The AF1 and AF2 Domains of the Androgen Receptor Interact with Distinct Regions of SRC1

REFERENCES

• Alen, P., F. Claessens, E. Schoenmakers, J. V. Swinnen, G. Verhoeven, W. Rombauts, and J. Peeters 1999. Interaction of the putative androgen receptor-specific coactivator ARA70/ELE1a with multiple steroid receptors and identification of an internally deleted ELE1β isoform. Mol. Endocrinol. 13:117–128.
   PubMedGoogle Scholar
• Anzick, S. L., J. Kononen, R. L. Walker, D. O. Azorsa, M. M. Tanner, X.-Y. Guan, G. Sauter, O.-P. Kallioniemi, J. M. Trent, and J. Meltzer 1997. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277:965–968.
   PubMed Web of Science ®Google Scholar
• Baniahmad, A., I. Ha, D. Reinberg, S. Tsai, M.-J. Tsai, and J. O’Malley 1993. Interaction of human thyroid hormone receptor β with transcription factor TFIIB may mediate target gene derepression and activation by thyroid hormone. Proc. Natl. Acad. Sci. USA 90:8832–8836.
   PubMedGoogle Scholar
• Bannister, A. J., and J. Kouzarides 1996. The CBP co-activator is a histone acetyltransferase. Nature 1996:641–643.
   Google Scholar
• Barettino, D., M. Vivanco Ruiz, and J. Stunnenburg 1994. Characterization of the ligand-dependent transactivation domain of thyroid hormone receptor. EMBO J. 13:3039–3049.
   PubMed Web of Science ®Google Scholar
• Beato, M., P. Herrlich, and J. Schutz 1995. Steroid hormone receptors—many actors in search of a plot. Cell 83:851–857.
   PubMed Web of Science ®Google Scholar
• Berrevoets, C. A., P. Doesburg, K. Sketetee, J. Trapman, and J. Brinkmann 1998. Functional interactions of the AF-2 domain core region of the human androgen receptor with the amino-terminal domain and with the transcriptional coactivator TIF-2 (transcriptional intermediary factor-2). Mol. Endocrinol. 12:1172–1183.
   PubMed Web of Science ®Google Scholar
• Brinkmann, A. O., P. W. Faber, H. C. J. van Rooij, G. G. J. M. Kuiper, C. Ris, P. Klaasen, J. A. G. M. van der Korput, M. M. Voorhorst, J. H. van Laar, E. Mulder, and J. Trapman 1989. The human androgen receptor: domain structure, genomic organisation and regulation of expression. J. Steroid Biochem. 34:307–310.
   PubMedGoogle Scholar
• Brou, C., S. Chaudhary, I. Davidson, Y. Lutz, J. Wu, J.-M. Egly, L. Tora, and J. Chambon 1993. Distinct TFIID complexes mediate the effect of different transcriptional activators. EMBO J. 12:489–499.
   PubMedGoogle Scholar
• Brou, C., J. Wu, S. Ali, E. Scheer, C. Lang, I. Davidson, P. Chambon, and J. Tora 1993. Different TBP-associated factors are required for mediating the stimulation of transcription in vitro by the acidic transactivator GAL-VP16 and the two nonacidic activation functions of the estrogen receptor. Nucleic Acids Res. 21:5–12.
   PubMed Web of Science ®Google Scholar
• Buchert, M., S. Schneider, M. T. Adams, H. Hefti, K. Moelling, and J. Hovens 1997. Useful vectors for the two-hybrid system in mammalian cells. BioTechniques 23:396–402.
   PubMedGoogle Scholar
• Cavailles, V., S. Dauvois, F. L’Horset, G. Lopez, S. Hoare, P. J. Kushner, and J. Parker 1995. Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J. 14:3741–3751.
   PubMed Web of Science ®Google Scholar
• Chen, C., and J. Okayama 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745–2752.
   PubMed Web of Science ®Google Scholar
• Chen, H., R. J. Lin, R. L. Schiltz, D. Chakravarti, A. Nash, L. Nagy, M. L. Privalsky, Y. Nakatani, and J. Evans 1997. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with p/CAF and CBP/p300. Cell 90:569–580.
   PubMed Web of Science ®Google Scholar
• Danielian, P. S., R. White, J. A. Lees, and J. Parker 1992. Identification of a conserved region required for hormone dependent transcriptional activation by steroid hormone receptors. EMBO J. 11:1025–1033.
