997) Role of coagulase in a murine model of hematogenous pulmonary infection induced by intravenous injection of Staphylococcus aureus enmeshed in agar beads. Infect Immun 65:466–471PubMed
132.
go back to reference Cheng AG, McAdow M, Kim HK, Bae T, Missiakas DM, Schneewind O Contribution of coagulases towards Staphylococcus aureus disease and protective immunity. PLoS Pathog 6:e1001036. Cheng AG, McAdow M, Kim HK, Bae T, Missiakas DM, Schneewind O Contribution of coagulases towards Staphylococcus aureus disease and protective immunity. PLoS Pathog 6:e1001036.
133.
go back to reference Panizzi P, Nahrendorf M, Figueiredo JL, Panizzi J, Marinelli B, Iwamoto Y, Keliher E, Maddur AA, Waterman P, Kroh HK et al In vivo detection of Staphylococcus aureus endocarditis by targeting pathogen-specific prothrombin activation. Nat Med 17:1142–1146 Panizzi P, Nahrendorf M, Figueiredo JL, Panizzi J, Marinelli B, Iwamoto Y, Keliher E, Maddur AA, Waterman P, Kroh HK et al In vivo detection of Staphylococcus aureus endocarditis by targeting pathogen-specific prothrombin activation. Nat Med 17:1142–1146
134.
go back to reference Ganesh VK, Rivera JJ, Smeds E, Ko YP, Bowden MG, Wann ER, Gurusiddappa S, Fitzgerald JR, Hook M (2008) A structural model of the Staphylococcus aureus ClfA–fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog 4:e1000226PubMedCrossRef Ganesh VK, Rivera JJ, Smeds E, Ko YP, Bowden MG, Wann ER, Gurusiddappa S, Fitzgerald JR, Hook M (2008) A structural model of the Staphylococcus aureus ClfA–fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog 4:e1000226PubMedCrossRef
135.
go back to reference McDevitt D, Francois P, Vaudaux P, Foster TJ (1995) Identification of the ligand-binding domain of the surface-located fibrinogen receptor (clumping factor) of Staphylococcus aureus. Mol Microbiol 16:895–907PubMedCrossRef McDevitt D, Francois P, Vaudaux P, Foster TJ (1995) Identification of the ligand-binding domain of the surface-located fibrinogen receptor (clumping factor) of Staphylococcus aureus. Mol Microbiol 16:895–907PubMedCrossRef
136.
go back to reference McDevitt D, Nanavaty T, House-Pompeo K, Bell E, Turner N, McIntire L, Foster T, Hook M (1997) Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem 247:416–424PubMedCrossRef McDevitt D, Nanavaty T, House-Pompeo K, Bell E, Turner N, McIntire L, Foster T, Hook M (1997) Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem 247:416–424PubMedCrossRef
137.
go back to reference Walsh EJ, Miajlovic H, Gorkun OV, Foster TJ (2008) Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the alphaC-domain of human fibrinogen. Microbiology 154:550–558PubMedCrossRef Walsh EJ, Miajlovic H, Gorkun OV, Foster TJ (2008) Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the alphaC-domain of human fibrinogen. Microbiology 154:550–558PubMedCrossRef
138.
go back to reference McAdow M, Kim HK, DeDent AC, Hendrickx APA, Missiakas DM, Schneewind O (2011) Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog [Epub ahead of print] McAdow M, Kim HK, DeDent AC, Hendrickx APA, Missiakas DM, Schneewind O (2011) Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog [Epub ahead of print]
139.
go back to reference Hall AE, Domanski PJ, Patel PR, Vernachio JH, Syribeys PJ, Gorovits EL, Johnson MA, Ross JM, Hutchins JT, Patti JM (2003) Characterization of a protective monoclonal antibody recognizing Staphylococcus aureus MSCRAMM protein clumping factor A. Infect Immun 71:6864–6870PubMedCrossRef Hall AE, Domanski PJ, Patel PR, Vernachio JH, Syribeys PJ, Gorovits EL, Johnson MA, Ross JM, Hutchins JT, Patti JM (2003) Characterization of a protective monoclonal antibody recognizing Staphylococcus aureus MSCRAMM protein clumping factor A. Infect Immun 71:6864–6870PubMedCrossRef
140.
