Combinatorial stresses kill pathogenic Candida species

References

• Odds FC. Candida and Candidosis, 2nd ed. London, UK: Baillière Tindall, 1988.
   Google Scholar
• Calderone RA. Candida and Candidiasis. Washington DC: ASM Press, 2002
   Google Scholar
• Perlroth DJ, Sanders GD, Gould MK. Effectiveness and cost-effectiveness of thrombolysis in submassive pulmonary embolism. Arch Intern Med 2007; 167: 74–80.
   PubMedGoogle Scholar
• Miceli MH, Diaz JA, Lee SA. Emerging opportunistic yeast infections. Lancet Infect Dis 2011; 11: 142–151.
   PubMed Web of Science ®Google Scholar
• Odds FC, Brown AJP, Gow NAR. Antifungal agents: mechanisms of action. Trends Microbiol 2003; 11: 272–279.
   PubMed Web of Science ®Google Scholar
• White TC, Marr KA, Bowden RA. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 1998; 11: 382–402.
   PubMed Web of Science ®Google Scholar
• Dadarkar SS, Fonseca LC, Mishra PB, . Phenotypic and genotypic assessment of concomitant drug-induced toxic effects in liver, kidney and blood. J Appl Toxicol 2011; 31: 117–130.
   PubMedGoogle Scholar
• Brown JP, Haynes K, Quinn J. Nitrosative and oxidative stress responses in fungal pathogenicity. Curr Opin Micro 2009; 12: 384–391.
   PubMed Web of Science ®Google Scholar
• Mansour MK, Levitz SM. Interactions of fungi with phagocytes. Curr Opin Microbiol 2002; 5: 359–365.
   PubMed Web of Science ®Google Scholar
• Gross NT, Nessa K, Camner P, Jarstrand C. Production of nitric oxide by rat alveolar macrophages stimulated by Cryptococcus neoformans or Aspergillus fumigatus. Med Myco 1999; 37: 151–157.
   PubMed Web of Science ®Google Scholar
• Steinberg BE, Huynh KK, Brodovitch A, . A cation counterflux supports lysosomal acidification. J Cell Biol 2010; 189: 1171–1186.
   Google Scholar
• Jamieson DJ, Stephen DW, Terrière EC. Analysis of the adaptive oxidative stress response of Candida albicans. FEMS Microbiol Lett 1996; 15: 83–88.
   Google Scholar
• Hromatka BS, Noble SM, Johnson AD. Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol Biol Cell 2005; 16: 4814–4826.
   PubMed Web of Science ®Google Scholar
• Chiranand W, McLeod I, Zhou H, . CTA4 transcription factor mediates induction of nitrosative stress response in Candida albicans. Eukary Cell 2008; 7: 268–278.
   PubMedGoogle Scholar
• Nikolaou E, Agrafioti I, Stumpf M, . Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 2009; 9: 44.
   PubMed Web of Science ®Google Scholar
• Smith DA, Morgan BA, Quinn J. Stress signalling to fungal stress-activated protein kinase pathways. FEMS Microbiol Lett 2010; 306: 1–8.
   PubMed Web of Science ®Google Scholar
• Smith DA, Nicholls S, Morgan BA, Brown AJP, Quinn J. A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol Biol Cell 2004; 15: 4179–4190.
   PubMed Web of Science ®Google Scholar
• Enjalbert B, Smith DA, Cornell MJ, . Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol Biol Cell 2006; 17: 1018–1032.
   PubMed Web of Science ®Google Scholar
• Gregori C, Schuller C, Roetzer A, . The high-osmolarity glycerol response pathway in the human fungal pathogen Candida glabrata strain ATCC 2001 lacks a signaling branch that operates in baker's yeast. Eukary Cell 2007; 6: 1635–1645.
   PubMedGoogle Scholar
• Cheetham J, Smith DA, da Silva Dantas A, . A single MAPKKK regulates the Hog1 MAPK pathway in the pathogenic fungus Candida albicans. Mol Biol Cell 2007; 18: 4603–4614.
