Stepwise androgen receptor dimerization

Journal of Cell Science

Volumn 125, Issue 8, 2012, Pages 1970-1979

  van Royen, Martin E ^a   van Cappellen, Wiggert A ^b   de Vos, Carola ^a   Houtsmuller, Adriaan B ^a   Trapman, Jan ^a  

^a JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Androgen receptor; DBD; Dimerization; N C interaction; Quantitative live cell imaging; Target genes

Indexed keywords

ANDROGEN RECEPTOR; HOMODIMER;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; DNA BINDING; GENE EXPRESSION REGULATION; GENE POOL; GENE TARGETING; HUMAN; HUMAN CELL; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANDROGENS; CELL NUCLEUS; CYTOPLASM; DIMERIZATION; GENE EXPRESSION REGULATION; HUMANS; LIGANDS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANDROGEN;

EID: 84863111874     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.096792     Document Type: Article

References (46)

1. Bai, S., He, B. and Wilson, E. M. (2005). Melanoma antigen gene protein MAGE-11 regulates androgen receptor function by modulating the interdomain interaction. Mol. Cell. Biol. 25, 1238-1257.
2. Bastiaens, P. I. H. and Jovin, T. M. (1996). Microspectroscopic imaging tracks the intracellular processing of a signal transduction protein: fluorescent-labeled protein kinase C beta I. Proc. Natl. Acad. Sci. USA 93, 8407-8412.
3. Bastiaens, P. I. H., Majoul, I. V., Verveer, P. J., Söling, H.-D. and Jovin, T. M. (1996). Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J. 15, 4246-4253.
4. Bledsoe, R. K., Montana, V. G., Stanley, T. B., Delves, C. J., Apolito, C. J., McKee, D. D., Consler, T. G., Parks, D. J., Stewart, E. L., Willson, T. M. et al. (2002). Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell 110, 93-105.
5. Brinkmann, A. O., Faber, P. W., van Rooij, H. C. J., Kuiper, G. G. J. M., Ris, C., Klaassen, P., van der Korput, J. A. G. M., Voorhorst, M. M., van Laar, J. H., Mulder, E. et al. (1989). The human androgen receptor: domain structure, genomic organization and regulation of expression. J. Steroid Biochem. 34, 307-310.
6. Centenera, M. M., Harris, J. M., Tilley, W. D. and Butler, L. M. (2008). The contribution of different androgen receptor domains to receptor dimerization and signaling. Mol. Endocrinol. 22, 2373-2382.
7. Claessens, F., Denayer, S., Van Tilborgh, N., Kerkhofs, S., Helsen, C. and Haelens, A. (2008). Diverse roles of androgen receptor (AR) domains in AR-mediated signaling. Nucl. Recept. Signal. 6, e008.
8. Dahlman-Wright, K., Wright, A., Gustafsson, J. A. and Carlstedt-Duke, J. (1991). Interaction of the glucocorticoid receptor DNA-binding domain with DNA as a dimer is mediated by a short segment of five amino acids. J. Biol. Chem. 266, 3107-3112.
9. de Ruiter, P. E., Teuwen, R., Trapman, J., Dijkema, R. and Brinkmann, A. O. (1995). Synergism between androgens and protein kinase-C on androgen-regulated gene expression. Mol. Cell. Endocrinol. 110, R1-R6.
10. Denayer, S., Helsen, C., Thorrez, L., Haelens, A. and Claessens, F. (2010). The rules of DNA recognition by the androgen receptor. Mol. Endocrinol. 24, 898-913.
11. Dinant, C., van Royen, M. E., Vermeulen, W. and Houtsmuller, A. B. (2008). Fluorescence resonance energy transfer of GFP and YFP by spectral imaging and quantitative acceptor photobleaching. J. Microsc. 231, 97-104.
12. Dubbink, H. J., Hersmus, R., Verma, C. S., van der Korput, H. A., Berrevoets, C. A., van Tol, J., Ziel-van der Made, A. C. J., Brinkmann, A. O., Pike, A. C. W. and Trapman, J. (2004). Distinct recognition modes of FXXLF and LXXLL motifs by the androgen receptor. Mol. Endocrinol. 18, 2132-2150.
13. Farla, P., Hersmus, R., Geverts, B., Mari, P. O., Nigg, A. L., Dubbink, H. J., Trapman, J. and Houtsmuller, A. B. (2004). The androgen receptor ligand-binding domain stabilizes DNA binding in living cells. J. Struct. Biol. 147, 50-61.
