Ligand-specific dynamics of the androgen receptor at its response element in living cells

Molecular and Cellular Biology

Volumn 27, Issue 5, 2007, Pages 1823-1843

  Klokk, Tove I ^a   Kurys, Piotr ^a   Elbi, Cem ^b,d   Nagaich, Akhilesh K ^b,e   Hendarwanto, Anindya ^b   Slagsvold, Thomas ^a   Chang, Ching Yi ^c   Hager, Gordon L ^b   Saatcioglu, Fahri ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NATIONAL CANCER INSTITUTE   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

^e CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; BICALUTAMIDE; CYPROTERONE ACETATE; FLUTAMIDE; METRIBOLONE; MIFEPRISTONE; TESTOSTERONE; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DRUG RECEPTOR BINDING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION REGULATION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; RECEPTOR INTRINSIC ACTIVITY; SEX DIFFERENTIATION; TRANSCRIPTION INITIATION;

ADENOCARCINOMA; ANDROGEN ANTAGONISTS; ANDROGENS; ANILIDES; ANIMALS; CELL LINE, TUMOR; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYPROTERONE ACETATE; DIHYDROTESTOSTERONE; FEMALE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUTAMIDE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; IN SITU HYBRIDIZATION, FLUORESCENCE; LIGANDS; LUCIFERASES; MAMMARY NEOPLASMS, ANIMAL; MAMMARY TUMOR VIRUS, MOUSE; METRIBOLONE; MICE; MICROSCOPY, VIDEO; MIFEPRISTONE; MODELS, BIOLOGICAL; NITRILES; PLASMIDS; PROMOTER REGIONS (GENETICS); RECEPTORS, ANDROGEN; RESPONSE ELEMENTS; TESTOSTERONE; TOSYL COMPOUNDS; TRANSCRIPTION, GENETIC;

EID: 33847224474     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01297-06     Document Type: Article

References (85)

1. Agresti, A., P. Scaffidi, A. Riva, V. R. Caiolfa, and M. E. Bianchi. 2005. GR and HMGB1 interact only within chromatin and influence each other's residence time. Mol. Cell 18:109-121.
2. Anderson, J. 2003. The role of antiandrogen monotherapy in the treatment of prostate cancer. BJU Int. 91:455-461.
3. Avancès, C., V. Georget, B. Terouanne, F. Orio, O. Cussenot, N. Mottet, P. Costa, and C. Sultan. 2001. Human prostatic cell line PNT1A, a useful tool for studying androgen receptor transcriptional activity and its differential subnuclear localization in the presence of androgens and antiandrogens. Mol. Cell. Endocrinol. 184:13-24.
4. Becker, M., C. Baumann, S. John, D. A. Walker, M. Vigneron, J. G. McNally, and G. L. Hager. 2002. Dynamic behavior of transcription factors on a natural promoter in living cells. EMBO Rep. 3:1188-1194.
5. Becker, P., R. Renkawitz, and G. Schutz. 1984. Tissue-specific DNaseI hypersensitive sites in the 5′-flanking sequences of the tryptophan oxygenase and the tyrosine aminotransferase genes. EMBO J. 3:2015-2020.
6. Belandia, B., and M. G. Parker. 2003. Nuclear receptors: a rendezvous for chromatin remodeling factors. Cell 114:277-280.
7. Berrevoets, C. A., A. Umar, J. Trapman, and A. O. Brinkmann. 2004. Differential modulation of androgen receptor transcriptional activity by the nuclear receptor co-repressor (N-CoR). Biochem. J. 379:731-738.
8. Bohl, C. E., W. Gao, D. D. Miller, C. E. Bell, and J. T. Dalton. 2005. Structural basis for antagonism and resistance of bicalutamide in prostate cancer. Proc. Natl. Acad. Sci. USA 102:6201-6206.
9. Bourachot, B., M. Yaniv, and C. Muchardt. 1999. The activity of mammalian brm/SNF2α is dependent on a high-mobility-group protein I/Y-like DNA binding domain. Mol. Cell. Biol. 19:3931-3939.
10. Bracci, U. 1979. Antiandrogens in the treatment of prostatic cancer. Eur. Urol. 5:303-306.
11. Debril, M. B., L. Gelman, E. Fayard, J. S. Annicotte, S. Rocchi, and J. Auwerx. 2004. Transcription factors and nuclear receptors interact with the SWI/SNF complex through the BAF60c subunit. J. Biol. Chem. 279:16677-16686.