go back to reference Vernachio J, Bayer AS, Le T, Chai YL, Prater B, Schneider A, Ames B, Syribeys P, Robbins J, Patti JM (2003) Anti-clumping factor A immunoglobulin reduces the duration of methicillin-resistant Staphylococcus aureus bacteremia in an experimental model of infective endocarditis. Antimicrob Agents Chemother 47:3400–3406PubMedCrossRef Vernachio J, Bayer AS, Le T, Chai YL, Prater B, Schneider A, Ames B, Syribeys P, Robbins J, Patti JM (2003) Anti-clumping factor A immunoglobulin reduces the duration of methicillin-resistant Staphylococcus aureus bacteremia in an experimental model of infective endocarditis. Antimicrob Agents Chemother 47:3400–3406PubMedCrossRef
141.
go back to reference Weems JJ Jr, Steinberg JP, Filler S, Baddley JW, Corey GR, Sampathkumar P, Winston L, John JF, Kubin CJ, Talwani R et al (2006) Phase II, randomized, double-blind, multicenter study comparing the safety and pharmacokinetics of tefibazumab to placebo for treatment of Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 50:2751–2755PubMedCrossRef Weems JJ Jr, Steinberg JP, Filler S, Baddley JW, Corey GR, Sampathkumar P, Winston L, John JF, Kubin CJ, Talwani R et al (2006) Phase II, randomized, double-blind, multicenter study comparing the safety and pharmacokinetics of tefibazumab to placebo for treatment of Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 50:2751–2755PubMedCrossRef
142.
go back to reference Hair PS, Echague CG, Sholl AM, Watkins JA, Geoghegan JA, Foster TJ, Cunnion KM Clumping factor A interaction with complement factor I increases C3b cleavage on the bacterial surface of Staphylococcus aureus and decreases complement-mediated phagocytosis. Infect Immun 78:1717–1727 Hair PS, Echague CG, Sholl AM, Watkins JA, Geoghegan JA, Foster TJ, Cunnion KM Clumping factor A interaction with complement factor I increases C3b cleavage on the bacterial surface of Staphylococcus aureus and decreases complement-mediated phagocytosis. Infect Immun 78:1717–1727
143.
go back to reference Donahue JP, Patel H, Anderson WF, Hawiger J (1994) Three-dimensional structure of the platelet integrin recognition segment of the fibrinogen gamma chain obtained by carrier protein-driven crystallization. Proc Natl Acad Sci USA 91:12178–12182PubMedCrossRef Donahue JP, Patel H, Anderson WF, Hawiger J (1994) Three-dimensional structure of the platelet integrin recognition segment of the fibrinogen gamma chain obtained by carrier protein-driven crystallization. Proc Natl Acad Sci USA 91:12178–12182PubMedCrossRef
144.
go back to reference Ware S, Donahue JP, Hawiger J, Anderson WF (1999) Structure of the fibrinogen gamma-chain integrin binding and factor XIIIa cross-linking sites obtained through carrier protein driven crystallization. Protein Sci 8:2663–2671PubMedCrossRef Ware S, Donahue JP, Hawiger J, Anderson WF (1999) Structure of the fibrinogen gamma-chain integrin binding and factor XIIIa cross-linking sites obtained through carrier protein driven crystallization. Protein Sci 8:2663–2671PubMedCrossRef
146.
go back to reference Gallin JI (1991) Interferon-gamma in the management of chronic granulomatous disease. Rev Infect Dis 13:973–978PubMedCrossRef Gallin JI (1991) Interferon-gamma in the management of chronic granulomatous disease. Rev Infect Dis 13:973–978PubMedCrossRef
147.
go back to reference Hair PS, Ward MD, Semmes OJ, Foster TJ, Cunnion KM (2008) Staphylococcus aureus clumping factor A binds to complement regulator factor I and increases factor I cleavage of C3b. J Infect Dis 198:125–133PubMedCrossRef Hair PS, Ward MD, Semmes OJ, Foster TJ, Cunnion KM (2008) Staphylococcus aureus clumping factor A binds to complement regulator factor I and increases factor I cleavage of C3b. J Infect Dis 198:125–133PubMedCrossRef
148.
go back to reference Rooijakkers SH, Wu J, Ruyken M, van Domselaar R, Planken KL, Tzekou A, Ricklin D, Lambris JD, Janssen BJ, van Strijp JA et al (2009) Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat Immunol 10:721–727PubMedCrossRef Rooijakkers SH, Wu J, Ruyken M, van Domselaar R, Planken KL, Tzekou A, Ricklin D, Lambris JD, Janssen BJ, van Strijp JA et al (2009) Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat Immunol 10:721–727PubMedCrossRef
149.
