Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin

PLoS Pathogens

Volumn 5, Issue 7, 2009, Pages

  Singh, Sheena D ^a   Robbins, Nicole ^a   Zaas, Aimee K ^b   Schell, Wiley A ^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

CALCINEURIN; ECHINOCANDIN; HEAT SHOCK PROTEIN 90; MICAFUNGIN; PYRROLE DERIVATIVE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CRZ1; UNCLASSIFIED DRUG; ANTIFUNGAL AGENT; DNA BINDING PROTEIN; FUNGAL PROTEIN; LIPOPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIFUNGAL RESISTANCE; ARTICLE; BIOSYNTHESIS; CANDIDA ALBICANS; CELL WALL; CONTROLLED STUDY; DRUG TOLERANCE; FUNGAL CELL; FUNGAL STRAIN; FUNGICIDAL ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENETICS; IMMUNOPRECIPITATION; INVASIVE CANDIDIASIS; MALE; MOUSE; NONHUMAN; PROTEIN INTERACTION; STRESS; ANALYSIS OF VARIANCE; ANIMAL; CANDIDIASIS; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; MICROBIOLOGY; PHYSIOLOGICAL STRESS;

CANDIDA ALBICANS; MURINAE; SACCHAROMYCES CEREVISIAE;

ANALYSIS OF VARIANCE; ANIMALS; ANTIFUNGAL AGENTS; AZOLES; CALCINEURIN; CANDIDA ALBICANS; CANDIDIASIS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DRUG RESISTANCE, FUNGAL; ECHINOCANDINS; FUNGAL PROTEINS; HSP90 HEAT-SHOCK PROTEINS; LIPOPEPTIDES; MALE; MICE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 70049109583     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000532     Document Type: Article

References (60)