12. Denis, L. J., and K. Griffiths. 2000. Endocrine treatment in prostate cancer. Semin. Surg. Oncol. 18:52-74.
13. Dilworth, F. J., and P. Chambon. 2001. Nuclear receptors coordinate the activities of chromatin remodeling complexes and coactivators to facilitate initiation of transcription. Oncogene 20:3047-3054.
14. Doesburg, P., C. W. Kuil, C. A. Berrevoets, K. Steketee, P. W. Faber, E. Mulder, A. O. Brinkmann, and J. Trapman. 1997. Functional in vivo interaction between the amino-terminal, transactivation domain and the ligand binding domain of the androgen receptor. Biochemistry 36:1052-1064.
15. Elbi, C., D. A. Walker, G. Romero, W. P. Sullivan, D. O. Toft, G. L. Hager, and D. B. DeFranco. 2004. Molecular chaperones function as steroid receptor nuclear mobility factors. Proc. Natl. Acad. Sci. USA 101:2876-2881.
16. Farla, P., R. Hersmus, B. Geverts, P. O. Mari, A. L. Nigg, H. J. Dubbink, J. Trapman, and A. B. Houtsmuller. 2004. The androgen receptor ligand-binding domain stabilizes DNA binding in living cells. J. Struct. Biol. 147:50-61.
17. Farla, P., R. Hersmus, J. Trapman, and A. B. Houtsmuller. 2005. Antiandrogens prevent stable DNA-binding of the androgen receptor. J. Cell Sci. 118:4187-4198.
18. Fletcher, T. M., N. Xiao, G. Mautino, C. T. Baumann, R. Wolford, B. S. Warren, and G. L. Hager. 2002. ATP-dependent mobilization of the glucocorticoid receptor during chromatin remodeling. Mol. Cell. Biol. 22:3255-3263.
19. Fragoso, G., W. D. Pennie, S. John, and G. L. Hager. 1998. The position and length of the steroid-dependent hypersensitive region in the mouse mammary tumor virus long terminal repeat are invariant despite multiple nucleosome B frames. Mol. Cell. Biol. 18:3633-3644.
20. Freeman, B. C., and K. R. Yamamoto. 2002. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 296:2232-2235.
21. Frønsdal, K., N. Engedal, T. Slagsvold, and F. Saatcioglu. 1998. CREB binding protein is a coactivator for the androgen receptor and mediates cross-talk with AP-1. J. Biol. Chem. 273:31853-31859.
22. Fryer, C. J., and T. K. Archer. 1998. Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex. Nature 393:88-91.
23. Georget, V., J. M. Lobaccaro, B. Terouanne, P. Mangeat, J. C. Nicolas, and C. Sultan. 1997. Trafficking of the androgen receptor in living cells with fused green fluorescent protein-androgen receptor. Mol. Cell. Endocrinol. 129:17-26.
24. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
25. Greschik, H., and M. D. 2003. Structure-activity relationship of nuclear receptor-ligand interactions. Curr. Top. Med. Chem. 3:1573-1599.
26. Hager, G. L. 2001. Understanding nuclear receptor function: from DNA to chromatin to the interphase nucleus. Prog. Nucleic Acid Res. Mol. Biol. 66:279-305.
27. He, B., J. A. Kemppainen, and E. M. Wilson. 2000. FXXLF and WXXLF sequences mediate the NH2-terminal interaction with the ligand binding domain of the androgen receptor. J. Biol. Chem. 275:22986-22994.
28. Hodgson, M. C., I. Astapova, S. Cheng, L. J. Lee, M. C. Verhoeven, E. Choi, S. P. Balk, and A. N. Hollenberg. 2005. The androgen receptor recruits nuclear receptor CoRepressor (N-CoR) in the presence of mifepristone via its N and C termini revealing a novel molecular mechanism for androgen receptor antagonists. J. Biol. Chem. 280:6511-6519.
29. Huang, Z. Q., J. Li, L. M. Sachs, P. A. Cole, and J. Wong. 2003. A role for cofactor-cofactor and cofactor-histone interactions in targeting p300, SWI/SNF and Mediator for transcription. EMBO J. 22:2146-2155.
