Response of pathogenic and non-pathogenic yeasts to steroids

Journal of Steroid Biochemistry and Molecular Biology

Volumn 129, Issue 1-2, 2012, Pages 61-69

  Prasad, Rajendra ^a   Devaux, Frédéric ^b   Dhamgaye, Sanjiveeni ^a   Banerjee, Dibyendu ^a,c  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b CNRS   (France)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Candida albicans; Cellular stress; Progesterone; Saccharomyces cerevisiae; Transcriptome; Estradiol

Indexed keywords

ABC TRANSPORTER; ALDOSTERONE; CHLORAMPHENICOL; CORTICOSTERONE; CORTODOXONE; CYCLOHEXIMIDE; DEXAMETHASONE; ESTRADIOL; FLUCONAZOLE; MULTIDRUG RESISTANCE PROTEIN; PHENANTHROLINE; PREGNANEDIONE; PROGESTERONE; STEROID HORMONE; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

CANDIDA ALBICANS; CELL CYCLE REGULATION; CELL GROWTH; CELL STRUCTURE; DNA MICROARRAY; DRUG RESPONSE; FUNGAL VIRULENCE; GENE ACTIVATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION AND TRANSLATION; MOLECULAR EVOLUTION; MORPHOGENESIS; MULTIDRUG RESISTANCE; NONHUMAN; PROTEOMICS; REVIEW; SACCHAROMYCES CEREVISIAE; STRESS; YEAST;

CANDIDA ALBICANS; EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETES;

EID: 84857784295     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2010.11.011     Document Type: Article

References (67)

