[en] Intracellular invasion of Staphyloccocus aureus in nonphagocytic cells Staphylococcus aureus often causes chronic diseases. It is now believed that recurrence of these infections could be related to the ability of S. aureus to invade and persist within nonphagocytic cells. Adherence to eucaryotic cells is crucial for S. aureus to invade and persist within invasion and depends on interactions between bacterial fibronectin-binding proteins, fibronectin and the host cell fibronectin receptor, integrin alpha(5)beta(1). It is currently established that fibronectin acts as a bridging molecule. Penetration of S. aureus in host cells requires also activation of protein tyrosine kinases that mediate signal transduction and actin polymerization leading to cytoskeletal rearrangements. After internalization, S. aureus either remains in membrane-bound vacuoles or appears free in the cytoplasm. After bacterial proliferation, S. aureus induces host cell apoptosis or persist inside cells as small colony variants, which represent a less virulent subpopulation of S. aureus that grows slower. Although numerous in vitro and in vivo studies have demonstrated the ability of S. aureus to invade nonphagocytic cells, additional experiments have to be realized to understand the relevance of intracellular localization in vivo. [fr] Staphylococcus aureus est souvent à l’origine de maladies chroniques. La récurrence de ce type d’infection peut être mise en relation avec la capacité qu’a S. aureus à pénétrer et survivre à l’intérieur des cellules non-phagocytaires. L’adhérence de S. aureus aux cellules-hôtes est essentielle à l’invasion de la bactérie et dépend, d’une part, des protéines de surface bactériennes capables de se lier à la fibronectine et, d’autre part, des intégrines α5β1 des cellules-hôtes. La pénétration de S. aureus à l’intérieur des cellules-hôtes nécessite l’activation de protéines tyrosine-kinases, impliquées dans l’initiation d’un signal intracellulaire et la polymérisation des microfilaments d’actine à la base d’un réarrangement du cytosquelette. À l’intérieur de la cellule-hôte, S. aureus est soit logé dans un endosome, soit libre dans le cytoplasme. Après avoir proliféré, S. aureus peut induire l’apoptose des cellules qu’il envahit, mais peut également persister dans les cellules sous forme de variants qui se caractérisent par une faible activité métabolique et une moindre virulence. Enfin, bien que S. aureus pénètre à l’intérieur de cellules non-phagocytaires, tant in vitro que chez l’animal, des études supplémentaires sont nécessaires pour déterminer l’impact d’une présence intracellulaire de S. aureus in vivo
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Boulanger, Delphine; Université de Liège - ULiège
Bureau, Fabrice ; Université de Liège - ULiège > Département de sciences fonctionnelles > Biochimie et biologie moléculaire
Lekeux, Pierre ; Université de Liège - ULiège > Département de sciences fonctionnelles > Physiologie
Language :
French
Title :
Invasion intracellulaire des cellules non-phagocytaires par Staphylococcus aureus
Alternative titles :
[en] Intracellular invasion of Staphyloccocus aureus in nonphagocytic cells
ABDELNOUR A., ARVIDSON S., BREMELL T., RYDEN C., TARKOWSKI A. The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect. Immun., 1993, 61, 3879-3885.
AGERER F., MICHEL A., OHLSEN K., HAUCK C.R. Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J. Biol. Chem., 2003, 278, 42524-42531.
ALEXANDER E.H., HUDSON M.C. Factors influencing the internalization of Staphylococcus aureus and impacts on the course of infections in humans. Appl. Microbiol. Biotechnol., 2001, 56, 361-366.
ALMEIDA R.A., MATTHEWS K.R., CIFRIAN E., GUIDRY A.J., OLIVER S.P. Staphylococcus aureus invasion of bovine mammary epithelial cells. J. Dairy Sci., 1996, 79, 1021-1026.
ANDERSON J.C., CHANDLER R.L. Experimental Staphylococcal mastitis in the mouse. Histological, ultrastructural and bacteriological changes caused by a virulent strain of Staphylococcus aureus. J. Comp. Pathol., 1975, 85, 499-510.
ASHKENAZI A., DIXIT V.M. Death receptors : signaling and modulation. Science, 1998, 281, 1305-1308.
BALWIT J.M., VAN LANGEVELDE P., VANN J.M., PROCTOR R.A. Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J. Infect. Dis., 1994, 170, 1033-1037.
