Mapping the Hsp90 genetic interaction network in candida albicans reveals environmental contingency and rewired circuitry

PLoS Genetics

Volumn 8, Issue 3, 2012, Pages

  Diezmann, Stephanie ^a   Michaut, Magali ^b   Shapiro, Rebecca S ^a   Bader, Gary D ^b   Cowen, Leah E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; HEAT SHOCK PROTEIN 90; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE HOG 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AHR1; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BENZOQUINONE DERIVATIVE; GELDANAMYCIN; MACROCYCLIC LACTAM; PHOSPHOTRANSFERASE;

ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENVIRONMENTAL CONTINGENCY; FUNGAL PHENOMENA AND FUNCTIONS; FUNGUS GROWTH; GENE INTERACTION; GENE MAPPING; GENETIC INTERACTION NETWORK; NONHUMAN; CULTURE MEDIUM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

CANDIDA ALBICANS; EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; BENZOQUINONES; CANDIDA ALBICANS; CULTURE MEDIA; ENVIRONMENTAL MICROBIOLOGY; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; HSP90 HEAT-SHOCK PROTEINS; LACTAMS, MACROCYCLIC; PHOSPHOTRANSFERASES; PROTEIN INTERACTION MAPS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84859223051     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002562     Document Type: Article

References (53)

