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DOI: 10.1160/TH05-04-0235
Mechanism and consequences of invasion of endothelial cells by Staphylococcus aureus
Publication History
Received: 05 April 2005
Accepted after major revision: 01 July 2005
Publication Date:
05 December 2017 (online)
Summary
It has become clear that Staphylococcus aureus is a facultative intracellular microorganism. Adherence and invasion are a prerequisite for endovascular infections caused by S. aureus, such as infective endocarditis. These phenomena may also be involved in the pathogenesis of invasive and metastatic infection upon hematogenous dissemination, such as osteomyelitis and abscess formation. The underlying molecular mechanism has been elucidated in detail, including its likely relevance in vivo. However, the mode of action of recently identified modulators of invasion, such as pls/Pls have not yet been clarified. The potential outcome for host cells and S. aureus following invasion are diverse. Surprisingly, induction of apoptosis in human endothelial cells is more complex than previously thought, since it appears to involve multiple virulence factors. In the light of increasing resistance to antimicrobial therapy, understanding the multifacetted pathogenesis of S. aureus infection in detail is needed for a better prevention and therapy.
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References
- 1 Lowy FD. Staphylococcus aureus infections. N Engl J Med 1998; 339: 520-32.
- 2 von Eiff C, Becker K, Machka K. et al. Nasal carriage as a journal-title of Staphylococcus aureus bacteremia. N Engl J Med 2001; 344: 11-6.
- 3 Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus?. Trends Microbiol 2001; 9: 605-10.
- 4 Luzar MA, Coles GA, Faller B. et al. Staphylococcus aureus nasal carriage and infection in patients on continuous ambulatory peritoneal dialysis. N Engl J Med 1990; 322: 505-9.
- 5 Maki DG. Risk factors for nosocomial infection in intensive care. ‘Devices vs. nature’ and goals for the next decade. Arch Intern Med 1989; 149: 30-5.
- 6 Schaberg DR, Culver DH, Gaynes RP. Major trends in the microbial etiology of nosocomial infection. Am J Med 1991; 91: 72S-5S.
- 7 Waldvogel FA. Staphylococcus aureus (including toxic shock syndrome). Principles and Practice of Infectious Diseases.. Churchill Livingstone: 1995: 1754-76.
- 8 Verhoef J, Fluit AC, Schmitz F-J. Staphylococci and other Micrococcaceae. Infectious Diseases.. Mosby: 2004: 2119-32.
- 9 Lew DP, Waldvogel FA. Osteomyelitis. N Engl J Med 1997; 336: 999-1007.
- 10 Foster TJ, Höök M. Surface protein adhesins of Staphylococcus aureus . Trends Microbiol 1998; 6: 484-8.
- 11 Yeaman MR. The role of platelets in antimicrobial host defense. Clin Infect Dis 1997; 25: 951-68.
- 12 Vaudaux P, Yasuda H, Velazco MI. et al. Role of host and bacterial factors in modulating staphylococcal adhesion to implanted polymer surfaces. J Biomater Appl 1990; 5: 134-53.
- 13 Ing MB, Baddour L, Bayer AS. Bacteremia and infective endocarditis: Pathogenesis, diagnosis, and complications. The staphylococci in human disease.. Churchill Livingstone: 1997: 331-54.
- 14 Patti JM, Allen BL, McGavin MJ. et al. MSCRAMMmediated adherence of microorganisms to host tissues. Annu Rev Microbiol 1994; 48: 585-617.
- 15 Yeaman MR, Bayer AS. Staphylococcus aureus, platelets, and the heart. Curr Infect Dis Rep 2000; 2: 281-98.
- 16 Hamill RJ, Vann JM, Proctor RA. Phagocytosis of Staphylococcus aureus by cultured bovine aortic endothelial cells: model for postadherence events in endovascular infections. Infect Immun 1986; 54: 833-6.
- 17 Vann JM, Proctor RA. Ingestion of Staphylococcus aureus by bovine endothelial cells results in time- and inoculum-dependent damage to endothelial cell monolayers. Infect Immun 1987; 55: 2155-63.