BANFI B., MATURANA A., JACONI S., ARNAUDEAU S., LAFORGE T., SINHA B., LIGETI E., DEMAUREX N., KRAUSE K.-H. A mammalian H+ channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science, 2000, 287, 138-142.
BAYLES K.W., WESSON C.A., LIOU L.E., FOX L.K., BOHACH G.A., TRUMBLE W.R. Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect. Immun., 1998, 66, 336-342.
BROUILLETTE E., GRONDIN G., SHKRETA L., LACASSE P., TALBOT B.G. In vivo and in vitro demonstration that Staphylococcus aureus is an intracellular pathogen in the presence or absence of fibronectin-binding proteins. Microb. Pathog., 2003, 35, 159-168.
BROUILLETTE E., MARTINEZ A., BOYLL B.J., ALLEN N.E., MALOUIN F. Persistence of a Staphylococcus aureus small-colony variant under antibiotic pressure in vivo. FEMS Immunol. Med. Microbiol., 2004, 41, 35-41.
BUNCE C., WHEELER L., REED G., MUSSER J., BARG N. Murine model of cutaneous infection with gram-positive cocci. Infect. Immun., 1992, 60, 2636-2640.
CHANDLER R.L., SMITH K., TURFREY B.A. Studies on the phagocytic potential of secretory epithelial cells in experimental mastitis. J. Comp. Pathol., 1980, 90, 385-394.
CHEUNG A.L., COOMEY J.M., BUTLER C.A., PROJAN S.J., FISCHETTI V.A. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. Proc. Natl Acad. Sci. USA, 1992, 89, 6462-6466.
CHEUNG A.L., EBERHARDT K.J., CHUNG E., YEAMAN M.R., SULLAM P.M., RAMOS M., BAYER A.S. Diminished virulence of a sar-/agr- mutant of Staphylococcus aureus in the rabbit model of endocarditis. J. Clin. Invest., 1994, 94, 1815-1822.
CHEUNG A.L., EBERHARDT K., HEINRICHS J.H. Regulation of protein A synthesis by the sar and agr loci of Staphylococcus aureus. Infect. Immun., 1997, 65, 2243-2249.
CHIEN Y., CHEUNG A.L. Molecular interactions between two global regulators, sar and agr, in Staphylococcus aureus. J. Biol. Chem., 1998, 273, 2645-2652.
CHIEN Y., MANNA A.C., PROJAN S.J., CHEUNG A.L. SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J. Biol. Chem., 1999, 274, 37169-37176.
CLEMENTS M.O., WATSON S.P., FOSTER S.J. Characterization of the major superoxide dismutase of Staphylococcus aureus and its role in starvation survival, stress resistance, and pathogenicity. J. Bacteriol., 1999, 181, 3898-3903.
CRAVEN N., ANDERSON J.-C. Phagocytosis of Staphylococcus aureus by bovine mammary gland macrophages and intracellular protection from antibiotic action in vitro and in vivo. J. Dairy Res., 1984, 4, 513-523.
DEITCH E.A., HASKEL Y., CRUZ N., XU D., KVIETYS P.R. Caco-2 and IEC-18 intestinal epithelial cells exert bactericidal activity through an oxidant-dependent pathway. Shock, 1995, 4, 345-350.
DZIEWANOWSKA K., PATTI J.M., DEOBALD C.F., BAYLES K.W., TRUMBLE W.R., BOHACH G.A. Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect. Immun., 1999, 67, 4673-4678.
DZIEWANOWSKA K., CARSON A.R., PATTI J.M., DEOBALD C.F., BAYLES K.W., BOHACH G.A. Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins : role in internalization by epithelial cells. Infect. Immun., 2000, 68, 6321-6328.
ELLINGTON J.K., ELHOFY A., BOST K.L., HUDSON M.C. Involvement of mitogen-activated protein kinase pathways in Staphylococcus aureus invasion of normal osteoblasts. Infect Immun. 2001, 9, 5235-5242.
FERENS W.A., BOHACH G.A. Persistence of Staphylococcus aureus on mucosal membranes : superantigens and internalization by host cells. J. Lab. Clin. Med., 2000, 135, 225-230.
