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Semin Thromb Hemost 2016; 42(04): 408-421
DOI: 10.1055/s-0036-1579635
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Fibrinogen Is at the Interface of Host Defense and Pathogen Virulence in Staphylococcus aureus Infection

Ya-Ping Ko
1   Center for Infectious and Inflammatory Diseases, Institute for Biosciences and Technology, Texas A&M Health Science Center, Houston, Texas
,
Matthew J. Flick
2   Division of Experimental Hematology and Cancer Biology, Cancer and Blood Diseases Institute, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
› Author Affiliations
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Publication History

Publication Date:
07 April 2016 (online)

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Abstract

Fibrinogen not only plays a pivotal role in hemostasis but also serves key roles in antimicrobial host defense. As a rapidly assembled provisional matrix protein, fibrin(ogen) can function as an early line of host protection by limiting bacterial growth, suppressing dissemination of microbes to distant sites, and mediating host bacterial killing. Fibrinogen-mediated host antimicrobial activity occurs predominantly through two general mechanisms, namely, fibrin matrices functioning as a protective barrier and fibrin(ogen) directly or indirectly driving host protective immune function. The potential of fibrin to limit bacterial infection and disease has been countered by numerous bacterial species evolving and maintaining virulence factors that engage hemostatic system components within vertebrate hosts. Bacterial factors have been isolated that simply bind fibrinogen or fibrin, promote fibrin polymer formation, or promote fibrin dissolution. Staphylococcus aureus is an opportunistic gram-positive bacterium, the causative agent of a wide range of human infectious diseases, and a prime example of a pathogen exquisitely sensitive to host fibrinogen. Indeed, current data suggest fibrinogen serves as a context-dependent determinant of host defense or pathogen virulence in Staphylococcus infection whose ultimate contribution is dictated by the expression of S. aureus virulence factors, the path of infection, and the tissue microenvironment.

Keywords

fibrinogen - infection - Staphylococcus aureus - host defense
 

  • References

  • 1 Fish RJ, Neerman-Arbez M. Fibrinogen gene regulation. Thromb Haemost 2012; 108 (3) 419-426
    Article in Thieme ConnectPubMedGoogle Scholar
  • 2 Pottinger BE, Read RC, Paleolog EM, Higgins PG, Pearson JD. von Willebrand factor is an acute phase reactant in man. Thromb Res 1989; 53 (4) 387-394
    CrossrefPubMedGoogle Scholar
  • 3 Begbie M, Notley C, Tinlin S, Sawyer L, Lillicrap D. The Factor VIII acute phase response requires the participation of NFkappaB and C/EBP. Thromb Haemost 2000; 84 (2) 216-222
    PubMedGoogle Scholar
  • 4 Dofferhoff AS, Bom VJ, de Vries-Hospers HG , et al. Patterns of cytokines, plasma endotoxin, plasminogen activator inhibitor, and acute-phase proteins during the treatment of severe sepsis in humans. Crit Care Med 1992; 20 (2) 185-192
    CrossrefPubMedGoogle Scholar
  • 5 Ji Y, Fish PM, Strawn TL , et al. C-reactive protein induces expression of tissue factor and plasminogen activator inhibitor-1 and promotes fibrin accumulation in vein grafts. J Thromb Haemost 2014; 12 (10) 1667-1677
    CrossrefPubMedGoogle Scholar
  • 6 Koyama K, Madoiwa S, Nunomiya S , et al. Combination of thrombin-antithrombin complex, plasminogen activator inhibitor-1, and protein C activity for early identification of severe coagulopathy in initial phase of sepsis: a prospective observational study. Crit Care 2014; 18 (1) R13
    CrossrefPubMedGoogle Scholar
  • 7 Yende S, D'Angelo G, Mayr F , et al; GenIMS Investigators. Elevated hemostasis markers after pneumonia increases one-year risk of all-cause and cardiovascular deaths. PLoS ONE 2011; 6 (8) e22847
    CrossrefPubMedGoogle Scholar
  • 8 Milbrandt EB, Reade MC, Lee M , et al; GenIMS Investigators. Prevalence and significance of coagulation abnormalities in community-acquired pneumonia. Mol Med 2009; 15 (11–12) 438-445
    PubMedGoogle Scholar
  • 9 Gando S, Nanzaki S, Sasaki S, Kemmotsu O. Significant correlations between tissue factor and thrombin markers in trauma and septic patients with disseminated intravascular coagulation. Thromb Haemost 1998; 79 (6) 1111-1115
    PubMedGoogle Scholar
  • 10 Bokarewa MI, Tarkowski A. Thrombin generation and mortality during Staphylococcus aureus sepsis. Microb Pathog 2001; 30 (4) 247-252
    CrossrefPubMedGoogle Scholar
  • 11 Starr ME, Takahashi H, Okamura D , et al. Increased coagulation and suppressed generation of activated protein C in aged mice during intra-abdominal sepsis. Am J Physiol Heart Circ Physiol 2015; 308 (2) H83-H91
    CrossrefPubMedGoogle Scholar
  • 12 Kager LM, Wiersinga WJ, Roelofs JJ , et al. Endogenous tissue-type plasminogen activator impairs host defense during severe experimental Gram-negative sepsis (melioidosis)*. Crit Care Med 2012; 40 (7) 2168-2175