1. S. Tanaka, S. Hasegawa, F. Hishinuma, and S. Kurata Estrogen can regulate the cell cycle in the early phase of yeast by increasing the amount of adenylate cyclase mRNA Cell 57 1989 675 681
2. M. Zakelj-Mavrik, A. Kastelic-Suhadolk, A. Plementas, T.L. Rizner, and I. Belic Steroid hormone signaling system and fungi Comp. Biochem. Physiol. 112B 1995 637 642 (Pubitemid 26033967)
3. P.R. Gujjar, M. Finucane, and B. Larsen The effect of estradiol on Candida albicans growth Ann. Clin. Lab. Sci. 27 1997 151 156 (Pubitemid 27157439)
4. X. Zhang, M. Essman, E.T. Burt, and B. Larsen Estrogen effects on Candida albicans: a potential virulence-regulating mechanism J. Infect. Dis. 181 2000 1441 1446 (Pubitemid 30252551)
5. L. Romani, F. Bistoni, and P. Puccetti Adaptation of Candida albicans to the host environment: the role of morphogenesis in virulence and survival in mammalian hosts Curr. Opin. Microbiol. 6 2003 338 343 (Pubitemid 37075349)
6. O.S. Kinsman, and A.E. Collard Hormonal factors in vaginal candidiasis in rats Infect. Immun. 1986 498 504 (Pubitemid 16053166)
7. S. White, and B. Larsen Candida albicans morphogenesis is influenced by estrogen Cell Mol. Life Sci. 53 1997 744 749 (Pubitemid 27477968)
8. X. Zhang, M. deMicheli, S.T. Coleman, D. Sanglard, and W.S. Moye-Rowley Analysis of the oxidative stress regulation of the Candida albicans transcription factor, Cap1p Mol. Microbiol. 36 2000 618 629 (Pubitemid 30258846)
9. O.S. Kinsman, K. Pitblado, and C.J. Coulson Effect of mammalian steroid hormones and luteinizing hormone on the germination of Candida albicans and implications for vaginal candidosis Mycoses 31 2002 617 626
10. Jr.P.L. Fidel, J. Cutright, C. Steele, Effects of reproductive hormones on experimental vaginal candidiasis, in: Anonymous, 2001, pp. 651-657.
11. N.D. Madani, P.J. Malloy, P. Rodrigues-Pombo, A.V. Krishnan, and D. Feldman Candida albicans estrogen-binding protein gene encodes an oxidoreductase that is inhibited by estradiol Proc. Natl. Acad. Sci. U.S.A. 91 1994 922 926 (Pubitemid 24048480)
12. P.J. Malloy, X. Zhao, N.D. Madani, and D. Feldman Cloning and expression of the gene from Candida albicans that encodes a high-affinity corticosteroid-binding protein Proc. Natl. Acad. Sci. U.S.A. 90 1993 1902 1906 (Pubitemid 23069965)
13. M. Das, and A. Datta Steroid binding protein(s) in yeasts Biochem. Int. 11 1985 171 176 (Pubitemid 15000142)
14. D. Banerjee, B. Pillai, N. Karnani, G. Mukhopadhyay, and R. Prasad Genome-wide expression profile of steroid response in Saccharomyces cerevisiae Biochem. Biophys. Res. Commun. 317 2004 406 413 (Pubitemid 38452498)
15. G. Cheng, K.M. Yeater, and L.L. Hoyer Cellular and molecular biology of Candida albicans estrogen response Eukaryot. Cell 5 2006 180 191 (Pubitemid 43113464)
16. D. Banerjee, N. Martin, S. Nandi, S. Shukla, A. Dominguez, G. Mukhopadhyay, and R. Prasad A genome-wide steroid response study of the major human fungal pathogen Candida albicans Mycopathologia 164 2007 1 17 (Pubitemid 46988162)
17. D. Banerjee, G. Lelandais, S. Shukla, G. Mukhopadhyay, C. Jacq, F. Devaux, and R. Prasad Responses of pathogenic and nonpathogenic yeast species to steroids reveal the functioning and evolution of multidrug resistance transcriptional networks Eukaryot. Cell 7 2008 68 77 (Pubitemid 351959595)
18. M.E. Fling, J. Kopf, A. Tamarkin, J.A. Gorman, H.A. Smith, and Y. Koltin Analysis of a Candida albicans gene that encodes a novel mechanism for resistance to benomyl and methotrexate Mol. Gen. Genet. 227 1991 318 329