FINLAY B.B., COSSART P. Exploitation of mammalian host cell functions by bacterial pathogens. Science, 1997, 276, 718-725.
FLOCK J.-I., HIENZ S.A., HEIMDAHL A., SCHENNINGS T. Reconsideration of the role of fibronectin binding in endocarditis caused by Staphylococcus aureus. Infect. Immun., 1996, 64, 1876-1878.
FOSTER T.J., O'REILLY M., PHONIMDAENG P., COONEY J., PATEL A.H., BRAMLEY A.J. Genetic studies of virulence factors of Staphylococcus aureus : properties of coagulase and gammatoxin, alpha-toxin, beta-toxin and protein A in the pathogenesis of S. aureus infections. In : Novick R.P. (Eds.), Molecular biology of the Staphylococci. VCH Publishers : New York, 1990, 403-420.
FOWLER T., WANN E.R., JOH D., JOHANSSON S., FOSTER T.J., HÖÖK M. Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial f ibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur. J. Cell. Biol., 2000, 79, 672-679.
FOWLER T., JOHANSSON S., WARY K.K., HOOK M. Src kinase has a central role in in vitro cellular internalization of Staphylococcus aureus. Cell. Microbiol., 2003, 5, 417-426.
FROMAN G., SWITALSKI L.M., SPEZIALE P., HOOK M. Isolation and characterization of a fibronectin receptor from Staphylococcus aureus. J. Biol. Chem., 1987, 14, 6564-6571.
GRESHAM H.D., LOWRANCE J.H., CAVER T.E., WILSON B.S., CHEUNG A.L., LINDBERG F.P. Survival of Staphylococcus aureus inside neutrophils contributes to infection. J. Immunol., 2000, 164, 3713-3722.
HAGGAR A., HUSSAIN M., LÖNNIES H., HERRMANN M., NORRBY-TEGLUND A., FLOCK J.-I. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect. Immun., 2003, 71, 2310-2317.
HAMILL R.J., VANN J.M., PROCTOR R.A. Phagocytosis of Staphylococcus aureus by cultured bovine aortic endothelial cells : model for postadherence events in endovascular infections. Infect. Immun., 1986, 54, 833-836.
HAUCK C.R. Cell adhesion receptors-signaling capacity and exploitation by bacterial pathogens. Med. Microbiol. Immunol. (Berl.), 2002, 191, 55-62.
HEBERT A., SAYASITH K., SENECHAL S., DUBREUIL P., LAGACE J. Demonstration of intracellular Staphylococcus aureus in bovine mastitis alveolar cells and macrophages isolated from naturally infected cow milk. FEMS Microbiol. Lett., 2000, 1, 57-62.
HEYER G., SABA S., ADAMO R., RUSH W., SOONG G., CHEUNG A., PRINCE A. Staphylococcus aureus agr and sarA functions are required for invasive infection but not inflammatory responses in the lung. Infect. Immun., 2002, 70, 127-133.
HORWITZ A., DUGGAN K., BUCK C., BECKERLE M.C., BURRIDGE K. Interaction of plasma membrane fibronectin receptor with talin-a transmembrane linkage. Nature, 1986, 320, 531-533.
HUDSON M.C., RAMP W.K., NICHOLSON N.C., WILLIAMS A.S., NOUSIAINEN M.T. Internalization of Staphylococcus aureus by cultured osteoblasts. Microb. Pathog., 1995, 19, 409-419.
HUFF S., MATSUKA Y.V., MCGAVIN M.J., INGHAM K.C. Interaction of N-terminal fragments of fibronectin with synthetic and recombinant D motifs from its binding protein on Staphylococcus aureus studied using fluorescence anisotropy. J. Biol. Chem., 1994, 269, 15563-15570.
HYNES R.O. Integrins : a family of cell surface receptors. Cell, 1987, 48, 549-554.
HYNES R.O. Integrins : versatility, modulation, and signaling in cell adhesion. Cell, 1992, 69, 11-25.
ISBERG R.R., FALKOW S. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature, 1985, 317, 262-264.
ISBERG R.R. Pathways for the penetration of enteroinvasive Yersinia into mammalian cells. Mol. Biol. Med., 1990, 7, 73-82.
ISBERG R.R., LEONG J.M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell, 1990, 60, 861-871.
