Fungicide Xylaria sp. BCC 1067 extract induces reactive oxygen species and activates multidrug resistance system in Saccharomyces cerevisiae

Papers of special interest have been highlighted as: • of interest; •• of considerable interest

References

• 1 Teodoro GR, Brighenti FL, Delbem AC et al. Antifungal activity of extracts and isolated compounds from Buchenavia tomentosa on Candida albicans and non-albicans. Future Microbiol. 10(6), 917–927 (2015).
  CASGoogle Scholar
• 2 Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20(1), 133–163 (2007).
  Medline CASGoogle Scholar
• 3 Zavrel M, White TC. Medically important fungi respond to azole drugs: an update. Future Microbiol. 10(8), 1355–1373 (2015).
  CASGoogle Scholar
• 4 Odds FC, Brown AJP, Gow NaR. Antifungal agents: mechanisms of action. Trends Microbiol. 11(6), 272–279 (2003).
  Medline CASGoogle Scholar
• 5 Mesa-Arango AC, Scorzoni L, Zaragoza O. It only takes one to do many jobs: amphotericin B as antifungal and immunomodulatory drug. Front. Microbiol. 3, 286 (2012).
  Medline CASGoogle Scholar
• 6 Ferreira GF, Baltazar Lde M, Santos JR et al. The role of oxidative and nitrosative bursts caused by azoles and amphotericin B against the fungal pathogen Cryptococcus gattii. J. Antimicrob. Chemother. 68(8), 1801–1811 (2013).
  Medline CASGoogle Scholar
• 7 Dockrell DH. Salvage therapy for invasive aspergillosis. J. Antimicrob. Chemother. 61(h 1), i41–i44 (2008).
  Medline CASGoogle Scholar
• 8 Laniado-Laborin R, Cabrales-Vargas MN. Amphotericin B: side effects and toxicity. Rev. Iberoam. Micol. 26(4), 223–227 (2009).
  MedlineGoogle Scholar
• 9 Sanguinetti M, Posteraro B, Lass-Florl C. Antifungal drug resistance among Candida species: mechanisms and clinical impact. Mycoses 58(h 2), 2–13 (2015).
  MedlineGoogle Scholar
• 10 Hoehamer CF, Cummings ED, Hilliard GM, Rogers PD. Changes in the proteome of Candida albicans in response to azole, polyene, and echinocandin antifungal agents. Antimicrob. Agents Chemother. 54(5), 1655–1664 (2010).
  Medline CASGoogle Scholar
• 11 Liu TT, Lee RE, Barker KS et al. Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob. Agents Chemother. 49(6), 2226–2236 (2005).
  Medline CASGoogle Scholar
• 12 Agarwal AK, Rogers PD, Baerson SR et al. Genome-wide expression profiling of the response to polyene, pyrimidine, azole, and echinocandin antifungal agents in Saccharomyces cerevisiae. J. Biol. Chem. 278(37), 34998–35015 (2003).
  Medline CASGoogle Scholar
• 13 Davies BW, Kohanski MA, Simmons LA, Winkler JA, Collins JJ, Walker GC. Hydroxyurea induces hydroxyl radical-mediated cell death in Escherichia coli. Mol. Cell 36(5), 845–860 (2009).
  Medline CASGoogle Scholar
• 14 Herrero E, Ros J, Bellí G, Cabiscol E. Redox control and oxidative stress in yeast cells. Biochim. Biophys. Acta 1780(11), 1217–1235 (2008).
  Medline CASGoogle Scholar
• 15 Carmel-Harel O, Storz G. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol. 54, 439–461 (2000).
  Medline CASGoogle Scholar
• 16 Morano KA, Grant CM, Moye-Rowley WS. The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190(4), 1157–1195 (2012).
  Medline CASGoogle Scholar
• 17 Gulshan K, Rovinsky SA, Coleman ST, Moye-Rowley WS. Oxidant-specific folding of Yap1p regulates both transcriptional activation and nuclear localization. J. Biol. Chem. 280(49), 40524–40533 (2005).