    CrossrefPubMedGoogle Scholar
  • 13 Renckens R, Roelofs JJ, ter Horst SA , et al. Absence of thrombin-activatable fibrinolysis inhibitor protects against sepsis-induced liver injury in mice. J Immunol 2005; 175 (10) 6764-6771
    CrossrefPubMedGoogle Scholar
  • 14 van Veen SQ, Cheung CW, Meijers JC, van Gulik TM, Boermeester MA. Anticoagulant and anti-inflammatory effects after peritoneal lavage with antithrombin in experimental polymicrobial peritonitis. J Thromb Haemost 2006; 4 (11) 2343-2351
    CrossrefPubMedGoogle Scholar
  • 15 Levi M. The diagnosis of disseminated intravascular coagulation made easy. Neth J Med 2007; 65 (10) 366-367
    PubMedGoogle Scholar
  • 16 Levi M. Disseminated intravascular coagulation. Crit Care Med 2007; 35 (9) 2191-2195
    CrossrefPubMedGoogle Scholar
  • 17 Levi M, van der Poll T. Inflammation and coagulation. Crit Care Med 2010; 38 (2, Suppl): S26-S34
    CrossrefPubMedGoogle Scholar
  • 18 Flick MJ, Du X, Witte DP , et al. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 2004; 113 (11) 1596-1606
    CrossrefPubMedGoogle Scholar
  • 19 Goguen JD, Bugge T, Degen JL. Role of the pleiotropic effects of plasminogen deficiency in infection experiments with plasminogen-deficient mice. Methods 2000; 21 (2) 179-183
    CrossrefPubMedGoogle Scholar
  • 20 Mullarky IK, Szaba FM, Berggren KN , et al. Infection-stimulated fibrin deposition controls hemorrhage and limits hepatic bacterial growth during listeriosis. Infect Immun 2005; 73 (7) 3888-3895
    CrossrefPubMedGoogle Scholar
  • 21 Sun H, Wang X, Degen JL, Ginsburg D. Reduced thrombin generation increases host susceptibility to group A streptococcal infection. Blood 2009; 113 (6) 1358-1364
    CrossrefPubMedGoogle Scholar
  • 22 Engel LS, Hill JM, Caballero AR, Green LC, O'Callaghan RJ. Protease IV, a unique extracellular protease and virulence factor from Pseudomonas aeruginosa. J Biol Chem 1998; 273 (27) 16792-16797
    CrossrefPubMedGoogle Scholar
  • 23 Hartford OM, Wann ER, Höök M, Foster TJ. Identification of residues in the Staphylococcus aureus fibrinogen-binding MSCRAMM clumping factor A (ClfA) that are important for ligand binding. J Biol Chem 2001; 276 (4) 2466-2473
    CrossrefPubMedGoogle Scholar
  • 24 Ringnér M, Valkonen KH, Wadström T. Binding of vitronectin and plasminogen to Helicobacter pylori. FEMS Immunol Med Microbiol 1994; 9 (1) 29-34
    CrossrefPubMedGoogle Scholar
  • 25 Korhonen TK. Fibrinolytic and procoagulant activities of Yersinia pestis and Salmonella enterica. J Thromb Haemost 2015; 13 (Suppl. 01) S115-S120
    CrossrefPubMedGoogle Scholar
  • 26 Marcum JA, Kline DL. Species specificity of streptokinase. Comp Biochem Physiol B 1983; 75 (3) 389-394
    PubMedGoogle Scholar
  • 27 McCoy HE, Broder CC, Lottenberg R. Streptokinases produced by pathogenic group C streptococci demonstrate species-specific plasminogen activation. J Infect Dis 1991; 164 (3) 515-521
    CrossrefPubMedGoogle Scholar
  • 28 Schroeder B, Boyle MD, Sheerin BR, Asbury AC, Lottenberg R. Species specificity of plasminogen activation and acquisition of surface-associated proteolytic activity by group C streptococci grown in plasma. Infect Immun 1999; 67 (12) 6487-6495
    PubMedGoogle Scholar
  • 29 Sun H, Ringdahl U, Homeister JW , et al. Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 2004; 305 (5688) 1283-1286
    CrossrefPubMedGoogle Scholar
  • 30 Davies WA, Ackerman VP, Nelson DS. Mechanism for nonspecific immunity of Listeria monocytogenes in rats mediated by platelets and the clotting system. Infect Immun 1981; 33 (2) 477-481
    PubMedGoogle Scholar
  • 31 Rubel C, Fernández GC, Dran G, Bompadre MB, Isturiz MA, Palermo MS. Fibrinogen promotes neutrophil activation and delays apoptosis. J Immunol 2001; 166 (3) 2002-2010
    CrossrefPubMedGoogle Scholar
  • 32 Rubel C, Fernández GC, Rosa FA , et al. Soluble fibrinogen modulates neutrophil functionality through the activation of an extracellular signal-regulated kinase-dependent pathway. J Immunol 2002; 168 (7) 3527-3535
    CrossrefPubMedGoogle Scholar
  • 33 Sitrin RG, Pan PM, Srikanth S, Todd III RF. Fibrinogen activates NF-kappa B transcription factors in mononuclear phagocytes. J Immunol 1998; 161 (3) 1462-1470
    PubMedGoogle Scholar
  • 34 Forsyth CB, Solovjov DA, Ugarova TP, Plow EF. Integrin alpha(M)beta(2)-mediated cell migration to fibrinogen and its recognition peptides. J Exp Med 2001; 193 (10) 1123-1133
    CrossrefPubMedGoogle Scholar
  • 35 Shi C, Zhang X, Chen Z, Robinson MK, Simon DI. Leukocyte integrin Mac-1 recruits toll/interleukin-1 receptor superfamily signaling intermediates to modulate NF-kappaB activity. Circ Res 2001; 89 (10) 859-865
    CrossrefPubMedGoogle Scholar
  • 36 Tuluc F, Garcia A, Bredetean O, Meshki J, Kunapuli SP. Primary granule release from human neutrophils is potentiated by soluble fibrinogen through a mechanism depending on multiple intracellular signaling pathways. Am J Physiol Cell Physiol 2004; 287 (5) C1264-C1272