JETT B.D., GILMORE M.S. Internalization of Staphylococcus aureus by human corneal epithelial cells : role of bacterial fibronectin-binding protein and host cell factors. Infect. Immun., 2002, 70, 4697-4700.
JEVON M., GUO C., MA B., MORDAN N., NAIR S.P., HARRIS M., HENDERSON B., BENTLEY G., MEGHJI S. Mechanisms of internalization of Staphylococcus aureus by cultured human osteoblasts. Infect. Immun., 1999, 67, 2677-2681.
JI G., BEAVIS R.C., NOVICK R.P. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc. Natl. Acad. Sci. USA, 1995, 92, 12055-12059.
JI G., BEAVIS R., NOVICK R.P. Bacterial interference caused by autoinducing peptide variants. Science, 1997, 276, 2027-2030.
JÖNSSON K., SIGNÄS C., MÜLLER H.-P., LINDBERG M. 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, 1041-1048.
KAHL B., HERRMANN M., EVERDING A.S., KOCH H.G., BECKER K., HARMS E., PROCTOR R.A., PETERS G. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J. Infect. Dis., 1998, 177, 1023-1029.
KAHL B.C., GOULIAN M., VAN WAMEL W., HERRMANN M., SIMON S.M., KAPLAN G., PETERS G., CHEUNG A.L. Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line. Infect. Immun., 2000, 68, 5385-5392.
KARAVOLOS M.H., HORSBURGH M.J., INGHAM E., FOSTER S.J. Role and regulation of the superoxide dismutases of Staphylococcus aureus. Microbiology, 2003, 149, 2749-2758.
KINTARAK S., WHAWELL S.A., SPEIGHT P.M., PACKER S., NAIR S.P. Internalization of Staphylococcus aureus by human keratinocytes. Infect. Immun., 2004, 72, 5668-5675.
KUUSELA P., VARTIO T., VUENTO M., MYHRE E.B. Binding sites for streptococci and staphylococci in fibronectin. Infect. Immun., 1984, 45, 433-436.
LAMMERS A., NUIJTEN P.J., SMITH H.E. The fibronectin binding proteins of Staphylococcus aureus are required for adhesion to and invasion of bovine mammary gland cells. FEMS Microbiol. Lett., 1999, 180, 103-109.
LINA G., JARRAUD S., JI G., GREENLAND T., PEDRAZA A., ETIENNE J., NOVICK R.P., VANDENESCH F. Transmembrane topology and histidine protein kinase activity of AgrC, the agr signal receptor in Staphylococcus aureus. Mol. Microbiol., 1998, 28, 655-662.
LODISH H., BALTIMORE D., BERK A., ZIPURSKY L., MATSUDAIRA P., DARNELL J. Biologie moléculaire de la cellule. DeBoeck Université : Bruxelles, 1997, 1344 p.
LOWY F.D. Staphylococcus aureus infections. N. Engl. J. Med., 1998, 339, 520-532.
MAMO W., JONSSON P., FLOCK J.I., LINDBERG M., MÜLLER H.-P., WADSTRÖM T., NELSON L. Vaccination against Staphylococcus aureus mastitis : immunological response of mice vaccinated with fibronectin-binding protein (FnBP-A) to challenge with S. aureus. Vaccine, 1994, 12, 988-992.
MASSEY R.C., KANTZANOU M.N., FOWLER T., DAY N.P., SCHOFIELD K., WANN E.R., BERENDT A.R., HÖÖK M., PEACOCK S.J. 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, 839-851.
MAXE I., RYDÉN C., WADSTRÖM T., RUBIN K. Specif ic attachment of Staphylococcus aureus to immobilized fibronectin. Infect. Immun., 1986, 54, 695-704.
MCELROY M.C., CAIN D.J., TYRRELL C., FOSTER T.J., HASLETT C. Increased virulence of a fibronectin-binding protein mutant of Staphylococcus aureus in a rat model of pneumonia. Infect. Immun., 2002, 70, 3865-3873.
MEMPEL M., SCHNOPP C., HOJKA M., FESQ H., WEIDINGER S., SCHALLER M., KORTING H.C., RING J., ABECK D. Invasion of human keratinocytes by Staphylococcus aureus and intracellular bacterial persistence represent haemolysin-independent virulence mechanisms that are followed by features of necrotic and apoptotic keratinocyte cell death. Br. J. Dermatol., 2002, 146, 943-951.