   PubMed Web of Science ®Google Scholar
• Darimont, B. D., R. L. Wagner, J. W. Apriletti, M. R. Stallcup, P. J. Kushner, J. D. Baxter, R. J. Fletterick, and J. Yamamoto 1998. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev. 12:3343–3356.
   PubMed Web of Science ®Google Scholar
• Dodou, E., and J. Treisman 1997. The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol. Cell. Biol. 17:1848–1859.
   PubMed Web of Science ®Google Scholar
• 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, transactivating domain and the ligand binding domain of the androgen receptor. Biochemistry 36:1052–1064.
   PubMed Web of Science ®Google Scholar
• Durand, B., M. Saunders, C. Gaudon, B. Roy, R. Losson, and J. Chambon 1994. Activation function 2 (AF-2) of retinoic acid receptor and 9-cis retinoic acid receptor: presence of a conserved autonomous constitutive activating domain and influence of the nature of the response element on AF-2 activity. EMBO J. 13:5370–5382.
   PubMed Web of Science ®Google Scholar
• Folkers, G. E., and J. van der Saag 1995. Adenovirus E1A functions as a cofactor for retinoic acid receptor β (RARβ) through direct interaction with RARβ Mol. Cell. Biol. 15:5868–5878.
   Google Scholar
• Freedman, L. P. 1999. Increasing the complexity of coactivation in nuclear receptor signaling. Cell 97:5–8.
   PubMed Web of Science ®Google Scholar
• Fronsdal, K., N. Engedal, T. Slagsvold, and J. 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.
   PubMed Web of Science ®Google Scholar
• Glass, C., D. W. Rose, and J. Rosenfeld 1997. Nuclear receptor coactivators. Curr. Opin. Cell Biol. 9:222–232.
   PubMed Web of Science ®Google Scholar
• Glynne, R., L. A. Kerr, I. Mockridge, S. Beck, A. Kelly, and J. Trowsdale 1993. The major histocompatibility complex-encoded proteosome component LMP7: alternative first exons and post-translational processing. Eur. J. Immunol. 23:860–866.
   PubMedGoogle Scholar
• Heery, D. M. Unpublished data.
   Google Scholar
• Heery, D. M., E. Kalkhoven, S. Hoare, and J. Parker 1997. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733–736.
   PubMed Web of Science ®Google Scholar
• Heery, D. M., T. Zacharewski, B. Pierrat, H. Gronemeyer, P. Chambon, and J. Losson 1993. Efficient transactivation by retinoic acid receptors in yeast requires retinoid X receptors. Proc. Natl. Acad. Sci. USA 90:4281–4285.
   PubMedGoogle Scholar
• Henttu, P. M., E. Kalkhoven, and J. Parker 1997. AF-2 activity and recruitment of steroid receptor coactivator-1 to the estrogen receptor depend on a lysine residue conserved in nuclear receptors. Mol. Cell. Biol. 17:1832–1839.
   PubMedGoogle Scholar
• Higuchi, R. 1990. Recombinant PCR, p. 177–183. In M. Innis, D. Gelfand, J. Sninsky, T. White (ed.), PCR protocols: a guide to methods and applications. Academic Press Ltd., London, United Kingdom.
   Google Scholar
• Hong, H., K. Kohli, A. Trivedi, D. L. Johnson, and J. Stallcup 1996. GRIP1, a novel mouse protein that serves as a transcriptional coactivator in yeast for the hormone binding domains of steroid receptors. Proc. Natl. Acad. Sci. USA 93:4948–4952.
   PubMedGoogle Scholar
• Ikonen, T., J. J. Palvimo, and J. Janne 1998. Heterodimerization is mainly responsible for the dominant negative activity of amino-terminally truncated rat androgen receptor forms. FEBS Lett. 430:393–396.
   PubMedGoogle Scholar
• Ikonen, T., J. J. Palvimo, and J. 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.
   PubMedGoogle Scholar
• Ing, N., J. M. Beekman, S. Y. Tsai, M.-J. Tsai, and J. O’Malley 1992. Members of the steroid hormone superfamily interact with TFIIB (S300-II). J. Biol. Chem. 267:17617–17623.
   PubMedGoogle Scholar
• Ito, M., C.-X. Yuan, S. Malik, W. Gu, J. D. Fondell, S. Yamamura, Z.-Y. Fu, X. Zhang, J. Qin, and J. Roeder 1999. Identity between TRAP and SMCC complexes indicates novel pathways for the function of nuclear receptors and diverse mammalian activators. Mol. Cell 3:361–370.
