Fatores de virulência de Staphylococcus aureus
DOI:
https://doi.org/10.26605/medvet-n4-1955Abstract
Nas últimas décadas, Staphylococcus aureus (S. aureus) adquiriu considerável importância relacionada à saúde animal e humana pela elevada patogenicidade e aumento na prevalência de cepas multirresistentes aos antibióticos. Sua elevada patogenicidade está relacionada com mecanismos multifatoriais e complexos determinados pela capacidade da bactéria de expressar uma variedade de fatores de virulência que facilitam a ocorrência de doenças. Objetivou-se com esta revisão compilar informações referentes aos fatores de virulência associados à superfície ou secretados por S. aureus que promovem adesão aos componentes da matriz extracelular do hospedeiro, danificam células hospedeiras e interferem no sistema imunológico. A implementação de estratégias para a prevenção e terapia em infecções associadas a S. aureus exige o aprofundamento dos estudos nos diferentes mecanismos de ação dos fatores de virulência.Downloads
References
Aarestrup, F.M.; Larsen, H.; Eriksen, N.; Elsberg, C.; Jensen, N. Frequency of α‐and βhaemolysin in Staphylococcus aureus of bovine and human origin. Acta Pathologica, Microbiologica, et Immunologica Scandinavica, 107(1‐6): 425-430, 1999.
Adhikari, R.P.; Ajao, A.O.; Aman, M.J.; Karauzum, H.; Sarwar, J.; Lydecker, A.D.; Johnson, J.K.; Nguyen, C.; Chen, W.H.; Roghmann, M.-C. Lower antibody levels to Staphylococcus aureus exotoxins are associated with sepsis in hospitalized adults with invasive S aureus infections. The Journal of Infectious Diseases, 206(6): 915923, 2012.
Al-Dabbagh, M.; Dobson S. Infectious hazards from pets and domestic animals. In: Curtis, N.; Finn, A.; Pollard, A.J. Hot topics in infection and immunity in children VII. Springer New York, 2011, p.261-272.
Altboum, Z.; Hertman, I.; Sarid, S. Penicillinase plasmid-linked genetic determinants for enterotoxins B and C1 production in Staphylococcus aureus. Infection and Immunity, 47(2): 514-521, 1985.
Arbeit, R.D.; Karakawa, W.W.; Vann, W.F.; Robbins, J.B. Predominance of two newly described capsular polysaccharide types among clinical isolates of Staphylococcus aureus. Diagnostic Microbiology and Infectious Disease, 2(2): 85-91, 1984.
Balaban, N.; Rasooly, A. Staphylococcal enterotoxins. International Journal of Food Microbiology, 61(1): 1-10, 2000.
Bardiau, M.; Caplin, J.; Detilleux, J.; Graber, H.; Moroni, P.; Taminiau, B.; Mainil, J.G. Existence of two groups of Staphylococcus aureus strains isolated from bovine mastitis based on biofilm formation, intracellular survival, capsular profile and agr-typing. Veterinary Microbiology, 185: 1-6, 2016.
Barrio, B.; Vangroenweghe, F.; Dosogne, H.; Burvenich, C. Decreased neutrophil bactericidal activity during phagocytosis of a slime-producing Staphylococcus aureus strain. Veterinary Research, 31(6): 603-609, 2000.
Bayles, K.W.; Iandolo, J.J. Genetic and molecular analyses of the gene encoding staphylococcal enterotoxin D. Journal of Bacteriology, 171(9): 4799-4806, 1989.
Beloin, C.; Renard, S.; Ghigo, J.M.; Lebeaux, D. Novel approaches to combat bacterial biofilms. Current Opinion in Pharmacology, 18: 61-68, 2014.
Bergdoll, M.S.; Borja, C.R.; Avena, R.M. Identification of a new enterotoxin as enterotoxin C. Journal of Bacteriology, 90(5): 1481-1485, 1965. Bernheimer, A.W.; Avigad, L.S.; Kim, K.S. Staphylococcal sphingomyelinase (βhemolysin). Annals of the New York Academy of Sciences, 236(1): 292-306, 1974.
Berube, B.J.; Wardenburg, J.B. Staphylococcus aureus α-toxin: Nearly a century of intrigue. Toxins, 5(6): 1140-1166, 2013.
Betley, M.; Mekalanos, J. Nucleotide sequence of the type A staphylococcal enterotoxin gene. Journal of Bacteriology, 170(1): 34-41, 1988.
Betley, M.J.; Mekalanos, J.J. Staphylococcal enterotoxin A is encoded by phage. Science, 229(4709): 185-187, 1985.
Blackledge, M.S.; Worthington R.J.; Melander C. Biologically inspired strategies for combating bacterial biofilms. Current Opinion in Pharmacology, 13(5): 699-706, 2013.
Boles, B. R.; Horswill, A.R. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathogens, 4(4): e1000052, 2008.
