Role for the fibrinogen-binding proteins Coagulase and Efb in the Staphylococcus aureus–Candida interaction

Campoccia, 2006, The significance of infection related to orthopedic devices and issues of antibiotic resistance, Biomaterials, 27, 2331, 10.1016/j.biomaterials.2005.11.044 Carlson, 1982, Synergistic effect of Candida albicans and Staphylococcus aureus on mouse mortality, Infect. Immun., 38, 921, 10.1128/IAI.38.3.921-924.1982 Chavakis, 2005, Staphylococcus aureus interactions with the endothelium: the role of bacterial “secretable expanded repertoire adhesive molecules” (SERAM) in disturbing host defense systems, Thromb. Haemost., 94, 278, 10.1160/TH05-05-0306 Cheng, 2010, Contribution of coagulases towards Staphylococcus aureus disease and protective immunity, PLoS Pathog., 6 Clarke, 2006, Surface adhesins of Staphylococcus aureus, Adv. Microb. Physiol., 51, 187, 10.1016/S0065-2911(06)51004-5 Coleman, 1997, Candida dubliniensis, J. Clin. Microbiol., 35, 3011, 10.1128/JCM.35.11.3011-3012.1997 Corrigan, 2007, The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation, Microbiology, 153, 2435, 10.1099/mic.0.2007/006676-0 Costerton, 1985, Phenomena of bacterial adhesion Costerton, 1999, Bacterial biofilms: a common cause of persistent infections, Science, 284, 1318, 10.1126/science.284.5418.1318 Cramton, 1999, The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation, Infect. Immun., 67, 5427, 10.1128/IAI.67.10.5427-5433.1999 Dougherty, 1988, Pathobiology of infection in prosthetic devices, Rev. Infect. Dis., 10, 1102, 10.1093/clinids/10.6.1102 Fridkin, 1996, Epidemiology of nosocomial fungal infections, Clin. Microbiol. Rev., 9, 499, 10.1128/CMR.9.4.499 Friedrich, 2003, Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation, Nature, 425, 535, 10.1038/nature01962 Gallwitz, 2012, The extended cleavage specificity of human thrombin, PLoS ONE, 7, e31756, 10.1371/journal.pone.0031756 Gaur, 1997, Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins, Infect. Immun., 65, 5289, 10.1128/IAI.65.12.5289-5294.1997 Götz, 2002, Staphylococcus and biofilms, Mol. Microbiol., 43, 1367, 10.1046/j.1365-2958.2002.02827.x Grodberg, 1988, ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification, J. Bacteriol., 170, 1245, 10.1128/jb.170.3.1245-1253.1988 Guggenberger, 2012, Two distinct coagulase-dependent barriers protect Staphylococcus aureus from neutrophils in a three dimensional in vitro infection model, PLoS Pathog., 8, e1002434, 10.1371/journal.ppat.1002434 Harriott, 2009, Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance, Antimicrob. Agents Chemother., 53, 3914, 10.1128/AAC.00657-09 Heilmann, 2011, Adhesion mechanisms of staphylococci, 105, 10.1007/978-94-007-0940-9_7 Heilmann, 1996, Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation, Infect. Immun., 64, 277, 10.1128/IAI.64.1.277-282.1996 Heilmann, 2005, The multifunctional Staphylococcus aureus autolysin Aaa mediates adherence to immobilized fibrinogen and fibronectin, Infect. Immun., 73, 4793, 10.1128/IAI.73.8.4793-4802.2005 Heilmann, 2002, Platelet-binding domains in 2 fibrinogen-binding proteins of Staphylococcus aureus identified by phage display, J. Infect. Dis., 186, 32, 10.1086/341081 Heilmann, 1997, Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface, Mol. Microbiol., 24, 1013, 10.1046/j.1365-2958.1997.4101774.x Heilmann, 2004, Staphylococcus aureus fibronectin-binding protein (FnBP)-mediated adherence to platelets, and aggregation of platelets induced by FnBPA but not by FnBPB, J. Infect. Dis., 190, 321, 10.1086/421914 Heilmann, 1996, Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis, Mol. Microbiol., 20, 1083, 10.1111/j.1365-2958.1996.tb02548.x Hendrix, 1983, Activation of human prothrombin by stoichiometric levels of staphylocoagulase, J. Biol. Chem., 258, 3637, 10.1016/S0021-9258(18)32713-3 Hirschhausen, 2010, A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor, Cell. Microbiol., 12, 1746, 10.1111/j.1462-5822.2010.01506.x Hostetter, 1994, Adhesins and ligands involved in the interaction of Candida spp. with epithelial and endothelial surfaces, Clin. Microbiol. Rev., 7, 29, 10.1128/CMR.7.1.29 Hube, 2004, From commensal to pathogen: stage- and tissue-specific gene expression of Candida albicans, Curr. Opin. Microbiol., 7, 336, 10.1016/j.mib.2004.06.003 Jacobsson, 1996, Phage display shot-gun cloning of ligand-binding domains of prokaryotic receptors approaches 100% correct clones, Biotechniques, 20, 1070, 10.2144/96206rr04 Jacobsson, 2003, Shotgun phage display – selection for bacterial receptins or other exported proteins, Biol. Proced. Online, 5, 123, 10.1251/bpo54 Klotz, 2007, Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature, Diagn. Microbiol. Infect. Dis., 59, 401, 10.1016/j.diagmicrobio.2007.07.001 Kuhn, 