Red wines and flavonoids diminish Staphylococcus aureus virulence with anti-biofilm and anti-hemolytic activities

References

• Akiyama H, Fujii K, Yamasaki O, Oono T, Iwatsuki K. 2001. Antibacterial action of several tannins against Staphylococcus aureus. J Antimicrob Chemother. 48:487–491.10.1093/jac/48.4.487
   PubMed Web of Science ®Google Scholar
• Begun J, Gaiani JM, Rohde H, Mack D, Calderwood SB, Ausubel FM, Sifri CD. 2007. Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog. 3:e57.10.1371/journal.ppat.0030057
   Google Scholar
• Boles BR, Horswill AR. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4:e1000052.10.1371/journal.ppat.1000052
   PubMed Web of Science ®Google Scholar
• Caiazza NC, O’Toole GA. 2003. Alpha-toxin is required for biofilm formation by Staphylococcus aureus. J Bacteriol. 185:3214–3217.10.1128/JB.185.10.3214-3217.2003
   PubMed Web of Science ®Google Scholar
• Careri M, Corradini C, Elviri L, Nicoletti I, Zagnoni I. 2003. Direct HPLC analysis of quercetin and trans-resveratrol in red wine, grape, and winemaking byproducts. J Agric Food Chem. 51:5226–5231.10.1021/jf034149g
   PubMed Web of Science ®Google Scholar
• Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ. 2008. The biology and future prospects of antivirulence therapies. Nat Rev Microbiol. 6:17–27.10.1038/nrmicro1818
   PubMed Web of Science ®Google Scholar
• Conseil G, Baubichon-Cortay H, Dayan G, Jault JM, Barron D, Di Pietro A. 1998. Flavonoids: a class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proc Natl Acad Sci USA. 95:9831–9836.10.1073/pnas.95.17.9831
   PubMed Web of Science ®Google Scholar
• Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science. 284:1318–1322.10.1126/science.284.5418.1318
   PubMed Web of Science ®Google Scholar
• Cottart CH, Nivet-Antoine V, Laguillier-Morizot C, Beaudeux JL. 2010. Resveratrol bioavailability and toxicity in humans. Mol Nutr Food Res. 54:7–16.10.1002/(ISSN)1613-4133
   PubMed Web of Science ®Google Scholar
• Daglia M, Papetti A, Grisoli P, Aceti C, Dacarro C, Gazzani G. 2007. Antibacterial activity of red and white wine against oral streptococci. J Agric Food Chem. 55:5038–5042.10.1021/jf070352q
   PubMed Web of Science ®Google Scholar
• Dinges MM, Orwin PM, Schlievert PM. 2000. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev. 13:16–34.10.1128/CMR.13.1.16-34.2000
   PubMed Web of Science ®Google Scholar
• Forester SC, Waterhouse AL. 2009. Metabolites are key to understanding health effects of wine polyphenolics. J Nutr. 139:1824S–1831S.10.3945/jn.109.107664
   PubMedGoogle Scholar
• German JB, Walzem RL. 2000. The health benefits of wine. Annu Rev Nutr. 20:561–593.10.1146/annurev.nutr.20.1.561
   PubMed Web of Science ®Google Scholar
• Hancock V, Dahl M, Vejborg RM, Klemm P. 2010. Dietary plant components ellagic acid and tannic acid inhibit Escherichia coli biofilm formation. J Med Microbiol. 59:496–498.10.1099/jmm.0.013680-0
   PubMed Web of Science ®Google Scholar
• Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, et al. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology. 148:87–102.
   PubMed Web of Science ®Google Scholar
• Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersbøll BK, Molin S. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology. 146:2395–2407.