- 18 Vann JM, Proctor RA. Cytotoxic effects of ingested Staphylococcus aureus on bovine endothelial cells: role of S. aureus α-hemolysin. Microb Pathog 1988; 4: 443-53.
- 19 Kuroda M, Ohta T, Uchiyama I. et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus . Lancet 2001; 357: 1225-40.
- 20 Baba T, Takeuchi F, Kuroda M. et al. Genome and virulence determinants of high virulence communityacquired MRSA. Lancet 2002; 359: 1819-27.
- 21 Holden MT, Feil EJ, Lindsay JA. et al. Complete genomes of two clinical Staphylococcus aureus strains: Evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA 2004; 101: 9786-91.
- 22 Novick RP, Schlievert P, Ruzin A. Pathogenicity and resistance islands of staphylococci. Microbes Infect 2001; 3: 585-94.
- 23 Novick RP. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus . Plasmid 2003; 49: 93-105.
- 24 Bohach GA, Dinges MM, Mitchell DT. et al. Exotoxins. The staphylococci in human disease.. Churchill Livingstone: 1997: 83-111.
- 25 Bohach GA, Foster TJ. Staphylococcus aureus exotoxins. Gram-positive pathogens.. ASM Press; 2000: 367-78.
- 26 Arvidson S. Extracellular enzymes. Gram-positive pathogens.. ASM Press; 2000: 379-85.
- 27 Bronner S, Monteil H, Prévost G. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev 2004; 28: 183-200.
- 28 Steinhuber A, Goerke C, Bayer MG. et al. Molecular architecture of the regulatory locus sae of Staphylococcus aureus and its impact on expression of virulence factors. J Bacteriol 2003; 185: 6278-86.
- 29 Kleerebezem M, Quadri LE, Kuipers OP. et al. Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol Microbiol 1997; 24: 895-904.
- 30 Hastings JW, Greenberg EP. Quorum sensing: the explanation of a curious phenomenon reveals a common characteristic of bacteria. J Bacteriol 1999; 181: 2667-8.
- 31 Cheung AL, Projan SJ, Gresham H. The genomic aspect of virulence, sepsis, and resistance to killing mechanisms in Staphylococcus aureus . Curr Infect Dis Rep 2002; 4: 400-10.
- 32 Cheung AL, Bayer AS, Zhang G. et al. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus . FEMS Immunol Med Microbiol 2004; 40: 1-9.
- 33 Clarke SR, Wiltshire MD, Foster SJ. IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol Microbiol 2004; 51: 1509-19.
- 34 Weidenmaier C, Peschel A, Xiong YQ. et al. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 2005; 191: 1771-7.
- 35 Roche FM, Massey R, Peacock SJ. et al. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology SGM 2003; 149: 643-54.
- 36 Lowy FD. Is Staphylococcus aureus an intracellular pathogen?. Trends Microbiol 2000; 8: 341-3.
- 37 Sinha B, François PP, Nüße O. et al. Fibronectinbinding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin α5β1. Cell Microbiol 1999; 1: 101-17.
- 38 Dziewanowska K, Patti JM, Deobald CF. et al. Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aur- eus by epithelial cells. Infect Immun 1999; 67: 4673-8.
- 39 Peacock SJ, Foster TJ, Cameron BJ. et al. Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology SGM 1999; 145: 3477-86.
- 40 Lammers A, Nuijten PJ, Smith HE. The fibronectin binding proteins of Staphylococcus aureus are required for adhesion to and invasion of bovine mammary gland cells. FEMS Microbiol Lett 1999; 180: 103-9.
- 41 Sinha B, François PP, Que Y-A. et al. Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect Immun 2000; 68: 6871-8.
- 42 Liang OD, Flock JI, Wadström T. Isolation and characterisation of a vitronectin-binding surface protein from Staphylococcus aureus . Biochim Biophys Acta 1995; 1250: 110-6.
- 43 Mongodin E, Bajolet O, Cutrona J. et al. Fibronectin- binding proteins of Staphylococcus aureus are involved in adherence to human airway epithelium. Infect Immun 2002; 70: 620-30.