MENZIES B.E., KOURTEVA I. Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect. Immun., 1998, 66, 5994-5998.
MENZIES B.E., KOURTEVA Y., KAISER A.B., KERNODLE D.S. 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, 937-943.
MILLER R.A., BRITIGAN B.E. Role of oxidants in microbial pathophysiology. Clin. Microbiol. Rev., 1997, 10, 1-18.
MIYAMOTO S., TERAMOTO H., COSO O.A., GUTKIND J.S., BURBELO P.D., AKIYAMA S.K., YAMADA K.M. Integrin function : molecular hierarchies of cytoskeletal and signaling molecules. J. Cell. Biol., 1995, 131, 791-805.
MORFELDT E., JANZON L., ARVIDSON S., LOFDAHL S. Cloning of a chromosomal locus (exp) which regulates the expression of several exoprotein genes in Staphylococcus aureus. Mol. Gen. Genet., 1988, 211, 435-440.
MORFELDT E., TAYLOR D., VON GABAIN A., ARVIDSON S. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J., 1995, 14, 4569-4577.
MORFELDT E., TEGMARK K., ARVIDSON S. Transcriptional control of the agr-dependent virulence gene regulator, RNAIII, in Staphylococcus aureus. Mol. Microbiol., 1996, 21, 1227-1237.
MOSHER D.F., PROCTOR R.A. Binding and factor XIIIa-mediated cross-linking of a 27-kilodalton fragment of fibronectin to Staphylococcus aureus. Science, 1980, 209, 927-929.
NOVICK R.P., ROSS H.F., PROJAN S.J., KORNBLUM J., KREISWIRTH B., MOGHAZEH S. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J., 1993, 12, 3967-3975.
NOVICK R.P., PROJAN S.J., KORNBLUM J., ROSS H.F., JI G., KREISWIRTH B., VANDENESCH F., MOGHAZEH S. The agr P2 operon : an autocatalytic sensory transduction system in Staphylococcus aureus. Mol. Gen. Genet., 1995, 248, 446-458.
OGAWA S.K., YURBERG E.R., HATCHER V.B., LEVITT M.A., LOWY F.D. Bacterial adherence to human endothelial cells in vitro. Infect. Immun., 1985, 50, 218-224.
OTEY C.A., PAVALKO F.M., BURRIDGE K. An interaction between alpha-actinin and the beta 1 integrin subunit in vitro. J. Cell. Biol., 1990, 111, 721-729.
OZERI V., ROSENSHINE I., MOSHER D.F., FÄSSLER R., HANSKI E. Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol. Microbiol., 1998, 30, 625-637.
OZERI V., ROSENSHINE I., BENZE'EV A., BOKOCH G.M., JOU T.S., HANSKI E. De novo formation of focal complex-like structures in host cells by invading Streptococci. Mol. Microbiol., 2001, 41, 561-573.
PALMA M., HAGGAR A, FLOCK J.I. Adherence of Staphylococcus aureus is enhanced by an endogenous secreted protein with broad binding activity. J. Bacteriol., 1999, 9, 2840-2845.
PATTI J.M., ALLEN B.L., MCGAVIN M.J., HÖÖK M. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol., 1994, 48, 585-617.
PEACOCK S.J., FOSTER T.J., CAMERON B.J., BERENDT A.R. Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology, 1999, 145, 3477-3486.
PEACOCK S.J., DAY N.P.J., THOMAS M.G., BERENDT A.R., FOSTER T.J. Clinical isolates of Staphylococcus aureus exhibit diversity in fnb genes and adhesion to human fibronectin. J. Infect., 2000, 41, 23-31.
PENG H.L., NOVICK R.P., KREISWIRTH B., KORNBLUM J., SCHLIEVERT P. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol., 1988, 170, 4365-4372.
PEPE J.C., MILLER V.L. Yersinia enterocolitica invasin : a primary role in the initiation of infection. Proc. Natl. Acad. Sci. USA, 1993, 90, 6473-6477.
PIERSCHBACHER M.D., RUOSLAHTI E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature, 1984a, 309, 30-33.