    CrossrefPubMedGoogle Scholar
  • 37 Podolnikova NP, Yakovlev S, Yakubenko VP, Wang X, Gorkun OV, Ugarova TP. The interaction of integrin αIIbβ3 with fibrin occurs through multiple binding sites in the αIIb β-propeller domain. J Biol Chem 2014; 289 (4) 2371-2383
    CrossrefPubMedGoogle Scholar
  • 38 Zhang P, Ozdemir T, Chung CY, Robertson GP, Dong C. Sequential binding of αVβ3 and ICAM-1 determines fibrin-mediated melanoma capture and stable adhesion to CD11b/CD18 on neutrophils. J Immunol 2011; 186 (1) 242-254
    CrossrefPubMedGoogle Scholar
  • 39 Ugarova TP, Lishko VK, Podolnikova NP , et al. Sequence gamma 377-395(P2), but not gamma 190-202(P1), is the binding site for the alpha MI-domain of integrin alpha M beta 2 in the gamma C-domain of fibrinogen. Biochemistry 2003; 42 (31) 9365-9373
    CrossrefPubMedGoogle Scholar
  • 40 Podolnikova NP, Yakubenko VP, Volkov GL, Plow EF, Ugarova TP. Identification of a novel binding site for platelet integrins alpha IIb beta 3 (GPIIbIIIa) and alpha 5 beta 1 in the gamma C-domain of fibrinogen. J Biol Chem 2003; 278 (34) 32251-32258
    CrossrefPubMedGoogle Scholar
  • 41 Corbett SA, Schwarzbauer JE. Requirements for alpha(5)beta(1) integrin-mediated retraction of fibronectin-fibrin matrices. J Biol Chem 1999; 274 (30) 20943-20948
    CrossrefPubMedGoogle Scholar
  • 42 Yokoyama K, Zhang XP, Medved L, Takada Y. Specific binding of integrin alpha v beta 3 to the fibrinogen gamma and alpha E chain C-terminal domains. Biochemistry 1999; 38 (18) 5872-5877
    CrossrefPubMedGoogle Scholar
  • 43 Gailit J, Clarke C, Newman D, Tonnesen MG, Mosesson MW, Clark RA. Human fibroblasts bind directly to fibrinogen at RGD sites through integrin alpha(v)beta3. Exp Cell Res 1997; 232 (1) 118-126
    CrossrefPubMedGoogle Scholar
  • 44 Bach TL, Barsigian C, Chalupowicz DG , et al. VE-Cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Exp Cell Res 1998; 238 (2) 324-334
    CrossrefPubMedGoogle Scholar
  • 45 Bach TL, Barsigian C, Yaen CH, Martinez J. Endothelial cell VE-cadherin functions as a receptor for the beta15-42 sequence of fibrin. J Biol Chem 1998; 273 (46) 30719-30728
    CrossrefPubMedGoogle Scholar
  • 46 Pillay J, Kamp VM, Pennings M , et al. Acute-phase concentrations of soluble fibrinogen inhibit neutrophil adhesion under flow conditions in vitro through interactions with ICAM-1 and MAC-1 (CD11b/CD18). J Thromb Haemost 2013; 11 (6) 1172-1182
    CrossrefPubMedGoogle Scholar
  • 47 Kim S, Nadel JA. Fibrinogen binding to ICAM-1 promotes EGFR-dependent mucin production in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2009; 297 (1) L174-L183
    CrossrefPubMedGoogle Scholar
  • 48 Duperray A, Languino LR, Plescia J , et al. Molecular identification of a novel fibrinogen binding site on the first domain of ICAM-1 regulating leukocyte-endothelium bridging. J Biol Chem 1997; 272 (1) 435-441
    CrossrefPubMedGoogle Scholar
  • 49 Altieri DC, Duperray A, Plescia J, Thornton GB, Languino LR. Structural recognition of a novel fibrinogen gamma chain sequence (117-133) by intercellular adhesion molecule-1 mediates leukocyte-endothelium interaction. J Biol Chem 1995; 270 (2) 696-699
    CrossrefPubMedGoogle Scholar
  • 50 Yakovlev S, Gao Y, Cao C , et al. Interaction of fibrin with VE-cadherin and anti-inflammatory effect of fibrin-derived fragments. J Thromb Haemost 2011; 9 (9) 1847-1855
    CrossrefPubMedGoogle Scholar
  • 51 Busso N, Péclat V, Van Ness K , et al. Exacerbation of antigen-induced arthritis in urokinase-deficient mice. J Clin Invest 1998; 102 (1) 41-50
    CrossrefPubMedGoogle Scholar
  • 52 Pawlinski R, Pedersen B, Schabbauer G , et al. Role of tissue factor and protease-activated receptors in a mouse model of endotoxemia. Blood 2004; 103 (4) 1342-1347
    PubMedGoogle Scholar
  • 53 Adams RA, Bauer J, Flick MJ , et al. The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 2007; 204 (3) 571-582
    CrossrefPubMedGoogle Scholar
  • 54 Flick MJ, LaJeunesse CM, Talmage KE , et al. Fibrin(ogen) exacerbates inflammatory joint disease through a mechanism linked to the integrin alphaMbeta2 binding motif. J Clin Invest 2007; 117 (11) 3224-3235
    CrossrefPubMedGoogle Scholar
  • 55 Steinbrecher KA, Horowitz NA, Blevins EA , et al. Colitis-associated cancer is dependent on the interplay between the hemostatic and inflammatory systems and supported by integrin alpha(M)beta(2) engagement of fibrinogen. Cancer Res 2010; 70 (7) 2634-2643
    CrossrefPubMedGoogle Scholar
  • 56 Sodeinde OA, Subrahmanyam YV, Stark K, Quan T, Bao Y, Goguen JD. A surface protease and the invasive character of plague. Science 1992; 258 (5084) 1004-1007
    CrossrefPubMedGoogle Scholar
  • 57 Degen JL, Bugge TH, Goguen JD. Fibrin and fibrinolysis in infection and host defense. J Thromb Haemost 2007; 5 (Suppl. 01) 24-31
    CrossrefPubMedGoogle Scholar