Carfora, V.; Caprioli, A.; Marri, N.; Sagrafoli, D.; Boselli, C.; Giacinti, G.; Giangolini, G.; Sorbara, L.; Dottarelli, S.; Battisti, A.; Amatiste, S. Enterotoxin genes, enterotoxin production, and methicillin resistance in Staphylococcus aureus isolated from milk and dairy products in Central Italy. International Dairy Journal, 42: 12-15, 2015.
Cassidy, P.; Harshman, S. Studies on the binding of staphylococcal 125I-labeled α-toxin to rabbit erythrocytes. Biochemistry, 15(11): 2348-2355, 1976.
Cassidy, P.S.; Harshman, S. The binding of staphylococcal 125I-α-toxin (b) to erythrocytes. The Journal of Biological Chemistry, 248(15): 5545-5546, 1973.
Chavakis, T.; Preissner, K.T.; Herrmann, M. The anti-inflammatory activities of Staphylococcus aureus. Trends in Immunology, 28(9): 408-418, 2007.
Choi, Y.-W.; Kotzin, B.; Herron, L.; Callahan, J.; Marrack, P.; Kappler, J. Interaction of Staphylococcus aureus toxin" superantigens" with human T cells. Proceedings of the National Academy of Sciences, 86(22): 8941-8945, 1989.
Choi, Y.; Herman, A.; DiGiusto, D.; Wade, T.; Marrack, P.; Kappler, J. Residues of the variable region of the T-cell-receptor β-chain that interact with S. aureus toxin superantigens. Nature, 346: 471-473, 1990.
Cifrian, E.; Guidry, A.J.; Bramley, A.J.; Norcross, N.L.; Bastida-Corcuera, F.D.; Marquardt, W.W. Effect of staphylococcal β toxin on the cytotoxicity, proliferation and adherence of Staphylococcus aureus to bovine mammary epithelial cells. Veterinary Microbiology, 48(3): 187-198, 1996.
Clarke, S.R.; Foster S.J. Surface adhesins of Staphylococcus aureus. Advances in Microbial Physiology, 51: 187-224, 2006.
Cocchiaro, J.L.; Gomez, M.I.; Risley, A.; Solinga, R.; Sordelli, D. O.; Lee, J. C. Molecular characterization of the capsule locus from non‐typeable Staphylococcus aureus. Molecular Microbiology, 59(3): 948-960, 2006. Cooney, J.; Mulvey, M.; Arbuthnott, J. P.; Foster, T.J. Molecular cloning and genetic analysis of the determinant for gamma-lysin, a twocomponent toxin of Staphylococcus aureus. Journal of General Microbiology, 134(8): 2179-2188, 1988.
Costerton, J. Overview of microbial biofilms. Journal of Industrial Microbiology, 15(3): 137-140, 1995.
Costerton, J.W.; Stewart, P. S.; Greenberg, E.P. Bacterial biofilms: a common cause of persistent infections. Science, 284(5418): 1318-1322, 1999.
Couch, J.L.; Betley, M.J. Nucleotide sequence of the type C3 staphylococcal enterotoxin gene suggests that intergenic recombination causes antigenic variation. Journal of Bacteriology, 171(8): 4507-4510, 1989.
Couch, J.L.; Soltis, M.T.; Betley, M.J. Cloning and nucleotide sequence of the type E staphylococcal enterotoxin gene. Journal of Bacteriology, 170(7): 2954-2960, 1988.
Cretenet, M.; Even S.; Le Loir, Y. Unveiling Staphylococcus aureus enterotoxin production in dairy products: a review of recent advances to face new challenges. Dairy Science & Technology, 91(2): 127-150, 2011. Cucarella, C.; Tormo, M.Á.; Ubeda, C.; Trotonda, M.P.; Monzón, M.; Peris, C.; Amorena, B.; Lasa, Í.; Penadés, J.R. Role of biofilmassociated protein bap in the pathogenesis of bovine Staphylococcus aureus. Infection and Immunity, 72(4): 2177-2185, 2004.
Dassy, B.; Stringfellow, W.; Lieb, M.; Fournier, J. Production of type 5 capsular polysaccharide by Staphylococcus aureus grown in a semisynthetic medium. Journal of General Microbiology, 137(5): 1155-1162, 1991.
DeLeo, F.R.; Kennedy, A.D.; Chen, L.; Wardenburg, J.B.; Kobayashi, S.D.; Mathema, B.; Braughton, K.R.; Whitney, A.R., Villaruz, A. E.; Martens, C. A. Molecular differentiation of historic phagetype 80/81 and contemporary epidemic Staphylococcus aureus. Proceedings of the National Academy of Sciences, 108(44): 18091-18096, 2011.
Diegelmann, R.F. Excessive neutrophils characterize chronic pressure ulcers. Wound Repair and Regeneration, 11(6): 490-495, 2003.
