A nuclear receptor-like pathway regulating multidrug resistance in fungi

Nature

Volumn 452, Issue 7187, 2008, Pages 604-609

  Thakur, Jitendra K ^a,b   Arthanari, Haribabu ^b   Yang, Fajun ^a,b   Pan, Shih Jung ^c   Fan, Xiaochun ^b   Breger, Julia ^d   Frueh, Dominique P ^b   Gulshan, Kailash ^e   Li, Darrick K ^a   Mylonakis, Eleftherios ^d   Struhl, Kevin ^b   Moye Rowley, W Scott ^e   Cormack, Brendan P ^c   Wagner, Gerhard ^b   Näär, Anders M ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; CELL NUCLEUS RECEPTOR; CYCLOHEXIMIDE; DEXAMETHASONE; FLUCONAZOLE; GAL11P PROTEIN; GENE PRODUCT; KETOCONAZOLE; PDR1P PROTEIN; PREGNANE X RECEPTOR; RIFAMPICIN; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

CHEMOTHERAPY; CYTOLOGY; DRUG RESISTANCE; FUNGAL DISEASE; GENE EXPRESSION; XENOBIOTICS; YEAST;

ARTICLE; CANDIDA GLABRATA; CONTROLLED STUDY; DRUG TRANSPORT; FUNGUS; GENE CONTROL; GENE EXPRESSION; HUMAN; METAZOON; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; VERTEBRATE;

CANDIDA GLABRATA; FUNGI; METAZOA; SACCHAROMYCES CEREVISIAE; VERTEBRATA;

EID: 41649118757     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature06836     Document Type: Article

References (61)

