Gene regulation by the glucocorticoid receptor: Structure:function relationship

Journal of Steroid Biochemistry and Molecular Biology

Volumn 94, Issue 5, 2005, Pages 383-394

  Kumar, Raj ^a   Thompson, E Brad ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Activation domain; Gene regulation; Glucocorticoid receptor; Protein folding; Structure:function relationship

Indexed keywords

GLUCOCORTICOID RECEPTOR; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATION; DNA BINDING; DNA RESPONSIVE ELEMENT; GENE CONTROL; HUMAN; LIGAND BINDING; MOLECULAR GENETICS; MOLECULAR MODEL; NONHUMAN; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; STRUCTURE ACTIVITY RELATION;

EID: 18144424777     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2004.12.046     Document Type: Article

References (106)

1. Y. Morishima, K.C. Kanelakis, P.J.M. Murphy, E.R. Lowe, G.J. Jenkins, Y. Osawa, R.K. Sunahara, and W.B. Pratt The Hsp90 cochaperone p23 is the limiting component of the multiprotein Hsp90/Hsp70-based chaperone system in vivo where it acts to stabilize the client protein Hsp90 complex J. Biol. Chem. 278 2003 48754 48763
2. W.B. Pratt, and D.O. Toft Steroid receptor interactions with heat shock protein and immunophilin chaperones Endocrinol. Rev. 18 1997 306 360
3. W.B. Pratt, and D.O. Toft Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery Exp. Biol. Med. 228 2003 111 133
4. D.M. Dean, and M.M. Sanders Ten years after: reclassification of steroid-responsive genes Mol. Endocrinol. 10 1996 1489 1495
5. G.M. Ringold, K.R. Yamamoto, J.M. Bishop, and H.E. Varmus Glucocorticoid-stimulated accumulation of mouse mammary tumor virus RNA: increased rate of synthesis of viral RNA Proc. Natl. Acad. Sci. U.S.A. 74 1977 2879 2883
6. C.R. Mendelson Mechanism of hormone action J.E. Griffin S.R. Ojeda Text Book of Endocrine Physiology 5th ed. 2004 Chapter 3, pp. 49-88
7. I. Rogatsky, J.C. Wang, M.K. Derynck, D.F. Nonaka, D.B. Khodabakhsh, C.M. Haqq, B.D. Darimont, M.J. Garabedian, and K.R. Yamamoto Target-specific utilization of transcriptional regulatory surfaces by the glucocorticoid receptor Proc. Natl. Acad. Sci. U.S.A. 100 2003 13845 13850
8. R.M. Nissen, and K.R. Yamamoto The glucocorticoid receptor inhibits NFkappaB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain Genes Dev. 14 2000 2314 2329
9. M.D. Medh, M.S. Webb, A.L. Miller, B.H. Johnson, Y. Fofanov, T. Li, T.G. Wood, B.A. Luxon, and E.B. Thomson Gene expression profile of human lymphoid CEM cells sensitive and resistant to glucocorticoid-evoked apoptosis Genomics 81 2003 543 555
10. M.S. Webb, A.L. Miller, B.H. Johnson, Y. Fofanov, T. Li, T.G. Wood, and E.B. Thompson Gene networks in glucocorticoid-evoked apoptosis of leukemic cells J. Steroid Biochem. Mol. Biol. 85 2003 183 193
11. N. Shikama, H.M. Chan, M. Krstic-Demonacos, L. Smith, C.W. Lee, W. Cairns, and N.B. La Thangue Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators Mol. Cell. Biol. 20 2000 8933 8943
12. E. Korzus, J. Torchia, D.W. Rose, L. Xu, R. Kurokawa, E.M. McInerney, T.M. Mullen, C.K. Glass, and M.G. Rosenfeld Transcription factor-specific requirements for coactivators and their acetyltransferase functions Science 279 1998 703 707
13. B.A. Lewis, and D. Reinberg The mediator coactivator complex: functional and physical roles in transcriptional regulation J. Cell Sci. 116 2003 3667 3675
14. R. Kumar, and E.B. Thompson The structure of the nuclear hormone receptors Steroids 64 1999 310 319