Dinges, M.M.; Orwin P.M.; Schlievert, P.M. Exotoxins of Staphylococcus aureus. Clinical Microbiology Reviews, 13(1): 16-34, 2000.
Dunne, W.M. Bacterial adhesion: seen any good biofilms lately? Clinical Microbiology Reviews, 15(2): 155-166, 2002.
Fairweather, N.; Kennedy, S.; Foster, T.; Kehoe, M.; Dougan, G. Expression of a cloned Staphylococcus aureus alpha-hemolysin determinant in Bacillus subtilis and Staphylococcus aureus. Infection and Immunity, 41(3): 1112-1117, 1983.
Felipe, V.; Morgante, C.A.; Somale, P.S.; Varroni, F.; Zingaretti, M.L.; Bachetti, R.A.; Correa, S.G.; Porporatto, C. Evaluation of the biofilm forming ability and its associated genes in Staphylococcus species isolates from bovine mastitis in Argentinean dairy farms. Microbial Pathogenesis, 104: 278-286, 2017.
Fields, B.A.; Malchiodi, E.L.; Li, H.; Ysern, X.; Stauffacher, C.V.; Schlievert P.M.; Karjalainen K.; Mariuzza, R.A. Crystal structure of a T-cell receptor β-chain complexed with a superantigen. Nature, 384(14): 118-192, 1996. Fink, P.J.; Matis, L.A.; McElligott, D.L.; Bookman, M.; Hedrick, S.M. Correlations between T-cell specificity and the structure of the antigen receptor. Nature, 321(6067): 219226, 1986.
Fitzgerald, J.R.; Monday, S.R.; Foster, T.J.; Bohach, G.A.; Hartigan, P.J.; Meaney, W. J.; Smyth, C.J. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. Journal of Bacteriology, 183(1): 63-70, 2001.
Fluit, A. Livestock‐associated Staphylococcus aureus. Clinical Microbiology and Infection, 18(8): 735-744, 2012. Foster, T.J. Immune evasion by staphylococci. Nature Reviews Microbiology, 3(12): 948958, 2005.
Foster, T. J.; Höök, M. Surface protein adhesins of Staphylococcus aureus. Trends in Microbiology, 6(12): 484-488, 1998.
Fournier, J.-M.; Vann, W. F.; Karakawa, W.W. Purification and characterization of Staphylococcus aureus type 8 capsular polysaccharide. Infection and Immunity, 45(1): 87-93, 1984.
Fox, L.K., Zadoks, R.N.; Gaskins, C.T. Biofilm production by Staphylococcus aureus associated with intramammary infection. Veterinary Microbiology, 107(3–4): 295299, 2005.
Freer, J.; Birkbeck, T. Possible conformation of delta-lysin, a membrane-damaging peptide of Staphylococcus aureus. Journal of Theoretical Biology, 94(3): 535-540, 1982.
Fritz, S.A.; Tiemann, K.M.; Hogan, P.G.; Epplin, E.K.; Rodriguez, M.; Al-Zubeidi, D.N.; Wardenburg, J. B.; Hunstad, D.A.A serologic correlate of protective immunity against community-onset Staphylococcus aureus infection. Clinical Infectious Diseases, 56(11): 1554-1561, 2013.
Glenny, A.T.; Stevens, N.F. Staphylococcal toxins and antitoxins. The Journal of Pathology and Bacteriology, 40: 210, 1935.
Gray, G.S.; Kehoe, M. Primary sequence of the alpha-toxin gene from Staphylococcus aureus wood 46. Infection and Immunity, 46(2): 615-618, 1984.
Haim, M.; Trost, A.; Maier, C.; Achatz, G.; Feichtner, S.; Hintner, H.; Bauer, J.; Önder, K. Cytokeratin 8 interacts with clumping factor B: a new possible virulence factor target. Microbiology, 156(12): 3710-3721, 2010.
Hair, P.S.; Echague, C.G.; Sholl, A.M.; Watkins, J.A.; Geoghegan, J.A.; Foster, T.J.; Cunnion, K.M. Clumping factor A interaction with complement factor I increases C3b cleavage on the bacterial surface of Staphylococcus aureus and decreases complement-mediated phagocytosis. Infection and Immunity, 78(4): 1717-1727, 2010.
Hanessian, S.; Haskell T.H. Structural studies on staphylococcal polysaccharide antigen. The Journal of Biological Chemistry, 239(9): 2758-2764, 1964.
Harris, T.; Grossman, D.; Kappler, J.; Marrack, P.; Rich, R.; Betley, M. Lack of complete correlation between emetic and T-cellstimulatory activities of staphylococcal enterotoxins. Infection and Immunity, 61(8): 3175-3183, 1993.
Hasman, H.; Moodley, A.; Guardabassi, L.; Stegger, M.; Skov, R.; Aarestrup, F.M. spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Veterinary Microbiology, 141(3): 326-331, 2010.
