Heat shock protein 90 (Hsp90): A novel antifungal target against Aspergillus fumigatus

References

• Ali MM, Roe SM, Vaughan CK, et al. (2006). Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440:1013–17
   PubMed Web of Science ®Google Scholar
• Bali P, Pranpat M, Bradner J, et al. (2005). Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors. J Biol Chem 280:26729–34
   PubMed Web of Science ®Google Scholar
• Blum G, Kainzner B, Grif K, et al. (2013). In vitro and in vivo role of heat shock protein 90 in Amphotericin B resistance of Aspergillus terreus. Clin Microbiol Infect 19:50–5
   PubMed Web of Science ®Google Scholar
• Borkovich KA, Farrelly FW, Finkelstein DB, et al. (1989). hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9:3919–30
   PubMed Web of Science ®Google Scholar
• Burnie JP, Matthews RC. (1991). Heat shock protein 88 and Aspergillus infection. J Clin Microbiol 29:2099–106
   PubMed Web of Science ®Google Scholar
• Chamilos G, Kontoyiannis DP. (2005). Update on antifungal drug resistance mechanisms of Aspergillus fumigatus. Drug Resist Updat 8:344–58
   PubMed Web of Science ®Google Scholar
• Cohen LA, Amin S, Marks PA, et al. (1999). Chemoprevention of carcinogen-induced mammary tumorigenesis by the hybrid polar cytodifferentiation agent, suberanilohydroxamic acid (SAHA). Anticancer Res 19:4999–5005
   PubMed Web of Science ®Google Scholar
• Colot HV, Park G, Turner GE, et al. (2006). A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103:10352–7
   PubMed Web of Science ®Google Scholar
• Cowen LE. (2008). The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat Rev Microbiol 6:187–98
   PubMed Web of Science ®Google Scholar
• Cowen LE. (2013). The fungal Achilles' heel: targeting Hsp90 to cripple fungal pathogens. Curr Opin Microbiol 16:377–84
   PubMed Web of Science ®Google Scholar
• Cowen LE, Lindquist S. (2005). Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309:2185–9
   PubMed Web of Science ®Google Scholar
• Cowen LE, Carpenter AE, Matangkasombut O, et al. (2006). Genetic architecture of Hsp90-dependent drug resistance. Eukaryot Cell 5:2184–8
   PubMed Web of Science ®Google Scholar
• Cowen LE, Singh SD, Kohler JR, et al. (2009). Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci USA 106:2818–23
   PubMed Web of Science ®Google Scholar
• Denikus N, Orfaniotou F, Wulf G, et al. (2005). Fungal antigens expressed during invasive aspergillosis. Infect Immun 73:4704–13
   PubMed Web of Science ®Google Scholar
• Diezmann S, Michaut M, Shapiro RS, et al. (2012). Mapping the Hsp90 genetic interaction network in Candida albicans reveals environmental contingency and rewired circuitry. PLoS Genet 8:e1002562
   PubMed Web of Science ®Google Scholar
• Du C, Wingard JR, Cheng S, et al. (2012). Serum IgG responses against Aspergillus proteins before hematopoietic stem cell transplantation or chemotherapy identify patients who develop invasive aspergillosis. Biol Blood Marrow Transplant 18:1927–34
   PubMed Web of Science ®Google Scholar
• Elaut G, Torok G, Vinken M, et al. (2002). Major phase I biotransformation pathways of Trichostatin a in rat hepatocytes and in rat and human liver microsomes. Drug Metab Dispos 30:1320–8
   PubMed Web of Science ®Google Scholar
• Elaut G, Torok G, Papeleu P, et al. (2004). Rat hepatocyte suspensions as a suitable in vitro model for studying the biotransformation of histone deacetylase inhibitors. Altern Lab Anim 32:105–12
   PubMed Web of Science ®Google Scholar
• Elaut G, Laus G, Alexandre E, et al. (2007). A metabolic screening study of trichostatin A (TSA) and TSA-like histone deacetylase inhibitors in rat and human primary hepatocyte cultures. J Pharmacol Exp Ther 321:400–8