  • 58 Luo D, Szaba FM, Kummer LW , et al. Protective roles for fibrin, tissue factor, plasminogen activator inhibitor-1, and thrombin activatable fibrinolysis inhibitor, but not factor XI, during defense against the gram-negative bacterium Yersinia enterocolitica. J Immunol 2011; 187 (4) 1866-1876
    CrossrefPubMedGoogle Scholar
  • 59 Lowy FD. Staphylococcus aureus infections. N Engl J Med 1998; 339 (8) 520-532
    CrossrefPubMedGoogle Scholar
  • 60 Active Bacterial Core Surveillance Report. Emerging Infections Program Network . Methicillin-resistant Staphylococcus aureus 2012
    PubMed
  • 61 Grundmann H, Aanensen DM, van den Wijngaard CC, Spratt BG, Harmsen D, Friedrich AW ; European Staphylococcal Reference Laboratory Working Group. Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLoS Med 2010; 7 (1) e1000215
    CrossrefPubMedGoogle Scholar
  • 62 Dulon M, Peters C, Schablon A, Nienhaus A. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infect Dis 2014; 14: 363
    CrossrefPubMedGoogle Scholar
  • 63 Stryjewski ME, Corey GR. Methicillin-resistant Staphylococcus aureus: an evolving pathogen. Clin Infect Dis 2014; 58 (Suppl. 01) S10-S19
    CrossrefPubMedGoogle Scholar
  • 64 Nair R, Ammann E, Rysavy M, Schweizer ML. Mortality among patients with methicillin-resistant Staphylococcus aureus USA300 versus non-USA300 invasive infections: a meta-analysis. Infect Control Hosp Epidemiol 2014; 35 (1) 31-41
    CrossrefPubMedGoogle Scholar
  • 65 Paterson GK, Harrison EM, Holmes MA. The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends Microbiol 2014; 22 (1) 42-47
    CrossrefPubMedGoogle Scholar
  • 66 Iwamoto M, Mu Y, Lynfield R , et al. Trends in invasive methicillin-resistant Staphylococcus aureus infections. Pediatrics 2013; 132 (4) e817-e824
    CrossrefPubMedGoogle Scholar
  • 67 Dunn DL, Simmons RL. Fibrin in peritonitis. III. The mechanism of bacterial trapping by polymerizing fibrin. Surgery 1982; 92 (3) 513-519
    PubMedGoogle Scholar
  • 68 Kapral FA. Clumping of Staphylococcus aureus in the peritoneal cavity of mice. J Bacteriol 1966; 92 (4) 1188-1195
    PubMedGoogle Scholar
  • 69 Leak LV. Interaction of mesothelium to intraperitoneal stimulation. I. Aggregation of peritoneal cells. Lab Invest 1983; 48 (4) 479-491
    PubMedGoogle Scholar
  • 70 Woolverton CJ, Huebert K, Burkhart B, MacPhee M. Subverting bacterial resistance using high dose, low solubility antibiotics in fibrin. Infection 1999; 27 (1) 28-33
    CrossrefPubMedGoogle Scholar
  • 71 Prasad JM, Gorkun OV, Raghu H , et al. Mice expressing a mutant form of fibrinogen that cannot support fibrin formation exhibit compromised antimicrobial host defense. Blood 2015; 126 (17) 2047-2058
    CrossrefPubMedGoogle Scholar
  • 72 Mullins ES, Kombrinck KW, Talmage KE , et al. Genetic elimination of prothrombin in adult mice is not compatible with survival and results in spontaneous hemorrhagic events in both heart and brain. Blood 2009; 113 (3) 696-704
    CrossrefPubMedGoogle Scholar
  • 73 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 (8) e1001036
    CrossrefPubMedGoogle Scholar
  • 74 Foster TJ, Höök M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 1998; 6 (12) 484-488
    CrossrefPubMedGoogle Scholar
  • 75 Loughman A, Fitzgerald JR, Brennan MP , et al. Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol Microbiol 2005; 57 (3) 804-818
    CrossrefPubMedGoogle Scholar
  • 76 McAdow M, DeDent AC, Emolo C , et al. Coagulases as determinants of protective immune responses against Staphylococcus aureus. Infect Immun 2012; 80 (10) 3389-3398
    CrossrefPubMedGoogle Scholar
  • 77 McDevitt D, Nanavaty T, House-Pompeo K , et al. Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem 1997; 247 (1) 416-424
    CrossrefPubMedGoogle Scholar
  • 78 Panizzi P, Friedrich R, Fuentes-Prior P, Richter K, Bock PE, Bode W. Fibrinogen substrate recognition by staphylocoagulase.(pro)thrombin complexes. J Biol Chem 2006; 281 (2) 1179-1187
    CrossrefPubMedGoogle Scholar
  • 79 Guggenberger C, Wolz C, Morrissey JA, Heesemann J. Two distinct coagulase-dependent barriers protect Staphylococcus aureus from neutrophils in a three dimensional in vitro infection model. PLoS Pathog 2012; 8 (1) e1002434
    CrossrefPubMedGoogle Scholar
  • 80 Foster TJ, Geoghegan JA, Ganesh VK, Höök M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 2014; 12 (1) 49-62
    PubMedGoogle Scholar
  • 81 Patti JM, Allen BL, McGavin MJ, Höök M. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 1994; 48: 585-617
    CrossrefPubMedGoogle Scholar
  • 82 Deivanayagam CC, Wann ER, Chen W , et al. A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J 2002; 21 (24) 6660-6672
    CrossrefPubMedGoogle Scholar
  • 83 Ton-That H, Liu G, Mazmanian SK, Faull KF, Schneewind O. Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proc Natl Acad Sci U S A 1999; 96 (22) 12424-12429
    CrossrefPubMedGoogle Scholar