14. Farla, P., Hersmus, R., Trapman, J. and Houtsmuller, A. B. (2005). Antiandrogens prevent stable DNA-binding of the androgen receptor. J. Cell Sci. 118, 4187-4198.
15. Freedman, L. P., Yamamoto, K. R., Luisi, B. F. and Sigler, P. B. (1988). More fingers in hand. Cell 54, 444.
16. Haelens, A., Verrijdt, G., Callewaert, L., Christiaens, V., Schauwaers, K., Peeters, B., Rombauts, W. and Claessens, F. (2003). DNA recognition by the androgen receptor: evidence for an alternative DNA-dependent dimerization, and an active role of sequences flanking the response element on transactivation. Biochem. J. 369, 141-151.
17. Härd, T., Dahlman, K., Carlstedt-Duke, J., Gustafsson, J. A. and Rigler, R. (1990a). Cooperativity and specificity in the interactions between DNA and the glucocorticoid receptor DNA-binding domain. Biochemistry 29, 5358-5364.
18. Härd, T., Kellenbach, E., Boelens, R., Maler, B. A., Dahlman, K., Freedman, L. P., Carlstedt-Duke, J., Yamamoto, K. R., Gustafsson, J. A. and Kaptein, R. (1990b). Solution structure of the glucocorticoid receptor DNA-binding domain. Science 249, 157-160.
19. He, B., Bowen, N. T., Minges, J. T. and Wilson, E. M. (2001). Androgen-induced NH2- and COOH-terminal Interaction Inhibits p160 coactivator recruitment by activation function 2. J. Biol. Chem. 276, 42293-42301.
20. Houtsmuller, A. B. (2005). Fluorescence recovery after photobleaching: application to nuclear proteins. Adv. Biochem. Eng. Biotechnol. 95, 177-199.
21. Hur, E., Pfaff, S. J., Payne, E. S., Grøn, H., Buehrer, B. M. and Fletterick, R. J. (2004). Recognition and accommodation at the androgen receptor coactivator binding interface. PLoS Biol. 2, e274.
22. Jia, L., Berman, B. P., Jariwala, U., Yan, X., Cogan, J. P., Walters, A., Chen, T., Buchanan, G., Frenkel, B. and Coetzee, G. A. (2008). Genomic androgen receptoroccupied regions with different functions, defined by histone acetylation, coregulators and transcriptional capacity. PLoS ONE 3, e3645.
23. Karpova, T. S., Baumann, C. T., He, L., Wu, X., Grammer, A., Lipsky, P., Hager, G. L. and McNally, J. G. (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.
24. Kenworthy, A. K. (2001). Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 24, 289-296.
25. Luisi, B. F., Xu, W. X., Otwinowski, Z., Freedman, L. P., Yamamoto, K. R. and Sigler, P. B. (1991). Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature 352, 497-505.
26. Massie, C. E., Adryan, B., Barbosa-Morais, N. L., Lynch, A. G., Tran, M. G., Neal, D. E. and Mills, I. G. (2007). New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. EMBO Rep. 8, 871-878.
27. Matias, P. M., Donner, P., Coelho, R., Thomaz, M., Peixoto, C., Macedo, S., Otto, N., Joschko, S., Scholz, P., Wegg, A. et al. (2000). Structural evidence for ligand specificity in the binding domain of the human androgen receptor. Implications for pathogenic gene mutations. J. Biol. Chem. 275, 26164-26171.
28. Roemer, S. C., Donham, D. C., Sherman, L., Pon, V. H., Edwards, D. P. and Churchill, M. E. A. (2006). Structure of the progesterone receptor-deoxyribonucleic acid complex: novel interactions required for binding to half-site response elements. Mol. Endocrinol. 20, 3042-3052.
29. Rosenfeld, M. G., Lunyak, V. V. and Glass, C. K. (2006). Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 20, 1405-1428.
30. Sack, J. S., Kish, K. F., Wang, C., Attar, R. M., Kiefer, S. E., An, Y., Wu, G. Y., Scheffler, J. E., Salvati, M. E., Krystek, S. R., Jr et al. (2001). Crystallographic structures of the ligand-binding domains of the androgen receptor and its T877A mutant complexed with the natural agonist dihydrotestosterone. Proc. Natl. Acad. Sci. USA 98, 4904-4909.