15. R. Kumar, and E.B. Thompson Transactivation functions of the N-terminal domains of nuclear hormone receptors:protein folding and coactivator interactions Mol. Endocrinol. 17 2003 1 10
16. E.S. Dieken, and R.L. Miesfeld Transcriptional transactivation functions localized to the glucocorticoid receptor N terminus are necessary for steroid induction of lymphocyte apoptosis Mol. Cell. Biol. 12 1992 5895 5897
17. B.W. O'Malley The steroid receptor superfamily: more excitement predicted for the future Mol. Endocrinol. 4 1990 363 378
18. P.J. Godowski, S. Rusconi, R.L. Miesfeld, and K.R. Yamamoto Glucocorticoid receptor mutants that are constitutive activators of transcriptional enhancement Nature 325 1987 365 368
19. V. Giguere, S.M. Hollenberg, M.G. Rosenfeld, and R.M. Evans Functional domains of the human glucocorticoid receptor Cell 46 1986 545 552
20. R.L. Miesfeld, P.J. Godowski, B.A. Maler, and K.R. Yamamoto Glucocorticoid receptor mutants that define a small region sufficient for enhancer activation Science 236 1987 423 427
21. M.T. Bocquel, V. Kumar, C. Stricker, P. Chambon, and H. Gronemeyer The contribution of the N- and C-terminal regions of steroid receptors to activation of transcription is both receptor and cell-specific Nucl. Acids Res. 17 1989 2581 2595
22. S. Hahn Structure and function of acidic transcription activators Cell 72 1993 481 483
23. P.B. Sigler Acid blobs and negative noodles Nature 333 1988 210 212
24. T. Almlof, A.P.H. Wright, and J.A. Gustafsson Role of acidic and phosphorylated residues in gene activation by the glucocorticoid receptor J. Biol. Chem. 270 1995 17535 17540
25. E. Orti, J.E. Bodwell, and A. Munck Phosphorylation of steroid hormone receptors Endocrinol. Rev. 13 1992 105 128
26. J.E. Bodwell, E. Orti, J.M. Coull, D.J.C. Pappin, L.I. Smith, and F. Swift Identification of phosphorylated sites in the mouse glucocorticoid receptor J. Biol. Chem. 266 1991 7549 7555
27. T. Hard, E. Kellenbach, R. Boelens, B.A. Maler, K. Dahlman, L.P. Freedman, J. Carlstedt-Duke, K.R. Yamamoto, J.A. Gustafsson, and R. Kaptein Solution structure of the DNA binding domain of the glucocorticoid receptor Science 249 1990 157 160
28. B.F. Luisi, W.X. Xu, Z. Otwinowski, L.P. Freedman, K.R. Yamamoto, and P.B. Sigler Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA Nature 352 1991 497 505
29. T. Kucera, M. Waltner-Law, D.K. Scott, R. Prasad, and D.K. Granner A point mutation of the AF2 transactivation domain of the glucocorticoid receptor disrupts its interaction with steroid receptor coactivator 1 J. Biol. Chem. 277 2002 26098 27101
30. P.R. Mittelstadt, and J.D. Ashwell Disruption of glucocorticoid receptor exon 2 yields a ligand-responsive c-terminal fragment that regulates gene expression Mol. Endocrinol. 17 2003 1534 1542
31. K. Dahlman-Wright, H. Baumann, I.J. McEwan, T. Almlof, A.P.H. Wright, J.A. Gustafsson, and T. Hard Structural characterization of a minimal functional transactivation domain from the human glucocorticoid receptor Proc. Natl. Acad. Sci. U.S.A. 92 1995 1699 1703
32. I.V. Baskakov, R. Kumar, G. Srinivasan, Y. Ji, D.W. Bolen, and E.B. Thompson Trimethylamine N-oxide-induced cooperative folding of an intrinsically unfolded transcription-activating fragment of human glucocorticoid receptor J. Biol. Chem. 274 1999 10693 10696
33. R. Kumar, I.V. Baskakov, G. Srinivasan, D.W. Bolen, J.C. Lee, and E.B. Thompson Interdomain signaling in a two-domain fragment of the human glucocorticoid receptor J. Biol. Chem. 274 1999 24737 24741
