The Hsp90 Co-Chaperone Sgt1 Governs Candida albicans Morphogenesis and Drug Resistance

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Shapiro, Rebecca S ^a   Zaas, Aimee K ^b   Betancourt Quiroz, Marisol ^b   Perfect, John R ^b   Cowen, Leah E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ANTIFUNGAL AGENT; CALCINEURIN; CHAPERONE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOXYCYCLINE; ECHINOCANDIN; FLUCONAZOLE; HEAT SHOCK PROTEIN 90; MICAFUNGIN; PROTEIN; SGT 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFUNGAL RESISTANCE; ARTICLE; BIOFILM; CANDIDA ALBICANS; DRUG MECHANISM; DRUG TARGETING; DRUG TOLERABILITY; FUNGAL STRUCTURES; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS MORPHOGENESIS; MORPHOGENESIS; MOUSE; MYCOSIS; NONHUMAN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE; ANTIFUNGAL AGENTS; AZOLES; CANDIDA ALBICANS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DRUG RESISTANCE, FUNGAL; HSP90 HEAT-SHOCK PROTEINS; MORPHOGENESIS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

CANDIDA ALBICANS; MURINAE;

EID: 84866114557     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044734     Document Type: Article

References (72)

1. Martin GS, Mannino DM, Eaton S, Moss M, (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348: 1546-1554.
2. Pfaller MA, Diekema DJ, (2010) Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36: 1-53.
3. Wilson LS, Reyes CM, Stolpman M, Speckman J, Allen K, et al. (2002) The direct cost and incidence of systemic fungal infections. Value Health 5: 26-34.
4. Pfaller MA, Diekema DJ, (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20: 133-163.
5. Calderone R (2002) Candida and Candidiasis. Washington, D.C.: ASM Press.
6. Zhu W, Filler SG, (2010) Interactions of Candida albicans with epithelial cells. Cell Microbiol 12: 273-282.
7. Naglik J, Albrecht A, Bader O, Hube B, (2004) Candida albicans proteinases and host/pathogen interactions. Cell Microbiol 6: 915-926.
8. d'Enfert C, (2006) Biofilms and their role in the resistance of pathogenic Candida to antifungal agents. Curr Drug Targets 7: 465-470.
9. Shapiro RS, Robbins N, Cowen LE, (2011) Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 75: 213-267.
10. Bahn YS, Staab J, Sundstrom P, (2003) Increased high-affinity phosphodiesterase PDE2 gene expression in germ tubes counteracts CAP1-dependent synthesis of cyclic AMP, limits hypha production and promotes virulence of Candida albicans. Mol Microbiol 50: 391-409.
11. Braun BR, Head WS, Wang MX, Johnson AD, (2000) Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156: 31-44.
12. Braun BR, Kadosh D, Johnson AD, (2001) NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J 20: 4753-4761.
13. Leberer E, Harcus D, Dignard D, Johnson L, Ushinsky S, et al. (2001) Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. Mol Microbiol 42: 673-687.
14. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, et al. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
15. Rocha CR, Schroppel K, Harcus D, Marcil A, Dignard D, et al. (2001) Signaling through adenylyl cyclase is essential for hyphal growth and virulence in the pathogenic fungus Candida albicans. Mol Biol Cell 12: 3631-3643.
16. Noble SM, French S, Kohn LA, Chen V, Johnson AD, (2010) Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat Genet 42: 590-598.
17. Krueger KE, Ghosh AK, Krom BP, Cihlar RL, (2004) Deletion of the NOT4 gene impairs hyphal development and pathogenicity in Candida albicans. Microbiology 150: 229-240.
18. Richard ML, Nobile CJ, Bruno VM, Mitchell AP, (2005) Candida albicans biofilm-defective mutants. Eukaryot Cell 4: 1493-1502.
19. Kumamoto CA, Vinces MD, (2005) Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol 7: 1546-1554.
20. Gow NA, van de Veerdonk FL, Brown AJ, Netea MG, (2012) Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10: 112-122.
21. Xu XL, Lee RT, Fang HM, Wang YM, Li R, et al. (2008) Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host Microbe 4: 28-39.