Herbert, S.; Worlitzsch, D.; Dassy, B.; Boutonnier, A.; Fournier, J.-M.; Bellon, G.; Dalhoff, A.; Döring, G. Regulation of Staphylococcus aureus capsularpolysaccharidetype 5: CO2 inhibition in vitro and in vivo. The Journal of Infectious Diseases, 176(2): 431-438, 1997.
Hildebrand, A.; Pohl, M.; Bhakdi, S. Staphylococcus aureus alpha-toxin. Dual mechanism of binding to target cells. The Journal of Biological Chemistry, 266(26): 17195-17200, 1991.
Hovde, C.; Hackett, S.; Bohach, G. Nucleotide sequence of the staphylococcal enterotoxin C3 gene: sequence comparison of all three type C staphylococcal enterotoxins. Molecular Genetics and Genomics, 220(2): 329-333, 1990.
Hu, C.; Gong, R.; Guo, A.; Chen, H. Protective effect of ligand-binding domain of fibronectin-binding protein on mastitis induced by Staphylococcus aureus in mice. Vaccine, 28(24): 4038-4044, 2010.
Hu, D.-L.; Suga, S.; Omoe, K.; Abe, Y.; Shinagawa, K.; Wakui, M.; Nakane, A. Staphylococcal enterotoxin A modulates intracellular Ca2+ signal pathway in human intestinal epithelial cells. FEBS Letters, 579(20): 4407-4412, 2005.
Huang, I.; Hughes, J.; Bergdoll, M.; Schantz, E. Complete amino acid sequence of staphylococcal enterotoxin A. The Journal of Biological Chemistry, 262(15): 7006, 1987.
Huseby, M.; Shi, K.; Brown, C.K.; Digre, J.; Mengistu, F.; Seo, K.S.; Bohach, G.A.; Schlievert, P.M.; Ohlendorf, D.H.; Earhart, C.A. Structure and biological activities of beta toxin from Staphylococcus aureus. Journal of Bacteriology, 189(23): 8719-8726, 2007.
Huseby, M.J.; Kruse, A.C.; Digre, J.; Kohler, P.L.; Vocke, J.A., Mann, E.E.; Bayles, K.W.; Bohach, G.A., Schlievert P. M.,Ohlendorf D. H. Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. Proceedings of the National Academy of Sciences, 107(32): 1440714412, 2010.
Jarraud, S.; Cozon, G.; Vandenesch, F.; Bes, M.; Etienne, J.; Lina, G. Involvement of enterotoxins G and I in staphylococcal toxic shock syndrome and staphylococcal scarlet fever. Journal of Clinical Microbiology, 37(8): 2446-2449, 1999.
Jarraud, S.; Peyrat, M.A.; Lim, A.; Tristan, A.; Bes, M.; Mougel, C.; Etienne, J.; Vandenesch, F.; Bonneville, M.; Lina, G. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. The Journal of Immunology, 166(1): 669-677, 2001.
Johns, M.; Khan S.A. Staphylococcal enterotoxin B gene is associated with a discrete genetic element. Journal of Bacteriology, 170(9): 4033-4039, 1988.
Johnson, G.M.; Lee, D.; Regelmann, W.; Gray, E.; Peters, G.; Quie, P. Interference with granulocyte function by Staphylococcus epidermidis slime. Infection and Immunity, 54(1): 13-20, 1986.
Jolivet-Gougeon, A.; Bonnaure-Mallet, M. Biofilms as a mechanism of bacterial resistance. Drug Discovery Today: Technologies, 11: 49-56, 2014. Jones, C. Revised structures for the capsular polysaccharides from Staphylococcus aureus Types 5 and 8, components of novel glycoconjugate vaccines. Carbohydrate Research, 340(6): 1097-1106, 2005.
Jönsson, K.; Signäs, C.; Müller, H.P.; Lindberg, M. Two different genes encode fibronectin binding proteins in Staphylococcus aureus.
European Journal of Biochemistry, 202(3): 1041-1048, 1991.
Kappler, J.; White, J.; Kozono, H.; Clements, J.; Marrack, P. Binding of a soluble alpha beta Tcell receptor to superantigen/major histocompatibility complex ligands. Proceedings of the National Academy of Sciences, 91(18): 8462-8466, 1994.
Karakawa, W.; Vann, W.F. Capsular polysaccharides of Staphylococcus aureus. Seminars in Infectious Diseases, 4: 285–293, 1982.
Katayama, Y.; Baba, T.; Sekine, M.; Fukuda, M.; Hiramatsu, K. Beta-hemolysin promotes skin colonization by Staphylococcus aureus. Journal of Bacteriology, 195(6): 1194-1203, 2013.
Kehoe, M.; Duncan, J.; Foster, T.; Fairweather, N.; Dougan, G. Cloning, expression, and mapping of the Staphylococcus aureus alphahemolysin determinant in Escherichia coli K12. Infection and Immunity, 41(3): 11051111, 1983.