  Medline CASGoogle Scholar
• 18 Toone WM, Morgan BA, Jones N. Redox control of AP-1-like factors in yeast and beyond. Oncogene 20(19), 2336–2346 (2001).
  Medline CASGoogle Scholar
• 19 Rodrigues-Pousada C, Menezes RA, Pimentel C. The Yap family and its role in stress response. Yeast 27(5), 245–258 (2010).
  Medline CASGoogle Scholar
• 20 Thepnok P, Ratanakhanokchai K, Soontorngun N. The novel zinc cluster regulator Tog1 plays important roles in oleate utilization and oxidative stress response in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 450(4), 1276–1282 (2014).
  Medline CASGoogle Scholar
• 21 Tangsombatvichit P, Semkiv MV, Sibirny AA, Jensen LT, Ratanakhanokchai K, Soontorngun N. Zinc cluster protein Znf1, a novel transcription factor of non-fermentative metabolism in Saccharomyces cerevisiae. FEMS Yeast Res. 15(2), pii: fou002 (2015).
  MedlineGoogle Scholar
• 22 Jansuriyakul S, Somboon P, Rodboon N, Kurylenko O, Sibirny A, Soontorngun N. The zinc cluster transcriptional regulator Asg1 transcriptionally coordinates oleate utilization and lipid accumulation in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 100(10), 4549–4560 (2016).
  Medline CASGoogle Scholar
• 23 Schüller C, Mamnun YM, Wolfger H, Rockwell N, Thorner J, Kuchler K. Membrane-active compounds activate the transcription factors Pdr1 and Pdr3 connecting pleiotropic drug resistance and membrane lipid homeostasis in Saccharomyces cerevisiae. Mol. Biol. Cell 18(12), 4932–4944 (2007).
  Medline CASGoogle Scholar
• 24 Macpherson S, Larochelle M, Turcotte B. A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol. Biol. Rev. 70(3), 583–604 (2006).
  Medline CASGoogle Scholar
• 25 Katzmann DJ, Burnett PE, Golin J, Mahe Y, Moye-Rowley WS. Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol. Cell. Biol. 14(7), 4653–4661 (1994).
  Medline CASGoogle Scholar
• 26 Akache B, Turcotte B. New regulators of drug sensitivity in the family of yeast zinc cluster proteins. J. Biol. Chem. 277(24), 21254–21260 (2002).
  Medline CASGoogle Scholar
• 27 Larochelle M, Drouin S, Robert F, Turcotte B. Oxidative stress-activated zinc cluster protein Stb5 has dual activator/repressor functions required for pentose phosphate pathway regulation and NADPH production. Mol. Cell. Biol. 26(17), 6690–6701 (2006).
  Medline CASGoogle Scholar
• 28 Fardeau V, Lelandais G, Oldfield A et al. The central role of PDR1 in the foundation of yeast drug resistance. J. Biol. Chem. 282(7), 5063–5074 (2007).
  Medline CASGoogle Scholar
• 29 Leppert G, Mcdevitt R, Falco SC, Van Dyk TK, Ficke MB, Golin J. Cloning by gene amplification of two loci conferring multiple drug resistance in Saccharomyces. Genetics 125(1), 13–20 (1990).
  Medline CASGoogle Scholar
• 30 Golin J, Ambudkar SV. The multidrug transporter Pdr5 on the 25th anniversary of its discovery: an important model for the study of asymmetric ABC transporters. Biochem. J. 467(3), 353–363 (2015).
  Medline CASGoogle Scholar
• 31 Lamping E, Monk BC, Niimi K et al. Characterization of three classes of membrane proteins involved in fungal azole resistance by functional hyperexpression in Saccharomyces cerevisiae. Eukaryot. Cell. 6(7), 1150–1165 (2007).