- 44 Rice K, Huesca M, Vaz D. et al. Variance in fibronectin binding and fnb locus polymorphisms in Staphylococcus aureus: identification of antigenic variation in a fibronectin binding protein adhesin of the epidemic CMRSA-1 strain of methicillin-resistant S. aureus. Infect Immun 2001; 69: 3791-9.
- 45 Peacock SJ, Day NP, Thomas MG. et al. Clinical isolates of Staphylococcus aureus exhibit diversity in fnb genes and adhesion to human fibronectin. J Infect 2000; 41: 23-31.
- 46 Smeltzer MS, Gillaspy AF, Pratt FL. Jr. et al. Prevalence and chromosomal map location of Staphylococcus aureus adhesin genes. Gene 1997; 196: 249-59.
- 47 Minhas T, Ludlam HA, Wilks M. et al. Detection by PCR and analysis of the distribution of a fibronectinbinding protein gene (fbn) among staphylococcal isolates. J Med Microbiol 1995; 42: 96-101.
- 48 Shopsin B, Gomez M, Montgomery SO. et al. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 1999; 37: 3556-63.
- 49 Hussain M, Becker K, von Eiff C. et al. Analogs of Eap protein are conserved and prevalent in clinical Staphylococcus aureus isolates. Clin Diagn Lab Immunol 2001; 8: 1271-6.
- 50 Hussain M, Becker K, von Eiff C. et al. 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: 6778-86.
- 51 Mazmanian SK, Liu G, Ton-That H. et al. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 1999; 285: 760-3.
- 52 Navarre WW, Schneewind O. Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria. Mol Microbiol 1994; 14: 115-21.
- 53 Hildén P, Savolainen K, Tyynelä J. et al. Purification and characterisation of a plasmin-sensitive surface protein of Staphylococcus aureus . Eur J Biochem 1996; 236: 904-10.
- 54 Espersen F, Clemmensen I. Clumping of Staphylococcus aureus by human fibronectin. Acta Pathol Microbiol Scand [B] 1981; 89: 317-21.
- 55 Fröman G, Switalski LM, Speziale P. et al. Isolation and characterization of a fibronectin receptor from Staphylococcus aureus . J Biol Chem 1987; 262: 6564-71.
- 56 Flock JI, Fröman G, Jönsson K. et al. Cloning and expression of the gene for a fibronectin-binding protein from Staphylococcus aureus . EMBO J 1987; 6: 2351-7.
- 57 Signäs C, Raucci G, Jönsson K. et al. Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc Natl Acad Sci U S A 1989; 86: 699-703.
- 58 Jönsson K, Signäs C, Müller HP. et al. Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem 1991; 202: 1041-8.
- 59 Fowler T, Wann ER, Joh D. et al. Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell β1 integrins. Eur J Cell Biol 2000; 79: 672-9.
- 60 Massey RC, Kantzanou MN, Fowler T. et al. Fibronectin- binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell Microbiol 2001; 3: 839-51.
- 61 Mosher DF, Proctor RA. Binding and factor XIIIamediated cross-linking of a 27-kilodalton fragment of fibronectin to Staphylococcus aureus . Science 1980; 209: 927-9.
- 62 Schwarz-Linek U, Werner JM, Pickford AR. et al. Pathogenic bacteria attach to human fibronectin through a tandem β-zipper. Nature 2003; 423: 177-81.
- 63 Wann ER, Gurusiddappa S, Höök M. The fibronectin- binding MSCRAMM FnBPA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 2000; 275: 13863-71.
- 64 Heilmann C, Niemann S, Sinha B. et al. Staphylococcus aureus Fibronectin-binding Protein (FnBP)- mediated adherence to platelets, and aggregation of platelets induced by FnBPA, but not by FnBPB. J Infect Dis 2004; 190: 321-9.
- 65 Miyamoto YJ, Wann ER, Fowler T. et al. Fibronectin- binding protein A of Staphylococcus aureus can mediate human T lymphocyte adhesion and coactivation. J Immunol 2001; 166: 5129-38.
- 66 Que YA, François P, Haefliger JA. et al. Reassessing the role of Staphylococcus aureus clumping factor and fibronectin-binding protein by expression in Lactococcus lactis. Infect Immun 2001; 69: 6296-302.