34. D.L. Bain, M.A. Franden, J.L. McManaman, G.S. Takimoto, and K.B. Horwitz The N-terminal region of the human progesterone A-receptor. Structural analysis and the influence of the DNA binding domain J. Biol. Chem. 275 2000 7313 7320
35. J. Reid, S.M. Kelly, K. Watt, N.C. Price, and I.J. McEwan Conformational analysis of the androgen receptor amino-terminal domain involved in transactivation J. Biol. Chem. 277 2002 20079 20086
36. R. Kumar, R. Betney, J. Li, E.B. Thompson, and I.J. McEwan Induced alpha-helical structure in AF1 of the androgen receptor upon binding transcription factor TFIIF Biochemistry 43 2004 3008 3013
37. A. Henriksson, T. Almlof, J. Ford, I.J. McEvan, J.A. Gustafsson, and A.P.H. Wright Role of Ada adapter complex in gene activation by the glucocorticoid receptor Mol. Cell. Biol. 17 1997 3065 3073
38. J. Ford, I.J. McEwan, A.P.H. Wright, and J.A. Gustafsson Involvement of the transcription factor IID protein complex in gene activation by the N-terminal transactivation domain of the glucocorticoid receptor in vitro Mol. Endocrinol. 11 1997 1467 1475
39. T. Almlof, A.E. Wallberg, J.A. Gustafsson, and A.P.H. Wright Role of important hydrophobic amino acids in the interaction between the glucocorticoid receptor tau1-core activation domain and target factors Biochemistry 37 1998 9586 9594
40. A. Wärnmark, J.A. Gustafsson, and A.P.H. Wright Architectural principles for the structure and function of the glucocorticoid receptor τ1 core activation domain J. Biol. Chem. 275 2000 15014 15018
41. R. Kumar, J.C. Lee, D.W. Bolen, and E.B. Thompson Osmolyte-induced conformation of the glucocorticoid receptor AF1/tau1 domain binds coregulators J. Biol. Chem. 276 2001 18146 18152
42. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41 2000 415 427
43. R.L. Baldwin, and D.G. Rose Is protein folding hierarchic? Local structure and peptide folding TIBS 24 1999 26 33
44. I.V. Baskakov, and D.W. Bolen Forcing thermodynamically unfolded proteins to fold J. Biol. Chem. 273 1998 4831 4834
45. I.V. Baskakov, and D.W. Bolen TMAO counteracts urea effects on rabbit muscle LDH function: a test of the counteraction hypothesis Biophysics 74 1998 2666 2673
46. P.H. Yancey, M.E. Clarke, S.C. Hand, R.D. Bowlus, and G.N. Somero Living with water stress; evolution of osmolyte systems Science 217 1982 1214 1222
47. M.D. Burg Molecular basis of osmolyte regulation Am. J. Physiol. 268 1995 F983 F996
48. Y. Liu, and D.W. Bolen The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes Biochemistry 34 1995 2884 2891
49. C. Bia, J. Biwersi, A.S. Verkman, and M.A. Matthay A mouse model to test the in vivo efficacy of chemical chaperones J. Pharmacol. Toxicol. Meth. 40 1998 39 45
50. Y. Qu, C.L. Bolen, and D.W. Bolen Osmolyte-driven contraction of a random coil protein Proc. Natl. Acad. Sci. U.S.A. 95 1998 9268 9273
51. M. Tanaka, Y. Machida, S. Niu, T. Ikeda, N.R. Jana, H. Doi, M. Kurosawa, M. Nekooki, and N. Nukina Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease Nat. Med. 10 2004 148 154
52. J.A. Lefstin, and K.R. Yamamoto Allosteric effects of DNA on transcriptional regulators Nature 392 1998 885 888
53. I. Rogatsky, H.F. Luecke, D.C. Leitman, and K.R. Yamamoto Altered surfaces of transcriptional coregulator GRIP1 function in different glucocorticoid receptor activation and repression context Proc. Natl. Acad. Sci. U.S.A. 99 2002 16701 16706