  • 84 Ponnuraj K, Bowden MG, Davis S , et al. A “dock, lock, and latch” structural model for a staphylococcal adhesin binding to fibrinogen. Cell 2003; 115 (2) 217-228
    CrossrefPubMedGoogle Scholar
  • 85 Wann ER, Gurusiddappa S, Hook M. The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 2000; 275 (18) 13863-13871
    CrossrefPubMedGoogle Scholar
  • 86 Kloczewiak M, Timmons S, Bednarek MA, Sakon M, Hawiger J. Platelet receptor recognition domain on the gamma chain of human fibrinogen and its synthetic peptide analogues. Biochemistry 1989; 28 (7) 2915-2919
    CrossrefPubMedGoogle Scholar
  • 87 Farrell DH, Thiagarajan P, Chung DW, Davie EW. Role of fibrinogen alpha and gamma chain sites in platelet aggregation. Proc Natl Acad Sci U S A 1992; 89 (22) 10729-10732
    CrossrefPubMedGoogle Scholar
  • 88 Hettasch JM, Bolyard MG, Lord ST. The residues AGDV of recombinant gamma chains of human fibrinogen must be carboxy-terminal to support human platelet aggregation. Thromb Haemost 1992; 68 (6) 701-706
    PubMedGoogle Scholar
  • 89 Liu CZ, Shih MH, Tsai PJ. ClfA(221-550), a fibrinogen-binding segment of Staphylococcus aureus clumping factor A, disrupts fibrinogen function. Thromb Haemost 2005; 94 (2) 286-294
    PubMedGoogle Scholar
  • 90 Liu CZ, Huang TF, Tsai PJ, Tsai PJ, Chang LY, Chang MC. A segment of Staphylococcus aureus clumping factor A with fibrinogen-binding activity (ClfA221-550) inhibits platelet-plug formation in mice. Thromb Res 2007; 121 (2) 183-191
    CrossrefPubMedGoogle Scholar
  • 91 Ganesh VK, Rivera JJ, Smeds E , et al. A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLoS Pathog 2008; 4 (11) e1000226
    CrossrefPubMedGoogle Scholar
  • 92 Xiao T, Takagi J, Coller BS, Wang JH, Springer TA. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature 2004; 432 (7013) 59-67
    CrossrefPubMedGoogle Scholar
  • 93 Hair PS, Echague CG, Sholl AM , et al. 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 2010; 78 (4) 1717-1727
    CrossrefPubMedGoogle Scholar
  • 94 Higgins J, Loughman A, van Kessel KP, van Strijp JA, Foster TJ. Clumping factor A of Staphylococcus aureus inhibits phagocytosis by human polymorphonuclear leucocytes. FEMS Microbiol Lett 2006; 258 (2) 290-296
    CrossrefPubMedGoogle Scholar
  • 95 Moreillon P, Entenza JM, Francioli P , et al. Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun 1995; 63 (12) 4738-4743
    PubMedGoogle Scholar
  • 96 Josefsson E, Hartford O, O'Brien L, Patti JM, Foster T. Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J Infect Dis 2001; 184 (12) 1572-1580
    CrossrefPubMedGoogle Scholar
  • 97 Que YA, Haefliger JA, Piroth L , et al. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med 2005; 201 (10) 1627-1635
    CrossrefPubMedGoogle Scholar
  • 98 McAdow M, Kim HK, Dedent AC, Hendrickx AP, Schneewind O, Missiakas DM. Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog 2011; 7 (10) e1002307
    CrossrefPubMedGoogle Scholar
  • 99 Ní Eidhin D, Perkins S, Francois P, Vaudaux P, Höök M, Foster TJ. Clumping factor B (ClfB), a new surface-located fibrinogen-binding adhesin of Staphylococcus aureus. Mol Microbiol 1998; 30 (2) 245-257
    CrossrefPubMedGoogle Scholar
  • 100 Walsh EJ, O'Brien LM, Liang X, Hook M, Foster TJ. Clumping factor B, a fibrinogen-binding MSCRAMM (microbial surface components recognizing adhesive matrix molecules) adhesin of Staphylococcus aureus, also binds to the tail region of type I cytokeratin 10. J Biol Chem 2004; 279 (49) 50691-50699
    CrossrefPubMedGoogle Scholar
  • 101 Mulcahy ME, Geoghegan JA, Monk IR , et al. Nasal colonisation by Staphylococcus aureus depends upon clumping factor B binding to the squamous epithelial cell envelope protein loricrin. PLoS Pathog 2012; 8 (12) e1003092
    CrossrefPubMedGoogle Scholar
  • 102 Xiang H, Feng Y, Wang J , et al. Crystal structures reveal the multi-ligand binding mechanism of Staphylococcus aureus ClfB. PLoS Pathog 2012; 8 (6) e1002751
    CrossrefPubMedGoogle Scholar
  • 103 Ganesh VK, Barbu EM, Deivanayagam CC , et al. Structural and biochemical characterization of Staphylococcus aureus clumping factor B/ligand interactions. J Biol Chem 2011; 286 (29) 25963-25972
    CrossrefPubMedGoogle Scholar
  • 104 Miajlovic H, Loughman A, Brennan M, Cox D, Foster TJ. Both complement- and fibrinogen-dependent mechanisms contribute to platelet aggregation mediated by Staphylococcus aureus clumping factor B. Infect Immun 2007; 75 (7) 3335-3343
    CrossrefPubMedGoogle Scholar
  • 105 Wertheim HF, Walsh E, Choudhurry R , et al. Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med 2008; 5 (1) e17
    CrossrefPubMedGoogle Scholar
  • 106 Schwarz-Linek U, Höök M, Potts JR. The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol Microbiol 2004; 52 (3) 631-641
    CrossrefPubMedGoogle Scholar
  • 107 Stemberk V, Jones RP, Moroz O , et al. Evidence for steric regulation of fibrinogen binding to Staphylococcus aureus fibronectin-binding protein A (FnBPA). J Biol Chem 2014; 289 (18) 12842-12851
    CrossrefPubMedGoogle Scholar