1. Richardson, M. D. Changing patterns and trends in systemic fungal infections. J. Antimicrob. Chemother. 56, i5-i11 (2005).
2. Aperis, G., Myriounis, N., Spanakis, E. K. & Mylonakis, E. Developments in the treatment of candidiasis: more choices and new challenges. Expert Opin. Investig. Drugs 15, 1319-1336 (2006).
3. Pfaller, M. A. & Diekema, D. J. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20, 133-163 (2007).
4. Wisplinghoff, H. et al. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39, 309-317 (2004).
5. Klepser, M. E. Candida resistance and its clinical relevance. Pharmacotherapy 26, 68S-75S (2006).
6. Sipos, G. & Kuchler, K. Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Curr. Drug Targets 7, 471-481 (2006).
7. Balzi, E. et al. The multidrug resistance gene PDR1 from Saccharomyces cerevisiae. J. Biol. Chem. 262, 16871-16879 (1987).
8. Meyers, S. et al. Interaction of the yeast pleiotropic drug resistance genes PDR1 and PDR5. Curr. Genet. 21, 431-436 (1992).
9. Balzi, E. et al. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269, 2206-2214 (1994).
10. Katzmann, D. J. et al. Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol. Cell. Biol. 14, 4653-4661 (1994).
11. Delaveau, T. et al. PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls the multidrug resistance phenomenon. Mol. Gen. Genet. 244, 501-511 (1994).
12. Decottignies, A. et al. Identification and characterization of SNQ2, a new multidrug ATP binding cassette transporter of the yeast plasma membrane. J. Biol. Chem. 270, 18150-18157 (1995).
13. Katzmann, D. J. et al. Expression of an ATP-binding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 6875-6883 (1995).
14. van den Hazel, H. B. et al. PDR16 and PDR17, two homologous genes of Saccharomyces cerevisiae, affect lipid biosynthesis and resistance to multiple drugs. J. Biol. Chem. 274, 1934-1941 (1999).
15. Moye-Rowley, W. S. Transcriptional control of multidrug resistance in the yeast Saccharomyces. Prog. Nucleic Acid Res. Mol. Biol. 73, 251-279 (2003).
16. Mamnun, Y. M., Schuller, C. & Kuchler, K. Expression regulation of the yeast PDR5 ATP-binding cassette (ABC) transporter suggests a role in cellular detoxification during the exponential growth phase. FEBS Lett. 559, 111-117 (2004).
17. Gao, C., Wang, L., Milgrom, E. & Shen, W. C. On the mechanism of constitutive Pdr1 activator-mediated PDR5 transcription in Saccharomyces cerevisiae: evidence for enhanced recruitment of coactivators and altered nucleosome structures. J. Biol. Chem. 279, 42677-42686 (2004).
18. Lucau-Danila, A. et al. Early expression of yeast genes affected by chemical stress. Mol. Cell. Biol. 25, 1860-1868 (2005).
19. Alenquer, M., Tenreiro, S. & Sa-Correia, I. Adaptive response to the antimalarial drug artesunate in yeast involves Pdr1p/Pdr3p-mediated transcriptional activation of the resistance determinants TPO1 and PDR5. FEMS Yeast Res. 6, 1130-1139 (2006).
20. Fardeau, V. et al. The central role of PDR1 in the foundation of yeast drug resistance. J. Biol. Chem. 282, 5063-5074 (2007).
21. Vermitsky, J. P. & Edlind, T. D. Azole resistance in Candida glabrata: coordinate upregulation of multidrug transporters and evidence for a Pdr1-like transcription factor. Antimicrob. Agents Chemother. 48, 3773-3781 (2004).
22. Tsai, H. F., Krol, A. A., Sarti, K. E. & Bennett, J. E. Candida glabrata PDR1, a transcriptional regulator of a pleiotropic drug resistance network, mediates azole resistance in clinical isolates and petite mutants. Antimicrob. Agents Chemother. 50, 1384-1392 (2006).
23. Vermitsky, J. P. et al. Pdr1 regulates multidrug resistance in Candida glabrata: gene disruption and genome-wide expression studies. Mol. Microbiol. 61, 704-722 (2006).
24. Kliewer, S. A., Goodwin, B. & Willson, T. M. The nuclear pregnane X receptor: a key regulator of xenobiotic metabolism. Endocr. Rev. 23, 687-702 (2002).
25. Willson, T. M. & Kliewer, S. A. PXR, CAR and drug metabolism. Nature Rev. Drug Discov. 1, 259-266 (2002).
26. Näär, A. M., Lemon, B. D. & Tjian, R. Transcriptional coactivator complexes. Annu. Rev. Biochem. 70, 475-501 (2001).
27. Kornberg, R. D. Mediator and the mechanism of transcriptional activation. Trends Biochem. Sci. 30, 235-239 (2005).
28. Kean, L. S. et al. Plasma membrane translocation of fluorescent-labeled phosphatidylethanolamine is controlled by transcription regulators, PDR1 and PDR3. J. Cell Biol. 138, 255-270 (1997).
29. Gulshan, K., Rovinsky, S. A., Coleman, S. T. & Moye-Rowley, W. S. Oxidant-specific folding of Yap1p regulates both transcriptional activation and nuclear localization. J. Biol. Chem. 280, 40524-40533 (2005).
30. Novatchkova, M. & Eisenhaber, F. Linking transcriptional mediators via the GACKIX domain super family. Curr. Biol. 14, R54-R55 (2004).