go back to reference Chen H, Ricklin D, Hammel M, Garcia BL, McWhorter WJ, Sfyroera G, Wu YQ, Tzekou A, Li S, Geisbrecht BV et al Allosteric inhibition of complement function by a staphylococcal immune evasion protein. Proc Natl Acad Sci USA 107:17621–17626 Chen H, Ricklin D, Hammel M, Garcia BL, McWhorter WJ, Sfyroera G, Wu YQ, Tzekou A, Li S, Geisbrecht BV et al Allosteric inhibition of complement function by a staphylococcal immune evasion protein. Proc Natl Acad Sci USA 107:17621–17626
150.
go back to reference Postma B, Kleibeuker W, Poppelier MJ, Boonstra M, Van Kessel KP, Van Strijp JA, de Haas CJ (2005) Residues 10–18 within the C5a receptor N terminus compose a binding domain for chemotaxis inhibitory protein of Staphylococcus aureus. J Biol Chem 280:2020–2027PubMedCrossRef Postma B, Kleibeuker W, Poppelier MJ, Boonstra M, Van Kessel KP, Van Strijp JA, de Haas CJ (2005) Residues 10–18 within the C5a receptor N terminus compose a binding domain for chemotaxis inhibitory protein of Staphylococcus aureus. J Biol Chem 280:2020–2027PubMedCrossRef
151.
go back to reference Thammavongsa V, Kern JW, Missiakas DM, Schneewind O (2009) Staphylococcus aureus synthesizes adenosine to escape host immune responses. J Exp Med 206:2417–2427PubMedCrossRef Thammavongsa V, Kern JW, Missiakas DM, Schneewind O (2009) Staphylococcus aureus synthesizes adenosine to escape host immune responses. J Exp Med 206:2417–2427PubMedCrossRef
152.
go back to reference Thakker M, Park JS, Carey V, Lee JC (1998) Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model. Infect Immun 66:5183–5189PubMed Thakker M, Park JS, Carey V, Lee JC (1998) Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model. Infect Immun 66:5183–5189PubMed
153.
go back to reference Nilsson IM, Lee JC, Bremell T, Ryden C, Tarkowski A (1997) The role of staphylococcal polysaccharide microcapsule expression in septicemia and septic arthritis. Infect Immun 65:4216–4221PubMed Nilsson IM, Lee JC, Bremell T, Ryden C, Tarkowski A (1997) The role of staphylococcal polysaccharide microcapsule expression in septicemia and septic arthritis. Infect Immun 65:4216–4221PubMed
154.
go back to reference Megiovanni AM, Sanchez F, Robledo-Sarmiento M, Morel C, Gluckman JC, Boudaly S (2006) Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J Leukoc Biol 79:977–988PubMedCrossRef Megiovanni AM, Sanchez F, Robledo-Sarmiento M, Morel C, Gluckman JC, Boudaly S (2006) Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J Leukoc Biol 79:977–988PubMedCrossRef
155.
go back to reference van Gisbergen KP, Sanchez-Hernandez M, Geijtenbeek TB, van Kooyk Y (2005) Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med 201:1281–1292PubMedCrossRef van Gisbergen KP, Sanchez-Hernandez M, Geijtenbeek TB, van Kooyk Y (2005) Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med 201:1281–1292PubMedCrossRef
156.
go back to reference Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY (2011) Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol 23:317–326PubMedCrossRef Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY (2011) Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol 23:317–326PubMedCrossRef
157.
go back to reference Yang CW, Strong BS, Miller MJ, Unanue ER (2010) Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 185:2927–2934PubMedCrossRef Yang CW, Strong BS, Miller MJ, Unanue ER (2010) Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 185:2927–2934PubMedCrossRef
158.
go back to reference Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DT (1996) C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 271:348–350PubMedCrossRef Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DT (1996) C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 271:348–350PubMedCrossRef
159.
go back to reference Fischer MB, Goerg S, Shen L, Prodeus AP, Goodnow CC, Kelsoe G, Carroll MC (1998) Dependence of germinal center B cells on expression of CD21/CD35 for survival. Science 280:582–585PubMedCrossRef Fischer MB, Goerg S, Shen L, Prodeus AP, Goodnow CC, Kelsoe G, Carroll MC (1998) Dependence of germinal center B cells on expression of CD21/CD35 for survival. Science 280:582–585PubMedCrossRef
160.