1. McNeil MM, Nash SL, Hajjeh RA, Phelan MA, Conn LA, et al. (2001) Trends in mortality due to invasive mycotic diseases in the United States, 1980-1997. Clin Infect Dis 33: 641-647.
2. Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20: 133-163.
3. 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 Infect Dis 41: 1232-1239. (Pubitemid 41532664)
4. Enoch DA, Ludlam HA, Brown NM (2006) Invasive fungal infections: a review of epidemiology and management options. J Med Microbiol 55: 809-818. (Pubitemid 43974685)
5. 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. (Pubitemid 34160368)
6. 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. (Pubitemid 24008678)
7. Wainright PO, Hinkle G, Sogin ML, Stickel SK (1993) Monophyletic origins of the metazoa: an evolutionary link with fungi. Science 260: 340-342. (Pubitemid 23160139)
8. Cowen LE (2008) The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat Rev Microbiol 6: 187-198. (Pubitemid 351256314)
9. Cowen LE, Steinbach WJ (2008) Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance. Eukaryot Cell 7: 747-764.
10. Anderson JB (2005) Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat Rev Microbiol 3: 547-556. (Pubitemid 40903878)
11. Perlin DS (2007) Resistance to echinocandin-class antifungal drugs. Drug Resist Updat 10: 121-130.
12. 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. (Pubitemid 43807526)
13. Garcia-Effron G, Park S, Perlin DS (2009) Correlating echinocandin MIC and kinetic inhibition of fks1 mutant glucan synthases for Candida albicans: implications for interpretive breakpoints. Antimicrob Agents Chemother 53: 112-122.
14. Wiederhold NP (2007) Attenuation of echinocandin activity at elevated concentrations: a review of the paradoxical effect. Curr Opin Infect Dis 20: 574-578.
15. Munro CA, Selvaggini S, de Bruijn I, Walker L, Lenardon MD, et al. (2007) The PKC, HOG and Ca2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol Microbiol 63: 1399-1413.
16. Walker LA, Munro CA, de Bruijn I, Lenardon MD, McKinnon A, et al. (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4: e1000040. doi:10.1371/journal.ppat.1000040. (Pubitemid 351631083)
17. Pearl LH, Prodromou C (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75: 271-294. (Pubitemid 44118034)
18. 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. (Pubitemid 36187918)
19. Wandinger SK, Richter K, Buchner J (2008) The Hsp90 chaperone machinery. J Biol Chem 283: 18473-18477.
20. Cowen LE, Carpenter AE, Matangkasombut O, Fink GR, Lindquist S (2006) Genetic architecture of Hsp90-dependent drug resistance. Eukaryot Cell 5: 2184-2188. (Pubitemid 44956829)
21. Cowen LE, Lindquist S (2005) Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309: 2185-2189.
22. Cowen LE, Singh SD, Köhler 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.
23. Imai J, Yahara I (2000) Role of HSP90 in salt stress tolerance via stabilization and regulation of calcineurin. Mol Cell Biol 20: 9262-9270. (Pubitemid 32246112)
24. 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. (Pubitemid 40343082)
25. Herbrecht R, Denning DW, Patterson TF, Bennett JE, Greene RE, et al. (2002) Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N Engl J Med 347: 408-415. (Pubitemid 34851833)
26. Singh N, Paterson DL (2005) Aspergillus infections in transplant recipients. Clin Microbiol Rev 18: 44-69.
27. Fortwendel JR, Juvvadi PR, Pinchai N, Perfect BZ, Alspaugh JA, 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: 476-482.
28. Steinbach WJ, Cramer RA Jr, Perfect BZ, Henn C, Nielsen K, et al. (2007) Calcineurin inhibition or mutation enhances cell wall inhibitors against Aspergillus fumigatus. Antimicrob Agents Chemother 51: 2979-2981. (Pubitemid 47206239)
29. Wiederhold NP, Kontoyiannis DP, Prince RA, Lewis RE (2005) Attenuation of the activity of caspofungin at high concentrations against Candida albicans: possible role of cell wall integrity and calcineurin pathways. Antimicrob Agents Chemother 49: 5146-5148.
30. Sanglard D, Ischer F, Marchetti O, Entenza J, Bille J (2003) Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 48: 959-976. (Pubitemid 36628262)
31. Cruz MC, Goldstein AL, Blankenship JR, Del Poeta M, Davis D, et al. (2002) Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J 21: 546-559. (Pubitemid 34174036)
32. Roe SM, Prodromou C, O'Brien R, Ladbury JE, Piper PW, et al. (1999) Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J Med Chem 42: 260-266. (Pubitemid 29069861)
33. 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. (Pubitemid 24273656)
34. Hemenway CS, Heitman J (1999) Calcineurin. Structure, function, and inhibition. Cell Biochem Biophys 30: 115-151.
35. Kaneko A, Umeyama T, Hanaoka N, Monk BC, Uehara Y, et al. (2004) Tandem affinity purification of the Candida albicans septin protein complex. Yeast 21: 1025-1033. (Pubitemid 39387489)
36. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741. (Pubitemid 37314318)
37. 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.
38. Roy J, Li H, Hogan PG, Cyert MS (2007) A conserved docking site modulates substrate affinity for calcineurin, signaling output, and in vivo function. Mol Cell 25: 889-901. (Pubitemid 46436530)
39. Stathopoulos-Gerontides A, Guo JJ, Cyert MS (1999) Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev 13: 798-803. (Pubitemid 29169839)
40. 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.
41. Yoshimoto H, Saltsman K, Gasch AP, Li HX, Ogawa N, et al. (2002) Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J Biol Chem 277: 31079-31088. (Pubitemid 34970813)
42. Onyewu C, Wormley FL Jr, Perfect JR, Heitman J (2004) The calcineurin target, Crz1, functions in azole tolerance but is not required for virulence of Candida albicans. Infect Immun 72: 7330-7333. (Pubitemid 39552408)
43. Navarro-Garcia F, Eisman B, Fiuza SM, Nombela C, Pla J (2005) The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans. Microbiology 151: 2737-2749. (Pubitemid 41149794)
44. Markovich S, Yekutiel A, Shalit I, Shadkchan Y, Osherov N (2004) Genomic approach to identification of mutations affecting caspofungin susceptibility in Saccharomyces cerevisiae. Antimicrob Agents Chemother 48: 3871-3876. (Pubitemid 39304616)
45. Reinoso-Martin C, Schuller C, Schuetzer-Muehlbauer M, Kuchler K (2003) The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling. Eukaryot Cell 2: 1200-1210. (Pubitemid 38047229)
46. Stathopoulos AM, Cyert MS (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev 11: 3432-3444.
47. Zhao C, Jung US, Garrett-Engele P, Roe T, Cyert MS, et al. (1998) Temperature-induced expression of yeast FKS2 is under the dual control of protein kinase C and calcineurin. Mol Cell Biol 18: 1013-1022. (Pubitemid 28063435)
48. Gould CM, Kannan N, Taylor SS, Newton AC (2009) The chaperones Hsp90 and Cdc37 mediate the maturation and stabilization of protein kinase C through a conserved PXXP motif in the C-terminal tail. J Biol Chem 284: 4921-4935.
49. 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. (Pubitemid 40697749)
50. Truman AW, Millson SH, Nuttall JM, Mollapour M, Prodromou C, et al. (2007) In the yeast heat shock response, Hsf1-directed induction of Hsp90 facilitates the activation of the Slt2 (Mpk1) mitogen-activated protein kinase required for cell integrity. Eukaryot Cell 6: 744-752.
51. Dudgeon DD, Zhang N, Ositelu OO, Kim H, Cunningham KW (2008) Nonapoptotic death of Saccharomyces cerevisiae cells that is stimulated by Hsp90 and inhibited by calcineurin and Cmk2 in response to endoplasmic reticulum stresses. Eukaryot Cell 7: 2037-2051.
52. Pachl J, Svoboda P, Jacobs F, Vandewoude K, van der Hoven B, 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: 1404-1413.
53. Hodgetts S, Nooney L, Al-Akeel R, Curry A, Awad S, et al. (2008) Efungumab and caspofungin: pre-clinical data supporting synergy. J Antimicrob Chemother 61: 1132-1139.
54. Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2: 185-194. (Pubitemid 37328765)
55. Stewart GR, Young DB (2004) Heat-shock proteins and the host-pathogen interaction during bacterial infection. Curr Opin Immunol 16: 506-510. (Pubitemid 38881680)
56. 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. (Pubitemid 40461894)
57. Steinbach WJ, Reedy JL, Cramer RA Jr, Perfect JR, Heitman J (2007) Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiol 5: 418-430.
58. Withee JL, Mulholland J, Jeng R, Cyert MS (1997) An essential role of the yeast pheromone-induced Ca2+ signal is to activate calcineurin. Mol Biol Cell 8: 263-277. (Pubitemid 27097942)
59. 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. (Pubitemid 36337003)
60. Borkovich KA, Farrelly FW, Finkelstein DB, Taulien J, Lindquist S (1989) Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9: 3919-3930. (Pubitemid 19216285)