   PubMed Web of Science ®Google Scholar
• Jenster, G., H. van der Korput, J. Trapman, and J. Brinkmann 1995. Identification of two transcription activation units in the N-terminal domain of the human androgen receptor. J. Biol. Chem. 270:7341–7346.
   PubMed Web of Science ®Google Scholar
• Jenster, G., H. A. G. M. van der Korput, C. van Vroonhoven, T. H. van der Kwast, J. Trapman, and J. Brinkmann 1991. Domains of the human androgen receptor involved in steroid binding, transcriptional activation, and subcellular localization. Mol. Endocrinol. 5:1396–1404.
   PubMed Web of Science ®Google Scholar
• Kaiser, C., S. Michaelis, A. Mitchell 1994. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Kalkhoven, E., J. E. Valentine, D. M. Heery, and J. Parker 1998. Isoforms of steroid receptor co-activator 1 differ in their ability to potentiate transcription by the oestrogen receptor. EMBO J. 17:232–243.
   PubMed Web of Science ®Google Scholar
• Karvonen, U., P. J. Kallio, O. A. Janne, and J. Palvimo 1997. Interaction of androgen receptors with androgen response element in intact cells. Roles of amino- and carboxyl-terminal regions and the ligand. J. Biol. Chem. 272:15973–15979.
   PubMed Web of Science ®Google Scholar
• Langley, E., J. A. Kemppainen, and J. Wilson 1998. Intermolecular NH2-/carboxy-terminal interactions in androgen receptor dimerization revealed by mutations that cause androgen insensitivity. J. Biol. Chem. 273:92–101.
   PubMed Web of Science ®Google Scholar
• Langley, E., Z.-X. Zhou, and J. Wilson 1995. Evidence for anti-parallel orientation of the ligand-activated human androgen receptor dimer. J. Biol. Chem. 270:29983–29990.
   PubMed Web of Science ®Google Scholar
• Lanz, R. B., N. J. McKenna, S. Onate, U. Albrecht, J. Wong, S. Y. Tsai, M.-J. Tsai, and J. O’Malley 1999. A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97:17–27.
   PubMed Web of Science ®Google Scholar
• Le Douarin, B., B. Pierrat, E. vom Baur, P. Chambon, and J. Losson 1995. A new version of the two-hybrid assay for detection of protein-protein interactions. Nucleic Acids Res. 23:876–878.
   PubMed Web of Science ®Google Scholar
• Li, H., P. J. Gomes, and J. Chen 1997. RAC3, a steroid/nuclear receptor-associated protein that is related to SRC-1 and TIF-2. Proc. Natl. Acad. Sci. USA 94:8479–8484.
   PubMed Web of Science ®Google Scholar
• Mak, H. Y., S. Hoare, P. M. Henttu, and J. Parker 1999. Molecular determinants of the estrogen receptor-coactivator interface. Mol. Cell. Biol. 19:3895–3903.
   PubMedGoogle Scholar
• Mangelsdorf, D. J., C. Thummel, M. Beato, P. Herrlich, G. Schütz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and J. Evans 1995. The nuclear receptor superfamily: the second decade. Cell 83:835–839.
   PubMed Web of Science ®Google Scholar
• McEwan, I. J., and J. Gustafsson 1997. Interaction of the human androgen receptor transactivation function with the general transcription factor TFIIF. Proc. Natl. Acad. Sci. USA 94:8485–8490.
   PubMed Web of Science ®Google Scholar
• McInerney, E., M.-J. Tsai, B. O’Malley, and J. Katzenellenbogen 1998. Analysis of estrogen receptor transcriptional enhancement by a nuclear hormone coactivator. Proc. Natl. Acad. Sci. USA 93:10069–10073.
   Google Scholar
• Metzger, D., R. Losson, J.-M. Bornet, Y. Lemoine, and J. Chambon 1992. Promoter specificity of the two transcriptional activation functions of the human oestrogen receptor in yeast. Nucleic Acids Res. 20:2813–2817.
   PubMedGoogle Scholar
• Moilanen, A., N. Rouleau, T. Ikonen, J. J. Palvimo, and J. Janne 1998. The presence of a transcription activation function in the hormone-binding domain of androgen receptor is revealed by studies in yeast cells. FEBS Lett. 412:355–358.
   Google Scholar
• Needham, M., et al. Unpublished observations.
   Google Scholar
• Nolte, R. T., G. B. Wisely, S. Westin, J. E. Cobb, M. H. Lambert, R. Kurokawa, M. G. Rosenfeld, T. M. Willson, C. K. Glass, and J. Milburn 1998. Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 395:137–143.