22. Baldauf SL, Palmer JD, (1993) Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci U S A 90: 11558-11562.
23. Wainright PO, Hinkle G, Sogin ML, Stickel SK, (1993) Monophyletic origins of the metazoa: an evolutionary link with fungi. Science 260: 340-342.
24. Cowen LE, (2008) The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat Rev Microbiol 6: 187-198.
25. Cowen LE, Steinbach WJ, (2008) Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance. Eukaryot Cell 7: 747-764.
26. Anderson JB, (2005) Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat Rev Microbiol 3: 547-556.
27. Perlin DS, (2007) Resistance to echinocandin-class antifungal drugs. Drug Resist Updat 10: 121-130.
28. Robbins N, Uppuluri P, Nett J, Rajendran R, Ramage G, et al. (2011) Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog 7: e1002257.
29. Pearl LH, Prodromou C, (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75: 271-294.
30. Taipale M, Jarosz DF, Lindquist S, (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528.
31. Pratt WB, Toft DO, (2003) Regulation of signaling protein function and trafficking by the Hsp90/Hsp70-based chaperone machinery. Exp Biol Med 228: 111-133.
32. 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: 268-283.
33. Shapiro RS, Sellam A, Tebbji F, Whiteway M, Nantel A, et al. (2012) Pho85, Pcl1 and Hms1 Signaling Governs Candida albicans Morphogenesis Induced by High Temperature or Hsp90 Compromise. Curr Biol 22: 461-470.
34. Shapiro RS, Uppuluri P, Zaas AK, Collins C, Senn H, et al. (2009) Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr Biol 19: 621-629.
35. Cowen LE, Lindquist S, (2005) Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309: 2185-2189.
36. Cowen LE, Singh SD, Kohler JR, Collins C, Zaas AK, et al. (2009) Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci USA 106: 2818-2823.
37. Singh SD, Robbins N, Zaas AK, Schell WA, Perfect JR, et al. (2009) Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog 5: e1000532.
38. LaFayette SL, Collins C, Zaas AK, Schell WA, Betancourt-Quiroz M, 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.
39. Zuehlke A, Johnson JL, (2010) Hsp90 and co-chaperones twist the functions of diverse client proteins. Biopolymers 93: 211-217.
40. Wang X, Venable J, LaPointe P, Hutt DM, Koulov AV, et al. (2006) Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127: 803-815.
41. Caplan AJ, Mandal AK, Theodoraki MA, (2007) Molecular chaperones and protein kinase quality control. Trends Cell Biol 17: 87-92.
42. Pearl LH, (2005) Hsp90 and Cdc37 - a chaperone cancer conspiracy. Curr Opin Genet Dev 15: 55-61.
43. Bansal PK, Abdulle R, Kitagawa K, (2004) Sgt1 associates with Hsp90: an initial step of assembly of the core kinetochore complex. Mol Cell Biol 24: 8069-8079.
44. Kitagawa K, Skowyra D, Elledge SJ, Harper JW, Hieter P, (1999) SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol Cell 4: 21-33.
45. Dubacq C, Guerois R, Courbeyrette R, Kitagawa K, Mann C, (2002) Sgt1p contributes to cyclic AMP pathway activity and physically interacts with the adenylyl cyclase Cyr1p/Cdc35p in budding yeast. Eukaryot Cell 1: 568-582.
46. Hunter T, Poon RY, (1997) Cdc37: a protein kinase chaperone? Trends Cell Biol 7: 157-161.
47. Gerber MR, Farrell A, Deshaies RJ, Herskowitz I, Morgan DO, (1995) Cdc37 is required for association of the protein kinase Cdc28 with G1 and mitotic cyclins. Proc Natl Acad Sci U S A 92: 4651-4655.
48. Lee YT, Jacob J, Michowski W, Nowotny M, Kuznicki J, et al. (2004) Human Sgt1 binds HSP90 through the CHORD-Sgt1 domain and not the tetratricopeptide repeat domain. J Biol Chem 279: 16511-16517.
49. Takahashi A, Casais C, Ichimura K, Shirasu K, (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci U S A 100: 11777-11782.
50. Hnisz D, Majer O, Frohner IE, Komnenovic V, Kuchler K, (2010) The Set3/Hos2 histone deacetylase complex attenuates cAMP/PKA signaling to regulate morphogenesis and virulence of Candida albicans. PLoS Pathog 6: e1000889.