30. Huggins, C., and C. V. Hodges. 1941. Studies on prostatic cancer: effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. Cancer Res. 1:293-297.
31. Ikonen, T., J. J. Palvimo, and O. A. Janne. 1997. Interaction between the amino- and carboxyl-terminal regions of the rat androgen receptor modulates transcriptional activity and is influenced by nuclear receptor coactivators. J. Biol. Chem. 272:29821-29828.
32. Iwasaki, Y., M. Morishita, M. Asai, A. Onishi, M. Yoshida, Y. Oiso, and K. Inoue. 2004. Effects of hormones targeting nuclear receptors on transcriptional regulation of the growth hormone gene in the MtT/S rat somatotrope cell line. Neuroendocrinology 79:229-236.
33. Janicki, S. M., T. Tsukamoto, S. E. Salghetti, W. P. Tansey, R. Sachidanandam, K. V. Prasanth, T. Ried, Y. Shav-Tal, E. Bertrand, R. H. Singer, and D. L. Spector. 2004. From silencing to gene expression: real-time analysis in single cells. Cell 116:683-698.
34. Jenster, G. 1999. The role of the androgen receptor in the development and progression of prostate cancer. Semin. Oncol. 26:407-421.
35. Karpova, T. S., C. T. Baumann, L. He, X. Wu, A. Grammer, P. Lipsky, G. L. Hager, and J. G. McNally. 2003. Fluorescence resonance energy transfer from cyan to yellow fluorescent protein detected by acceptor photobleaching using confocal microscopy and a single laser. J. Microsc. 209:56-70.
36. Kemppainen, J. A., M. V. Lane, M. Sar, and E. M. Wilson. 1992. Androgen receptor phosphorylation, turnover, nuclear transport, and transcriptional activation. Specificity for steroids and antihormones. J. Biol. Chem. 267:968-974.
37. Kokontis, J. M., and S. Liao. 1999. Molecular action of androgen in the normal and neoplastic prostate. Vitam. Horm. 55:219-307.
38. Korkmaz, C. G., K. Fronsdal, Y. Zhang, P. I. Lorenzo, and F. Saatcioglu. 2004. Potentiation of androgen receptor transcriptional activity by inhibition of histone deacetylation-rescue of transcriptionally compromised mutants. J. Endocrinol. 182:377-389.
39. Kraus, W. L., E. M. McInerney, and B. S. Katzenellenbogen. 1995. Ligand-dependent, transcriptionally productive association of the amino- and carboxyl-terminal regions of a steroid hormone nuclear receptor. Proc. Natl. Acad. Sci. USA 92:12314-12318.
40. Langley, E., J. A. Kemppainen, and E. M. Wilson. 1998. Intermolecular NH2-/carboxyl-terminal interactions in androgen receptor dimerization revealed by mutations that cause androgen insensitivity. J. Biol. Chem. 273:92-101.
41. Langley, E., Z. X. Zhou, and E. M. Wilson. 1995. Evidence for an antiparallel orientation of the ligand-activated human androgen receptor dimer. J. Biol. Chem. 270:29983-29990.
42. Lefebvre, P., D. S. Berard, M. G. Cordingley, and G. L. Hager. 1991. Two regions of the mouse mammary tumor virus long terminal repeat regulate the activity of its promoter in mammary cell lines. Mol. Cell. Biol. 11:2529-2537.
43. Lever, M. A., J. P. Th'ng, X. Sun, and M. J. Hendzel. 2000. Rapid exchange of histone H1.1 on chromatin in living human cells. Nature 408:873-876.
44. Liao, G., L. Y. Chen, A. Zhang, A. Godavarthy, F. Xia, J. C. Ghosh, H. Li, and J. D. Chen. 2003. Regulation of androgen receptor activity by the nuclear receptor corepressor SMRT. J. Biol. Chem. 278:5052-5061.
45. Marshall, T. W., K. A. Link, C. E. Petre-Draviam, and K. E. Knudsen. 2003. Differential requirement of SWI/SNF for androgen receptor activity. J. Biol. Chem. 278:30605-30613.
46. Maruvada, P., C. T. Baumann, G. L. Hager, and P. M. Yen. 2003. Dynamic shuttling and intranuclear mobility of nuclear hormone receptors. J. Biol. Chem. 278:12425-12432.