  Medline CASGoogle Scholar
• 32 Fleming A. On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. 1929. Bull. World Health Org. 79(8), 780–790 (2001).
  Medline CASGoogle Scholar
• 33 Isaka M, Jaturapat A, Kladwang W et al. Antiplasmodial compounds from the wood-decayed fungus Xylaria sp. BCC 1067. Planta. Med. 66(5), 473–475 (2000).
  Medline CASGoogle Scholar
• 34 Liu X, Dong M, Chen X, Jiang M, Lv X, Zhou J. Antimicrobial activity of an endophytic Xylaria sp.YX-28 and identification of its antimicrobial compound 7-amino-4-methylcoumarin. Appl. Microbiol. Biotechnol. 78(2), 241–247 (2008). • Identifies new antifungals from microorganism.
  Medline CASGoogle Scholar
• 35 Phonghanpot S, Punya J, Tachaleat A et al. Biosynthesis of Xyrrolin, a new cytotoxic hybrid polyketide/non-ribosomal peptide pyrroline with anticancer potential, in Xylaria sp. BCC 1067. Chembiochem 13(6), 895–903 (2012).
  Medline CASGoogle Scholar
• 36 Wang XN, Tan RX, Liu JK. Xylactam, a new nitrogen-containing compound from the fruiting bodies of ascomycete Xylaria euglossa. J. Antibiot. (Tokyo) 58(4), 268–270 (2005).
  Medline CASGoogle Scholar
• 37 Jang YW, Lee IK, Kim YS et al. Xylarinic acids A and B, new antifungal polypropionates from the fruiting body of Xylaria polymorpha. J. Antibiot. (Tokyo) 60(11), 696–699 (2007).
  Medline CASGoogle Scholar
• 38 Hu QX, Zhang GQ, Zhang RY, Hu DD, Wang HX, Ng TB. A novel aspartic protease with HIV-1 reverse transcriptase inhibitory activity from fresh fruiting bodies of the wild mushroom Xylaria hypoxylon. J. Biomed. Biotechnol. 2012, 728975 (2012).
  MedlineGoogle Scholar
• 39 Song F, Wu S-H, Zhai Y-Z, Xuan Q-C, Wang T. Secondary metabolites from the genus Xylaria and their bioactivities. Chem. Biodivers. 11(5), 673–694 (2014).
  Medline CASGoogle Scholar
• 40 Amnuaykanjanasin A, Punya J, Paungmoung P et al. Diversity of type I polyketide synthase genes in the wood-decay fungus Xylaria sp. BCC 1067. FEMS Microbiol. Lett. 251(1), 125–136 (2005).
  Medline CASGoogle Scholar
• 41 Winzeler EA, Shoemaker DD, Astromoff A et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285(5429), 901–906 (1999).
  Medline CASGoogle Scholar
• 42 Jensen AN, Chindaudomsate W, Thitiananpakorn K, Mongkolsuk S, Jensen LT. Improper protein trafficking contributes to artemisinin sensitivity in cells lacking the KDAC Rpd3p. FEBS Lett. 588(21), 4018–4025 (2014).
  Medline CASGoogle Scholar
• 43 Decottignies A, Grant AM, Nichols JW, De Wet H, Mcintosh DB, Goffeau A. ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem. 273(20), 12612–12622 (1998).
  Medline CASGoogle Scholar
• 44 Longtine MS, Mckenzie A 3rd, Demarini DJ et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14(10), 953–961 (1998).
  Medline CASGoogle Scholar
• 45 Adams A, Gottschling DE, Kaiser CA, Stearns T. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, NY, USA, 12 (1998).
  Google Scholar
• 46 Standards NCFCL. Reference methods for broth dilution antifungal susceptibility testing of yeast: approved standard. NCCLS document M27-A (2002).