54. R. Kumar, D.E. Volk, J. Li, J.C. Lee, D.G. Gorenstein, and E.B. Thompson TATA box binding protein induces structure in the recombinant glucocorticoid receptor AF1 domain Proc. Natl. Acad. Sci. U.S.A. 101 2004 16425 16430
55. A. Warnmark, A. Wikstrom, A.P.H. Wright, J.A. Gustafsson, and T. Hard The N-terminal regions of estrogen receptor alpha and beta are unstructured in vitro and show different TBP binding properties J. Biol. Chem. 276 2001 45939 45944
56. I.J. McEwan, K. Dahlman-Wright, J. Ford, and A.P.H. Wright Functional interaction of the c-Myc transactivation domain with TATA binding protein: evidence for an induced fit model of transactivation domain folding Biochemistry 35 1996 9584 9593
57. H. Baumann, K. Paulsen, H. Kovacs, H. Berglund, A.P.H. Wright, J.A. Gustafsson, and T. Hard Refined solution structure of the glucocorticoid receptor DNA binding domain Biochemistry 32 1993 13463 13471
58. M.A. Eriksson, and L. Nilsson Structure, thermodynamics and cooperativity of the glucocorticoid receptor DNA-binding domain in complex with different response elements. Molecular dynamics simulation and free energy perturbation studies J. Mol. Biol. 253 1995 453 572
59. M. Touray, F. Ryan, R. Jaggi, and F. Martin Characterization of functional inhibition of the glucocorticoid receptor by Fos/Jun Oncogene 6 1991 1227 1234
60. L. Ko, G.R. Cardona, A. Henrion-Caude, and W.W. Chin Identification and characterization of a tissue-specific coactivator, GT198, that interacts with the DNA-binding domains of nuclear receptors Mol. Cell. Biol. 22 2002 357 369
61. R.K. Bledsoe, V.G. Montana, T.B. Stanley, C.J. Delves, C.J. Apolito, D.D. McKee, T.G. Consler, D.G. Parks, E.L. Stewart, T.M. Willson, M.H. Lambert, J.T. Moore, K.H. Pearce, and H.E. Xu Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition Cell 110 2002 93 105
62. M.G. Parker Transcriptional activation by oestrogen receptors Biochem. Soc. Symp. 63 1998 45 50
63. K.B. Horwitz, T.A. Jackson, D.L. Bain, J.K. Richer, G.S. Takimoto, and L. Tung Nuclear receptor coactivators and corepressors Mol. Endocrinol. 10 1996 1167 1177
64. N.J. McKenna, R.B. Lanz, and B.W. O'Malley Nuclear receptor coregulators: cellular and molecular biology Endocr. Rev. 20 1999 321 344
65. K.R. Yamamoto, B.D. Darimont, R.L. Wagner, and J.A. Iniguez-Lluhi Building transcriptional regulatory complexes: signals and surfaces Cold Spring Harbor Symp. Quant. Biol. 63 1998 5875 5898
66. T. Fujita, Y. Kobayashi, O. Wada, Y. Tateshi, L. Kitada, Y. Yamamoto, H. Takeshima, A. Murayama, T. Yano, S. Kato, Y. Kawabe, and J. Yanagisawa Full activation of estrogen receptor alpha activation function-1 induces proliferation of breast cancer cells J. Biol. Chem. 278 2003 26704 26714
67. A.M. Loven, N. Muster, J.R. Yates, and A.M. Nardulli A novel estrogen receptor alpha-associated protein, template-activating factor Ibeta, inhibits acetylation and transactivation Mol. Endocrinol. 17 2003 67 78
68. C.K. Glass, D.W. Rose, and M.G. Rosenfeld Nuclear receptor coactivators Curr. Opin. Cell Biol. 9 1997 222 232
69. H.M. Reichardt, K.H. Kaestner, J. Tuckerman, O. Kretz, O. Wessely, R. Bock, P. Gass, W. Schmid, P. Herrlich, P. Angel, and G. Schutz DNA binding of the glucocorticoid receptor is not essential for survival Cell 93 1998 531 541
70. H. Pan, J.C. Lee, and V.J. Hilser Binding sites in Escherichia coli dihydrofolte reductase communicate by modulating the conformational ensemble Proc. Natl. Acad. Sci U.S.A. 97 2000 12020 12025