- 67 Savolainen K, Paulin L, Westerlund-Wikstrom B. et al. Expression of pls, a gene closely associated with the mecA gene of methicillin-resistant Staphylococcus aureus, prevents bacterial adhesion in vitro. Infect Immun 2001; 69: 3013-20.
- 68 Juuti KM, Sinha B, Werbick C. et al. Reduced adherence and host cell invasion by methicillin-resistant Staphylococcus aureus expressing the surface protein Pls. J Infect Dis 2004; 189: 1574-84.
- 69 Roche FM, Meehan M, Foster TJ. The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology SGM 2003; 149: 2759-67.
- 70 Chavakis T, Wiechmann K, Preissner KT. et al. Staphylococcus aureus interactions with the endothelium: The role of bacterial ‘‘secretable expanded repertoire adhesive molecules” (SERAM) in disturbing host defense systems. Thromb Haemost 2005; 94: 278-85.
- 71 Flock M, Flock JI. Rebinding of extracellular adherence protein Eap to Staphylococcus aureus can occur through a surface-bound neutral phosphatase. J Bacteriol 2001; 183: 3999-4003.
- 72 Clarke SR, Harris LG, Richards RG. et al. Analysis of Ebh, a 1.1-megadalton cell wall-associated fibronectin- binding protein of Staphylococcus aureus . Infect Immun 2002; 70: 6680-7.
- 73 Harraghy N, Hussain M, Haggar A. et al. The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology SGM 2003; 149: 2701-07.
- 74 Aumailley M, Gayraud B. Structure and biological activity of the extracellular matrix. J Mol Med 1998; 76: 253-65.
- 75 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: 2840-5.
- 76 Jönsson K, McDevitt D, McGavin MH. et al. Staphylococcus aureus expresses a major histocompatibility complex class II analog. J Biol Chem 1995; 270: 21457-60.
- 77 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: 687-93.
- 78 Menzies BE, Kourteva I. Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect Immun 1998; 66: 5994-8.
- 79 Lowy FD, Fant J, Higgins LL. et al. Staphylococcus aureus-human endothelial cell interactions. J Ultrastruct Mol Struct Res 1988; 98: 137-46.
- 80 Ogawa SK, Yurberg ER, Hatcher VB. et al. Bacterial adherence to human endothelial cells in vitro. Infect Immun 1985; 50: 218-24.
- 81 Tompkins DC, Blackwell LJ, Hatcher VB. et al. Staphylococcus aureus proteins that bind to human endothelial cells. Infect Immun 1992; 60: 965-9.
- 82 Tompkins DC, Hatcher VB, Patel D. et al. A human endothelial cell membrane protein that binds Staphylococcus aureus in vitro. J Clin Invest 1990; 85: 1248-54.
- 83 Grundmeier M, Hussain M, Becker P. et al. Staphylococcus aureus strain Newman expresses truncated Fibronectin-Binding Proteins, which are not cell wallanchored, leading to a deficient adherence and host cell invasion. Infect Immun 2004; 72: 7155-63.
- 84 Lyons C. Bacteremic staphylococal infection. Surg Gynecol Obstet 1942; 74: 41-6.
- 85 Smith JM, Dubos RJ. The behavior of virulent and avirulent staphylococci in the tissues of normal mice. J Exp Med 1956; 103: 87-108.
- 86 Smith IM, Wilson AP, Hazard ECH. et al. Death from staphylococci in mice. J Infect Dis 1960; 107: 369-78.
- 87 Sinha B, Herrmann M, Krause KH. Is Staphylococcus aureus an intracellular pathogen? – Response. Trends Microbiol 2000; 8: 343-44.
- 88 Ellington JK, Elhofy A, Bost KL. et al. Involvement of mitogen-activated protein kinase pathways in Staphylococcus aureus invasion of normal osteoblasts. Infect Immun 2001; 69: 5235-42.
- 89 Fowler T, Johansson S, Wary KK. et al. Src kinase has a central role in in vitro cellular internalization of Staphylococcus aureus . Cell Microbiol 2003; 5: 417-26.