PIERSCHBACHER M.D., RUOSLAHTI E. Variants of the cell recognition site of fibronectin that retain attachment-promoting activity. Proc. Natl. Acad. Sci. USA, 1984b, 19, 5985-5988.
PROCTOR R.A., PRENDERGAST E., MOSHER D.F. Fibronectin mediates attachment of Staphylococcus aureus to human neutrophils. Blood, 1982, 59, 681-687.
PROCTOR R.A., CHRISTMAN G., MOSHER D.F. Fibronectin-induced agglutination of Staphylococcus aureus correlates with invasiveness. J. Lab. Clin. Med., 1984, 104, 455-469.
PROCTOR R.A., BALWIT J.M., VESGA O. Variant subpopulations of Staphylococcus aureus as cause of persistent and recurrent infections. Infect. Agents Dis., 1994, 3, 302-312.
PROCTOR R.A., VAN LANGEVELDE P., KRISTJANSSON M., MASLOW J.N., ARBEIT R.D. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin. Infect. Dis., 1995, 20, 95-102.
QAZI S.N.A., COUNIL E., MORRISSEY J., REES C.E.D., COCKAYNE A., WINZER K., CHAN W.C., WILLIAMS P., HILL P.J. agr Expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect. Immun., 2001, 69, 7074-7082.
QAZI S.N.A., HARRISON S.E., SELF T., WILLIAMS P., HILL P.J. Real-time monitoring of intracellular Staphylococcus aureus replication. J. Bacteriol., 2004, 186, 1065-1077.
QUIE P.G. Microcolonies (G-variants) of Staphylococcus aureus. Yale J. Biol. Med., 1969, 41, 394-403.
QUE Y.-A., FRANÇOIS P., HAEFLIGER J.-A., ENTENZA J.-M., VAUDAUX P., MOREILLON P. Reassessing the role of Staphylococcus aureus clumping factor and f ibronectin-binding protein by expression in Lactococcus lactis. Infect Immun., 2001, 69, 6296-6302.
RECSEI P, KREISWIRTH B, O'REILLY M, SCHLIEVERT P, GRUSS A, NOVICK RP. Regulation of exoprotein gene expression in Staphylococcus aureus by agar. Mol. Gen. Genet., 1986, 202, 58-61.
REILLY S.S., HUDSON M.C., KELLAM J.F., RAMP W.K. In vivo inter nalization of Staphylococcus aureus by embryonic chick osteoblasts. Bone, 2000, 26, 63-70.
ROHDE M., MÜLLER E., CHHATWAL G.S., TALAY S.R. Host cell caveolae act as an entry-port for group A streptococci. Cell Microbiol., 2003, 5, 323-342.
ROZALSKA B., WADSTRÖM T. Protective opsonic activity of antibodies against fibronectin-binding proteins (FnBPs) of Staphylococcus aureus. Scand. J. Immunol., 1993, 37, 575-580.
SARAVIA-OTTEN P., MULLER H.P., ARVIDSON S. Transcription of Staphylococcus aureus fibronectin binding protein genes is negatively regulated by agr and an agr-independent mechanism. J. Bacteriol., 1997, 179, 5259-5263.
SCHALLER M.D., BORGMAN C.A., COBB B.S., VINES R.R., REYNOLDS A.B., PARSONS J.T. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA., 1992, 89, 5192-5196.
SCHENNINGS T., HEIMDAHL A., COSTER K., FLOCK J.I. Immunization with fibronectin binding protein from Staphylococcus aureus protects against experimental endocarditis in rats. Microb. Pathog., 1993, 15, 227-236.
SCHNEEWIND O., FOWLER A., FAULL K.F. Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science, 1995, 268, 103-106.
SEARS P.M., MCCARTHY K.K. Management and treatment of staphylococcal mastitis. Vet. Clin. North Am. Food Anim. Pract., 2003, 19, 171-185.
SHOMPOLE S., HENON K.T., LIOU L.E., DZIEWANOWSKA K., BOHACH G.A., BAYLES K.W. Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agr-mediated diffusion sensing. Mol. Microbiol., 2003, 49, 919-927.