   PubMed Web of Science ®Google Scholar
• Erlejman AG, Lagadari M, Toneatto J, et al. (2014). Regulatory role of the 90-kDa-heat-shock protein (Hsp90) and associated factors on gene expression. Biochim Biophys Acta 1839:71–87
   PubMed Web of Science ®Google Scholar
• Fortwendel JR, Juvvadi PR, Perfect BZ, et al. (2010). Transcriptional regulation of chitin synthases by calcineurin controls paradoxical growth of Aspergillus fumigatus in response to caspofungin. Antimicrob Agents Chemother 54:1555–63
   PubMed Web of Science ®Google Scholar
• Fortwendel JR, Juvvadi PR, Pinchai N, et al. (2009). Differential effects of inhibiting chitin and 1,3-{beta}-D-glucan synthesis in ras and calcineurin mutants of Aspergillus fumigatus. Antimicrob Agents Chemother 53:476–82
   PubMed Web of Science ®Google Scholar
• Grandin N, Charbonneau M. (2001). Hsp90 levels affect telomere length in yeast. Mol Genet Genomics 265:126–34
   PubMed Web of Science ®Google Scholar
• High KP. (1994). The antimicrobial activities of cyclosporine, FK506, and rapamycin. Transplantation 57:1689–700
   PubMed Web of Science ®Google Scholar
• High KP, Washburn RG. (1997). Invasive aspergillosis in mice immunosuppressed with cyclosporin A, tacrolimus (FK506), or sirolimus (rapamycin). J Infect Dis 175:222–5
   PubMed Web of Science ®Google Scholar
• Hodgetts S, Matthews R, Morrissey G, et al. (1996). Over-expression of Saccharomyces cerevisiae hsp90 enhances the virulence of this yeast in mice. FEMS Immunol Med Microbiol 16:229–34
   PubMedGoogle Scholar
• Hodgetts S, Nooney L, Al-Akeel R, et al. (2008). Efungumab and caspofungin: pre-clinical data supporting synergy. J Antimicrob Chemother 61:1132–9
   PubMed Web of Science ®Google Scholar
• Huh WK, Falvo JV, Gerke LC, et al. (2003). Global analysis of protein localization in budding yeast. Nature 425:686–91
   PubMed Web of Science ®Google Scholar
• Imai J, Yahara I. (2000). Role of HSP90 in salt stress tolerance via stabilization and regulation of calcineurin. Mol Cell Biol 20:9262–70
   PubMed Web of Science ®Google Scholar
• Jackson SE. (2013). Hsp90: structure and function. Top Curr Chem 328:155–240
   PubMed Web of Science ®Google Scholar
• Jhaveri K, Taldone T, Modi S, Chiosis G. (2012). Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers. Biochim Biophys Acta 1823:742–55
   PubMed Web of Science ®Google Scholar
• Johnson JL. (2012). Evolution and function of diverse Hsp90 homologs and cochaperone proteins. Biochim Biophys Acta 1823:607–13
   PubMed Web of Science ®Google Scholar
• Juvvadi PR, Fortwendel JR, Pinchai N, et al. (2008). Calcineurin localizes to the hyphal septum in Aspergillus fumigatus: implications for septum formation and conidiophore development. Eukaryot Cell 7:1606–10
   PubMed Web of Science ®Google Scholar
• Juvvadi PR, Fortwendel JR, Rogg LE, et al. (2011). Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in Aspergillus fumigatus. Mol Microbiol 82:1235–59
   PubMed Web of Science ®Google Scholar
• Juvvadi PR, Gehrke C, Fortwendel JR, et al. (2013). Phosphorylation of Calcineurin at a novel serine-proline rich region orchestrates hyphal growth and virulence in Aspergillus fumigatus. PLoS Pathog 9:e1003564
   PubMed Web of Science ®Google Scholar
• Kelly WK, Richon VM, O'Connor O, et al. (2003). Phase I clinical trial of histone deacetylase inhibitor: suberoylanilide hydroxamic acid administered intravenously. Clin Cancer Res 9:3578–88
   PubMed Web of Science ®Google Scholar
• Kelly WK, O'Connor OA, Krug LM, et al. (2005). Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol 23:3923–31