19. R. Prasad, P.D. Worgifosse, A. Goffeau, and E. Balzi Molecular cloning and characterisation of a novel gene of C. albicans, CDR1, conferring multiple resistance to drugs and antifungals Curr. Genet. 27 1995 320 329
20. D. Sanglard, F. Ischer, M. Monod, and J. Bille Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterisation of CDR2, a new multidrug ABC transporter gene Microbiology 143 1997 405 416 (Pubitemid 27092176)
21. S. Krishnamurthy, V. Gupta, P. Snehlata, and R. Prasad Characterisation of human steroid hormone transport mediated by Cdr1p, multidrug transporter of Candida albicans, belonging to the ATP binding cassette super family FEMS Microbiol. Lett. 158 1998 69 74 (Pubitemid 28088104)
22. S. Krishnamurthy, U. Chatterjee, V. Gupta, R. Prasad, P. Das, P. Snehlata, S.E. Hasnain, and R. Prasad Deletion of transmembrane domain 12 of CDR1, a multidrug transporter from Candida albicans, leads to altered drug specificity: expression of a yeast multidrug transporter in Baculovirus expression system Yeast 14 1998 535 550 (Pubitemid 28189546)
23. M. Kolaczkowski, M.E. van der Rest, A. Cybularz-Kolaczkowska, J.-P. Soumillion, W.N. Konings, and A. Goffeau Anticancer drugs, ionophoric peptides, and steroids as substrates of the yeast multidrug transporter Pdr5p J. Biol. Chem. 271 1996 31543 31548 (Pubitemid 26408613)
24. Y. Mahe, A. Parle-McDermott, A. Nourani, A. Delahodde, A. Lamprecht, and K. Kuchler The ATP-binding cassette multidrug transporter Snq2 of Saccharomyces cerevisiae: a novel target for the transcription factors Pdr1 and Pdr3 Mol. Microbiol. 20 1996 109 117 (Pubitemid 26124792)
25. Y. Li, Y.H. Wang, L. Yang, S.W. Zhang, C.H. Liu, and S.L. Yang Comparison of steroid substrates and inhibitors of P-glycoprotein by 3D-QSAR analysis J. Mol. Struct. 733 2005 111 118 (Pubitemid 39472875)
26. S. Velamakanni, T. Janvilisri, S. Shahi, and H.W. van Veen A functional steroid-binding element in an ATP-binding cassette multidrug transporter Mol. Pharmacol. 73 2008 12 17 (Pubitemid 350294192)
27. E. Leberer, D. Harcus, I.D. Broadbent, K.L. Clark, D. Dignard, A.Y. Schmidt, N.A. Gow, A.J. Brown, and D. Thomas Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans Mol. Cell. Biol. 15 1995 601 613
28. R. Manoharlal, M. Sharma, and R. Prasad Molecular determinants of transient and reversible induced up-regulation of CaCDR1 in azole susceptible clinical isolates of Candida albicans Biosci. Rep. 2010
29. S. Krishnamurthy, V. Gupta, R. Prasad, S.L. Panwar, and R. Prasad Expression of CDR1, a multidrug resistance gene of Candida albicans: In vitro transcriptional activation by heat shock, drugs and human steroid hormones FEMS Microbiol. Lett. 160 1998 191 197 (Pubitemid 28129301)
30. M.L. Hernaez, C. Gil, J. Pla, and C. Nombela Induced expression of the Candida albicans multidrug resistance gene CDR1 in response to fluconazole and other antifungals Yeast 14 1998 517 526 (Pubitemid 28189544)
31. N. Puri, S. Krishnamurthy, S. Habib, S.E. Hasnain, S.K. Goswami, and R. Prasad CDR1, a multidrug resistance gene from Candida albicans, contains multiple regulatory domains in its promoter and the distal AP-1 element mediates its induction by miconazole FEMS Microbiol. Lett. 180 1999 213 219 (Pubitemid 29507569)
32. N. Karnani, N.A. Gaur, S. Jha, N. Puri, S. Krishnamurthy, S.K. Goswami, G. Mukhopadhyay, and R. Prasad SRE1, SRE2 are two specific steroid-responsive modules of Candida drug resistance gene 1 (CDR1) promoter Yeast 21 2004 219 239 (Pubitemid 38256422)
33. M. de Micheli, J. Bille, C. Schueller, and D. Sanglard A common drug-responsive element mediates the upregulation of the Candida albicans ABC transporters CDR1 and CDR2, two genes involved in antifungal drug resistance Mol Microbiol 43 2002 1197 1214 (Pubitemid 34304537)