   PubMed Web of Science ®Google Scholar
• Ogryzko, V. V., R. L. Schiltz, V. Russanova, B. H. Howard, and J. Nakaiani 1996. The transcriptional co-activator p300 and CBP are histone acetyltransferases. Cell 87:953–960.
   PubMed Web of Science ®Google Scholar
• Onate, S. A., V. Boonyaratanakornkit, T. E. Spencer, S. Y. Tsai, M.-J. Tsai, D. P. Edwards, and J. O’Malley 1998. The steroid receptor coactivator-1 contains multiple receptor interacting and activation domains that cooperatively enhance the activation function 1 (AF1) and AF2 domains of steroid receptors. J. Biol. Chem. 273:12101–12108.
   PubMed Web of Science ®Google Scholar
• Oñate, S. A., S. Y. Tsai, M.-J. Tsai, and J. O’Malley 1995. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270:1354–1357.
   PubMed Web of Science ®Google Scholar
• Parker, M. G., and J. White 1996. Nuclear receptors spring into action. Nat. Struct. Biol. 3:113–115.
   PubMedGoogle Scholar
• Rachez, C., B. D. Lemon, Z. Suldan, V. Bromleigh, M. Gamble, A. M. Näär, H. Erdjument-Bromage, P. Tempst, and J. Freedman 1999. Ligand-dependent transcription activation by nuclear receptors requires the DRIP complex. Nature 398:824–828.
   PubMed Web of Science ®Google Scholar
• Rundlett, S. E., X.-P. Wu, and J. Miesfeld 1990. Functional characterizations of the androgen receptor confirm that the molecular basis of androgen action is transcriptional regulation. Mol. Endocrinol. 4:708–714.
   PubMedGoogle Scholar
• Scheller, A., E. Hughes, K. L. Golden, and J. Robins 1998. Multiple receptor domains interact to permit, or restrict, androgen-specific gene activation. J. Biol. Chem. 273:24216–24222.
   PubMedGoogle Scholar
• Schüle, R., M. Muller, C. Kaltschmidt, and J. Renkawitz 1988. Many transcription factors interact synergistically with steroid receptors. Science 242:1418–1420.
   PubMedGoogle Scholar
• Schulman, I. G., D. Chakravarti, H. Juguilon, A. Romo, and J. Evans 1995. Interactions between the retinoid X receptor and a conserved region of the tata-binding protein mediate hormone-dependent transactivation. Proc. Natl. Acad. Sci. USA 92:8288–8292.
   PubMedGoogle Scholar
• Shikama, N., J. Lyon, and J. La Thangue 1997. The p300/CBP family: integrating signals with transcription factors and chromatin. Trends Cell Biol. 7:230–236.
   PubMedGoogle Scholar
• Simental, J. A., M. Sar, M. V. Lane, F. S. French, and J. Wilson 1991. Transcriptional activation and nuclear targeting signals of the human androgen receptor. J. Biol. Chem. 266:510–518.
   PubMed Web of Science ®Google Scholar
• Sleigh, M. J. 1986. A nonchromatographic assay for expression of the chloramphenicol acetyltransferase gene in eucaryotic cells. Anal. Biochem. 156:251–256.
   PubMed Web of Science ®Google Scholar
• Spencer, T. E., G. Jenster, M. M. Burcin, C. D. Allis, J. Zhou, C. A. Mizzen, N. J. McKenna, S. A. Onate, S. Y. Tsai, M. J. Tsai, and J. O’Malley 1997. Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389:194–198.
   PubMed Web of Science ®Google Scholar
• Takeshita, A., G. R. Cardona, N. Koibuchi, C. S. Suen, and J. Chin 1997. TRAM-1, a novel 160-kDa thyroid hormone receptor activator molecule, exhibits properties distinct from steroid receptor co-activator-1. J. Biol. Chem. 272:27629–27634.
   PubMedGoogle Scholar
• Tasset, D., L. Tora, C. Fromental, E. Scheer, and J. Chambon 1990. Distinct classes of transcriptional activating domains function by different mechanisms. Cell 62:1177–1187.
   PubMed Web of Science ®Google Scholar
• Tone, Y., T. N. Collingwood, M. Adams, and J. Chatterjee 1994. Functional analysis of a transactivation domain in the thyroid hormone receptor. J. Biol. Chem. 269:31157–31161.