   PubMed Web of Science ®Google Scholar
• Kontoyiannis DP, Lewis RE, Osherov N, et al. (2003). Combination of caspofungin with inhibitors of the calcineurin pathway attenuates growth in vitro in Aspergillus species. J Antimicrob Chemother 51:313–16
   PubMed Web of Science ®Google Scholar
• Kontoyiannis DP, Marr KA, Park BJ, et al. (2010). Prospective surveillance for invasive fungal infections in hematopoietic stem cell transplant recipients, 2001–2006: overview of the Transplant-Associated Infection Surveillance Network (TRANSNET) Database. Clin Infect Dis 50:1091–100
   PubMed Web of Science ®Google Scholar
• Kozubowski L, Aboobakar EF, Cardenas ME, Heitman J. (2011). Calcineurin colocalizes with P-bodies and stress granules during thermal stress in Cryptococcus neoformans. Eukaryot Cell 10:1396–402
   PubMed Web of Science ®Google Scholar
• Kumar R, Musiyenko A, Barik S. (2003). The heat shock protein 90 of Plasmodium falciparum and antimalarial activity of its inhibitor, geldanamycin. Malar J 2:30
   PubMed Web of Science ®Google Scholar
• LaFayette SL, Collins C, Zaas AK, et al. (2010). PKC signaling regulates drug resistance of the fungal pathogen Candida albicans via circuitry comprised of Mkc1, calcineurin, and Hsp90. PLoS Pathog 6:e1001069
   PubMed Web of Science ®Google Scholar
• Lamoth F, Juvvadi PR, Fortwendel JR, Steinbach WJ. (2012). Heat shock protein 90 is required for conidiation and cell wall integrity in Aspergillus fumigatus. Eukaryot Cell 11:1324–32
   PubMed Web of Science ®Google Scholar
• Lamoth F, Juvvadi PR, Gehrke C, Steinbach WJ. (2013). In vitro activity of calcineurin and heat shock protein 90 Inhibitors against Aspergillus fumigatus azole- and echinocandin-resistant strains. Antimicrob Agents Chemother 57:1035–9
   PubMed Web of Science ®Google Scholar
• Lamoth F, Juvvadi PR, Gehrke C, et al. (2014a). Transcriptional activation of heat shock protein 90 mediated via a proximal promoter region as trigger of caspofungin resistance in Aspergillus fumigatus. J Infect Dis 209:473–81
   PubMed Web of Science ®Google Scholar
• Lamoth F, Juvvadi PR, Soderblom EJ, et al. (2014b). A key lysine residue in the heat shock protein 90 (Hsp90) required for azole and echinocandin resistance in Aspergillus fumigatus. Antimicrob Agents Chemother 58:1889–96
   PubMed Web of Science ®Google Scholar
• Leach MD, Klipp E, Cowen LE, Brown AJ. (2012a). Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs. Nat Rev Microbiol 10:693–704
   PubMed Web of Science ®Google Scholar
• Leach MD, Budge S, Walker L, et al. (2012b). Hsp90 orchestrates transcriptional regulation by Hsf1 and cell wall remodelling by MAPK signalling during thermal adaptation in a pathogenic yeast. PLoS Pathog 8:e1003069
   PubMed Web of Science ®Google Scholar
• Lee CT, Graf C, Mayer FJ, et al. (2012). Dynamics of the regulation of Hsp90 by the co-chaperone Sti1. EMBO J 31:1518–28
   PubMed Web of Science ®Google Scholar
• Louie A, Stein DS, Zack JZ, et al. (2011). Dose range evaluation of Mycograb C28Y variant, a human recombinant antibody fragment to heat shock protein 90, in combination with amphotericin B-desoxycholate for treatment of murine systemic candidiasis. Antimicrob Agents Chemother 55:3295–304
   PubMed Web of Science ®Google Scholar
• Martinez-Ruiz A, Villanueva L, Gonzalez de Orduna C, et al. (2005). S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proc Natl Acad Sci USA 102:8525–30
   PubMed Web of Science ®Google Scholar
• Matsumoto K, Minami M, Shinozaki F, et al. (2011). Hsp90 is involved in the formation of P-bodies and stress granules. Biochem Biophys Res Commun 407:720–4