Kolata, J.; Bode, L.G.; Holtfreter, S.; Steil, L.; Kusch, H.; Holtfreter, B.; Albrecht, D.; Hecker, M.; Engelmann, S.; van Belkum, A. Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non‐carriers. Proteomics, 11(19): 3914-3927, 2011.
König, W.; Prevost, G. Composition of staphylococcal bi-component toxins determines pathophysiological reactions. Journal of Medical Microbiology, 46(6): 479-485, 1997.
Kumar, R.; Yadav, B.; Anand, S.; Singh, R. Prevalence of adhesin and toxin genes among isolates of Staphylococcus aureus; obtained from mastitic cattle. World Journal of Microbiology and Biotechnology, 27(3): 513-521, 2011.
Lam, J.S.; Macdonald, L.A.; Lam, M.; Duchesne, L.; Southam, G.G. Production and characterization of monoclonal antibodies against serotype strains of Pseudomonas aeruginosa. Infection and Immunity, 55(5): 1051-1057, 1987.
Lamaita, H.; Cerqueira, M.; Carmo, L.; Santos, D.; Penna, C.; Souza, M. Staphylococcus sp. counting and detection of staphylococcal enterotoxins and toxic shock toxin syndrome from cooled raw milk. Arquivo Brasileiro de
Medicina Veterinária e Zootecnia, 57(5): 702-709, 2005.
Lasa, I.; Penadés, J.R. Bap: a family of surface proteins involved in biofilm formation. Research in Microbiology, 157(2): 99-107, 2006.
Le Loir, Y.; Baron, F.; Gautier, M. Staphylococcus aureus and food poisoning. Genetics and Molecular Research, 2(1): 63-76, 2003.
Lee, J.C.; Takeda, S.; Livolsi, P.; Paoletti, L. Effects of in vitro and in vivo growth conditions on expression of type 8 capsular polysaccharide by Staphylococcus aureus. Infection and Immunity, 61(5): 1853-1858, 1993. Lee, K.; Fitton J.; Wüthrich, K. Nuclear magnetic resonance investigation of the conformation of δ-haemolysin bound to dodecylphosphocholine micelles. Biochimica et Biophysica Acta, 911(2): 144-153, 1987.
Leid, J.G.; Willson, C.J.; Shirtliff, M.E.; Hassett, D.J.; Parsek, M.R.; Jeffers, A.K. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. The Journal of Immunology, 175(11): 75127518, 2005.
Mack, D. Molecular mechanisms of Staphylococcus epidermidis biofilm formation. Journal of Hospital Infection, 43: S113-S125, 1999.
Marr, J.; Lyon, J.; Roberson, J.; Lupher, M.; Davis, W.; Bohach, G. Characterization of novel type C staphylococcal enterotoxins: biological and evolutionary implications. Infection and Immunity, 61(10): 4254-4262, 1993.
Marrack, P.; Kappler, J. The staphylococcal enterotoxins and their relatives. Science, 248(4956): 705-711, 1990.
Mazmanian, S.; Liu, G., Ton-That H.,Schneewind O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science, 285(5428): 760-763, 1999.
Melchior, M.B.; Vaarkamp, H.; Fink-Gremmels, J. Biofilms: A role in recurrent mastitis infections? The Veterinary Journal, 171(3): 398-407, 2006.
Monday, S.R.; Bohach G.A. Properties of Staphylococcus aureus enterotoxins and toxic shock syndrome-toxin-1. In: Alouf, J.; Freer, J.H. The comprehensive sourcebook of bacterial protein toxins, 1999, p.589-610.
Moreau, M.; Richards, J.C.; Fournier, J.-M.; Byrd, R.A.; Karakawa, W.W.; Vann, W.F. Structure of the type 5 capsular polysaccharide of Staphylococcus aureus. Carbohydrate Research, 201(2): 285-297, 1990. Munson, S.H.; Tremaine, M.T.; Betley, M.J.; Welch, R.A. Identification and characterization of staphylococcal enterotoxin types G and I fromStaphylococcus aureus. Infection and Immunity, 66(7): 3337-3348, 1998.
Murthy, S.V.K.N.; Ann, M.M.; Harris, T.M.; Hellerqvist, C.G.; Hash, J.H. The repeating sequence of the capsular polysaccharide of Staphylococcus aureus M. Carbohydrate Research, 117: 113-123, 1983.
Navarre, W.; Schneewind, O. Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria. Molecular Microbiology, 14(1): 115-121, 1994.
Ní Eidhin, D.; Perkins, S.; Francois, P.; Vaudaux, P.; Höök, M.; Foster, T.J. Clumping factor B (ClfB), a new surface-located fibrinogenbinding adhesin of Staphylococcus aureus. Molecular Microbiology, 30(2): 245-257, 1998. Niemann, S.; Spehr, N.; Van Aken, H.; Morgenstern, E.; Peters, G., Herrmann, M., Kehrel, B.E. Soluble fibrin is the main mediator of Staphylococcus aureus adhesion to platelets. Circulation, 110(2): 193-200, 2004.