   PubMed Web of Science ®Google Scholar
• Moye-Rowley WS. Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryot Cell 2003; 2: 381–389.
   PubMed Web of Science ®Google Scholar
• Toone WM, Jones N. AP-1 transcription factors in yeast. Curr Opin Genet Dev 1999; 9: 55–61.
   PubMed Web of Science ®Google Scholar
• Alarco AM, Raymond M. The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J Bacteriol 1999; 181: 700–708.
   PubMed Web of Science ®Google Scholar
• Zhang X, De Micheli M, Coleman ST, Sanglard D, Moye-Rowley WS. Analysis of the oxidative stress regulation of the Candida albicans transcription factor, Cap1p. Mol Microbiol 2000; 36: 618–629.
   PubMedGoogle Scholar
• Znaidi S, Barker KS, Weber S, . Identification of the Candida albicans Cap1p Regulon. Eukaryotic Cell 2009; 8: 806–820.
   PubMedGoogle Scholar
• Tillmann A, Gow NA, Brown AJP. Nitric oxide and nitrosative stress tolerance in yeast. Biochem Soc Trans 2011; 39: 219–223.
   PubMed Web of Science ®Google Scholar
• Martinez-Pastor MT, Marchler G, Schuller C, . The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 1996; 15: 2227–2235.
   PubMed Web of Science ®Google Scholar
• Estruch F. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 2000; 24: 469–486.
   PubMed Web of Science ®Google Scholar
• Gasch AP, Spellman PT, Kao CM, . Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000; 11: 4241–4257.
   PubMed Web of Science ®Google Scholar
• Causton HC, Ren B, Koh SS, . Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 2001; 12: 323–337.
   PubMed Web of Science ®Google Scholar
• Roetzer A, Gregori C, Jennings AM, . Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol Microbiol 2008; 69: 603–620.
   PubMed Web of Science ®Google Scholar
• Nicholls S, Straffon M, Enjalbert B, . Msn2- and Msn4-like transcription factors play no obvious roles in the stress responses of the fungal pathogen Candida albicans. Eukary Cell 2004; 3: 1111–1123.
   PubMed Web of Science ®Google Scholar
• Ramsdale M, Selway L, Stead D, . MNL1 regulates weak acid-induced stress responses of the fungal pathogen Candida albicans. Mol Biol Cell 2008; 19: 4393–4403.
   PubMed Web of Science ®Google Scholar
• Galagan JE, Henn MR, Ma LJ, Cuomo CA, Birren B. Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Res 2005; 15: 1620–1631
   PubMed Web of Science ®Google Scholar
• Fitzpatrick DA, Logue ME, Stajich JE, Butler G. A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 2006 6: 99.
   PubMed Web of Science ®Google Scholar
• Lewis JG, Learmonth RP, Watson K. Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae. Microbiology 1995; 141: 687–694.
   PubMed Web of Science ®Google Scholar
• Walker LA, MacCallum DM, Bertram G, . Genome-wide analysis of Candida albicans gene expression patterns during infection of the mammalian kidney. Fungal Gen Biol 2009; 46: 210–219.
   PubMedGoogle Scholar
• Fonzi WA, Irwin MY. Isogenic strain construction and gene mapping in Candida albicans. Genetics 1993; 134: 717–728.
   PubMed Web of Science ®Google Scholar
• Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJP. CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 2000; 16: 325–327.
   PubMedGoogle Scholar
• Gillum AM, Tsay EY, Kirsch DR. Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 1984; 198: 179–182.
   PubMedGoogle Scholar
• Nicholls S, Leach M, Priest C, Brown AJP. Role of the heat shock transcription factor, Hsf1, in a major fungal pathogen that is obligately associated with warm-blooded animals. Mol Microbiol 2009; 74: 844–861.