34. B. Panaretou, and P.W. Piper Plasma-membrane ATPase action affects severals stress tolerances of Saccharomyces cerevisiae and Schizosaccharomyces pombe as well as the extent and duration of the heat shock response J. Gen. Microbiol. 136 1990 1763 1770 (Pubitemid 20291276)
35. K. Miyahara, D. Hirata, and T. Miyakawa yAP-1- and yAP-2-mediated, heat shock-induced transcriptional activation of the multidrug resistance ABC transporter genes in Saccharomyces cerevisiae Curr. Genet. 29 1996 103 105 (Pubitemid 26034720)
36. H. Wolfger, Y.M. Mamnun, and K. Kuchler Fungal ABC proteins: pleiotropic drug resistance, stress response and cellular detoxification Res. Microbiol. 152 2001 375 389 (Pubitemid 32436496)
37. A.P. Gasch, A.P. Spellman, M.C. Kao, O. Carmel-Harel, M.B. Eisen, G. Storz, D. Botstein, and P.O. Brown Genomic expression programs in the response of yeast cells to environmental changes Mol. Biol. Cell 11 2000 4241 4257
38. T. Ketala, R. Green, and H. Bussey Saccharomyces cerevisiae Mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway J. Bacteriol. 181 1999 3330 3340 (Pubitemid 29259281)
39. G. Marchler, C. Schuller, G. Adam, and H. Ruis A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions EMBO J. 1993 1997 2003 (Pubitemid 23157716)
40. N. Kobayashi, and K. McEntee Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae Mol. Cell. Biol. 13 1993 248 256 (Pubitemid 23006902)
41. J.L. DeRisi, V.R. Iyver, and P.O. Brown Exploring the metabolic and genetic control of gene expression on a genome scale Science 278 1997 680 686 (Pubitemid 27464965)
42. E. Moskvina, C. Schuller, C.T.C. Maurer, W.H. Mager, and H. Ruis Yeast functional analysis reports Yeast 14 1998 1041 1050
43. J.L. Parrou, M.A. Teste, J. Francois, Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose, in: Anonymous, 1997, pp. 1891-1900. (Pubitemid 27290279)
44. K Barnes, B. Dickstein, G.B. Cutler, T. Fojo, and S.E. Bates Steroid accumulation, and antagonism of P-glycoprtein in multidrug resistant cells Biochemistry 35 1996 4820 4827 (Pubitemid 26126700)
45. M. Sukhai, M. Piquette-Miller, Regulation of the multidrug resistance genes by stress signals, in: Anonymous, 2000, pp. 268-280.
46. S. Labialle, L. Gayet, E. Marthinet, D. Rigal, and L.G. Baggetto Transcriptional regulators of the human multidrug resistance 1 gene: recent reviews Biochem. Pharmacol. 64 2003 943 948
47. P.D. Rogers, and K.S. Barker Evaluation of differential gene expression in fluconazole-susceptible and -resistant isolates of Candida albicans by cDNA analysis Antimicrob. Agents Chemother. 46 2002 3412 3417 (Pubitemid 35192905)
48. R. Ernst, R. Klemm, L. Schmitt, and K. Kuchler Yeast ATP-binding cassette transporters: cellular cleaning pumps Methods Enzymology 400 2005 460 484 (Pubitemid 43052435)
49. Y. Wang, Y.Y. Cao, X.M. Jia, Y.B. Cao, P.H. Gao, X.P. Fu, K. Ying, W.S. Chen, and Y.Y. Jiang Cap1p is involved in multiple pathways of oxidative stress response in Candida albicans Free Radic. Biol. Med. 40 2006 1201 1209
50. J. DeRisi, B.v.d. Hazel, P. Marc, E. Balzi, P. Brown, C. Jacq, and A. Goffeau Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants FEBS Lett. 470 2000 156 160 (Pubitemid 30151088)
51. M. Sidorova, E. Drobna, V. Dzugasova, I. Hikkel, and J. Subik Loss-of-function pdr3 mutations convert the Pdr3p transcription activator to a protein suppressing multidrug resistance in Saccharomyces cerevisiae FEMS Yeast Res. 7 2007 254 264
52. W.S. Moye-Rowley Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences Eukaryot. Cell 2 2003 381 389 (Pubitemid 36774687)