- 90 Agerer F, Michel A, Ohlsen K. et al. Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J Biol Chem 2003; 278: 42524-31.
- 91 Que YA, Haefliger J-A, Piroth L. et al. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med 2005; 201: 1627-35.
- 92 Hudson MC, Ramp WK, Nicholson NC. et al. Internalization of Staphylococcus aureus by cultured osteoblasts. Microb Pathog 1995; 19: 409-19.
- 93 Jett BD, Gilmore MS. Internalization of Staphylococcus aureus by human corneal epithelial cells: role of bacterial fibronectin-binding protein and host cell factors. Infect Immun 2002; 70: 4697-700.
- 94 Schwarz-Linek U, Höök M, Potts JR. The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol Microbiol 2004; 52: 631-41.
- 95 Kullik I, Giachino P, Fuchs T. Deletion of the alternative σ factor σB in Staphylococcus aureus reveals its function as a global regulator of virulence genes. J Bacteriol 1998; 180: 4814-20.
- 96 Hussain M, Haggar A, Heilmann C. et al. Insertional inactivation of Eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect Immun 2002; 70: 2933-40.
- 97 Kreikemeyer B, McDevitt D, Podbielski A. The role of the Map protein in Staphylococcus aureus matrix protein and eukaryotic cell adherence. Int J Med Microbiol 2002; 292: 283-95.
- 98 Haggar A, Hussain M, Lonnies H. et al. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect Immun 2003; 71: 2310-17.
- 99 Becker P, Grundmeier M, Heilmann C. et al. An S. aureus clpC mutant displays reduced invasiveness for host cells but normal biofilm formation. 10th International Symposium on Staphylococci and Staphylococcal Infections. Tsukuba, Japan: October 2002, Abstract and Poster 225-03 2002;
- 100 Kahl BC, Goulian M, van Wamel W. et al. Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line. Infect Immun 2000; 68: 5385-92.
- 101 Qazi SN, Harrison SE, Self T. et al. Real-time monitoring of intracellular Staphylococcus aureus replication. J Bacteriol 2004; 186: 1065-77.
- 102 Chatterjee I, Becker P, Grundmeier M. et al. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J Bacteriol 2005; 187: 4488-96.
- 103 Bayles KW, Wesson CA, Liou LE. et al. Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect Immun 1998; 66: 336-42.
- 104 Deitch EA, Haskel Y, Cruz N. et al. Caco-2 and IEC-18 intestinal epithelial cells exert bactericidal activity through an oxidant-dependent pathway. Shock 1995; 4: 345-50.
- 105 Bánfi B, Maturana A, Jaconi S. et al. A mammalian H+ channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 2000; 287: 138-42.
- 106 Hess DJ, Henry-Stanley MJ, Erickson EA. et al. Intracellular survival of Staphylococcus aureus within cultured enterocytes. J Surg Res 2003; 114: 42-9.
- 107 Bantel H, Sinha B, Domschke W. et al. α-Toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J Cell Biol 2001; 155: 637-48.
- 108 Haslinger B, Strangfeld K, Peters G. et al. Staphylococcus aureus α-toxin induces apoptosis in peripheral blood mononuclear cells: role of endogenous tumour necrosis factor-α and the mitochondrial death pathway. Cell Microbiol 2003; 5: 729-41.
- 109 Essmann F, Bantel H, Totzke G. et al. Staphylococcus aureus α-toxin-induced cell death: predominant necrosis despite apoptotic caspase activation. Cell Death Differ 2003; 10: 1260-72.
- 110 Haslinger-Löffler B, Kahl BC, Grundmeier M. et al. Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell Microbiol 2005; 7: 1087-97.
- 111 McGavin MJ, Zahradka C, Rice K. et al. Modification of the Staphylococcus aureus fibronectin binding phenotype by V8 protease. Infect Immun 1997; 65: 2621-8.
- 112 McDevitt D, Foster TJ. Variation in the size of the repeat region of the fibrinogen receptor (clumping factor) of Staphylococcus aureus strains. Microbiology 1995; 141: 937-43.