   Google Scholar
• Alberghina L, Porro D, Shapiro H, Srienc F, Steen H. Microbial analysis at the single-cell level. J Microbiol Meth 2000; 42: 1–2.
   PubMedGoogle Scholar
• Runarsson TP, Yao X. Search biases in constrained evolutionary optimization. IEEE Trans Syst Man Cybern 2005; 35: 233–243.
   Web of Science ®Google Scholar
• Shapiro RS, Uppuluri P, Zaas AK, . Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr Biol 2009; 19: 621–629.
   PubMed Web of Science ®Google Scholar
• Enjalbert B, MacCallum DM, Odds FC, Brown AJP. Niche-specific activation of the oxidative stress response by the pathogenic fungus Candida albicans. Infect Immun 2007; 75: 2143–2151.
   PubMed Web of Science ®Google Scholar
• Bogdan C, Rollinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 2000; 12: 64–76.
   PubMed Web of Science ®Google Scholar
• Missall TA, Lodge JK, McEwen JE. Mechanisms of resistance to oxidative and nitrosative stress: implications for fungal survival in mammalian hosts. Eukary Cell 2004; 3: 835–846.
   PubMed Web of Science ®Google Scholar
• Hrabie JA, Klose JR, Wink DA, . New nitric oxide-releasing zwitterions derived from polyamines. J Org Chem 1993; 58: 1472–1476.
   Web of Science ®Google Scholar
• Keefer LK, Nims RW, Davies KM, Wink DA. ‘NONOates’ (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Meth Enzymol 1996; 268: 281–293.
   PubMed Web of Science ®Google Scholar
• Ullmann BD, Myers H, Chiranand W, . Inducible defense mechanism against nitric oxide in Candida albicans. Eukaryot Cell 2004; 3: 715–723.
   PubMed Web of Science ®Google Scholar
• Phillips AJ, Sudbery I, Ramsdale M. Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc Natl Acad Sci USA 2003; 100: 14327–14332.
   PubMed Web of Science ®Google Scholar
• Calcagno AM, Bignell E, Rogers TR, . Candida glabrata Ste11 is involved in adaptation to hypertonic stress, maintenance of wild type levels of filamentation and plays a role in virulence. Med Mycol 2005, 43: 355–364.
   PubMed Web of Science ®Google Scholar
• Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 2002; 66: 300–372.
   PubMed Web of Science ®Google Scholar
• San Jose C, Alonso-Monge R, Perez-Diaz R, Pla J, Nombela C. The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans. J Bacteriol 1996; 178: 5850–5952.
   PubMed Web of Science ®Google Scholar
• Quinn J, Findlay VJ, Dawson K, . Distinct regulatory proteins control the graded transcriptional response to increasing H2O2 levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 2002; 13: 805–816.
   PubMed Web of Science ®Google Scholar
• Roetzer A, Klopf E, Gratz N, . Regulation of Candida glabrata oxidative stress resistance is adapted to host environment. FEBS Lett 2011; 585: 319–327.
   PubMed Web of Science ®Google Scholar
• Kaur R, Ma B, Cormack BP. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci USA 2007; 104: 7628–7633.
   PubMed Web of Science ®Google Scholar
• Fradin C, De Groot P, MacCallum D, . Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 2005; 56: 397–415.
   PubMed Web of Science ®Google Scholar
• Alonso-Monge R, Navarro-Garcia F, Roman E, . The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryo Cell 2003; 2: 351–361.
   PubMed Web of Science ®Google Scholar
• Arana DM, Alonso-Monge R, Du C, Calderone R, Pla J. Differential susceptibility of mitogen-activated protein kinase pathway mutants to oxidative-mediated killing by phagocytes in the fungal pathogen Candida albicans. Cell Microbiol 2007; 9: 1647–1659.
   PubMed Web of Science ®Google Scholar
• Cowen LE, Lindquist S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 2005; 309: 2185–2189.
   PubMed Web of Science ®Google Scholar