go back to reference Thornton BP, Vetvicka V, Ross GD (1996) Function of C3 in a humoral response: iC3b/C3dg bound to an immune complex generated with natural antibody and a primary antigen promotes antigen uptake and the expression of co-stimulatory molecules by all B cells, but only stimulates immunoglobulin synthesis by antigen-specific B cells. Clin Exp Immunol 104:531–537PubMedCrossRef Thornton BP, Vetvicka V, Ross GD (1996) Function of C3 in a humoral response: iC3b/C3dg bound to an immune complex generated with natural antibody and a primary antigen promotes antigen uptake and the expression of co-stimulatory molecules by all B cells, but only stimulates immunoglobulin synthesis by antigen-specific B cells. Clin Exp Immunol 104:531–537PubMedCrossRef
161.
go back to reference Kopf M, Abel B, Gallimore A, Carroll M, Bachmann MF (2002) Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat Med 8:373–378PubMedCrossRef Kopf M, Abel B, Gallimore A, Carroll M, Bachmann MF (2002) Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat Med 8:373–378PubMedCrossRef
162.
go back to reference Lambris JD, Ricklin D, Geisbrecht BV (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6:132–142PubMedCrossRef Lambris JD, Ricklin D, Geisbrecht BV (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6:132–142PubMedCrossRef
163.
go back to reference Sahu A, Kozel TR, Pangburn MK (1994) Specificity of the thioester-containing reactive site of human C3 and its significance to complement activation. Biochem J 302(Pt 2):429–436PubMed Sahu A, Kozel TR, Pangburn MK (1994) Specificity of the thioester-containing reactive site of human C3 and its significance to complement activation. Biochem J 302(Pt 2):429–436PubMed
164.
go back to reference Langley R, Wines B, Willoughby N, Basu I, Proft T, Fraser JD (2005) The staphylococcal superantigen-like protein 7 binds IgA and complement C5 and inhibits IgA-Fc alpha RI binding and serum killing of bacteria. J Immunol 174:2926–2933PubMed Langley R, Wines B, Willoughby N, Basu I, Proft T, Fraser JD (2005) The staphylococcal superantigen-like protein 7 binds IgA and complement C5 and inhibits IgA-Fc alpha RI binding and serum killing of bacteria. J Immunol 174:2926–2933PubMed
165.
go back to reference Atkins KL, Burman JD, Chamberlain ES, Cooper JE, Poutrel B, Bagby S, Jenkins AT, Feil EJ, van den Elsen JM (2008) S. aureus IgG-binding proteins SpA and Sbi: host specificity and mechanisms of immune complex formation. Mol Immunol 45:1600–1611PubMedCrossRef Atkins KL, Burman JD, Chamberlain ES, Cooper JE, Poutrel B, Bagby S, Jenkins AT, Feil EJ, van den Elsen JM (2008) S. aureus IgG-binding proteins SpA and Sbi: host specificity and mechanisms of immune complex formation. Mol Immunol 45:1600–1611PubMedCrossRef
166.
go back to reference Sjodahl J (1977) Repetitive sequences in protein A from Staphylococcus aureus. Arrangement of five regions within the protein, four being highly homologous and Fc-binding. Eur J Biochem 73:343–351PubMedCrossRef Sjodahl J (1977) Repetitive sequences in protein A from Staphylococcus aureus. Arrangement of five regions within the protein, four being highly homologous and Fc-binding. Eur J Biochem 73:343–351PubMedCrossRef
167.
go back to reference Haupt K, Reuter M, van den Elsen J, Burman J, Halbich S, Richter J, Skerka C, Zipfel PF (2008) The Staphylococcus aureus protein Sbi acts as a complement inhibitor and forms a tripartite complex with host complement Factor H and C3b. PLoS Pathog 4:e1000250PubMedCrossRef Haupt K, Reuter M, van den Elsen J, Burman J, Halbich S, Richter J, Skerka C, Zipfel PF (2008) The Staphylococcus aureus protein Sbi acts as a complement inhibitor and forms a tripartite complex with host complement Factor H and C3b. PLoS Pathog 4:e1000250PubMedCrossRef
168.