2002, Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces, Infect. Immun., 70, 878, 10.1128/IAI.70.2.878-888.2002 Lee, 2004, Inhibition of complement activation by a secreted Staphylococcus aureus protein, J. Infect. Dis., 190, 571, 10.1086/422259 Lee, 2004, Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb), J. Biol. Chem., 279, 50710, 10.1074/jbc.M408570200 Li, 2003, EAP1, a Candida albicans gene involved in binding human epithelial cells, Eukaryot. Cell., 2, 1266, 10.1128/EC.2.6.1266-1273.2003 Mack, 1996, The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis, J. Bacteriol., 178, 175, 10.1128/jb.178.1.175-183.1996 Mollnes, 2002, Essential role of the C5a receptor in E coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation, Blood, 100, 1869 Moreillon, 1995, Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis, Infect. Immun., 63, 4738, 10.1128/IAI.63.12.4738-4743.1995 Novick, 1963, Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus, Virology, 33, 155, 10.1016/0042-6822(67)90105-5 O’Connor, 2005, Quantification of ALS1 gene expression in Candida albicans biofilms by RT-PCR using hybridisation probes on the LightCycler, Mol. Cell. Probes, 19, 153, 10.1016/j.mcp.2004.10.007 O’Neill, 2008, A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB, J. Bacteriol., 190, 3835, 10.1128/JB.00167-08 Palma, 1996, Lack of the extracellular 19-kilodalton fibrinogen-binding protein from Staphylococcus aureus decreases virulence in experimental wound infection, Infect. Immun., 64, 5284, 10.1128/IAI.64.12.5284-5289.1996 Panizzi, 2004, The staphylocoagulase family of zymogen activator and adhesion proteins, Cell. Mol. Life Sci., 61, 2793, 10.1007/s00018-004-4285-7 Peters, 1982, Adherence and growth of coagulase-negative staphylococci on surfaces of intravenous catheters, J. Infect. Dis., 146, 479, 10.1093/infdis/146.4.479 Pfaller, 1999, Diagn. Microbiol. Infect. Dis., 35, 19, 10.1016/S0732-8893(99)00046-2 Pittet, 1993, Association of secondary and polymicrobial nosocomial bloodstream infections with higher mortality, Eur. J. Clin. Microbiol. Infect. Dis., 12, 813, 10.1007/BF02000400 Ramage, 2001, Biofilm formation by Candida dubliniensis, J. Clin. Microbiol., 39, 3234, 10.1128/JCM.39.9.3234-3240.2001 Ramage, 2002, In vitro pharmacodynamic properties of three antifungal agents against preformed Candida albicans biofilms determined by time-kill studies, Antimicrob. Agents Chemother., 46, 3634, 10.1128/AAC.46.11.3634-3636.2002 Rohde, 2005, Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases, Mol. Microbiol., 55, 1883, 10.1111/j.1365-2958.2005.04515.x Rooijakkers, 2005, Staphylococcal innate immune evasion, Trends Microbiol., 13, 596, 10.1016/j.tim.2005.10.002 Sambrook, 1989 Sawai, 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, 10.1128/IAI.65.2.466-471.1997 Schmalreck, 2012, Species and susceptibility distribution of 1062 clinical yeast isolates to azoles, echinocandins, flucytosine and amphotericin B from a multi-centre study, Mycoses, 55, e124, 10.1111/j.1439-0507.2011.02165.x Schroeder, 2009, Molecular characterization of a novel Staphylococcus aureus surface protein (SasC) involved in cell aggregation and biofilm accumulation, PLoS ONE, 4, e7567, 10.1371/journal.pone.0007567 Shannon, 2004, Extracellular fibrinogen binding protein, Efb, from Staphylococcus aureus binds to platelets and inhibits platelet aggregation, Thromb. Haemost., 91, 779, 10.1160/TH03-05-0287 Sheppard, 2004, Functional and structural diversity in the Als protein family of Candida albicans, J. Biol. Chem., 279, 30480, 10.1074/jbc.M401929200 Shirtliff, 2009, Cross-kingdom interactions: Candida albicans and bacteria, FEMS Microbiol. Lett., 299, 1, 10.1111/j.1574-6968.2009.01668.x Staab, 2004, Expression of transglutaminase substrate activity on Candida albicans germ tubes through a coiled, disulfide-bonded N-terminal domain of Hwp1 requires C-terminal glycosylphosphatidylinositol modification, J. Biol. Chem., 279, 40737, 10.1074/jbc.M406005200 von Eiff, 2005, Infections associated with medical devices: pathogenesis, management and prophylaxis, Drugs, 65, 179, 10.2165/00003495-200565020-00003 Wann, 2000, The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen, J. Biol. Chem., 275, 13863, 10.1074/jbc.275.18.13863 Wargo, 2006, Fungal – bacterial interactions: a mixed bag of mingling microbes, Curr. Opin. Microbiol., 9, 359, 10.1016/j.mib.2006.06.001 Wey, 1988, Hospital-acquired candidemia. The attributable mortality and excess length of stay, Arch. Intern. Med., 148, 2642, 10.1001/archinte.1988.00380120094019 Wisplinghoff, 2004, Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study, Clin. Infect. Dis., 39, 309, 10.1086/421946 Wos-Oxley, 2010, A poke into the diversity and associations within human anterior nare microbial communities, ISME J., 4, 839, 10.1038/ismej.2010.15