  Google Scholar
• 47 Dhamgaye S, Devaux F, Manoharlal R et al. In vitro effect of malachite green on Candida albicans involves multiple pathways and transcriptional regulators UPC2 and STP2. Antimicrob. Agents Chemother. 56(1), 495–506 (2012).
  Medline CASGoogle Scholar
• 48 Zhou Y, Wang G, Li Y et al. In vitro interactions between Aspirin and Amphotericin B against planktonic cells and biofilm cells of Candida albicans and C. parapsilosis. Antimicrob. Agents Chemother. 56(6), 3250–3260 (2012).
  Medline CASGoogle Scholar
• 49 Odds FC. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52(1), 1 (2003).
  Medline CASGoogle Scholar
• 50 Wu X-Z, Cheng A-X, Sun L-M, Sun S-J, Lou H-X. Plagiochin E, an antifungal bis (bibenzyl), exerts its antifungal activity through mitochondrial dysfunction-induced reactive oxygen species accumulation in Candida albicans. Biochim. Biophys. Acta 1790(8), 770–777 (2009).
  Medline CASGoogle Scholar
• 51 Belenky P, Camacho D, Collins JJ. Fungicidal drugs induce a common oxidative-damage cellular death pathway. Cell. Rep. 3(2), 350–358 (2013). • Provides new perspective to antifungal drug research.
  Medline CASGoogle Scholar
• 52 Grintzalis K, Georgiou CD, Schneider YJ. An accurate and sensitive Coomassie Brilliant Blue G-250-based assay for protein determination. Anal. Biochem. 480, 28–30 (2015).
  Medline CASGoogle Scholar
• 53 Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65(1–2), 55–63 (1983).
  Medline CASGoogle Scholar
• 54 Zhao Y, Macgurn JA, Liu M, Emr S. The ART-Rsp5 ubiquitin ligase network comprises a plasma membrane quality control system that protects yeast cells from proteotoxic stress. eLife 2, e00459 (2013).
  MedlineGoogle Scholar
• 55 Hazen KC. Fungicidal versus fungistatic activity of terbinafine and itraconazole: an in vitro comparison. J. Am. Acad. Dermatol. 38(5 Pt 3), S37–S41 (1998).
  Medline CASGoogle Scholar
• 56 Vazquez JA. Combination antifungal therapy: the new frontier. Future Microbiol. 2(2), 115–139 (2007). • Provides a comprehensive overview of antifungal therapy.
  CASGoogle Scholar
• 57 Gruda I, Dussault N. Effect of the aggregation state of amphotericin B on its interaction with ergosterol. Biochem. Cell. Biol. 66(3), 177–183 (1988).
  Medline CASGoogle Scholar
• 58 De Nadal E, Ammerer G, Posas F. Controlling gene expression in response to stress. Nat. Rev. Genet. 12(12), 833–845 (2011).
  Medline CASGoogle Scholar
• 59 Redza-Dutordoir M, Averill-Bates DA. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta 1863(12), 2977–2992 (2016).
  Medline CASGoogle Scholar
• 60 Guha G, Mandal T, Rajkumar V, Ashok Kumar R. Antimycin A-induced mitochondrial apoptotic cascade is mitigated by phenolic constituents of Phyllanthus amarus aqueous extract in Hep3B cells. Food Chem. Toxicol. 48(12), 3449–3457 (2010).
  Medline CASGoogle Scholar
• 61 Kamata H, Hirata H. Redox regulation of cellular signalling. Cell Signal 11(1), 1–14 (1999).
  Medline CASGoogle Scholar
• 62 Vanden Berghe T, Denecker G, Brouckaert G, Krysko DV, D'herde K, Vandenabeele P. More than one way to die. In: Tumor Necrosis Factor: Methods and Protocols. Corti A, Ghezzi P (Eds). Humana Press Totowa, NJ, USA, 101–126 (2004).
  Google Scholar
• 63 Liu Y, Liu X, Qu Y, Wang X, Li L, Zhao X. Inhibitors of reactive oxygen species accumulation delay and/or reduce the lethality of several antistaphylococcal agents. Antimicrob. Agents Chemother. 56(11), 6048–6050 (2012).