Novick, R.P. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Molecular Microbiology, 48(6): 1429-1449, 2003. O'Neill, E.; Pozzi, C.; Houston, P.; Humphreys, H.; Robinson, D.A.; Loughman, A.; Foster T. J.; O'Gara, J.P. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. Journal of Bacteriology, 190(11): 3835-3850, 2008.
O'Riordan, K.; Lee J.C. Staphylococcus aureus capsular polysaccharides. Clinical Microbiology Reviews, 17(1): 218-234, 2004.
Oliveira, M.; Bexiga, R.; Nunes, S.F.; Carneiro, C.; Cavaco, L.M.; Bernardo, F.; Vilela, C.L. Biofilm-forming ability profiling of Staphylococcus aureus and Staphylococcus epidermidis mastitis isolates. Veterinary Microbiology, 118(1–2): 133-140, 2006.
Ono, H.K.; Sato'o, Y.; Narita, K.; Naito, I.; Hirose, S.; Hisatsune, J.; Asano, K.; Hu, D.L.; Omoe, K.; Sugai, M.; Nakane, A. Identification and characterization of a Novel Staphylococcal Emetic Toxin. Applied and Environmental Microbiology, 81(20): 7034-7040, 2015.
Ote, I.; Taminiau, B.; Duprez, J.-N.; Dizier, I.; Mainil, J.G. Genotypic characterization by polymerase chain reaction of Staphylococcus aureus isolates associated with bovine mastitis. Veterinary Microbiology, 153(3– 4): 285-292, 2011.
Patti, J.M.; Allen, B.L.; McGavin, M.J.; Hook, M. MSCRAMM-mediated adherence of microorganisms to host tissues. Annual Review of Microbiology, 48(1): 585-617, 1994.
Peacock, S.J.; Moore, C.E.; Justice, A.; Kantzanou, M.; Story, L.; Mackie, K.; O'Neill, G.; Day, N.P. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infection and Immunity, 70(9): 4987-4996, 2002.
Petersson, K.; Håkansson, M.; Nilsson, H.; Forsberg, G.; Svensson, L.A.; Liljas, A.; Walse, B. Crystal structure of a superantigen bound to MHC class II displays zinc and peptide dependence. The EMBO Journal, 20(13): 3306-3312, 2001.
Planchon, S.; Gaillard-Martinie, B.; DordetFrisoni, E.; Bellon-Fontaine, M.; Leroy, S.; Labadie, J.; Hébraud, M.; Talon, R. Formation of biofilm by Staphylococcus xylosus. International Journal of Food Microbiology, 109(1): 88-96, 2006.
Prevost, G.; Cribier, B.; Couppie, P.; Petiau, P.; Supersac, G.; Finck-Barbancon, V.; Monteil, H.; Piemont, Y. Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infection and Immunity, 63(10): 4121-4129, 1995.
Projan, S.J.; Kornblum, J.; Kreiswirth, B.; Moghazeh, S.L.; Eisner, W.; Novick, R.P. Nucleotide sequence: the beta-hemolysin gene of Staphylococcus aureus. Nucleic Acids Research, 17(8): 3305, 1989.
Rall, V.L.M.; Miranda, E.S.; Castilho, I.G.; Camargo, C.H.; Langoni, H.; Guimarães, F.F.; Araújo Júnior, J.P.; Fernandes Júnior, A. Diversity of Staphylococcus species and prevalence of enterotoxin genes isolated from milk of healthy cows and cows with subclinical mastitis. Journal of Dairy Science, 97(2): 829-837, 2014.
Recsei, P.; Kreiswirth, B.; O'Reilly, M.; Schlievert, P.; Gruss, A.; Novick, R.P. Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Molecular Genetics and Genomics, 202(1): 58-61, 1986.
Rellahan, B.L.; Jones, L.A.; Kruisbeek, A.M.; Fry, A.; Matis, L. In vivo induction of anergy in peripheral V beta 8+ T cells by staphylococcal enterotoxin B. The Journal of Experimental Medicine, 172(4): 1091-1100, 1990.
Ren, K.; Bannan, J.D.; Pancholi, V.; Cheung, A.L.; Robbins, J.C.; Fischetti, V.A.; Zabriskie, J.B. Characterization and biological properties of a new staphylococcal exotoxin. The Journal of Experimental Medicine, 180(5): 1675-1683, 1994.
Sá, M.E.P.; Cunha, M.L.R.S.; Elias, A.O.; Victória, C.; Langoni, H. Importância do Staphylococcus aureus nas mastites subclínicas: pesquisa de enterotoxinas e toxina do choque tóxico, ea relação com a contagem de células somáticas. Brazilian Journal of Veterinary Research and Animal Science, 41(5): 320-326, 2004.