53. A. Delahodde, T. Delaveau, and C. Jacq Positive autoregulation of the yeast transcription factor Pdr3p, which is involved in control of drug resistance Mol. Cell. Biol. 15 1995 4043 4051
54. E. Carvajal, H.B. Van Den Hazel, A. Cybularz-Kolaczkowska, E. Balzi, and A. Goffeau Molecular and phenotypic characterisation of yeast PDR1 mutants that show hyperactive transcription of various ABC multidrug transporter genes Mol. Gen. Genet. 256 1997 406 415
55. A. Nawrocki, S.J. Fey, A. Goffeau, P. Roepstorff, and P.M. Larsen The effects of transcription regulating genes PDR1, pdr1-3 and PDR3 in pleiotropic drug resistance Eur. J. Mass Spectrom. 7 2001 195 205 (Pubitemid 33672904)
56. M.S. Tuttle, D. Radisky, L. Li, and J. Kaplan A dominant allele of PDR1 alters transition metal resistance in yeast J. Biol. Chem. 278 2003 1273 1280 (Pubitemid 36790811)
57. S. MacPherson, B. Akache, S. Weber, D. De, X.M. Raymond, and B. Turcotte Candida albicans zinc cluster protein Upc2p confers resistance to antifungal drugs and is an activator of ergosterol biosynthetic genes Antimicrob. Agents Chemother. 49 2005 1745 1752 (Pubitemid 40631584)
58. T.T. Liu, R.E. Lee, K.S. Barker, R.E. Lee, L. Wei, R. Homayouni, and P.D. Rogers Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans Antimicrob. Agents Chemother. 49 2005 2226 2236 (Pubitemid 40734449)
59. A.T. Coste, V. Turner, F. Ischer, J. Morschhauser, A. Forche, A. Selmecki, J. Berman, J. Bille, and D. Sanglard A mutation in Tac1p, a transcription factor regulating CDR1 and CDR2, is coupled with loss of heterozygosity at Chromosome 5 to mediate antifungal resistance in Candida albicans Genetics 172 2006 2139 2156
60. A.T. Coste, M. Karababa, F. Ischer, J. Bille, and D. Sanglard TAC1, transcriptional activator of CDR genes, is a new transcription factor involved in the regulation of Candida albicans ABC transporters CDR1 and CDR2 Eukaryot. Cell 3 2004 1639 1652 (Pubitemid 40025121)
61. D. Banerjee, Transcriptome analysis of steroid response in yeasts, JNU, Ph.D. thesis, 2008.
62. T.T. Liu, S. Znaidi, K.S. Barker, L. Xu, R. Homayouni, S. Saidane, J. Morschhauser, A. Nantel, M. Raymond, and P.D. Rogers Genome-wide expression and location analyses of the Candida albicans Tac1p regulon Eukaryot. Cell 6 2007 2122 2138 (Pubitemid 350221281)
63. S. Znaidi, D. De, X.S. Weber, T. Rigby, A. Nantel, and M. Raymond The zinc cluster transcription factor Tac1p regulates PDR16 expression in Candida albicans Mol. Microbiol. 66 2007 440 452 (Pubitemid 47482385)
64. D. Talibi, and M. Raymond Isolation of a putative Candida albicans transcriptional regulator involved in pleiotropic drug resistance by functional complementation of a pdr1 pdr3 mutation in Saccharomyces cerevisiae J. Bacteriol. 181 1999 231 240 (Pubitemid 29013676)
65. V. Fardeau, G. Lelandais, A. Oldfield, H. Salin, S. Lemoine, M. Garcia, V. Tanty, C.S. Le, C. Jacq, and F. Devaux The central role of PDR1 in the foundation of yeast drug resistance J. Biol. Chem. 282 2007 5063 5074 (Pubitemid 47100939)
66. G. Conseil, J.M. Perez-Victoria, J.M. Renoir, A. Goffeau, and P.A. Di Potent competitive inhibition of drug binding to the Saccharomyces cerevisiae ABC exporter Pdr5p by the hydrophobic estradiol-derivative RU49953 Biochim. Biophys. Acta 1614 2003 131 134 (Pubitemid 36929976)
67. J.K. Thakur, H. Arthanari, F. Yang, S.J. Pan, X. Fan, J. Breger, D.P. Frueh, K. Gulshan, D.K. Li, E. Mylonakis, K. Struhl, W.S. Moye-Rowley, B.P. Cormack, G. Wagner, and A.M. Naar A nuclear receptor-like pathway regulating multidrug resistance in fungi Nature 452 2008 604 609 (Pubitemid 351483364)