31. Savory, J. G. A., Préfontaine, G. G., Lamprecht, C., Liao, M., Walther, R. F., Lefebvre, Y. A. and Haché, R. J. G. (2001). Glucocorticoid receptor homodimers and glucocorticoid-mineralocorticoid receptor heterodimers form in the cytoplasm through alternative dimerization interfaces. Mol. Cell. Biol. 21, 781-793.
32. Schaufele, F., Carbonell, X., Guerbadot, M., Borngraeber, S., Chapman, M. S., Ma, A. A. K., Miner, J. N. and Diamond, M. I. (2005). The structural basis of androgen receptor activation: intramolecular and intermolecular amino-carboxy interactions. Proc. Natl. Acad. Sci. USA 102, 9802-9807.
33. Schwabe, J. W., Chapman, L., Finch, J. T. and Rhodes, D. (1993a). The crystal structure of the estrogen receptor DNA-binding domain bound to DNA: how receptors discriminate between their response elements. Cell 75, 567-578.
34. Schwabe, J. W., Chapman, L., Finch, J. T., Rhodes, D. and Neuhaus, D. (1993b). DNA recognition by the oestrogen receptor: from solution to the crystal. Structure 1, 187-204.
35. Shaffer, P. L., Jivan, A., Dollins, D. E., Claessens, F. and Gewirth, D. T. (2004). Structural basis of androgen receptor binding to selective androgen response elements. Proc. Natl. Acad. Sci. USA 101, 4758-4763.
36. Sultan, C., Lumbroso, S., Poujol, N., Belon, C., Boudon, C. and Lobaccaro, J. M. (1993). Mutations of androgen receptor gene in androgen insensitivity syndromes. J. Steroid Biochem. Mol. Biol. 46, 519-530.
37. Takayama, K., Tsutsumi, S., Katayama, S., Okayama, T., Horie-Inoue, K., Ikeda, K., Urano, T., Kawazu, C., Hasegawa, A., Ikeo, K. et al. (2011). Integration of cap analysis of gene expression and chromatin immunoprecipitation analysis on array reveals genome-wide androgen receptor signaling in prostate cancer cells. Oncogene 30, 619-630.
38. Tanenbaum, D. M., Wang, Y., Williams, S. P. and Sigler, P. B. (1998). Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. Proc. Natl. Acad. Sci. USA 95, 5998-6003.
39. van de Wijngaart, D. J., van Royen, M. E., Hersmus, R., Pike, A. C. W., Houtsmuller, A. B., Jenster, G., Trapman, J. and Dubbink, H. J. (2006). Novel FXXFF and FXXMF motifs in androgen receptor cofactors mediate high affinity and specific interactions with the ligand-binding domain. J. Biol. Chem. 281, 19407-19416.
40. van Royen, M. E., Cunha, S. M., Brink, M. C., Mattern, K. A., Nigg, A. L., Dubbink, H. J., Verschure, P. J., Trapman, J. and Houtsmuller, A. B. (2007). Compartmentalization of androgen receptor protein-protein interactions in living cells. J. Cell Biol. 177, 63-72.
41. van Royen, M. E., Dinant, C., Farla, P., Trapman, J. and Houtsmuller, A. B. (2009a). FRAP and FRET methods to study nuclear receptors in living cells. In The Nuclear Receptor Superfamily, Vol. 505 (ed. I. J. McEwan), pp. 69-96. Totowa, NJ: Humana Press.
42. van Royen, M. E., Farla, P., Mattern, K. A., Geverts, B., Trapman, J. and Houtsmuller, A. B. (2009b). FRAP to study nuclear protein dynamics in living cells. In The Nucleus, Vol. 464 (ed. R. Hancock), pp. 363-384.
43. Wang, Q., Li, W., Liu, X. S., Carroll, J. S., Jänne, O. A., Keeton, E. K., Chinnaiyan, A. M., Pienta, K. J. and Brown, M. (2007). A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 27, 380-392.
44. Wang, Q., Li, W., Zhang, Y., Yuan, X., Xu, K., Yu, J., Chen, Z., Beroukhim, R., Wang, H., Lupien, M. et al. (2009). Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138, 245-256.
45. Williams, S. P. and Sigler, P. B. (1998). Atomic structure of progesterone complexed with its receptor. Nature 393, 392-396.
46. Yu, J., Yu, J., Mani, R. S., Cao, Q., Brenner, C. J., Cao, X., Wang, X., Wu, L., Li, J., Hu, M. et al. (2010). An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 17, 443-454.