Salasia, S.I.O.; Tato, S.; Sugiyono, N.; Ariyanti, D.; Prabawati, F. Genotypic characterization of Staphylococcus aureus isolated from bovines, humans, and food in Indonesia. Journal of Veterinary Science, 12(4): 353361, 2011. Senger, A.E.V.; Bizani, D. Pesquisa de Staphylococcus aureus em queijo minas frescal, produzido de forma artesanal e industrial, comercializado na cidade de Canoas/RS, Brasil. Revista de Ciências Ambientais, 5(2): 25-42, 2011.
Shafer, W.M.; Iandolo, J.J. Chromosomal locus for staphylococcal enterotoxin B. Infection and Immunity, 20(1): 273-278, 1978.
Shalita, Z.; Hertman, I.; Sarid, S. Isolation and characterization of a plasmid involved with enterotoxin B production in Staphylococcus aureus. Journal of Bacteriology, 129(1): 317-325, 1977.
Shanks, R.M.; Meehl, M.A.; Brothers, K.M.; Martinez, R.M.; Donegan, N.P.; Graber, M.L.; Cheung, A.L.; O'Toole, G.A. Genetic evidence for an alternative citrate-dependent biofilm formation pathway in Staphylococcus aureus that is dependent on fibronectin binding proteins and the GraRS twocomponent regulatory system. Infection and Immunity, 76(6): 2469-2477, 2008.
Shinji, H.; Yosizawa, Y.; Tajima, A.; Iwase, T.; Sugimoto, S.; Seki, K.; Mizunoe, Y. Role of fibronectin-binding proteins A and B in in vitro cellular infections and in vivo septic infections by Staphylococcus aureus. Infection and Immunity, 79(6): 2215-2223, 2011.
Signäs, C.; Raucci, G.; Jönsson, K.; Lindgren, P.; Anantharamaiah, G.; 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. Proceedings of the National Academy of Sciences, 86(2): 699-703, 1989.
Siqueira, J.; Speeg-Schatz, C.; Freitas, F.; Sahel, J.; Monteil, H.; Prevost, G. Channel-forming leucotoxins from Staphylococcus aureus cause severe inflammatory reactions in a rabbit eye model. Journal of Medical Microbiology, 46(6): 486-494, 1997.
Solano, C.; Echeverz M.; Lasa I. Biofilm dispersion and quorum sensing. Current Opinion in Microbiology, 18: 96-104, 2014.
Sompolinsky, D.; Samra, Z.; Karakawa, W.; Vann, W.; Schneerson, R.; Malik, Z. Encapsulation and capsular types in isolates of Staphylococcus aureus from different sources and relationship to phage types. Journal of Clinical Microbiology, 22(5): 828-834, 1985.
Song, L.; Hobaugh, M.R.; Shustak, C.; Cheley, S.; Bayley, H.; Gouaux, J.E. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science, 274(5294): 1859-1866, 1996.
Speziale, P.; Pietrocola, G.; Rindi, S.; Provenzano, M.; Provenza, G.; Di, Poto A.; Visai, L.; Arciola, C.R. Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host. Future Microbiology, 4(10): 13371352, 2009. Stewart, P.S. Mechanisms of antibiotic resistance in bacterial biofilms. International Journal of Medical Microbiology, 292(2): 107-113, 2002. Stoodley, P.; Sauer, K.; Davies, D.; Costerton, J.W. Biofilms as complex differentiatedcommunities. Annual Review of Microbiology, 56(1): 187-209, 2002.
Stringfellow, W.; Dassy, B.; Lieb, M.; Fournier J. Staphylococcus aureus growth and type 5 capsular polysaccharide production in synthetic media. Applied and Environmental Microbiology, 57(2): 618621, 1991. Su, Y.-C.; Wong, A. Identification and purification of a new staphylococcal enterotoxin, H. Applied and Environmental Microbiology, 61(4): 1438-1443, 1995.
Sutra, L.; Rainard, P.; Poutrel, B. Phagocytosis of mastitis isolates of Staphylococcus aureus and expression of type 5 capsular polysaccharide are influenced by growth in the presence of milk. Journal of Clinical Microbiology, 28(10): 2253-2258, 1990.
Tajima, A.; Iwase, T.; Shinji, H.; Seki, K.; Mizunoe, Y. Inhibition of endothelial interleukin-8 production and neutrophil transmigration by Staphylococcus aureus beta-hemolysin. Infection and Immunity, 77(1): 327-334, 2009.
Thakker, M.; Park, J.-S.; Carey, V.; Lee, J.C. Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model. Infection and Immunity, 66(11): 5183-5189, 1998.
Thurlow, L.R.; Hanke, M.L.; Fritz, T.; Angle, A.; Aldrich, A.; Williams, S.H.; Engebretsen, I.L.; Bayles, K.W.; Horswill, A.R.; Kielian T. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. The Journal of Immunology, 186(11): 6585-6596, 2011.