- 113 van Belkum A, Riewerts EN, Sijmons M. et al. Are variable repeats in the spa gene suitable targets for epidemiological studies of methicillin-resistant Staphylococcus aureus strains?. Eur J Clin Microbiol Infect Dis 1996; 15: 768-70.
- 114 Smeltzer MS, Gillaspy AF, Pratt FL. et al. Comparative evaluation of use of cna, fnbA, fnbB, and hlb for genomic fingerprinting in the epidemiological typing of Staphylococcus aureus . J Clin Microbiol 1997; 35: 2444-9.
- 115 Enright MC, Day NP, Davies CE. et al. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus . J Clin Microbiol 2000; 38: 1008-15.
- 116 Shopsin B, Gomez M, Waddington M. et al. Use of coagulase gene (coa) repeat region nucleotide sequences for typing of methicillin-resistant Staphylococcus aureus strains. J Clin Microbiol 2000; 38: 3453-6.
- 117 Harmsen D, Claus H, Witte W. et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 2003; 41: 5442-8.
- 118 van Belkum A, Riewarts Eriksen NH, Sijmons M. et al. Coagulase and protein A polymorphisms do not contribute to persistence of nasal colonisation by Staphylococcus aureus . J Med Microbiol 1997; 46: 222-32.
- 119 Mostov K, Su T, ter Beest M. Polarized epithelial membrane traffic: conservation and plasticity. Nat Cell Biol 2003; 5: 287-93.
- 120 Mongodin E, Bajolet O, Hinnrasky J. et al. Cell wall-associated protein A as a tool for immunolocalization of Staphylococcus aureus in infected human airway epithelium. J Histochem Cytochem 2000; 48: 523-34.
- 121 Laschke MW, Kerdudou S, Herrmann M. et al. Intravital fluorescence microscopy: a novel tool for the study of the interaction of Staphylococcus aureus with the microvascular endothelium in vivo. J Infect Dis 2005; 191: 435-43.
- 122 Strindhall J, Lindgren PE, Lofgren S. et al. Clinical isolates of Staphylococcus aureus vary in ability to stimulate cytokine expression in human endothelial cells. Scand J Immunol 2005; 61: 57-62.
- 123 Soderquist B, Kallman J, Holmberg H. et al. Secretion of IL-6, IL-8 and G-CSF by human endothelial cells in vitro in response to Staphylococcus aureus and staphylococcal exotoxins. APMIS 1998; 106: 1157-64.
- 124 Yao L, Lowy FD, Berman JW. Interleukin-8 gene expression in Staphylococcus aureus-infected endothelial cells. Infect Immun 1996; 64: 3407-9.
- 125 Yao L, Bengualid V, Lowy FD. et al. Internalization of Staphylococcus aureus by endothelial cells induces cytokine gene expression. Infect Immun 1995; 63: 1835-9.
- 126 Bengualid V, Hatcher VB, Diamond B. et al. Staphylococcus aureus infection of human endothelial cells potentiates Fc receptor expression. J Immunol 1990; 145: 4279-83.
- 127 Strindhall J, Lindgren PE, Lofgren S. et al. Variations among clinical isolates of Staphylococcus aureus to induce expression of E-selectin and ICAM-1 in human endothelial cells. FEMS Immunol Med Microbiol 2002; 32: 227-35.
- 128 Proctor RA, Christman G, Mosher DF. Fibronectin- induced agglutination of Staphylococcus aureus correlates with invasiveness. J Lab Clin Med 1984; 104: 455-69.
- 129 Li D, Renzoni A, Estoppey T. et al. Induction of fibronectin adhesins in quinolone-resistant Staphylococcus aureus by subinhibitory levels of ciprofloxacin or by σB transcription factor activity is mediated by two separate pathways. Antimicrob Agents Chemother 2005; 49: 916-24.
- 130 Reilly SS, Hudson MC, Kellam JF. et al. In vivo internalization of Staphylococcus aureus by embryonic chick osteoblasts. Bone 2000; 26: 63-70.
- 131 Vaudaux P, François P, Bisognano C. et al. Increased expression of clumping factor and fibronectinbinding proteins by hemB mutants of Staphylococcus aureus expressing small colony variant phenotypes. Infect Immun 2002; 70: 5428-37.