1. 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.
2. Wandinger SK, Richter K, Buchner J, (2008) The Hsp90 chaperone machinery. J Biol Chem 283: 18473-18477.
3. Trepel J, Mollapour M, Giaccone G, Neckers L, (2010) Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 10: 537-549.
4. Pearl LH, Prodromou C, (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75: 271-294.
5. Jarosz DF, Taipale M, Lindquist S, (2010) Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu Rev Genet 44: 189-216.
6. Cowen LE, Lindquist S, (2005) Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309: 2185-2189.
7. Jarosz DF, Lindquist S, (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330: 1820-1824.
8. Queitsch C, Sangster TA, Lindquist S, (2002) Hsp90 as a capacitator of phenotypic variation. Nature 417: 618-624.
9. Rutherford SL, Lindquist S, (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
10. Millson SH, Truman AW, King V, Prodromou C, Pearl LH, et al. (2005) A two-hybrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in the activity of a stress-activated mitogen-activated protein kinase, Slt2p (Mpk1p). Eukaryot Cell 4: 849-860.
11. Zhao R, Davey M, Hsu Y-C, 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.
12. McClellan AJ, Xia Y, Deutschbauer AM, Davis RW, Gerstein M, et al. (2007) Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 131: 121-135.
13. Johnson JL, Brown C, (2009) Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress & Chaperon 14: 83-94.
14. Cowen LE, (2008) The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat Rev Microbiol 6: 187-198.
15. 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 U S A 106: 2818-2823.
16. Pfaller MA, Diekema DJ, (2010) Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36: 1-53.
17. Cowen LE, Steinbach WJ, (2008) Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance. Eukaryot Cell 7: 747-764.
18. LaFayette SL, Collins C, Zaas AK, Schell WA, Betancourt-Quiroz M, et al. (2010) PKC signalling regulates drug resistance of the fungal pathogen Candida albicans via circuitry comprised of Mkc1, calcineurin, and Hsp90. PLoS Pathog 6: e1001069 doi:10.1371/journal.ppat.1001069.
19. 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 doi:10.1371/journal.ppat.1000532.
20. 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.
21. Pfaller MA, Diekema DJ, (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20: 133-163.
22. Zaoutis TE, Argon J, Chu J, Berlin JA, Walsh TJ, et al. (2005) The epidemiology and attributable outcomes of candidemia in adults and children hospitalized in the United States: a propensity analysis. Clin Inf Dis 41: 1232-1239.
23. Blankenship JR, Fanning S, Hamaker JJ, Mitchell AP, (2010) An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog 6: e1000752 doi:10.1371/journal.ppat.1000752.
24. Hohmann OR, Dea J, Noble SM, Johnson AD, (2009) A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 5: e1000783 doi:10.1371/journal.pgen.1000783.
25. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, et al. (2006) Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2: e63 doi:10.1371/journal.ppat.0020063.
26. 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.
27. Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM, (1994) Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc Natl Acad Sci U S A 91: 8324-8328.
28. Bonilla M, Cunningham KW, (2003) Mitogen-activated protein kinase stimulation of Ca(2+) signaling is required for survival of endoplasmic reticulum stress in yeast. Mol Biol Cell 14: 4296-4305.
29. Bonilla M, Nastase KK, Cunningham KW, (2002) Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J 21: 2343-2353.
30. Hawle P, Horst D, Bebelman JP, Yang XX, Siderius M, et al. (1997) Cdc37p is required for stress-induced high-osmolarity glycerol and protein kinase C mitogen-activated protein kinase pathway functionality by interaction with Hog1p and Slt2p (Mpk1p). Eukaryot Cell 6: 521-532.
31. Ota A, Zhang J, Ping P, Han J, Wang Y, (2010) Specific regulation of noncanonical p38α activation by Hsp90-Cdc37 chaperone complex in cardiomyocyte. Circ Res 106: 1404-1412.
32. Mollapour M, Tsutsumi S, Truman AW, Xu W, Vaughan CK, et al. (2011) Threonine 22 phosphorylation attenuates Hsp90 interaction with cochaperones and affects its chaperone activity. Mol Cell 41: 672-681.
33. Miyata Y, Yahara I, (1992) The 90-kDa heat shock protein, Hsp90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J Biol Chem 267: 7042-7047.
34. Bruno VM, Mitchell AP, (2005) Regulation of azole drug susceptibility by Candida albicans protein kinase CK2. Mol Microbiol 56: 559-573.
35. Chiang LY, Sheppard DC, Bruno VM, Mitchell AP, Edwards JE, et al. (2007) Candida albicans protein kinase CK2 governs virulence during oropharyngeal candidiasis. Cell Microbiol 9: 233-245.
36. Mollapour M, Tsutsumi S, Kim YS, Trepel J, Neckers L, (2011) Casein kinase 2 phosphorylation of Hsp90 threonine 22 modulates chaperone function and drug sensitivity. Oncotarget 2: 407-417.
37. Bandhakavi S, McCann RO, Hanna DE, Glover CVC, (2003) A positive feedback loop between protein kinase CKII and Cdc37 promotes the activity of multiple protein kinases. J Biol Chem 278: 2829-2836.
38. Pavithra SR, Kumar R, Tatu U, (2007) Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum. PLoS Comput Biol 3: e168 doi:10.1371/journal.pcbi.0030168.
39. LaCount DJ, Vignali M, Chettier R, Phansalkar A, Bell R, et al. (2005) A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438: 103-107.
40. Suthram S, Sittler T, Ideker T, (2005) The Plasmodium protein network diverges from those of other eukaryotes. Nature 438: 108-112.
41. Askew C, Sellam A, Epp E, Mallick J, Hogues H, et al. (2011) The zinc cluster transcription factor Ahr1p directs Mcm1p regulation of Candida albicans adhesion. Mol Microbiol 79: 940-953.
42. Yin Z, Stead D, Walker J, Selway L, Smith DA, et al. (2009) A proteomic analysis of the salt, cadmium and peroxide stress responses in Candida albicans and the role of the Hog1 stress-activated MAPK in regulating the stress-induced proteome. Proteomics 9: 4686-4703.
43. Alonso-Monge R, Navarro-Garcia F, Molero G, Diez-Orejas R, Gustin M, et al. (1999) Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J Bacteriol 181: 3058-3068.
44. Arana DM, Alonso-Monge R, Du C, Calderone R, Pla J, (2007) Differential susceptibility of mitogen-activated protein kinase pathway mutants to oxidative-mediated killing by phagocytes in the fungal pathogen Candida albicans. Cell Microbiol 9: 1647-1659.
45. Rodriguez-Caban J, Gonzalez-Velazquez W, Perez-Sanchez L, Gonzalez-Mendez R, Rodriguez-Del Valle N, (2011) Calcium/calmodulin kinase1 and its relation to thermotolerance and HSP90 in Sporothrix schenckii: an RNAi and yeast two-hybrid study. BMC Microbiol 11: 162.
46. Netea MG, Brown GD, Kullberg BJ, Gow NA, (2008) An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 6: 67-78.
47. Wheeler RT, Fink GR, (2006) A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog 2: e35 doi:10.1371/journal.ppat.0020035.
48. 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.
49. Saldanha AJ, (2004) Java Treeview- extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
50. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integreated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
51. Berriz GF, Beaver JE, Cenik C, Tasan M, Roth FP, (2009) Next generation software for functional trend analysis. Bioinformatics 25: 3043-3044.
52. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, et al. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nature 17: 1030-1032.
53. Lavoie H, Sellam A, Askew C, Nantel A, Whiteway M, (2008) A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans. BMC Genomics 9: 578-592.