47. Masiello, D., S. Cheng, G. J. Bubley, M. L. Lu, and S. P. Balk. 2002. Bicalutamide functions as an androgen receptor antagonist by assembly of a transcriptionally inactive receptor. J. Biol. Chem. 277:26321-26326.
48. McKenna, N. J., and B. W. O'Malley. 2002. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108:465-474.
49. McNally, J. G., W. G. Muller, D. Walker, R. Wolford, and G. L. Hager. 2000. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science 287:1262-1265.
50. Memedula, S., and A. S. Belmont. 2003. Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16. Curr. Biol. 13:241-246.
51. Métivier, R., G. Penot, M. R. Hubner, G. Reid, H. Brand, M. Kos, and F. Gannon. 2003. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115:751-763.
52. Michalides, R., A. Griekspoor, A. Balkenende, D. Verwoerd, L. Janssen, K. Jalink, A. Floore, A. Velds, L. van't Veer, and J. Neefjes. 2004. Tamoxifen resistance by a conformational arrest of the estrogen receptor alpha after PKA activation in breast cancer. Cancer Cell 5:597-605.
53. Miyamoto, H., E. M. Messing, and C. Chang. 2004. Androgen deprivation therapy for prostate cancer: current status and future prospects. Prostate 61:332-353.
54. Muchardt, C., and M. Yaniv. 1993. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J. 12:4279-4290.
55. Mymryk, J. S., and T. K. Archer. 1995. Dissection of progesterone receptor-mediated chromatin remodeling and transcriptional activation in vivo. Genes Dev. 9:1366-1376.
56. Nagaich, A. K., and G. L. Hager. 2004. UV laser cross-linking: a real-time assay to study dynamic protein/DNA interactions during chromatin remodeling. Sci. STKE 2004:pl13. [Online.] doi:10.1126/stke.2562004pl13.
57. Nagaich, A. K., D. A. Walker, R. Wolford, and G. L. Hager. 2004. Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol. Cell 14:163-174.
58. Pederson, T. 2001. Protein mobility within the nucleus-what are the right moves? Cell 104:635-638.
59. Phair, R. D., S. A. Gorski, and T. Misteli. 2004. Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol. 375:393-414.
60. Phair, R. D., P. Scaffidi, C. Elbi, J. Vecerova, A. Dey, K. Ozato, D. T. Brown, G. Hager, M. Bustin, and T. Misteli. 2004. Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol. 24:6393-6402.
61. Pirtskhalaishvili, G., R. L. Hrebinko, and J. B. Nelson. 2001. The treatment of prostate cancer: an overview of current options. Cancer Pract. 9:295-306.
62. Rayasam, G. V., C. Elbi, D. A. Walker, R. Wolford, T. M. Fletcher, D. P. Edwards, and G. L. Hager. 2005. Ligand-specific dynamics of the progesterone receptor in living cells and during chromatin remodeling in vitro. Mol. Cell. Biol. 25:2406-2418.
63. Rigaud, G., J. Roux, R. Pictet, and T. Grange. 1991. In vivo footprinting of rat TAT gene: dynamic interplay between the glucocorticoid receptor and a liver-specific factor. Cell 67:977-986.
64. Salma, N., H. Xiao, E. Mueller, and A. N. Imbalzano. 2004. Temporal recruitment of transcription factors and SWI/SNF chromatin-remodeling enzymes during adipogenic induction of the peroxisome proliferator-activated receptor gamma nuclear hormone receptor. Mol. Cell. Biol. 24:4651-4663.
65. Schaffner, W. 1988. Gene regulation. A hit-and-run mechanism for transcriptional activation? Nature 336:427-428.
66. Schaufele, F., X. Carbonell, M. Guerbadot, S. Borngraeber, M. S. Chapman, A. A. Ma, J. N. Miner, and M. I. Diamond. 2005. The structural basis of androgen receptor activation: intramolecular and intermolecular amino-carboxy interactions. Proc. Natl. Acad. Sci. USA 102:9802-9807.
67. Schaaf, M. J., and J. A. Cidlowski. 2003. Molecular determinants of glucocorticoid receptor mobility in living cells: the importance of ligand affinity. Mol. Cell. Biol. 23:1922-1934.
68. Shang, Y., M. Myers, and M. Brown. 2002. Formation of the androgen receptor transcription complex. Mol. Cell 9:601-610.