  • 108 Peacock SJ, Foster TJ, Cameron BJ, Berendt AR. Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology 1999; 145 (Pt 12): 3477-3486
    CrossrefPubMedGoogle Scholar
  • 109 McCourt J, O'Halloran DP, McCarthy H, O'Gara JP, Geoghegan JA. Fibronectin-binding proteins are required for biofilm formation by community-associated methicillin-resistant Staphylococcus aureus strain LAC. FEMS Microbiol Lett 2014; 353 (2) 157-164
    CrossrefPubMedGoogle Scholar
  • 110 O'Neill E, Humphreys H, O'Gara JP. Carriage of both the fnbA and fnbB genes and growth at 37 degrees C promote FnBP-mediated biofilm development in meticillin-resistant Staphylococcus aureus clinical isolates. J Med Microbiol 2009; 58 (Pt 4): 399-402
    CrossrefPubMedGoogle Scholar
  • 111 Herman-Bausier P, El-Kirat-Chatel S, Foster TJ, Geoghegan JA, Dufrêne YF. Staphylococcus aureus Fibronectin-Binding Protein A Mediates Cell-Cell Adhesion through Low-Affinity Homophilic Bonds. MBio 2015; 6 (3) e00413-e00415
    PubMedGoogle Scholar
  • 112 Tung Hs, Guss B, Hellman U, Persson L, Rubin K, Rydén C. A bone sialoprotein-binding protein from Staphylococcus aureus: a member of the staphylococcal Sdr family. Biochem J 2000; 345 (Pt 3): 611-619
    CrossrefPubMedGoogle Scholar
  • 113 Yacoub A, Lindahl P, Rubin K, Wendel M, Heinegård D, Rydén C. Purification of a bone sialoprotein-binding protein from Staphylococcus aureus. Eur J Biochem 1994; 222 (3) 919-925
    CrossrefPubMedGoogle Scholar
  • 114 Vazquez V, Liang X, Horndahl JK , et al. Fibrinogen is a ligand for the Staphylococcus aureus microbial surface components recognizing adhesive matrix molecules (MSCRAMM) bone sialoprotein-binding protein (Bbp). J Biol Chem 2011; 286 (34) 29797-29805
    CrossrefPubMedGoogle Scholar
  • 115 Sharp JA, Echague CG, Hair PS , et al. Staphylococcus aureus surface protein SdrE binds complement regulator factor H as an immune evasion tactic. PLoS ONE 2012; 7 (5) e38407
    CrossrefPubMedGoogle Scholar
  • 116 Hair PS, Foley CK, Krishna NK , et al. Complement regulator C4BP binds to Staphylococcus aureus surface proteins SdrE and Bbp inhibiting bacterial opsonization and killing. Res Immunol 2013; 3: 114-121
    PubMedGoogle Scholar
  • 117 Lee LY, Liang X, Höök M, Brown EL. Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb). J Biol Chem 2004; 279 (49) 50710-50716
    CrossrefPubMedGoogle Scholar
  • 118 Jongerius I, von Köckritz-Blickwede M, Horsburgh MJ, Ruyken M, Nizet V, Rooijakkers SH. Staphylococcus aureus virulence is enhanced by secreted factors that block innate immune defenses. J Innate Immun 2012; 4 (3) 301-311
    CrossrefPubMedGoogle Scholar
  • 119 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 (10) 3393-3404
    CrossrefPubMedGoogle Scholar
  • 120 Ko YP, Liang X, Smith CW, Degen JL, Höök M. Binding of Efb from Staphylococcus aureus to fibrinogen blocks neutrophil adherence. J Biol Chem 2011; 286 (11) 9865-9874
    CrossrefPubMedGoogle Scholar
  • 121 Ko Y-P, Kang M, Ganesh VK, Ravirajan D, Li B, Höök M. Coagulase and Efb of Staphylococcus aureus have a common fibrinogen binding motif. MBio 2016; 7 (1) e01885-e15
    PubMedGoogle Scholar
  • 122 Ko YP, Kuipers A, Freitag CM , et al. Phagocytosis escape by a Staphylococcus aureus protein that connects complement and coagulation proteins at the bacterial surface. PLoS Pathog 2013; 9 (12) e1003816
    CrossrefPubMedGoogle Scholar
  • 123 Jongerius I, Köhl J, Pandey MK , et al. Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med 2007; 204 (10) 2461-2471
    CrossrefPubMedGoogle Scholar
  • 124 Lee LY, Höök M, Haviland D , et al. Inhibition of complement activation by a secreted Staphylococcus aureus protein. J Infect Dis 2004; 190 (3) 571-579
    CrossrefPubMedGoogle Scholar
  • 125 Shannon O, Flock JI. Extracellular fibrinogen binding protein, Efb, from Staphylococcus aureus binds to platelets and inhibits platelet aggregation. Thromb Haemost 2004; 91 (4) 779-789
    PubMedGoogle Scholar
  • 126 Shannon O, Uekötter A, Flock JI. Extracellular fibrinogen binding protein, Efb, from Staphylococcus aureus as an antiplatelet agent in vivo. Thromb Haemost 2005; 93 (5) 927-931
    PubMedGoogle Scholar
  • 127 Palma M, Nozohoor S, Schennings T, Heimdahl A, Flock JI. Lack of the extracellular 19-kilodalton fibrinogen-binding protein from Staphylococcus aureus decreases virulence in experimental wound infection. Infect Immun 1996; 64 (12) 5284-5289
    PubMedGoogle Scholar
  • 128 Fitzgerald JR, Foster TJ, Cox D. The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006; 4 (6) 445-457
    CrossrefPubMedGoogle Scholar
  • 129 Hussain M, Becker K, von Eiff C, Schrenzel J, Peters G, Herrmann M. Identification and characterization of a novel 38.5-kilodalton cell surface protein of Staphylococcus aureus with extended-spectrum binding activity for extracellular matrix and plasma proteins. J Bacteriol 2001; 183 (23) 6778-6786
    CrossrefPubMedGoogle Scholar