51. Fang HM, Wang Y, (2006) RA domain-mediated interaction of Cdc35 with Ras1 is essential for increasing cellular cAMP level for Candida albicans hyphal development. Mol Microbiol 61: 484-496.
52. Kelly SL, Lamb DC, Kelly DE, Manning NJ, Loeffler J, et al. (1997) Resistance to fluconazole and cross-resistance to amphotericin B in Candida albicans from AIDS patients caused by defective sterol delta5,6-desaturation. FEBS Lett 400: 80-82.
53. Robbins N, Collins C, Morhayim J, Cowen LE, (2009) Metabolic control of antifungal drug resistance. Fungal Genet Biol 47: 81-93.
54. Balashov SV, Park S, Perlin DS, (2006) Assessing resistance to the echinocandin antifungal drug caspofungin in Candida albicans by profiling mutations in FKS1. Antimicrob Agents Chemother 50: 2058-2063.
55. Wiederhold NP, Grabinski JL, Garcia-Effron G, Perlin DS, Lee SA, (2008) Pyrosequencing to detect mutations in FKS1 that confer reduced echinocandin susceptibility in Candida albicans. Antimicrob Agents Chemother 52: 4145-4148.
56. Karababa M, Valentino E, Pardini G, Coste AT, Bille J, et al. (2006) CRZ1, a target of the calcineurin pathway in Candida albicans. Mol Microbiol 59: 1429-1451.
57. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, et al. (2005) Navigating the chaperone network: An integrative map of physical and genetic interactions mediated by the Hsp90 chaperone. Cell 120: 715-727.
58. Diezmann S, Michaut M, Shapiro RS, Bader GD, Cowen LE, (2012) Mapping the Hsp90 genetic interaction network in Candida albicans reveals environmental contingency and rewired circuitry. PLoS Genet 8: e1002562.
59. Catlett MG, Kaplan KB, (2006) Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p. J Biol Chem 281: 33739-33748.
60. Lingelbach LB, Kaplan KB, (2004) The interaction between Sgt1p and Skp1p is regulated by HSP90 chaperones and is required for proper CBF3 assembly. Mol Cell Biol 24: 8938-8950.
61. Berman J, (2006) Morphogenesis and cell cycle progression in Candida albicans. Curr Opin Microbiol 9: 595-601.
62. Steensgaard P, Garre M, Muradore I, Transidico P, Nigg EA, et al. (2004) Sgt1 is required for human kinetochore assembly. EMBO Rep 5: 626-631.
63. Martins T, Maia AF, Steffensen S, Sunkel CE, (2009) Sgt1, a co-chaperone of Hsp90 stabilizes Polo and is required for centrosome organization. EMBO J 28: 234-247.
64. Bachewich C, Thomas DY, Whiteway M, (2003) Depletion of a polo-like kinase in Candida albicans activates cyclase-dependent hyphal-like growth. Mol Biol Cell 14: 2163-2180.
65. Flom GA, Langner E, Johnson JL, (2012) Identification of an Hsp90 mutation that selectively disrupts cAMP/PKA signaling in Saccharomyces cerevisiae. Curr Genet 58: 149-163.
66. da Silva Correia J, Miranda Y, Leonard N, Ulevitch R, (2007) SGT1 is essential for Nod1 activation. Proc Natl Acad Sci U S A 104: 6764-6769.
67. Chen G, Bradford WD, Seidel CW, Li R, (2012) Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy. Nature 482: 246-250.
68. Srivastava P, (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2: 185-194.
69. Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, et al. (1997) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90: 65-75.
70. Kumar R, Musiyenko A, Barik S, (2005) Plasmodium falciparum calcineurin and its association with heat shock protein 90: mechanisms for the antimalarial activity of cyclosporin A and synergism with geldanamycin. Mol Biochem Parasitol 141: 29-37.
71. Pallavi R, Roy N, Nageshan RK, Talukdar P, Pavithra SR, et al. (2010) Heat shock protein 90 as a drug target against protozoan infections: biochemical characterization of HSP90 from Plasmodium falciparum and Trypanosoma evansi and evaluation of its inhibitor as a candidate drug. J Biol Chem 285: 37964-37975.
72. Burt ET, Daly R, Hoganson D, Tsirulnikov Y, Essmann M, et al. (2003) Isolation and partial characterization of Hsp90 from Candida albicans. Ann Clin Lab Sci 33: 86-93.