   PubMed Web of Science ®Google Scholar
• Matthews RC, Burnie JP, Tabaqchali S. (1984). Immunoblot analysis of the serological response in systemic candidosis. Lancet 2:1415–18
   PubMed Web of Science ®Google Scholar
• Matthews RC, Burnie JP, Tabaqchali S. (1987). Isolation of immunodominant antigens from sera of patients with systemic candidiasis and characterization of serological response to Candida albicans. J Clin Microbiol 25:230–7
   PubMed Web of Science ®Google Scholar
• Matthews RC, Rigg G, Hodgetts S, et al. (2003). Preclinical assessment of the efficacy of mycograb, a human recombinant antibody against fungal HSP90. Antimicrob Agents Chemother 47:2208–16
   PubMed Web of Science ®Google Scholar
• Mollapour M, Neckers L. (2012). Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim Biophys Acta 1823:648–55
   PubMed Web of Science ®Google Scholar
• Morozov IY, Jones MG, Spiller DG, et al. (2010). Distinct roles for Caf1, Ccr4, Edc3 and CutA in the co-ordination of transcript deadenylation, decapping and P-body formation in Aspergillus nidulans. Mol Microbiol 76:503–16
   PubMed Web of Science ®Google Scholar
• Pachl J, Svoboda P, Jacobs F, et al. (2006). A randomized, blinded, multicenter trial of lipid-associated amphotericin B alone versus in combination with an antibody-based inhibitor of heat shock protein 90 in patients with invasive candidiasis. Clin Infect Dis 42:1404–13
   PubMed Web of Science ®Google Scholar
• Pappas PG, Alexander BD, Andes DR, et al. (2010). Invasive fungal infections among organ transplant recipients: results of the Transplant-Associated Infection Surveillance Network (TRANSNET). Clin Infect Dis 50:1101–11
   PubMed Web of Science ®Google Scholar
• Pfaller MA, Messer SA, Georgopapadakou N, et al. (2009). Activity of MGCD290, a Hos2 histone deacetylase inhibitor, in combination with azole antifungals against opportunistic fungal pathogens. J Clin Microbiol 47:3797–804
   PubMed Web of Science ®Google Scholar
• Retzlaff M, Stahl M, Eberl HC, et al. (2009). Hsp90 is regulated by a switch point in the C-terminal domain. EMBO Rep 10:1147–53
   PubMed Web of Science ®Google Scholar
• Richie DL, Ghannoum MA, Isham N, et al. (2012). Nonspecific effect of Mycograb on amphotericin B MIC. Antimicrob Agents Chemother 56:3963–4
   PubMed Web of Science ®Google Scholar
• Robbins N, Leach MD, Cowen LE. (2012). Lysine deacetylases Hda1 and Rpd3 regulate Hsp90 function thereby governing fungal drug resistance. Cell Rep 2:878–88
   PubMed Web of Science ®Google Scholar
• Sanderson L, Taylor GW, Aboagye EO, et al. (2004). Plasma pharmacokinetics and metabolism of the histone deacetylase inhibitor trichostatin a after intraperitoneal administration to mice. Drug Metab Dispos 32:1132–8
   PubMed Web of Science ®Google Scholar
• Scheufler C, Brinker A, Bourenkov G, et al. (2000). Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199–210
   PubMed Web of Science ®Google Scholar
• Schmid AB, Lagleder S, Grawert MA, et al. (2012). The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop. EMBO J 31:1506–17
   PubMed Web of Science ®Google Scholar
• Scroggins BT, Robzyk K, Wang D, et al. (2007). An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell 25:151–9
   PubMed Web of Science ®Google Scholar
• Senn H, Shapiro RS, Cowen LE. (2012). Cdc28 provides a molecular link between Hsp90, morphogenesis, and cell cycle progression in Candida albicans. Mol Biol Cell 23:268–83
   PubMed Web of Science ®Google Scholar
• Shapiro RS, Cowen L. (2010). Coupling temperature sensing and development: Hsp90 regulates morphogenetic signalling in Candida albicans. Virulence 1:45–8