71. J.C. Ferreon, J.B. Hamburger, and V.J. Hilser An experimental strategy to evaluate the thermodynamic stability of highly dynamic binding sites in proteins using hydrogen exchange J. Am. Chem. Soc. 126 2004 12774 12775
72. N. Fujitani, M. Kanagawa, T. Aizawa, T. Ohkubo, S. Kaya, M. Demura, K. Kawano, S. Nishimura, K. Taniguchi, and K. Nitta Structure determination and conformational change induced by tyrosine phosphorylation of the N-terminal domain of the alpha-chain of pig gastric H+/K+-ATPase Biochem. Biophys. Res. Commun. 300 2003 223 229
73. B.S. Frank, D. Vardar, A.H. Chishti, and C.J. McKnight The NMR structure of dematin headpiece reveals a dynamic loop that is conformationally altered upon phosphorylation at a distal site J. Biol. Chem. 279 2004 7909 7916
74. P. Fernando, L.A. Megeney, and J.J. Heikkila Phosphorylation-dependent structural alterations in the small hsp30 chaperone are associated with cellular recovery Exp. Cell Res. 286 2003 175 185
75. J.R. Wisniewski, Z. Szewczuk, I. Petry, R. Schwanbeck, and U. Renner Constitutive phosphorylation of the acidic tails of the high mobility group 1 proteins by casein kinase II alters their conformation, stability, and DNA binding specificity J. Biol. Chem. 274 1999 20116 20122
76. L.A. Denner, N.L. Weigel, B.L. Maxwell, W.T. Schrader, and B.W. O'Malley Regulation of progesterone receptor mediated transcription by phosphorylation Science 250 1990 1740 1743
77. W. Bai, and N.L. Weigel Phosphorylation and steroid hormone action Vitam. Horm. 51 1995 289 313
78. D. Gioeli, S.B. Ficarro, J.J. Kwiek, D. Aaronson, M. Hancock, A.D. Catling, F.M. White, R.E. Christian, R.E. Settlage, J. Shabanowitz, D.F. Hunt, and M.J. Weber Androgen receptor phosphorylation J. Biol. Chem. 32 2002 29304 29314
79. S. Ali, D. Metzer, J.M. Bornert, and P. Chambon Modulation of transcriptional activation by ligand-dependent phosphorylation of the human oestrogen receptor A/B region EMBO J. 12 1993 1153 1160
80. R. Metivier, F.A. Gay, M.R. Hubner, G. Flouriot, G. Salbert, F. Gannon, O. Kah, and F. Pakdel Formation of hERα-COUP-TF1 complex enhances hERα AF-1 through Ser118 phosphorylation by MAPK EMBO J. 21 2000 3443 3453
81. F. Barletta, L.P. Freedman, and S. Christakos Enhancement of VDR-mediated transcription by phosphorylation: correlation with increased interaction between the VDR and DRIP205, a subunit of the VDR-interacting protein coactivator complex Mol. Endocrinol. 16 2002 301 314
82. M. Desclozeaux, I.N. Krylova, F. Horn, R.J. Fletterick, and H.A. Ingraham Phosphorylation and intramolecular stabilization of ligand binding domain in the nuclear receptor steroidenic factor 1 Mol. Cell. Biol. 22 2002 7193 8203
83. J.E. Bodwell, J.C. Webster, C.M. Jewell, J.A. Cidlowski, J.M. Hu, and A. Munck Glucocorticoid receptor phosphorylation: overview, function and cell cycle-dependence J. Steroid Biochem. Mol. Biol. 65 1998 91 99
84. J.C. Webster, C.M. Jewell, J.E. Bodwell, A. Munck, M. Sar, and J.A. Cidlowski Mouse glucocorticoid receptor phosphorylation status influences multiple functions of the receptor protein J. Biol. Chem. 272 1997 9287 9293
85. R. Blind, M.J. Garabedian, Regulation of glucocorticoid receptor-mediated transcriptional activation: the role of receptor phosphorylation and cofactor recruitment, Abstract Book, Abstract no. 120, KeyStone Symposia on Nuclear Receptors, 2004, p. 153.