Tormo, M.A.; Knecht, E.; Götz, F.; Lasa, I.; Penades, J.R. Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer? Microbiology, 151(7): 2465-2475, 2005.
Torres, V.J.; Pishchany, G.; Humayun, M.; Schneewind, O.; Skaar, E. P. Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. Journal of Bacteriology, 188(24): 8421-8429, 2006. Tremaine, M.; Brockman, D.; Betley, M. Staphylococcal enterotoxin A gene (sea) expression is not affected by the accessory gene regulator (agr). Infection and Immunity, 61(1): 356-359, 1993.
Trengove, N.J.; Langton, S.R.; Stacey, M.C. Biochemical analysis of wound fluid from nonhealing and healing chronic leg ulcers. Wound Repair and Regeneration, 4(2): 234-239, 1996.
Tuchscherr, L.P.N.; Buzzola F.R.; Alvarez L.P.; Caccuri R.L.; Lee J.C.; Sordelli D.O. Capsulenegative Staphylococcus aureus induces chronic experimental mastitis in mice. Infection and Immunity, 73(12): 7932-7937, 2005.
Tweten, R.; Christianson K.; Iandolo J. Transport and processing of staphylococcal alpha-toxin. Journal of Bacteriology, 156(2): 524-528, 1983. Van Leeuwen, W.B.; Melles, D.C.; Alaidan, A.; Al-Ahdal, M.; Boelens, H.A.; Snijders, S.V.; Wertheim, H.; van Duijkeren, E.; Peeters, J.K.; van der Spek, P.J.; Gorkink, R.; Simons, G.; Verbrugh, H.A.; van Belkum, A. Host- and tissue-specific pathogenic traits of Staphylococcus aureus. Journal of bacteriology, 187(13): 4584-4591, 2005.
Veronesi, R.; Focaccia, R. Tratado de infectologia. v. 2. São Paulo: Atheneu; 2009, p.1351.
Vuong, C.; Saenz, H.L.; Götz, F.; Otto, M. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. The Journal of Infectious Diseases, 182(6): 1688-1693, 2000.
Walev, I.; Weller, U.; Strauch, S.; Foster, T.; Bhakdi, S. Selective killing of human monocytes and cytokine release provoked by sphingomyelinase (beta-toxin) of Staphylococcus aureus. Infection and Immunity, 64(8): 2974-2979, 1996.
Waryah, C.B.; Gogoi-Tiwari, J.; Wells, K.; Costantino, P.; Al-Salami, H.; Sunagar, R.; Isloor, S.; Hegde, N.; Richmond, P.; Mukkur, T. Serological versus molecular typing of surface-associated immune evading polysaccharide antigens-based phenotypes of Staphylococcus aureus. Journal of Medical Microbiology, 63(11): 1427-1431, 2014.
Wilke, G.A.;Wardenburg, J.B. Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus α-hemolysin–mediated cellular injury. Proceedings of the National Academy of Sciences, 107(30): 13473-13478, 2010.
Wilson, G.J.; Seo, K.S.; Cartwright, R.A.; Connelley, T.; Chuang-Smith, O.N.; Merriman, J. A.; Guinane, C.M.; Park, J.Y.; Bohach, G.A.; Schlievert, P.M.A novel core genome-encoded superantigen contributes to lethality of community-associated MRSA necrotizing pneumonia. PLoS pathogens, 7(10): e1002271, 2011.
Yarwood, J.M.; Schlievert, P.M. Quorum sensing in Staphylococcus infections. The Journal of Clinical Investigation, 112(11): 1620-1625, 2003. Yasuda, H.; Ajiki, Y.; Aoyama, J.; Yokota, T. Interaction between human polymorphonuclear leucocytes and bacteria released from in-vitro bacterial biofilm models. Journal of Medical Microbiology, 41(5): 359-367, 1994. Zecconi, A.; Scali, F. Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases. Immunology Letters, 150(1-2): 1222, 2013.
Zhang, S.; Iandolo, J.J.; Stewart, G.C. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS microbiology letters, 168(2): 227-233, 1998.
Published
How to Cite
Issue
Section
License
A Revista de Medicina Veterinária permite que o autor retenha os direitos de publicação sem restrições, utilizando para tal a licença Creative Commons CC BY-NC-SA 4.0.
De acordo com os termos seguintes:
Atribuição — Você deve dar o crédito apropriado, prover um link para a licença e indicar se mudanças foram feitas. Você deve fazê-lo em qualquer circunstância razoável, mas de nenhuma maneira que sugira que o licenciante apoia você ou o seu uso.
NãoComercial — Você não pode usar o material para fins comerciais.
CompartilhaIgual — Se você remixar, transformar, ou criar a partir do material, tem de distribuir as suas contribuições sob a mesma licença que o original.
Sem restrições adicionais — Você não pode aplicar termos jurídicos ou medidas de caráter tecnológico que restrinjam legalmente outros de fazerem algo que a licença permita.