  • 130 Jönsson K, McDevitt D, McGavin MH, Patti JM, Höök M. Staphylococcus aureus expresses a major histocompatibility complex class II analog. J Biol Chem 1995; 270 (37) 21457-21460
    CrossrefPubMedGoogle Scholar
  • 131 Hammel M, Nemecek D, Keightley JA, Thomas Jr GJ, Geisbrecht BV. The Staphylococcus aureus extracellular adherence protein (Eap) adopts an elongated but structured conformation in solution. Protein Sci 2007; 16 (12) 2605-2617
    CrossrefPubMedGoogle Scholar
  • 132 Palma M, Haggar A, Flock JI. Adherence of Staphylococcus aureus is enhanced by an endogenous secreted protein with broad binding activity. J Bacteriol 1999; 181 (9) 2840-2845
    PubMedGoogle Scholar
  • 133 Hussain M, Haggar A, Heilmann C, Peters G, Flock JI, Herrmann M. Insertional inactivation of Eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect Immun 2002; 70 (6) 2933-2940
    CrossrefPubMedGoogle Scholar
  • 134 Haggar A, Flock JI, Norrby-Teglund A. Extracellular adherence protein (Eap) from Staphylococcus aureus does not function as a superantigen. Clin Microbiol Infect 2010; 16 (8) 1155-1158
    CrossrefPubMedGoogle Scholar
  • 135 Chavakis T, Hussain M, Kanse SM , et al. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med 2002; 8 (7) 687-693
    CrossrefPubMedGoogle Scholar
  • 136 Lee LY, Miyamoto YJ, McIntyre BW , et al. The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J Clin Invest 2002; 110 (10) 1461-1471
    CrossrefPubMedGoogle Scholar
  • 137 Xie C, Alcaide P, Geisbrecht BV , et al. Suppression of experimental autoimmune encephalomyelitis by extracellular adherence protein of Staphylococcus aureus. J Exp Med 2006; 203 (4) 985-994
    CrossrefPubMedGoogle Scholar
  • 138 Athanasopoulos AN, Economopoulou M, Orlova VV , et al. The extracellular adherence protein (Eap) of Staphylococcus aureus inhibits wound healing by interfering with host defense and repair mechanisms. Blood 2006; 107 (7) 2720-2727
    CrossrefPubMedGoogle Scholar
  • 139 Stapels DA, Kuipers A, von Köckritz-Blickwede M , et al. Staphylococcus aureus protects its immune-evasion proteins against degradation by neutrophil serine proteases. Cell Microbiol 2015;
    PubMedGoogle Scholar
  • 140 Woehl JL, Stapels DA, Garcia BL , et al. The extracellular adherence protein from Staphylococcus aureus inhibits the classical and lectin pathways of complement by blocking formation of the C3 proconvertase. J Immunol 2014; 193 (12) 6161-6171
    CrossrefPubMedGoogle Scholar
  • 141 Friedrich R, Panizzi P, Fuentes-Prior P , et al. Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation. Nature 2003; 425 (6957) 535-539
    CrossrefPubMedGoogle Scholar
  • 142 Kroh HK, Panizzi P, Bock PE. Von Willebrand factor-binding protein is a hysteretic conformational activator of prothrombin. Proc Natl Acad Sci U S A 2009; 106 (19) 7786-7791
    CrossrefPubMedGoogle Scholar
  • 143 Bodén MK, Flock JI. Cloning and characterization of a gene for a 19 kDa fibrinogen-binding protein from Staphylococcus aureus. Mol Microbiol 1994; 12 (4) 599-606
    CrossrefPubMedGoogle Scholar
  • 144 Thomer L, Schneewind O, Missiakas D. Multiple ligands of von Willebrand factor-binding protein (vWbp) promote Staphylococcus aureus clot formation in human plasma. J Biol Chem 2013; 288 (39) 28283-28292
    CrossrefPubMedGoogle Scholar
  • 145 Collen D, Schlott B, Engelborghs Y , et al. On the mechanism of the activation of human plasminogen by recombinant staphylokinase. J Biol Chem 1993; 268 (11) 8284-8289
    PubMedGoogle Scholar
  • 146 Jin T, Bokarewa M, Foster T, Mitchell J, Higgins J, Tarkowski A. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J Immunol 2004; 172 (2) 1169-1176
    CrossrefPubMedGoogle Scholar
  • 147 Kwiecinski J, Jacobsson G, Karlsson M , et al. Staphylokinase promotes the establishment of Staphylococcus aureus skin infections while decreasing disease severity. J Infect Dis 2013; 208 (6) 990-999
    CrossrefPubMedGoogle Scholar
  • 148 Peetermans M, Vanassche T, Liesenborghs L , et al. Plasminogen activation by staphylokinase enhances local spreading of S. aureus in skin infections. BMC Microbiol 2014; 14: 310
    CrossrefPubMedGoogle Scholar
  • 149 Kwieciński J, Josefsson E, Mitchell J , et al. Activation of plasminogen by staphylokinase reduces the severity of Staphylococcus aureus systemic infection. J Infect Dis 2010; 202 (7) 1041-1049
    CrossrefPubMedGoogle Scholar
  • 150 Jin T, Bokarewa M, McIntyre L , et al. Fatal outcome of bacteraemic patients caused by infection with staphylokinase-deficient Staphylococcus aureus strains. J Med Microbiol 2003; 52 (Pt 10): 919-923
    CrossrefPubMedGoogle Scholar
  • 151 Kwiecinski J, Peetermans M, Liesenborghs L , et al. Staphylokinase control of staphylococcus aureus biofilm formation and detachment through host plasminogen activation. J Infect Dis 2016; 213 (1) 139-148
    CrossrefPubMedGoogle Scholar
  • 152 Sumby P, Waldor MK. Transcription of the toxin genes present within the Staphylococcal phage phiSa3ms is intimately linked with the phage's life cycle. J Bacteriol 2003; 185 (23) 6841-6851