   PubMed Web of Science ®Google Scholar
• Shapiro RS, Sellam A, Tebbji F, et al. (2012). Pho85, Pcl1, and Hms1 signaling governs Candida albicans morphogenesis induced by high temperature or Hsp90 compromise. Curr Biol 22:461–70
   PubMed Web of Science ®Google Scholar
• Shapiro RS, Uppuluri P, Zaas AK, et al. (2009). Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr Biol 19:621–9
   PubMed Web of Science ®Google Scholar
• Singh SD, Robbins N, Zaas AK, et al. (2009). Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog 5:e1000532
   PubMed Web of Science ®Google Scholar
• Smith WL, Edlind TD. (2002). Histone deacetylase inhibitors enhance Candida albicans sensitivity to azoles and related antifungals: correlation with reduction in CDR and ERG upregulation. Antimicrob Agents Chemother 46:3532–9
   PubMed Web of Science ®Google Scholar
• Soroka J, Wandinger SK, Mausbacher N, et al. (2012). Conformational switching of the molecular chaperone Hsp90 via regulated phosphorylation. Mol Cell 45:517–28
   PubMed Web of Science ®Google Scholar
• Steinbach WJ, Juvvadi PR, Fortwendel JR, Rogg LE. (2011). Newer combination antifungal therapies for invasive aspergillosis. Med Mycol 49:S77–81
   PubMed Web of Science ®Google Scholar
• Steinbach WJ, Schell WA, Blankenship JR, et al. (2004). In vitro interactions between antifungals and immunosuppressants against Aspergillus fumigatus. Antimicrob Agents Chemother 48:1664–9
   PubMed Web of Science ®Google Scholar
• Suzuki Y, Minami M, Suzuki M, et al. (2009). The Hsp90 inhibitor geldanamycin abrogates colocalization of eIF4E and eIF4E-transporter into stress granules and association of eIF4E with eIF4G. J Biol Chem 284:35597–604
   PubMed Web of Science ®Google Scholar
• Tapia H, Morano KA. (2010). Hsp90 nuclear accumulation in quiescence is linked to chaperone function and spore development in yeast. Mol Biol Cell 21:63–72
   PubMed Web of Science ®Google Scholar
• Trojer P, Brandtner EM, Brosch G, et al. (2003). Histone deacetylases in fungi: novel members, new facts. Nucleic Acids Res 31:3971–81
   PubMed Web of Science ®Google Scholar
• Tsou YL, Lin YW, Chang HW, et al. (2013). Heat shock protein 90: role in enterovirus 71 entry and assembly and potential target for therapy. PLoS One 8:e77133
   PubMed Web of Science ®Google Scholar
• Vermeulen E, Lagrou K, Verweij PE. (2013). Azole resistance in Aspergillus fumigatus: a growing public health concern. Curr Opin Infect Dis 26:493–500
   PubMed Web of Science ®Google Scholar
• Whitesell L, Lindquist SL. (2005). HSP90 and the chaperoning of cancer. Nat Rev Cancer 5:761–72
   PubMed Web of Science ®Google Scholar
• Wiederhold NP. (2007). Attenuation of echinocandin activity at elevated concentrations: a review of the paradoxical effect. Curr Opin Infect Dis 20:574–8
   PubMed Web of Science ®Google Scholar
• Yang Y, Rao R, Shen J, et al. (2008). Role of acetylation and extracellular location of heat shock protein 90alpha in tumor cell invasion. Cancer Res 68:4833–42
   PubMed Web of Science ®Google Scholar
• Yoshimoto H, Saltsman K, Gasch AP, et al. (2002). Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J Biol Chem 277:31079–88
   PubMed Web of Science ®Google Scholar
• Yu X, Guo ZS, Marcu MG, et al. (2002). Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J Natl Cancer Inst 94:504–13
   PubMed Web of Science ®Google Scholar
• Zhao H, Michaelis ML, Blagg BS. (2012). Hsp90 modulation for the treatment of Alzheimer's disease. Adv Pharmacol 64:1–25
   PubMedGoogle Scholar
• Zhao R, Davey M, Hsu YC, et al. (2005). Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120:715–27
   PubMed Web of Science ®Google Scholar