- 132 Vesga O, Groeschel MC, Otten MF. et al. Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J Infect Dis 1996; 173: 739-42.
- 133 Balwit JM, van Langevelde P, Vann JM. et al. Gentamicin- resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J Infect Dis 1994; 170: 1033-7.
- 134 Proctor RA, Peters G. Small colony variants in staphylococcal infections: diagnostic and therapeutic implications. Clin Infect Dis 1998; 27: 419-22.
- 135 Johansson A, Flock JI, Svensson O. Collagen and fibronectin binding in experimental staphylococcal osteomyelitis. Clin Orthop 2001; 382: 241-6.
- 136 Ellington JK, Reilly SS, Ramp WK. et al. Mechanisms of Staphylococcus aureus invasion of cultured osteoblasts. Microb Pathog 1999; 26: 317-23.
- 137 Entenza JM, Foster TJ, Ni ED. et al. Contribution of clumping factor B to pathogenesis of experimental endocarditis due to Staphylococcus aureus . Infect Immun 2000; 68: 5443-6.
- 138 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: 4738-43.
- 139 Sullam PM, Bayer AS, Foss WM. et al. Diminished platelet binding in vitro by Staphylococcus aureus is associated with reduced virulence in a rabbit model of infective endocarditis. Infect Immun 1996; 64: 4915-21.
- 140 Xiong YQ, Bayer AS, Yeaman MR. et al. Impacts of sarA and agr in Staphylococcus aureus strain Newman on fibronectin-binding protein A gene expression and fibronectin adherence capacity in vitro and in experimental infective endocarditis. Infect Immun 2004; 72: 1832-6.
- 141 O’Brien L, Kerrigan SW, Kaw G. et al. Multiple mechanisms for the activation of human platelet aggregation by Staphylococcus aureus: roles for the clumping factors ClfA and ClfB, the serine-aspartate repeat protein SdrE and protein A. Mol Microbiol 2002; 44: 1033-44.
- 142 Menzies BE, Kourteva Y, Kaiser AB. et al. Inhibition of staphylococcal wound infection and potentiation of antibiotic prophylaxis by a recombinant fragment of the fibronectin-binding protein of Staphylococcus aureus . J Infect Dis 2002; 185: 937-43.
- 143 Lee JC. The prospects for developing a vaccine against Staphylococcus aureus . Trends Microbiol 1996; 4: 162-6.
- 144 Ciborowski P, Flock JI, Wadström T. Immunological response to a Staphylococcus aureus fibronectinbinding protein. J Med Microbiol 1992; 37: 376-81.
- 145 Schennings T, Heimdahl A, Coster K. et al. Immunization with fibronectin binding protein from Staphylococcus aureus protects against experimental endocarditis in rats. Microb Pathog 1993; 15: 227-36.
- 146 Rozalska B, Wadström T. Protective opsonic activity of antibodies against fibronectin-binding pro- teins (FnBPs) of Staphylococcus aureus . Scand J Immunol 1993; 37: 575-80.
- 147 Mamo W, Bodén M, Flock JI. Vaccination with Staphylococcus aureus fibrinogen binding proteins (FgBPs) reduces colonisation of S. aureus in a mouse mastitis model. FEMS Immunol Med Microbiol 1994; 10: 47-53.
- 148 Mamo W, Jonsson P, Flock JI. et al. Vaccination against Staphylococcus aureus mastitis: immunological response of mice vaccinated with fibronectin-binding protein (FnBP-A) to challenge with S. aureus. Vaccine 1994; 12: 988-92.
- 149 Mamo W, Jonsson P, Müller HP. Opsonization of Staphylococcus aureus with a fibronectin-binding protein antiserum induces protection in mice. Microb Pathog 1995; 19: 49-55.
- 150 Speziale P, Joh D, Visai L. et al. A monoclonal antibody enhances ligand binding of fibronectin MSCRAMM (adhesin) from Streptococcus dysgalactiae. J Biol Chem 1996; 271: 1371-8.
- 151 House-Pompeo K, Xu Y, Joh D. et al. Conformational changes in the fibronectin binding MSCRAMMs are induced by ligand binding. J Biol Chem 1996; 271: 1379-84.