31. Yang, F. et al. An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442, 700-704 (2006).
32. Goodman, R. H. & Smolik, S. CBP/p300 in cell growth, transformation, and development. Genes Dev. 14, 1553-1577 (2000).
33. Kasper, L. H. et al. A transcription-factor-binding surface of coactivator p300 is required for haematopoiesis. Nature 419, 738-743 (2002).
34. Kasper, L. H. et al. Conditional knockout mice reveal distinct functions for the global transcriptional coactivators CBP and p300 in T-cell development. Mol. Cell. Biol. 26, 789-809 (2006).
35. Radhakrishnan, I. et al. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions. Cell 91, 741-752 (1997).
36. Näär, A. M. et al. Chromatin, TAFs, and a novel multiprotein coactivator are required for synergistic activation by Sp1 and SREBP-1a in vitro. Genes Dev. 12, 3020-3031 (1998).
37. Dai, P. et al. CBP as a transcriptional coactivator of c-Myb. Genes Dev. 10, 528-540 (1996).
38. Zor, T., De Guzman, R. N., Dyson, H. J. & Wright, P. E. Solution structure of the KIX domain of CBP bound to the transactivation domain of c-Myb. J. Mol. Biol. 337, 521-534 (2004).
39. De Guzman, R. N., Goto, N. K., Dyson, H. J. & Wright, P. E. Structural basis for cooperative transcription factor binding to the CBP coactivator. J. Mol. Biol. 355, 1005-1013 (2006).
40. Goto, N. K. et al. Cooperativity in transcription factor binding to the coactivator CREB-binding protein (CBP). The mixed lineage leukemia protein (MLL) activation domain binds to an allosteric site on the KIX domain. J. Biol. Chem. 277, 43168-43174 (2002).
41. Parker, D. et al. Analysis of an activator:coactivator complex reveals an essential role for secondary structure in transcriptional activation. Mol. Cell 2, 353-359 (1998).
42. Parker, D. et al. Role of secondary structure in discrimination between constitutive and inducible activators. Mol. Cell. Biol. 19, 5601-5607 (1999).
43. Radhakrishnan, I. et al. Structural analyses of CREB-CBP transcriptional activator-coactivator complexes by NMR spectroscopy: implications for mapping the boundaries of structural domains. J. Mol. Biol. 287, 859-865 (1999).
44. Prasad, R., Gaur, N. A., Gaur, M. & Komath, S. S. Efflux pumps in drug resistance of Candida. Infect. Disord. Drug Targets 6, 69-83 (2006).
45. Pfaller, M. A. et al. Results from the ARTEMIS DISK Global Antifungal Surveillance study, 1997 to 2005: an 8.5-year analysis of susceptibilities of Candida species and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J. Clin. Microbiol. 45, 1735-1745 (2007).
46. Breger, J. et al. Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathogens 3, e18 (2007).
47. Mylonakis, E. & Aballay, A. Worms and flies as genetically tractable animal models to study host-pathogen interactions. Infect. Immun. 73, 3833-3841 (2005).
48. Bertrand, S. et al. Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. Mol. Biol. Evol. 21, 1923-1937 (2004).
49. Phelps, C. et al. Fungi and animals may share a common ancestor to nuclear receptors. Proc. Natl Acad. Sci. USA 103, 7077-7081 (2006).
50. Taubert, S., Van Gilst, M. R., Hansen, M. & Yamamoto, K. R. A Mediator subunit, MDT-15, integrates regulation of fatty acid metabolism by NHR-49-dependent and -independent pathways in C. elegans. Genes Dev. 20, 1137-1149 (2006).
51. Sherman, F., Fink, G. R.&Hicks, J. B. Methods in Yeast Genetics (Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, 1986).
52. Gietz, D., St Jean, A., Woods, R. A. & Schiestl, R. H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20, 1425 (1992).
53. Cormack, B. P. & Falkow, S. Efficient homologous and illegitimate recombination in the opportunistic yeast pathogen Candida glabrata. Genetics 151, 979-987 (1999).
54. Aparicio, J. G., Viggiani, C. J., Gibson, D. G. & Aparicio, O. M. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 4769-4780 (2004).
55. Kepinski, S. & Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451 (2005).
56. Breger, J. et al. Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathogens 3, e18 (2007).
57. Ferentz, A. E. & Wagner, G. NMR spectroscopy: a multifaceted approach to macromolecular structure. Q. Rev. Biophys. 33, 29-65 (2000).
58. Frueh, D. P., Arthanari, H. & Wagner, G. Unambiguous assignment of NMR protein backbone signals with a time-shared triple-resonance experiment. J. Biomol. NMR 33, 187-196 (2005).
59. Takahashi, H. et al. A novel NMR method for determining the interfaces of large protein-protein complexes. Nature Struct. Mol. Biol. 7, 220-223 (2000).
60. Guntert, P., Mumenthaler, C. & Wuthrich, K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298 (1997).
61. Cornilescu, G., Delaglio, F. & Bax, A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (1999).