Candida albicans quorum-sensing molecule farnesol modulates staphyloxanthin production and activates the thiol-based oxidative-stress response in Staphylococcus aureus

References

• Morales D, Hogan D. Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathog. 2010;6(4):e1000886.
   PubMed Web of Science ®Google Scholar
• McGavin MJ, Heinrichs DE. The staphylococci and staphylococcal pathogenesis. Front Cell Infect Microbiol. 2012. DOI:10.3389/fcimb.2012.00066
   Web of Science ®Google Scholar
• Kong E, Johnson J, Jabra-Rizk M. Community-associated methicillin-resistant Staphylococcus aureus: an enemy amidst us. PLoS Pathog. 2016;12(10):e1005837.
   PubMed Web of Science ®Google Scholar
• Jabra-Rizk MA, Kong E, Tsui C, et al. Candida albicans pathogenesis: fitting within the host-microbe damage response framework. Infect Immun. 2016;84(10):2724–2739.
   PubMed Web of Science ®Google Scholar
• Ganguly S, Mitchell A. Mucosal biofilms of Candida albicans. Curr Opin Microbiol. 2011;14(4):380–385.
   PubMed Web of Science ®Google Scholar
• Pfaller M, Diekema D. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20(1):133–163.
   PubMed Web of Science ®Google Scholar
• Peters B, Jabra-Rizk MA, Scheper M, et al. Microbial interactions and differential protein expression in Staphylococcus aureus and Candida albicans dual-species biofilms. FEMS Imm Med Microbiol. 2010;59:493–503.
   PubMed Web of Science ®Google Scholar
• Peters B, Ovchinnikova E, Schlecht L, et al. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiol. 2012;158(Pt 12):2975–2986.
   PubMed Web of Science ®Google Scholar
• Schlecht L, Peters B, Krom B, et al. Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiol. 2015;161(Pt 1):168–181.
   PubMed Web of Science ®Google Scholar
• Kong E, Kucharíková S, Van Dijck P, et al. Clinical implications of oral candidiasis: host tissue damage and disseminated bacterial disease. Infect Immun. 2015;83(2):604–613.
   PubMed Web of Science ®Google Scholar
• Kong EF, Tsui C, Kucharíková S, et al. Modulation of Staphylococcus aureus response to antimicrobials by the Candida albicans quorum sensing molecule farnesol. Antimicrob Agents Chemother. 2017;61(12):e01573–17.
   PubMed Web of Science ®Google Scholar
• Kong E, Tsui C, Kucharíková S, et al. Commensal protection of Staphylococcus aureus against antimicrobials by Candida albicans biofilm matrix. mBio. 2016;7(5):e01365–16.
   PubMed Web of Science ®Google Scholar
• Demuyser L, Jabra-Rizk MA, Van Dijck P. Microbial cell surface proteins and secreted metabolites involved in multispecies biofilms. Pathog Dis. 2014;70:219–230.
   PubMed Web of Science ®Google Scholar
• Williams P. Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology. 2007;153:3923–3938.
   PubMed Web of Science ®Google Scholar
• Hornby JM, Jensen EC, Lisec AD, et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol. 2001;67(7):2982–2992.
   PubMed Web of Science ®Google Scholar
• Sato T, Watanabe T, Mikami T, et al. Farnesol, a morphogenetic autoregulatory substance in the dimorphic fungus Candida albicans, inhibits hyphae growth through suppression of a mitogen-activated protein kinase cascade. Biol Pharm Bullet. 2004;27(5):751–752.
   PubMed Web of Science ®Google Scholar
• Uppuluri P, Mekala S, Chaffin WL. Farnesol-mediated inhibition of Candida albicans yeast growth and rescue by adiacylglycerol analogue. Yeast. 2007;24(8):681–693.
   PubMed Web of Science ®Google Scholar
• Shirtliff ME, Krom B, Meijering RM, et al. Farnesol-induced apoptosis in Candida albicans. Antimicrob Agents Chemother. 2009;53:2392–2401.