86. N. Ismaili, and M.J. Garabedian Modulation of glucocorticoid receptor function via phosphorylation Ann. NY Acad. Sci. 1024 2004 86 101
87. E. Irusen, J.G. Matthews, A. Takahashi, P.J. Barnes, K.F. Chung, and I.M. Adcock p38 mitogen-activated protein kinase-induced glucocorticoid receptor phosphorylation reduces its activity: role in steroid-insensitive asthma J. Allergy Clin. Immunol. 109 2002 649 657
88. Z. Szatmary, M.J. Garabedian, and J. Vilcek Inhibition of glucocorticoid receptor-mediated transcriptional activation by p38 mitogen-activated protein (MAP) kinase J. Biol. Chem. 279 2004 43708 43715
89. I. Rogatsky, C.L. Waase, and M.J. Garabedian Phosphorylation and inhibition of rat glucocorticoid receptor transcriptional activation by glycogen synthase kinase-3 (GSK-3). Species-specific differences between human and rat glucocorticoid receptor signaling as revealed through GSK-3 phosphorylation J. Biol. Chem. 273 1998 14315 14321
90. J. Majors, and H.E. Varmus A small region of the mouse mammary tumor virus long terminal repeat confers glucocorticoid hormone regulation on a linked heterologous gene Proc. Natl. Acad. Sci. U.S.A. 80 1983 5866 5870
91. R.S. Spolar, and M.T. Record Jr. Coupling of local folding to site-specific binding of proteins to DNA Science 263 1994 777 784
92. O. Gandini, H. Kohno, S. Curtis, and K. Korach Two transcription activation functions in the amino terminus of the mouse estrogen receptor that are affected by the carboxy terminus Steroids 62 1997 508 515
93. D. Shao, S.M. Rangwala, S.T. Bailey, S.L. Krakow, M.J. Reginato, and M.A. Lazar Interdomain communication regulating ligand binding by PPAR Nature 396 1998 377 380
94. E.B. Thompson, and R. Kumar DNA binding of nuclear hormone receptors influences their structure and function Biochem. Biophys. Res. Commun. 306 2003 1 4
95. M.A. Loven, J.R. Wood, and A.M. Nardulli Interaction of estrogen receptors alpha and beta with estrogen response elements Mol. Cell. Endocrinol. 181 2001 151 163
96. P.C. Kulakosky, M.A. McCarty, S.C. Jernigan, K.E. Risinger, and C.M. Klinge Response element sequence modulates estrogen receptor alpha and beta affinity and activity J. Mol. Endocrinol. 29 2002 137 152
97. D. Pearce, W. Matsui, J.N. Miner, and K.R. Yamamoto Glucocorticoid receptor transcriptional activity determined by spacing of receptor and nonreceptor DNA sites J. Biol. Chem. 273 1998 30081 30085
98. M.J. Tetel, P.H. Giangrande, S.A. Leonhardt, D.P. McDonnell, and D.P. Edwards Hormone-dependent interaction between the amino- and carboxyl-terminal domains of progesterone receptor in vitro and in vivo Mol. Endocrinol. 13 1999 910 924
99. E. Langley, J.A. Kemppainen, and E.M. Wilson Intermolecular NH2-/carboxyl-terminal interactions in androgen receptor dimerization revealed by mutations that cause androgen insensitivity J. Biol. Chem. 273 1998 92 101
100. 2-terminal domain J. Biol. Chem. 274 1999 37219 37225
101. 2-terminal and carboxyl-terminal interaction in the human androgen receptor Mol. Genet. Metabol. 75 2002 293 298
102. R. Metivier, G. Penot, G. Flouriot, and F. Pakdel Synergism between ERα transactivation function 1 (AF-1) and AF-2 mediated by steroid receptor coactivator protein-1: requirement for the AF-1 α-helical core and for a direct interaction between the N- and C-terminal domains Mol. Endocrinol. 15 2001 1953 1970
103. A. Benecke, P. Chambon, H. Gronemeyer, Synergy between estrogen receptor alpha activation functions AF1 and AF2 mediated by transcription intermediary factor TIF2, EMBO Reports 1, 2000, pp. 151-157.
104. M. Bommer, A. Benecke, H. Gronemeyer, and C. Rochette-Egly TIF2 mediates the synergy between RARalpha 1 activation functions AF-1 and AF-2 J. Biol. Chem. 277 2002 37961 37966
105. A.B. Hittelman, D. Burakov, J.A. Iniguez-Lluhi, L.P. Freedman, and M.J. Garabedian Differential regulation of glucocorticoid receptor transcriptional activation via AF-1-associated proteins EMBO J. 18 1999 5380 5388
106. Y. Kobayashi, T. Kitamoto, Y. Masuhiro, M. Watanabe, T. Kase, D. Metzger, J. Yanagisawa, and S. Kato p300 mediates functional synergism between AF-1 and AF-2 of estrogen receptor alpha and beta by interacting directly with the N-terminal A/B domains J. Biol. Chem. 275 2000 15645 15651