   PubMedGoogle Scholar
• Tora, L., J. White, C. Brou, D. Tasset, N. Webster, E. Scheer, and J. Chambon 1989. The human estrogen receptor has two independent nonacidic transcriptional activation functions. Cell 59:477–497.
   PubMed Web of Science ®Google Scholar
• Torchia, J., C. Glass, and J. Rosenfeld 1998. Co-activators and co-repressors in the integration of transcriptional responses. Curr. Opin. Cell Biol. 10:373–383.
   PubMed Web of Science ®Google Scholar
• Torchia, J., D. W. Rose, J. Inostroza, Y. Kmei, S. Westin, C. Glass, and J. Rosenfeld 1997. The transcriptional coactivator p/CIP binds CBP and mediates nuclear-receptor function. Nature 382:677–684.
   Google Scholar
• Tremblay, A., G. B. Tremblay, F. Labrie, and J. Giguere 1999. Ligand-independent recruitment of SRC-1 to estrogen receptor β through phosphorylation of activation function AF-1. Mol. Cell 3:513–9.
   PubMed Web of Science ®Google Scholar
• Treuter, E., T. Albrektsen, L. Johansson, J. Leers, and J. Gustafsson 1998. A regulatory role for RIP140 in nuclear receptor activation. Mol. Endocrinol. 12:864–881.
   PubMedGoogle Scholar
• Voegel, J. J., M. J. S. Heine, M. Tini, V. Vivat, P. Chambon, and J. Gronemeyer 1998. The co-activator TIF2 contains three nuclear receptor binding motifs and mediates transactivation through CBP binding-dependent and -independent pathways. EMBO J. 17:507–519.
   PubMed Web of Science ®Google Scholar
• Voegel, J. J., M. J. S. Heine, C. Zechel, P. Chambon, and J. Gronemeyer 1996. TIF2, a 160kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nuclear receptors. EMBO J. 15:101–108.
   Google Scholar
• Vojtek, B. A., S. M. Hollenberg, and J. Cooper 1993. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74:205–214.
   PubMed Web of Science ®Google Scholar
• Webb, P., P. Nguyen, J. Shinsako, C. Anderson, W. Feng, M. P. Nguyen, D. Chen, S.-M. Huang, S. Subramanian, E. McKinerny, B. S. Katzenellenbogen, M. R. Stallcup, and J. Kushner 1998. Estrogen receptor activation function 1 works by binding p160 proteins. Mol. Endocrinol. 12:1605–1618.
   PubMed Web of Science ®Google Scholar
• Webster, N. J. G., S. Green, D. Tasset, M. Ponglikitmongkol, and J. Chambon 1988. The transcriptional activation function located in the hormone-binding domain of the human oestrogen receptor is not encoded in a single exon. EMBO J. 8:1441–1446.
   Google Scholar
• White, R., M. Sjöberg, E. Kalkhoven, and J. Parker 1997. Ligand-independent activation of the oestrogen receptor by mutation of a conserved tyrosine. EMBO J. 16:1427–1435.
   PubMed Web of Science ®Google Scholar
• Wurtz, J.-M., W. Bourguet, J.-P. Renaud, V. Vivat, P. Chambon, D. Moras, and J. Gronemeyer 1996. A canonical structure for the ligand-binding domain of nuclear receptors. Nat. Struct. Biol. 3:87–94.
   PubMedGoogle Scholar
• Yeh, S., H. Miyamoto, H. Shima, and J. Chang 1998. From estrogen to androgen receptor: a new pathway for sex hormones in prostate. Proc. Natl. Acad. Sci. USA 95:5527–5532.
   PubMed Web of Science ®Google Scholar
• Yeh, S. Y., and J. Chang 1996. Cloning and characterization of a specific coactivator, ARA(70), for the androgen receptor in human prostate cells. Proc. Natl. Acad. Sci. USA 93:5517–5521.
   PubMed Web of Science ®Google Scholar
• Zhou, Z.-X., M. V. Lane, J. A. Kemppainen, F. S. French, and J. Wilson 1995. Specificity of ligand-dependent androgen receptor stabilization: receptor domain interactions influence ligand dissociation and receptor stability. Mol. Endocrinol. 9:208–218.
   PubMed Web of Science ®Google Scholar
• Zhou, Z.-X., M. Sar, J. A. Simental, M. V. Lane, and J. Wilson 1994. A ligand-dependent bipartite nuclear targeting signal in the human androgen receptor. J. Biol. Chem. 269:13115–13123.
   PubMed Web of Science ®Google Scholar