   PubMed Web of Science ®Google Scholar
• Scheper MA, Shirtliff ME, Meiller TF, et al. Farnesol a fungal quorum sensing molecule triggers apoptosis in human oral squamous carcinoma cells. Neoplasia. 2008;10(9):954–963.
   PubMed Web of Science ®Google Scholar
• Gaupp R, Ledala N, Somerville GA. Staphylococcal response to oxidative stress. Front in Cell Infect Microbiol. 2012;2(33):1–19.
   PubMed Web of Science ®Google Scholar
• Liu G, Essex A, Buchanan J, et al. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med. 2005;18(202):209–215.
   Web of Science ®Google Scholar
• Clauditz A, Resch A, Wieland K, et al. Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect Immun. 2006;74(8):4950–4953.
   PubMed Web of Science ®Google Scholar
• Pelz A, Wieland KP, Putzbach K, et al. Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J Biol Chem. 2005;16(37):32493–32498.
   Web of Science ®Google Scholar
• McCarthy MW, Walsh TJ. Drug development challenges and strategies to address emerging and resistant fungal pathogens. Expert Rev Anti Infect Ther. 2017;15(6):577–584.
   PubMed Web of Science ®Google Scholar
• Sakoulas G, Moellering RC. Increasing antibiotic resistance among methicillin-resistant Staphylococcus aureus strains. Clin Infect Dis. 2008;46(5):S360–S7.
   PubMed Web of Science ®Google Scholar
• Liu C, Liu G, Song Y, et al. A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science. 2008;7(319):1391–1394.
   Web of Science ®Google Scholar
• Harrach MF, Drossel B. Structure and dynamics of TIP3P, TIP4P, and TIP5P water near smooth and atomistic walls of different hydroaffinity. J Chem Phys. 2014;140(17):174501.
   PubMed Web of Science ®Google Scholar
• Sharp KA, Nicholls A, Friedman R, et al. Extracting hydrophobic free energies from experimental data: relationship to protein folding and theoretical models. Biochemistry. 1991;30(40):9686–9697.
   PubMed Web of Science ®Google Scholar
• Wargo MJ, Hogan DA. Fungal-bacterial interactions: a mixed bag of mingling microbes. Curr Opin Microbiol. 2006;9:359–364.
   PubMed Web of Science ®Google Scholar
• Jabra-Rizk MA. Pathogenesis of polymicrobial biofilms. Open Mycol J. 2011;5:39–43.
   Google Scholar
• Kelley WL. Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon. Mol Microbiol. 2006;62(5):1228–1238.
   PubMed Web of Science ®Google Scholar
• Alcalde-Rico M, Hernando-Amado S, Blanco P, et al. Multidrug efflux pumps at the crossroad between antibiotic resistance and bacterial virulence. Front Microbiol. 2016;21(7):1483.
   Google Scholar
• Hillion M, Antelmann H. Thiol-based redox switches in prokaryotes. Biol Chem. 2015;396(5):415–444.
   PubMed Web of Science ®Google Scholar
• Wang C, Fan J, Niu C, et al. Role of spx in biofilm formation of Staphylococcus epidermidis. FEMS Immunol Med Microbiol. 2010;59:152–160.
   PubMedGoogle Scholar
• Pamp SJ, Frees D, Engelmann S, et al. Spx is a global effector impacting stress tolerance and bofilm formation in Staphylococcus aureus. J Bacteriol. 2006;188(13):4861–4870.
   PubMed Web of Science ®Google Scholar
• Cheung AL, Zhang G. Global regulation of virulence determinants in Staphylococcus aureus by the SarA protein family. Front Biosci. 2002;1(7):1825–1842.
   Google Scholar
• Horsburgh MJ, Ingham E, Simon SJ. In Staphylococcus aureus, Fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol. 2001;183(2):468–475.
   PubMed Web of Science ®Google Scholar
• Sun F, Ding Y, Ji Q, et al. Protein cysteine phosphorylation of SarA/MgrA family transcriptional regulators mediates bacterial virulence and antibiotic resistance. Proc Natl Acad Sci U S A. 2012;109(38):15461–15466.
