Metabolic control of antifungal drug resistance

Fungal Genetics and Biology

Volumn 47, Issue 2, 2010, Pages 81-93

  Robbins, Nicole ^a   Collins, Cathy ^a   Morhayim, Jess ^a   Cowen, Leah E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Antifungal drug resistance; Azole; Calcineurin; Candida albicans; Erg3; Hsp90; Nutrient signaling; Saccharomyces cerevisiae; Threonine; Tor

Indexed keywords

FLUCONAZOLE; FUNGAL PROTEIN; MICONAZOLE; PROTEIN ERG3; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CELL STRESS; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL METABOLISM; METABOLIC REGULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

AMINO ACIDS; ANTIFUNGAL AGENTS; AZOLES; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CALCINEURIN; CULTURE MEDIA; DRUG RESISTANCE, FUNGAL; GENE EXPRESSION; GENOME, FUNGAL; HSP90 HEAT-SHOCK PROTEINS; MICROBIAL SENSITIVITY TESTS; MUTATION; OXIDOREDUCTASES; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SIROLIMUS;

CANDIDA ALBICANS; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 73749084686     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2009.07.004     Document Type: Article

References (52)

1. Alarcon C.M., and Heitman J. FKBP12 physically and functionally interacts with aspartokinase in Saccharomyces cerevisiae. Mol. Cell. Biol. 17 (1997) 5968-5975
2. Albrecht G., et al. Monitoring the Gcn4 protein-mediated response in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 273 (1998) 12696-12702
3. Anderson J.B. Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat. Rev. Microbiol. 3 (2005) 547-556
4. Anderson J.B., et al. Mode of selection and experimental evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 163 (2003) 1287-1298
5. Arevalo-Rodriguez M., et al. FKBP12 controls aspartate pathway flux in Saccharomyces cerevisiae to prevent toxic intermediate accumulation. Eukaryot. Cell 3 (2004) 1287-1296
6. Ausubel F.M., et al. Current Protocols in Molecular Biology (1987), New York, John Wiley & Sons
7. Bahn Y.S., et al. Sensing the environment: lessons from fungi. Nat. Rev. Microbiol. 5 (2007) 57-69
8. Bastidas R.J., et al. The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog. 5 (2009) e1000294
9. Berman J., and Sudbery P.E. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet. 3 (2002) 918-930
10. Blankenship J.R., et al. Teaching old drugs new tricks: reincarnating immunosuppressants as antifungal drugs. Curr. Opin. Investig. Drugs 4 (2003) 192-199
11. Bonilla M., et al. Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J. 21 (2002) 2343-2353
12. Borkovich K.A., et al. Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 9 (1989) 3919-3930
13. Cardenas M.E., et al. Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands. EMBO J. 13 (1994) 5944-5957
14. Cowen L.E. The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat. Rev. Microbiol. 6 (2008) 187-198
15. Cowen L.E., et al. Evolution of drug resistance in Candida albicans. Annu. Rev. Microbiol. 56 (2002) 139-165
16. Cowen L.E., et al. Genetic architecture of Hsp90-dependent drug resistance. Eukaryot. Cell 5 (2006) 2184-2188
17. Cowen L.E., and Lindquist S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309 (2005) 2185-2189
18. Cowen L.E., et al. Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc. Natl. Acad. Sci. USA 106 (2009) 2818-2823
19. Cowen L.E., and Steinbach W.J. Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance. Eukaryot. Cell 7 (2008) 747-764
20. Cruz M.C., et al. Rapamycin and less immunosuppressive analogs are toxic to Candida albicans and Cryptococcus neoformans via FKBP12-dependent inhibition of TOR. Antimicrob. Agents Chemother. 45 (2001) 3162-3170
21. De Virgilio C., and Loewith R. Cell growth control: little eukaryotes make big contributions. Oncogene 25 (2006) 6392-6415
22. Fonzi W.A., and Irwin M.Y. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134 (1993) 717-728
23. Gasch A.P., et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11 (2000) 4241-4257
24. Giaever G., et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418 (2002) 387-391
25. Goldstein A.L., and McCusker J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15 (1999) 1541-1553
26. Hay N., and Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 18 (2004) 1926-1945
27. Heath V.L., et al. Hph1p and Hph2p, novel components of calcineurin-mediated stress responses in Saccharomyces cerevisiae. Eukaryot. Cell 3 (2004) 695-704
28. Heitman J., et al. The immunosuppressant FK506 inhibits amino acid import in Saccharomyces cerevisiae. Mol. Cell. Biol. 13 (1993) 5010-5019
29. Heitman J., et al. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253 (1991) 905-909
30. Hinnebusch A.G. A hierarchy of trans-acting factors modulates translation of an activator of amino acid biosynthetic genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 5 (1985) 2349-2360
31. Karababa M., et al. CRZ1, a target of the calcineurin pathway in Candida albicans. Mol. Microbiol. 59 (2006) 1429-1451
32. Kingsbury J.M., et al. Role of nitrogen and carbon transport, regulation, and metabolism genes for Saccharomyces cerevisiae survival in vivo. Eukaryot. Cell 5 (2006) 816-824
33. NCCLS, 1997. Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved standard M27-A. NCCLS, Wayne, PA.
34. Odds F.C., et al. Antifungal agents: mechanisms of action. Trends Microbiol. 11 (2003) 272-279
35. Onyewu C., et al. The calcineurin target, Crz1, functions in azole tolerance but is not required for virulence of Candida albicans. Infect. Immun. 72 (2004) 7330-7333
36. Pfaller M.A., and Diekema D.J. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20 (2007) 133-163
37. Roy J., et al. A conserved docking site modulates substrate affinity for calcineurin, signaling output, and in vivo function. Mol. Cell. 25 (2007) 889-901
38. Schmelzle T., and Hall M.N. TOR, a central controller of cell growth. Cell 103 (2000) 253-262
39. Shapiro R.S., et al. Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr. Biol. 19 (2009) 621-629
40. Shen J., et al. CaNAT1, a heterologous dominant selectable marker for transformation of Candida albicans and other pathogenic Candida species. Infect. Immun. 73 (2005) 1239-1242
41. Spiegel S., and Merrill Jr. A.H. Sphingolipid metabolism and cell growth regulation. FASEB J. 10 (1996) 1388-1397
42. Stathopoulos A.M., and Cyert M.S. Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev. 11 (1997) 3432-3444
43. Stathopoulos-Gerontides A., et al. Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev. 13 (1999) 798-803
44. Steinbach W.J., et al. Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat. Rev. Microbiol. 5 (2007) 418-430
45. Taldone T., et al. Targeting Hsp90: small-molecule inhibitors and their clinical development. Curr. Opin. Pharmacol. 8 (2008) 370-374
46. Whitesell L., and Lindquist S.L. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5 (2005) 761-772
47. Winzeler E.A., et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 (1999) 901-906
48. 2+ signal is to activate calcineurin. Mol. Biol. Cell 8 (1997) 263-277
49. Workman P., et al. Drugging the cancer chaperone HSP90: combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann. NY Acad. Sci. 1113 (2007) 202-216
50. Wullschleger S., et al. TOR signaling in growth and metabolism. Cell 124 (2006) 471-484
51. Yim G., et al. Antibiotics as signalling molecules. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362 (2007) 1195-1200
52. Yoshimoto H., et al. Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J. Biol. Chem. 277 (2002) 31079-31088