go back to reference Toapanta FR, Ross TM (2006) Complement-mediated activation of the adaptive immune responses: role of C3d in linking the innate and adaptive immunity. Immunol Res 36:197–210PubMedCrossRef Toapanta FR, Ross TM (2006) Complement-mediated activation of the adaptive immune responses: role of C3d in linking the innate and adaptive immunity. Immunol Res 36:197–210PubMedCrossRef
169.
go back to reference Ricklin D, Tzekou A, Garcia BL, Hammel M, McWhorter WJ, Sfyroera G, Wu YQ, Holers VM, Herbert AP, Barlow PN et al (2009) A molecular insight into complement evasion by the staphylococcal complement inhibitor protein family. J Immunol 183:2565–2574PubMedCrossRef Ricklin D, Tzekou A, Garcia BL, Hammel M, McWhorter WJ, Sfyroera G, Wu YQ, Holers VM, Herbert AP, Barlow PN et al (2009) A molecular insight into complement evasion by the staphylococcal complement inhibitor protein family. J Immunol 183:2565–2574PubMedCrossRef
170.
go back to reference Jongerius I, Kohl J, Pandey MK, Ruyken M, van Kessel KP, van Strijp JA, Rooijakkers SH (2007) Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med 204:2461–2471PubMedCrossRef Jongerius I, Kohl J, Pandey MK, Ruyken M, van Kessel KP, van Strijp JA, Rooijakkers SH (2007) Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med 204:2461–2471PubMedCrossRef
171.
go back to reference Isenman DE, Leung E, Mackay JD, Bagby S, van den Elsen JM (2010) Mutational analyses reveal that the staphylococcal immune evasion molecule Sbi and complement receptor 2 (CR2) share overlapping contact residues on C3d: implications for the controversy regarding the CR2/C3d cocrystal structure. J Immunol 184:1946–1955PubMedCrossRef Isenman DE, Leung E, Mackay JD, Bagby S, van den Elsen JM (2010) Mutational analyses reveal that the staphylococcal immune evasion molecule Sbi and complement receptor 2 (CR2) share overlapping contact residues on C3d: implications for the controversy regarding the CR2/C3d cocrystal structure. J Immunol 184:1946–1955PubMedCrossRef
172.
go back to reference Edwards CK 3rd, Watts LM, Parmely MJ, Linnik MD, Long RE, Borcherding DR (1994) Effect of the carbocyclic nucleoside analogue MDL 201,112 on inhibition of interferon-gamma-induced priming of Lewis (LEW/N) rat macrophages for enhanced respiratory burst and MHC class II Ia+ antigen expression. J Leukoc Biol 56:133–144PubMed Edwards CK 3rd, Watts LM, Parmely MJ, Linnik MD, Long RE, Borcherding DR (1994) Effect of the carbocyclic nucleoside analogue MDL 201,112 on inhibition of interferon-gamma-induced priming of Lewis (LEW/N) rat macrophages for enhanced respiratory burst and MHC class II Ia+ antigen expression. J Leukoc Biol 56:133–144PubMed
173.
go back to reference Panther E, Idzko M, Herouy Y, Rheinen H, Gebicke-Haerter PJ, Mrowietz U, Dichmann S, Norgauer J (2001) Expression and function of adenosine receptors in human dendritic cells. FASEB J 15:1963–1970PubMedCrossRef Panther E, Idzko M, Herouy Y, Rheinen H, Gebicke-Haerter PJ, Mrowietz U, Dichmann S, Norgauer J (2001) Expression and function of adenosine receptors in human dendritic cells. FASEB J 15:1963–1970PubMedCrossRef
174.
go back to reference Hasko G, Kuhel DG, Chen JF, Schwarzschild MA, Deitch EA, Mabley JG, Marton A, Szabo C (2000) Adenosine inhibits IL-12 and TNF-[alpha] production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J 14:2065–2074PubMedCrossRef Hasko G, Kuhel DG, Chen JF, Schwarzschild MA, Deitch EA, Mabley JG, Marton A, Szabo C (2000) Adenosine inhibits IL-12 and TNF-[alpha] production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J 14:2065–2074PubMedCrossRef
175.
go back to reference Schneewind O, Fowler A, Faull KF (1995) Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science 268:103–106PubMedCrossRef Schneewind O, Fowler A, Faull KF (1995) Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science 268:103–106PubMedCrossRef
176.