   PubMed Web of Science ®Google Scholar
• Cui L, Iwamoto A, Lian JQ, et al. Novel mechanism of antibiotic resistance originating in vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother. 2006;50:2.
   Web of Science ®Google Scholar
• Truong-Bolduc Q, Dunman P, Strahilevitz J, et al. MgrA is a multiple regulator of two new efflux pumps in Staphylococcus aureus. J Bacteriol. 2005;187(7):2395–2405.
   PubMed Web of Science ®Google Scholar
• Truong-Bolduc Q, Zhang X, Hooper D. Characterization of NorR protein, a multifunctional regulator of norA expression in Staphylococcus aureus. J Bacteriol. 2003;185(10):3127–3138.
   PubMed Web of Science ®Google Scholar
• Kaatz G, Thyagarajan R, Seo S. Effect of promoter region mutations and mgrA overexpression on transcription of norA, which encodes a Staphylococcus aureus multidrug efflux transporter. Antimicrob Agents Chemother. 2005;49(1):161–169.
   PubMed Web of Science ®Google Scholar
• Cosgrove K, Coutts G, Jonsson IM, et al. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol. 2007;189(3):1025–1035.
   PubMed Web of Science ®Google Scholar
• Ballal A, Manna AC. Regulation of superoxide dismutase (sod) genes by SarA in Staphylococcus aureus. J Bacteriol. 2009;191(10):3301–3310.
   PubMed Web of Science ®Google Scholar
• Hammer ND, Skaar EP. Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol. 2011;65:129–147.
   PubMed Web of Science ®Google Scholar
• Troxell B, Hassan HM. Transcriptional regulation by ferric uptake regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol. 2013;3(59). DOI:10.3389/fcimb.2013.00059
   Web of Science ®Google Scholar
• Neal D, Hammer ND, Skaar EP. Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol. 2011;65(10). DOI:10.1146/annurev-micro-090110-102851
   Web of Science ®Google Scholar
• Pang YY, Schwartz J, Bloomberg S, et al. Methionine sulfoxide reductases protect against oxidative stress in Staphylococcus aureus encountering exogenous oxidants and human neutrophils. J Innate Immun. 2014;6(3):353–364.
   PubMed Web of Science ®Google Scholar
• Zhao G, Ceci P, Ilari A, et al. Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli. J Biol Chem. 2002;277(31):27689–27696.
   PubMed Web of Science ®Google Scholar
• Intapa C, Basile J, Jabra-Rizk MA. Farnesol-induced apoptosis in oral squamous carcinoma cells is mediated by MRP1 extrusion and depletion of intracellular glutathione. Trends Cancer Res. 2014;10:1–6.
   Google Scholar
• Zhu J, Krom BP, Sanglard D, et al. Farnesol-induced apoptosis in Candida albicans is mediated by Cdr1-p extrusion and depletion of intracellular glutathione. PloS One. 2011;6(12):e28830.
   PubMed Web of Science ®Google Scholar
• Gillum AM, Tsay EY, Kirsch DR. Isolation of the Candida albicans gene for orotidine’5ʹ-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Molec Gen Genet. 1984;198:179–182.
   PubMedGoogle Scholar
• Krause J, Geginat G, Tammer I. Prostaglandin E2 from Candida albicans stimulates the growth of Staphylococcus aureus in mixed biofilms. PLoS One. 2015;10(8):e0135404.
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359.
   PubMed Web of Science ®Google Scholar
• Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:10.
   Web of Science ®Google Scholar
• Wang J, Wolf RM, Caldwell JW, et al. Development and testing of a general amber force field. J Comput Chem. 2004;25(9):1157–1174.
   PubMed Web of Science ®Google Scholar
• Wang J, Wang W, Kollman PA. D.A. C. automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model. 2006;25(2):247–260.
   PubMed Web of Science ®Google Scholar