SIELING P.A., ABRAMS J.S., YAMAMURA M., SALGAME P., BLOOM B.R., REA T.H., MODLIN R.L. Immunosuppressive roles for IL-10 and IL-4 in human infection : in vitro modulation of T cell responses in leprosy. J. Immunol., 1993, 150, 5501-5510.
SIGNÄS C., RAUCCI G., JÖNSSON K., LINDGREN P.-E., ANANTHARAMAIAH G.M., HÖÖK M., LINDBERG M. 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. USA., 1989, 86, 699-703.
SINHA B., FRANÇOIS P.P., NÜSSE O., FOTI M., HARTFORD O.M., VAUDAUX P., FOSTER T.J., LEW D.P., HERRMANN M., KRAUSE K.-H. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell. Microbiol., 1999, 1, 101-117.
SINHA B., FRANÇOIS P., QUE Y.-A., HUSSAIN M., HEILMANN C., MOREILLON P., LEW D., KRAUSE K.-H., PETERS G., HERRMANN M. Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are suff icient for invasion of host cells. Infect. Immun., 2000, 68, 6871-6878.
SUH Y.A., ARNOLD R.S., LASSEGUE B., SHI J., XU X., SORESCU D., CHUNG A.B., GRIENDLING K.K., LAMBETH J.D. Cell transformation by the superoxide-generating oxidase Mox1. Nature, 1999, 401, 79-82.
SUTRA L., POUTREL B. Virulence factors involved in the pathogenesis of bovine intramammary infections due to Staphylococcus aureus. J. Med. Microbiol., 1994, 40, 79-89.
TON-THAT H., FAULL K.F., SCHNEEWIND O. Anchor structure of staphylococcal surface proteins. A branched peptide that links the carboxyl terminus of proteins to the cell wall. J. Biol. Chem., 1997, 272, 22285-22292.
USUI A., MURAI M., SEKI K., SAKURADA J., MASUDA S. Conspicuous ingestion of Staphylococcus aureus organisms by murine fibroblasts in vitro. Microbiol. Immunol., 1992, 36, 545-550.
VAN DE WATER L., DESTREE A.T., HYNES R.O. Fibronectin binds to some bacteria but does not promote their uptake by phagocytic cells. Science, 1983, 220, 201-204.
VAN NHIEU G.T., ISBERG R.R. The Yersinia pseudotuberculosis invasin protein and human fibronectin bind to mutually exclusive sites on the alpha 5 beta 1 integrin receptor. J. Biol. Chem., 1991, 266, 24367-24375.
VAN NHIEU G.T., ISBERG R.R. Bacterial internalization mediated by beta 1 chain integrins is determined by ligand affinity and receptor density. EMBO J., 1993, 5, 1887-1895.
VANN J.M., PROCTOR R.A. Ingestion of Staphylococcus aureus by bovine endothelial cells results in time- and inoculum-dependent damage to endothelial cell monolayers. Infect. Immun., 1987, 55, 2155-2163.
VERBRUGH H.A., PETERSON P.K., SMITH D.E., NGUYEN B.-Y.T., HOIDAL J.R., WILKINSON B.J., VERHOEF J., FURCHT L.T. Human fibronectin binding to staphylococcal surface protein and its relative inefficiency in promoting phagocytosis by human polymorphonuclear leukocytes, monocytes, and alveolar macrophages. Infect. Immun., 1981, 33, 811-819.
VESGA O., GROESCHEL M.C., OTTEN M.F., BRAR D.W., VANN J.M., PROCTOR R.A. Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J. Infect. Dis., 1996, 173, 739-742.
VON EIFF C., BETTIN D., PROCTOR R.A., ROLAUFFS B., LINDNER N., WINKELMANN W., PETERS G. Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin. Infect. Dis., 1997, 25, 1250-1251.
WESSON C.A., LIOU L.E., TODD K.M., BOHACH G.A., TRUMBLE W.R., BAYLES K.W. Staphylococcus aureus Agr and Sar global regulators influence internalization and induction of apoptosis. Infect. Immun., 1998, 11, 5238-43.
WESSON C.A., DERINGER J., LIOU L.E., BAYLES K.W., BOHACH G.A., TRUMBLE W.R. Apoptosis induced by Staphylococcus aureus in epithelial cells utilizes a mechanism involving caspases 8 and 3. Infect. Immun., 2000, 68, 2998-3001.