69. Shockett, P., M. Difilippantonio, N. Hellman, and D. G. Schatz. 1995. A modified tetracycline-regulated system provides autoregulatory, inducible gene expression in cultured cells and transgenic mice. Proc. Natl. Acad. Sci. USA 92:6522-6526.
70. Sif, S., P. T. Stukenberg, M. W. Kirschner, and R. E. Kingston. 1998. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12:2842-2851.
71. Slagsvold, T., I. Kraus, T. Bentzen, J. Palvimo, and F. Saatcioglu. 2000. Mutational analysis of the androgen receptor AF-2 (activation function 2) core domain reveals functional and mechanistic differences of conserved residues compared with other nuclear receptors. Mol. Endocrinol. 14:1603-1617.
72. Song, L. N., M. Coghlan, and E. P. Gelmann. 2004. Antiandrogen effects of mifepristone on coactivator and corepressor interactions with the androgen receptor. Mol. Endocrinol. 18:70-85.
73. Stavreva, D. A., W. G. Muller, G. L. Hager, C. L. Smith, and J. G. McNally. 2004. Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes. Mol. Cell. Biol. 24:2682-2697.
74. Steketee, K., C. A. Berrevoets, H. J. Dubbink, P. Doesburg, R. Hersmus, A. O. Brinkmann, and J. Trapman. 2002. Amino acids 3-13 and amino acids in and flanking the 23FxxLF27 motif modulate the interaction between the N-terminal and ligand-binding domain of the androgen receptor. Eur. J. Biochem. 269:5780-5791.
75. Stenoien, D. L., A. C. Nye, M. G. Mancini, K. Patel, M. Dutertre, B. W. O'Malley, C. L. Smith, A. S. Belmont, and M. A. Mancini. 2001. Ligand-mediated assembly and real-time cellular dynamics of estrogen receptor α-coactivator complexes in living cells. Mol. Cell. Biol. 21:4404-4412.
76. Tomura, A., K. Goto, H. Morinaga, M. Nomura, T. Okabe, T. Yanase, R. Takayanagi, and H. Nawata. 2001. The subnuclear three-dimensional image analysis of androgen receptor fused to green fluorescence protein. J. Biol. Chem. 276:28395-28401.
77. Tyagi, R. K., Y. Lavrovsky, S. C. Ahn, C. S. Song, B. Chatterjee, and A. K. Roy. 2000. Dynamics of intracellular movement and nucleocytoplasmic recycling of the ligand-activated androgen receptor in living cells. Mol. Endocrinol. 14:1162-1174.
78. Walker, D., H. Htun, and G. L. Hager. 1999. Using inducible vectors to study intracellular trafficking of GFP-tagged steroid/nuclear receptors in living cells. Methods 19:386-393.
79. Wang, L., C. L. Hsu, and C. Chang. 2005. Androgen receptor compressors: an overview. Prostate 63:117-130.
80. Wang, Q., J. S. Carroll, and M. Brown. 2005. Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol. Cell 19:631-642.
81. Warriar, N., N. Page, M. Koutsilieris, and M. V. Govindan. 1993. Interaction of antiandrogen-androgen receptor complexes with DNA and transcription activation. J. Steroid Biochem. Mol. Biol. 46:699-711.
82. Wong, C. W., and M. L. Privalsky. 1998. Transcriptional silencing is defined by isoform- and heterodimer-specific interactions between nuclear hormone receptors and compressors. Mol. Cell. Biol. 18:5724-5733.
83. Ye, Q., Y. F. Hu, H. Zhong, A. C. Nye, A. S. Belmont, and R. Li. 2001. BRCA1-induced large-scale chromatin unfolding and allele-specific effects of cancer-predisposing mutations. J. Cell Biol. 155:911-921.
84. Zhang, J., R. E. Campbell, A. Y. Ting, and R. Y. Tsien. 2002. Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 3:906-918.
85. Zhu, P., S. H. Baek, E. M. Bourk, K, A. Ohgi, I. Garcia-Bassets, H. Sanjo, S. Akira, P. F. Kotol, C. K. Glass, M. G. Rosenfeld, and D. W. Rose. 2006. Macrophage/cancer cell interactions mediate hormone resistance by a nuclear receptor derepression pathway. Cell 124:615-629.