   PubMed Web of Science ®Google Scholar
• Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T, Mizunoe Y. 2010. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature. 465:346–349.10.1038/nature09074
   PubMed Web of Science ®Google Scholar
• Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, et al. 1997. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science. 275:218–220.10.1126/science.275.5297.218
   PubMed Web of Science ®Google Scholar
• Kim Y, Mylonakis E. 2012. Caenorhabditis elegans immune conditioning with the probiotic bacterium Lactobacillus acidophilus strain NCFM enhances Gram-positive immune responses. Infect Immun. 80:2500–2508.10.1128/IAI.06350-11
   PubMed Web of Science ®Google Scholar
• Korem M, Gov Y, Shirron N, Shuster A, Rosenberg M. 2007. Alcohol increases hemolysis by staphylococci. FEMS Microbiol Lett. 269:153–159.10.1111/fml.2007.269.issue-1
   PubMed Web of Science ®Google Scholar
• Lamuela-Raventós RM, Romero-Pérez AI, Waterhouse AL, Torre-Borona MC. 1995. Direct HPLC analysis of of cis- and trans-resveratrol and piceid isomers in Spanish red Vitis vinifera wines. J Agric Food Chem. 43:281–283.10.1021/jf00050a003
   Web of Science ®Google Scholar
• Larrauri JA, Sánchez-Moreno C, Rupérez P, Saura-Calixto F. 1999. Free radical scavenging capacity in the aging of selected red Spanish wines. J Agric Food Chem. 47:1603–1606.10.1021/jf980607n
   PubMed Web of Science ®Google Scholar
• Larzábal M, Mercado EC, Vilte DA, Salazar-González H, Cataldi A, Navarro-Garcia F. 2010. Designed coiled-coil peptides inhibit the type three secretion system of enteropathogenic Escherichia coli. PLoS One. 5:e9046.10.1371/journal.pone.0009046
   PubMed Web of Science ®Google Scholar
• Lee J-H, Park J-H, Cho HS, Joo SW, Cho MH, Lee J. 2013. Antibiofilm activities of quercetin and tannic acid against Staphylococcus aureus. Biofouling. 29:491–499.10.1080/08927014.2013.788692
   PubMed Web of Science ®Google Scholar
• Liu CI, Liu GY, Song Y, Yin F, Hensler ME, Jeng WY, Nizet V, Wang AH, Oldfield E. 2008. A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science. 319:1391–1394.10.1126/science.1153018
   PubMed Web of Science ®Google Scholar
• Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med. 339:520–532.10.1056/NEJM199808203390806
   PubMed Web of Science ®Google Scholar
• Mahendran B, Raman N, Kim DJ. 2006. Purification and characterization of tannase from Paecilomyces variotii: hydrolysis of tannic acid using immobilized tannase. Appl Microbiol Biotechnol. 70:444–450.10.1007/s00253-005-0082-y
   PubMed Web of Science ®Google Scholar
• McRae JM, Dambergs RG, Kassara S, Parker M, Jeffery DW, Herderich MJ, Smith PA. 2012. Phenolic compositions of 50 and 30 year sequences of Australian red wines: the impact of wine age. J Agric Food Chem. 60:10093–10102.10.1021/jf301571q
   PubMed Web of Science ®Google Scholar
• Merken HM, Beecher GR. 2000. Liquid chromatographic method for the separation and quantification of prominent flavonoid aglycones. J Chromatogr A. 897:177–184.10.1016/S0021-9673(00)00826-8
   PubMed Web of Science ®Google Scholar
• Møretrø T, Daeschel MA. 2004. Wine is bactericidal to foodborne pathogens. J Food Sci. 69:M251–M257.
   Web of Science ®Google Scholar
• Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C. 2003. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature. 424:277–283.10.1038/nature01789
   PubMed Web of Science ®Google Scholar
• Ohlsen K, Koller KP, Hacker J. 1997. Analysis of expression of the alpha-toxin gene (hla) of Staphylococcus aureus by using a chromosomally encoded hla:lacZ gene fusion. Infect Immun. 65:3606–3614.