go back to reference Guss B, Uhlen M, Nilsson B, Lindberg M, Sjoquist J, Sjodahl J (1984) Region X, the cell-wall-attachment part of staphylococcal protein A. Eur J Biochem 138:413–420PubMedCrossRef Guss B, Uhlen M, Nilsson B, Lindberg M, Sjoquist J, Sjodahl J (1984) Region X, the cell-wall-attachment part of staphylococcal protein A. Eur J Biochem 138:413–420PubMedCrossRef
177.
go back to reference Lindmark R, Thoren-Tolling K, Sjoquist J (1983) Binding of immunoglobulins to protein A and immunoglobulin levels in mammalian sera. J Immunol Methods 62:1–13PubMedCrossRef Lindmark R, Thoren-Tolling K, Sjoquist J (1983) Binding of immunoglobulins to protein A and immunoglobulin levels in mammalian sera. J Immunol Methods 62:1–13PubMedCrossRef
178.
go back to reference Sasso EH, Silverman GJ, Mannik M (1989) Human IgM molecules that bind staphylococcal protein A contain VHIII H chains. J Immunol 142:2778–2783PubMed Sasso EH, Silverman GJ, Mannik M (1989) Human IgM molecules that bind staphylococcal protein A contain VHIII H chains. J Immunol 142:2778–2783PubMed
179.
go back to reference 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 96:2149–2156PubMed 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 96:2149–2156PubMed
180.
go back to reference Nguyen T, Ghebrehiwet B, Peerschke EI (2000) Staphylococcus aureus protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infect Immun 68:2061–2068PubMedCrossRef Nguyen T, Ghebrehiwet B, Peerschke EI (2000) Staphylococcus aureus protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infect Immun 68:2061–2068PubMedCrossRef
181.
go back to reference 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 10:842–848PubMedCrossRef 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 10:842–848PubMedCrossRef
182.
go back to reference Mazmanian SK, Ton-That H, Schneewind O (2001) Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol Microbiol 40:1049–1057PubMedCrossRef Mazmanian SK, Ton-That H, Schneewind O (2001) Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol Microbiol 40:1049–1057PubMedCrossRef
183.
go back to reference Silverman GJ, Sasano M, Wormsley SB (1993) Age-associated changes in binding of human B lymphocytes to a VH3-restricted unconventional bacterial antigen. J Immunol 151:5840–5855PubMed Silverman GJ, Sasano M, Wormsley SB (1993) Age-associated changes in binding of human B lymphocytes to a VH3-restricted unconventional bacterial antigen. J Immunol 151:5840–5855PubMed
184.
go back to reference Goodyear CS, Silverman GJ (2004) Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes. Proc Natl Acad Sci USA 101:11392–11397PubMedCrossRef Goodyear CS, Silverman GJ (2004) Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes. Proc Natl Acad Sci USA 101:11392–11397PubMedCrossRef
185.
go back to reference Silverman GJ, Cary SP, Dwyer DC, Luo L, Wagenknecht R, Curtiss VE (2000) A B cell superantigen-induced persistent "Hole" in the B-1 repertoire. J Exp Med 192:87–98PubMedCrossRef Silverman GJ, Cary SP, Dwyer DC, Luo L, Wagenknecht R, Curtiss VE (2000) A B cell superantigen-induced persistent "Hole" in the B-1 repertoire. J Exp Med 192:87–98PubMedCrossRef
186.
go back to reference Kim HK, Cheng AG, Kim HY, Missiakas DM, Schneewind O Nontoxigenic protein A vaccine for methicillin-resistant Staphylococcus aureus infections in mice. J Exp Med 207:1863–1870 Kim HK, Cheng AG, Kim HY, Missiakas DM, Schneewind O Nontoxigenic protein A vaccine for methicillin-resistant Staphylococcus aureus infections in mice. J Exp Med 207:1863–1870
187.
go back to reference Kim HK, Kim HY, Schneewind O, Missiakas D Identifying protective antigens of Staphylococcus aureus, a pathogen that suppresses host immune responses. FASEB J 25:3605–3612 Kim HK, Kim HY, Schneewind O, Missiakas D Identifying protective antigens of Staphylococcus aureus, a pathogen that suppresses host immune responses. FASEB J 25:3605–3612
Metadata
Title
Exploring Staphylococcus aureus pathways to disease for vaccine development
Authors
Andrea DeDent
Hwan Keun Kim
Dominique Missiakas
Olaf Schneewind
Publication date
01-03-2012
Publisher
Springer-Verlag
Published in
Seminars in Immunopathology / Issue 2/2012
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-011-0299-z

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