    CrossrefPubMedGoogle Scholar
  • 153 Vanassche T, Verhaegen J, Peetermans WE , et al. Inhibition of staphylothrombin by dabigatran reduces Staphylococcus aureus virulence. J Thromb Haemost 2011; 9 (12) 2436-2446
    CrossrefPubMedGoogle Scholar
  • 154 Sawai T, Tomono K, Yanagihara K , et al. 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 (2) 466-471
    PubMedGoogle Scholar
  • 155 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 (4) 408-412
    PubMedGoogle Scholar
  • 156 Vanassche T, Peetermans M, Van Aelst LN , et al. The role of staphylothrombin-mediated fibrin deposition in catheter-related Staphylococcus aureus infections. J Infect Dis 2013; 208 (1) 92-100
    CrossrefPubMedGoogle Scholar
  • 157 Flick MJ, Du X, Prasad JM , et al. Genetic elimination of the binding motif on fibrinogen for the S. aureus virulence factor ClfA improves host survival in septicemia. Blood 2013; 121 (10) 1783-1794
    CrossrefPubMedGoogle Scholar
  • 158 Josefsson E, Higgins J, Foster TJ, Tarkowski A. Fibrinogen binding sites P336 and Y338 of clumping factor A are crucial for Staphylococcus aureus virulence. PLoS ONE 2008; 3 (5) e2206
    CrossrefPubMedGoogle Scholar
  • 159 Scully IL, Timofeyeva Y, Keeney D , et al. Demonstration of the preclinical correlate of protection for Staphylococcus aureus clumping factor A in a murine model of infection. Vaccine 2015; 33 (41) 5452-5457
    CrossrefPubMedGoogle Scholar
  • 160 Ugarova TP, Solovjov DA, Zhang L , et al. Identification of a novel recognition sequence for integrin alphaM beta2 within the gamma-chain of fibrinogen. J Biol Chem 1998; 273 (35) 22519-22527
    CrossrefPubMedGoogle Scholar
  • 161 Lishko VK, Kudryk B, Yakubenko VP, Yee VC, Ugarova TP. Regulated unmasking of the cryptic binding site for integrin alpha M beta 2 in the gamma C-domain of fibrinogen. Biochemistry 2002; 41 (43) 12942-12951
    CrossrefPubMedGoogle Scholar
  • 162 Aleman MM, Walton BL, Byrnes JR, Wolberg AS. Fibrinogen and red blood cells in venous thrombosis. Thromb Res 2014; 133 (Suppl. 01) S38-S40
    PubMedGoogle Scholar
  • 163 Loof TG, Mörgelin M, Johansson L , et al. Coagulation, an ancestral serine protease cascade, exerts a novel function in early immune defense. Blood 2011; 118 (9) 2589-2598
    CrossrefPubMedGoogle Scholar
  • 164 Tang YQ, Yeaman MR, Selsted ME. Antimicrobial peptides from human platelets. Infect Immun 2002; 70 (12) 6524-6533
    CrossrefPubMedGoogle Scholar
  • 165 Yeaman MR, Norman DC, Bayer AS. Staphylococcus aureus susceptibility to thrombin-induced platelet microbicidal protein is independent of platelet adherence and aggregation in vitro. Infect Immun 1992; 60 (6) 2368-2374
    PubMedGoogle Scholar
  • 166 Zhang X, Liu Y, Gao Y , et al. Inhibiting platelets aggregation could aggravate the acute infection caused by Staphylococcus aureus. Platelets 2011; 22 (3) 228-236
    CrossrefPubMedGoogle Scholar
  • 167 Yeaman MR. The role of platelets in antimicrobial host defense. Clin Infect Dis 1997; 25 (5) 951-968 , quiz 969–970
    CrossrefPubMedGoogle Scholar
  • 168 Yeaman MR. Bacterial-platelet interactions: virulence meets host defense. Future Microbiol 2010; 5 (3) 471-506
    CrossrefPubMedGoogle Scholar
  • 169 Yeaman MR. Platelets in defense against bacterial pathogens. Cell Mol Life Sci 2010; 67 (4) 525-544
    CrossrefPubMedGoogle Scholar
  • 170 Chapman GH, Berens C, Peters A, Curcio L. Coagulase and Hemolysin Tests as Measures of the Pathogenicity of Staphylococci. J Bacteriol 1934; 28 (4) 343-363
    PubMedGoogle Scholar
  • 171 Peacock SJ, Moore CE, Justice A , et al. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 2002; 70 (9) 4987-4996
    CrossrefPubMedGoogle Scholar
  • 172 Veloso TR, Mancini S, Giddey M , et al. Vaccination against Staphylococcus aureus experimental endocarditis using recombinant Lactococcus lactis expressing ClfA or FnbpA. Vaccine 2015; 33 (30) 3512-3517
    CrossrefPubMedGoogle Scholar
  • 173 Fowler Jr VG, Proctor RA. Where does a Staphylococcus aureus vaccine stand?. Clin Microbiol Infect 2014; 20 (Suppl. 05) 66-75
    CrossrefPubMedGoogle Scholar
  • 174 Colvin RB, Mosesson MW, Dvorak HF. Delayed-type hypersensitivity skin reactions in congenital afibrinogenemia lack fibrin deposition and induration. J Clin Invest 1979; 63 (6) 1302-1306
    CrossrefPubMedGoogle Scholar
  • 175 Huang SC, Yang YJ. Septic shock and hypofibrinogenemia predict a fatal outcome in childhood acute acalculous cholecystitis. J Pediatr Gastroenterol Nutr 2011; 53 (5) 548-552
    PubMedGoogle Scholar
  • 176 Edner J, Rudd E, Zheng C , et al. Severe bacteria-associated hemophagocytic lymphohistiocytosis in an extremely premature infant. Acta Paediatr 2007; 96 (11) 1703-1706
    CrossrefPubMedGoogle Scholar
  • 177 Datta Kanjilal S, Bagchi S. Acute osteomyelitis in congenital hypofibrinogenemia. Indian J Pediatr 2006; 73 (6) 529-530
    CrossrefPubMedGoogle Scholar