   PubMed Web of Science ®Google Scholar
• Opie LH, Lecour S. 2007. The red wine hypothesis: from concepts to protective signalling molecules. Eur Heart J. 28:1683–1693.10.1093/eurheartj/ehm149
   PubMed Web of Science ®Google Scholar
• Pace-Asciak CR, Hahn S, Diamandis EP, Soleas G, Goldberg DM. 1995. The red wine phenolics trans-resveratrol and quercetin block human platelet aggregation and eicosanoid synthesis: implications for protection against coronary heart disease. Clin Chim Acta. 235:207–219.10.1016/0009-8981(95)06045-1
   PubMed Web of Science ®Google Scholar
• Park J, Jagasia R, Kaufmann GF, Mathison JC, Ruiz DI, Moss JA, Meijler MM, Ulevitch RJ, Janda KD. 2007. Infection control by antibody disruption of bacterial quorum sensing signaling. Chem Biol. 14:1119–1127.10.1016/j.chembiol.2007.08.013
   PubMed Web of Science ®Google Scholar
• Payne DE, Martin NR, Parzych KR, Rickard AH, Underwood A, Boles BR. 2012. Tannic acid inhibits Staphylococcus aureus surface colonization in an IsaA dependent manner. Infect Immun. 81:496–504.
   PubMed Web of Science ®Google Scholar
• Pratt LA, Kolter R. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol. 30:285–293.10.1046/j.1365-2958.1998.01061.x
   PubMed Web of Science ®Google Scholar
• Scalbert A. 1991. Antimicrobial properties of tannins. Phytochemistry. 30:3875–3883.10.1016/0031-9422(91)83426-L
   Web of Science ®Google Scholar
• Selma MV, Larrosa M, Beltrán D, Lucas R, Morales JC, Tomás-Barberán FA, Espín de Gea JC. 2012. Resveratrol and some glucosyl-, glucosyl-acyl-, and glucuronide derivatives reduce E. coli O157:H7, S. Typhimurium, and L. monocytogenes Scott A adhesion to colonic epithelial cell lines. J Agric Food Chem. 60:7367–7374.10.1021/jf203967u
   PubMed Web of Science ®Google Scholar
• Sifri CD, Begun J, Ausubel FM, Calderwood SB. 2003. Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun. 71:2208–2217.10.1128/IAI.71.4.2208-2217.2003
   PubMed Web of Science ®Google Scholar
• Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE. 1996. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science. 274:1859–1865.10.1126/science.274.5294.1859
   PubMed Web of Science ®Google Scholar
• Stewart PS, Costerton JW. 2001. Antibiotic resistance of bacteria in biofilms. Lancet. 358:135–138.10.1016/S0140-6736(01)05321-1
   PubMed Web of Science ®Google Scholar
• Truchado P, Giménez-Bastida JA, Larrosa M, Castro-Ibáñez I, Espín JC, Tomás-Barberán F, García-Conesa MT, Allende A. 2012. Inhibition of quorum sensing (QS) in Yersinia enterocolitica by an orange extract rich in glycosylated flavanones. J Agric Food Chem. 60:8885–8894.10.1021/jf301365a
   PubMed Web of Science ®Google Scholar
• Truchado P, Tomás-Barberán F, Larrosa M, Allende A. 2012. Food phytochemicals act as quorum sensing inhibitors reducing production and/or degrading autoinducers of Yersinia enterocolitica and Erwinia carotovora. Food Control. 24:78–85.10.1016/j.foodcont.2011.09.006
   Web of Science ®Google Scholar
• Valenzano DR, Terzibasi E, Genade T, Cattaneo A, Domenici L, Cellerino A. 2006. Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr Biol. 16:296–300.10.1016/j.cub.2005.12.038
   PubMed Web of Science ®Google Scholar
• Vaquero MJR, Alberto MR, de Nadra MCM. 2007. Antibacterial effect of phenolic compounds from different wines. Food Control. 18:93–101.10.1016/j.foodcont.2005.08.010
   Web of Science ®Google Scholar
• Weston SA, Parish CR. 1990. New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J Immunol Methods. 133:87–97.10.1016/0022-1759(90)90322-M
   PubMed Web of Science ®Google Scholar
• Wyatt MA, Wang W, Roux CM, Beasley FC, Heinrichs DE, Dunman PM, Magarvey NA. 2010. Staphylococcus aureus nonribosomal peptide secondary metabolites regulate virulence. Science. 329:294–296.10.1126/science.1188888
   PubMed Web of Science ®Google Scholar