  Medline CASGoogle Scholar
• 64 Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic. Biol. Med. 51(5), 1000–1013 (2011).
  Medline CASGoogle Scholar
• 65 Sanglard D. Emerging threats in antifungal-resistant fungal pathogens. Front. Med. (Lausanne) 3, 11 (2016).
  MedlineGoogle Scholar
• 66 Odds FC. Interactions among amphotericin B, 5-fluorocytosine, ketoconazole, and miconazole against pathogenic fungi in vitro. Antimicrob. Agents Chemother. 22(5), 763–770 (1982).
  Medline CASGoogle Scholar
• 67 Spanakis EK, Aperis G, Mylonakis E. New agents for the treatment of fungal infections: clinical efficacy and gaps in coverage. Clin. Infect. Dis. 43(8), 1060–1068 (2006).
  Medline CASGoogle Scholar
• 68 Wu W, Dai H, Bao L et al. Isolation and structural elucidation of proline-containing cyclopentapeptides from an endolichenic Xylaria sp. J. Nat. Prod. 74(5), 1303–1308 (2011).
  Medline CASGoogle Scholar
• 69 Palacios DS, Dailey I, Siebert DM, Wilcock BC, Burke MD. Synthesis-enabled functional group deletions reveal key underpinnings of amphotericin B ion channel and antifungal activities. Proc. Natl Acad. Sci. USA 108(17), 6733–6738 (2011).
  Medline CASGoogle Scholar
• 70 Wilcock BC, Endo MM, Uno BE, Burke MD. The C2′-OH of Amphotericin B plays an important role in binding the primary sterol of human but not yeast cells. J. Am. Chem. Soc. 135(23), 8488–8491 (2013).
  Medline CASGoogle Scholar
• 71 Brasseur R, Vandenbosch C, Van Den Bossche H, Ruysschaert JM. Mode of insertion of miconazole, ketoconazole and deacylated ketoconazole in lipid layers. A conformational analysis. Biochem. Pharmacol. 32(14), 2175–2180 (1983).
  Medline CASGoogle Scholar
• 72 Cope JE. Mode of action of miconazole on Candida albicans: effect on growth, viability and K+ release. J. Gen. Microbiol. 119(1), 245–251 (1980).
  Medline CASGoogle Scholar
• 73 Arora D, Sharma N, Singamaneni V et al. Isolation and characterization of bioactive metabolites from Xylaria psidii, an endophytic fungus of the medicinal plant Aegle marmelos and their role in mitochondrial dependent apoptosis against pancreatic cancer cells. Phytomedicine 23(12), 1312–1320 (2016).
  Medline CASGoogle Scholar
• 74 Farrugia G, Balzan R. Oxidative stress and programmed cell death in yeast. Front. Oncol. 2, 64 (2012). •• Provides comprehensive overview of oxidative stress and programmed cell death in a model yeast. Present new knowledge and recent discovery.
  MedlineGoogle Scholar
• 75 Menezes Regina A, Amaral C, Batista-Nascimento L et al. Contribution of Yap1 towards Saccharomyces cerevisiae adaptation to arsenic-mediated oxidative stress. Biochem. J. 414(2), 301–311 (2008).
  Medline CASGoogle Scholar
• 76 Mesa-Arango AC, Trevijano-Contador N, Roman E et al. The production of reactive oxygen species is a universal action mechanism of Amphotericin B against pathogenic yeasts and contributes to the fungicidal effect of this drug. Antimicrob. Agents Chemother. 58(11), 6627–6638 (2014). • Describes a mechanism of action of Amphotericin B and its fungicidal effect.
  MedlineGoogle Scholar
• 77 Zhao X, Hong Y, Drlica K. Moving forward with reactive oxygen species involvement in antimicrobial lethality. J. Antimicrob. Chemother. 70(3), 639–642 (2015).