- 152 Casolini F, Visai L, Joh D. et al. Antibody response to fibronectin-binding adhesin FnBPA in patients with Staphylococcus aureus infections. Infect Immun 1998; 66: 5433-42.
- 153 Huesca M, Sun Q, Peralta R. et al. Synthetic peptide immunogens elicit polyclonal and monoclonal antibodies specific for linear epitopes in the D motifs of Staphylococcus aureus Fibronectin-binding Protein, which are composed of amino acids that are essential for fibronectin binding. Infect Immun 2000; 68: 1156-63.
- 154 Sun Q, Smith GM, Zahradka C. et al. Identification of D motif epitopes in Staphylococcus aureus fibronectin- binding protein for the production of antibody inhibitors of fibronectin binding. Infect Immun 1997; 65: 537-43.
- 155 Vernachio J, Bayer AS, Le T. et al. Anti-clumping factor A immunoglobulin reduces the duration of methicillin-resistant Staphylococcus aureus bacteremia in an experimental model of infective endocarditis. Antimicrob Agents Chemother 2003; 47: 3400-6.
- 156 Kupferwasser LI, Vernachio J, Ames B. et al. Efficacy of a clumping factor (ClfA)-based vaccine in mitigating experimental methicillin-resistant Staphylococcus aureus endocarditis. 103rd General Meeting, American Society for Microbiology. Washington, USA: May 2003, Abstract, Poster D-241.
- 157 Uhlén M, Guss B, Nilsson B. et al. Complete sequence of the staphylococcal gene encoding protein A: a gene evolved through multiple duplications. J Biol Chem 1984; 259: 1695-702.
- 158 Herrmann M, Hartleib J, Kehrel B. et al. Interaction of von Willebrand factor with Staphylococcus aureus . J Infect Dis 1997; 176: 984-91.
- 159 Hartleib J, Köhler N, Dickinson RB. et al. Protein A is the von Willebrand factor-binding protein on Staphylococcus aureus . Blood 2000; 96: 2149-56.
- 160 Ray PK, Das T, Sa G. et al. Protection of apoptotic cell death by protein A. Apoptosis 2000; 5: 509-14.
- 161 Silverman GJ, and Goodyear CS. A model B-cell superantigen and the immunobiology of B lymphocytes. Clin Immunol 2002; 102: 117-34.
- 162 Gomez MI, Lee A, Reddy B. et al. Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 2004; 10: 842-48.
- 163 Mazmanian SK, Ton-That H, Schneewind O. Sortase- catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus . Mol Microbiol 2001; 40: 1049-57.
- 164 Bodén MK, Flock JI. Cloning and characterization of a gene for a 19 kDa fibrinogen-binding protein from Staphylococcus aureus . Mol Microbiol 1994; 12: 599-606.
- 165 Palma M, Wade D, Flock M. et al. Multiple binding sites in the interaction between an extracellular fibrinogen- binding protein from Staphylococcus aureus and fibrinogen. J Biol Chem 1998; 273: 13177-81.
- 166 Wolz C, Pöhlmann-Dietze P, Steinhuber A. et al. Agr-independent regulation of fibronectin-binding protein(s) by the regulatory locus sar in Staphylococcus aureus . Mol Microbiol 2000; 36: 230-43.
- 167 Vaudaux PE, François P, Proctor RA. et al. Use of adhesion-defective mutants of Staphylococcus aureus to define the role of specific plasma proteins in promoting bacterial adhesion to canine arteriovenous shunts [published erratum appears in Infect Immun 1995 Aug;63(8):3239]. Infect Immun 1995; 63: 585-90.
- 168 Darouiche RO, Landon GC, Patti JM. et al. Role of Staphylococcus aureus surface adhesins in orthopaedic device infections: are results model-dependent?. J Med Microbiol 1997; 46: 75-9.
- 169 Weidenmaier C, Kokai-Kun JF, Kristian SA. et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 2004; 10: 243-5.
- 170 Roche FM, Downer R, Keane F. et al. The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J Biol Chem 2004; 279: 38433-40.