  Medline CASGoogle Scholar
• 78 Zhao X, Drlica K. Reactive oxygen species and the bacterial response to lethal stress. Curr. Opin. Microbiol. 21, 1–6 (2014).
  MedlineGoogle Scholar
• 79 Wang X, Zhao X. Contribution of oxidative damage to antimicrobial lethality. Antimicrob. Agents Chemother. 53(4), 1395–1402 (2009).
  Medline CASGoogle Scholar
• 80 Mangum LC, Borazjani A, Stokes JV et al. Organochlorine insecticides induce nadph oxidase-dependent reactive oxygen species in human monocytic cells via phospholipase a(2)/arachidonic acid. Chem. Res. Toxicol. 28(4), 570–584 (2015).
  Medline CASGoogle Scholar
• 81 Cohen BA, Pilpel Y, Mitra RD, Church GM. Discrimination between paralogs using microarray analysis: application to the Yap1p and Yap2p transcriptional networks. Mol. Biol. Cell 13(5), 1608–1614 (2002).
  Medline CASGoogle Scholar
• 82 Fernandes L, Rodrigues-Pousada C, Struhl K. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol. Cell. Biol. 17(12), 6982–6993 (1997).
  Medline CASGoogle Scholar
• 83 Burger RM, Drlica K. Superoxide protects Escherichia coli from bleomycin mediated lethality. J. Inorg. Biochem. 103(9), 1273–1277 (2009).
  Medline CASGoogle Scholar
• 84 Burger RM, Peisach J, Blumberg WE, Horwitz SB. Iron-bleomycin interactions with oxygen and oxygen analogues. Effects on spectra and drug activity. J. Biol. Chem. 254(21), 10906–10912 (1979).
  Medline CASGoogle Scholar
• 85 Thorpe GW, Reodica M, Davies MJ et al. Superoxide radicals have a protective role during H₂O₂ stress. Mol. Biol. Cell 24(18), 2876–2884 (2013).
  Medline CASGoogle Scholar
• 86 Shingu-Vazquez M, Traven A. Mitochondria and fungal pathogenesis: drug tolerance, virulence, and potential for antifungal therapy. Eukaryot. Cell 10(11), 1376–1383 (2011).
  Medline CASGoogle Scholar
• 87 Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130(5), 797–810 (2007).
  Medline CASGoogle Scholar
• 88 Kalyanaraman B, Darley-Usmar V, Davies KJ et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic. Biol. Med. 52(1), 1–6 (2012).
  Medline CASGoogle Scholar
• 89 Sun N, Fonzi W, Chen H et al. Azole susceptibility and transcriptome profiling in Candida albicans mitochondrial electron transport chain complex I mutants. Antimicrob. Agents Chemother. 57(1), 532–542 (2013).
  Medline CASGoogle Scholar
• 90 Gulshan K, Schmidt JA, Shahi P, Moye-Rowley WS. Evidence for the bifunctional nature of mitochondrial phosphatidylserine decarboxylase: role in Pdr3-dependent retrograde regulation of PDR5 expression. Mol. Cell. Biol. 28(19), 5851–5864 (2008).
  Medline CASGoogle Scholar
• 91 Shahi P, Moye-Rowley WS. Coordinate control of lipid composition and drug transport activities is required for normal multidrug resistance in fungi. Biochim. Biophys. Acta 1794(5), 852–859 (2009).
  Medline CASGoogle Scholar
• 92 Zhizhang M, Pingping Z, Wanru C. Studies on the sedative and sleeping effects of Wuling mycelia and its pharmacological mechanism. Chin. Pharm. J. 6 (1999).
  Google Scholar
• 93 Calderone R, Li D, Traven A. System-level impact of mitochondria on fungal virulence: to metabolism and beyond. FEMS Yeast Res. 15(4), fov027 (2015).
  MedlineGoogle Scholar