Steroid receptor phosphorylation: A key modulator of multiple receptor functions

Molecular Endocrinology

Volumn 21, Issue 10, 2007, Pages 2311-2319

  Weigel, Nancy L ^a   Moore, Nicole L ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STEROID RECEPTOR;

DNA BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SHORT SURVEY;

ANIMALS; HUMANS; PHOSPHORYLATION; RECEPTORS, STEROID; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 34948900221     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2007-0101     Document Type: Short Survey

References (71)

1. Picard D 2006 Chaperoning steroid hormone action. Trends Endocrinol Metab 17:229-235
2. Wang Z, Chen W, Kono E, Dang T, Garabedian MJ 2007 Modulation of glucocorticoid receptor phosphorylation and transcriptional activity by a C-terminal-associated protein phosphatase. Mol Endocrinol 21:625-634
3. Yang CS, Xin HW, Kelley JB, Spencer A, Brautigan DL, Paschal BM 2007 Ligand binding to the androgen receptor induces conformational changes that regulate phosphatase interactions. Mol Cell Biol 27:3390-3404
4. Métivier R, Penot G, Hübner MR, Reid G, Brand H, Koš M, Gannon F 2003 Estrogen receptor-α directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115:751-763
5. Kumar R, Thompson EB 1999 The structure of the nuclear hormone receptors. Steroids 64:310-319
6. Kumar R, Lee J-C, Bolen D, Thompson E 2001 The conformation of the glucocorticoid receptor AF1/τ1 domain induced by osmolyte binds co-regulatory proteins. J Biol Chem 276:18146-18152
7. Kumar R, Volk DE, Li J, Lee JC, Gorenstein DG, Thompson EB 2004 TATA box binding protein induces structure in the recombinant glucocorticoid receptor AF1 domain. Proc Natl Acad Sci USA 101:16425-16430
8. Kumar R, Betney R, Li J, Thompson EB, McEwan IJ 2004 Induced α-helix structure in AF1 of the androgen receptor upon binding transcription factor TFIIF. Biochemistry 43:3008-3013
9. Al-Dhaheri MH, Rowan BG 28 April 2006 Application of phosphorylation site-specific antibodies to measure nuclear receptor signaling: characterization of novel phosphoantibodies for estrogen receptor α. Nucl Recept Signal 4:e007
10. Knotts TA, Orkiszewski RS, Cook RG, Edward DP, Weigel NL 2001 Identification of a phosphorylation site in the hinge region of the human progesterone receptor and additional amino-terminal phosphorylation sites. J Biol Chem 276:8475-8483
11. Yi P, Wu RC, Sandquist J, Wong J, Tsai SY, Tsai MJ, Means AR, O'Malley BW 2005 Peptidyl-prolyl isomerase 1 (Pin1) serves as a coactivator of steroid receptor by regulating the activity of phosphorylated steroid receptor coactivator 3 (SRC-3/AIB1). Mol Cell Biol 25:9687-9699
12. Bodwell JE, Orti E, Coull JM, Pappin DJ, Swift F, Smith LI 1991 Identification of the phosphorylation sites in the mouse glucocorticoid receptor. J Biol Chem 266:7549-7555
13. Denner LA, Schrader WT, O'Malley BW, Weigel NL 1990 Hormonal regulation and identification of chicken progesterone receptor phosphorylation sites. J Biol Chem 265:16548-16555
14. Gioeli D, Ficarro SB, Kwiek JJ, Aaronson D, Hancock M, Catling AD, White FM, Christian RE, Settlage RE, Shabanowitz J, Hunt DF, Weber MJ 2002 Androgen receptor phosphorylation. Regulation and identification of the phosphorylation sites. J Biol Chem 277:29304-29314
15. LeGoff P, Montano MM, Schodin DJ, Katzenellenbogen BS 1994 Phosphorylation of the human estrogen receptor. Identification of hormone-regulated sites and examination of their influence on transcriptional activity. J Biol Chem 269:4458-4466
16. Zhang Y, Beck CA, Poletti A, Edwards DP, Weigel NL 1994 Identification of phosphorylation sites unique to the B form of human progesterone receptor: in vitro phosphorylation by casein kinase II. J Biol Chem 269:31034-31040
17. Zhang Y, Beck CA, Poletti A, Edwards DP, Weigel NL 1995 Identification of a group of Ser-Pro motif hormone-inducible phosphorylation sites in the human progesterone receptor. Mol Endocrinol 9:1029-1040
18. Zhou ZX, Kemppainen JA, Wilson EM 1995 Identification of three proline-directed phosphorylation sites in the human androgen receptor. Mol Endocrinol 9:605-615
19. Cheng X, Hart GW 2001 Alternative O-glycosylation/Ophosphorylation of serine-16 in murine estrogen receptor β: post-translational regulation of turnover and transactivation activity. J Biol Chem 276:10570-10575
20. Villen J, Beausoleil SA, Gerber SA, Gygi SP 2007 Largescale phosphorylation analysis of mouse liver. Proc Natl Acad Sci USA 104:1488-1493
21. Lahooti H, White R, Hoare SA, Rahman D, Pappin DJC, Parker MG 1995 Identification of phosphorylation sites in the mouse oestrogen receptor. J Steroid Biochem Mol Biol 55:305-313
22. Taneja SS, Ha S, Swenson NK, Huang HY, Lee P, Melamed J, Shapiro E, Garabedian MJ, Logan SK 2005 Cell specific regulation of androgen receptor phosphorylation in vivo. J Biol Chem 280:40916-40924
23. Yang CS, Vitto MJ, Busby SA, Garcia BA, Kesler CT, Gioeli D, Shabanowitz J, Hunt DF, Rundell K, Brautigan DL, Paschal BM 2005 Simian virus 40 small t antigen mediates conformation-dependent transfer of protein phosphatase 2A onto the androgen receptor. Mol Cell Biol 25:1298-1308
24. Clemm DL, Sherman L, Boonyaratanakornkit V, Schrader WT, Weigel NL, Edwards DP 2000 Differential hormone-dependent phosphorylation of progesterone receptor A and B forms revealed by phosphoserine site specific monoclonal antibodies. Mol Endocrinol 14:52-65
25. Narayanan R, Edwards DP, Weigel NL 2005 Human progesterone receptor displays cell cycle-dependent changes in transcriptional activity. Mol Cell Biol 25:2885-2898
26. Pierson-Mullany LK, Lange CA 2004 Phosphorylation of progesterone receptor serine 400 mediates ligand-independent transcriptional activity in response to activation of cyclin-dependent protein kinase 2. Mol Cell Biol 24:10542-10557
27. Lee H, Bai W 2002 Regulation of estrogen receptor nuclear export by ligand-induced and p38-mediated receptor phosphorylation. Mol Cell Biol 22:5835-5845
28. Al-Dhaheri MH, Rowan BG 2006 Protein kinase A exhibits selective modulation of estradiol dependent transcription in breast cancer cells that is associated with decreased ligand binding, altered estrogen receptor α promoter interaction and changes in receptor phosphorylation. Mol Endocrinol 21:439-456
29. Arnold SF, Obourn JD, Jaffe H, Notides AC 1995 Phosphorylation of the human estrogen receptor on tyrosine 537 in vivo and by Src family tyrosine kinases in vitro. Mol Endocrinol 9:24-33
30. Guo Z, Dai B, Jiang T, Xu K, Xie Y, Kim O, Nesheiwat I, Kong X, Melamed J, Handratta VD, Njar VC, Brodie AM, Yu LR, Veenstra TD, Chen H, Qiu Y 2006 Regulation of androgen receptor activity by tyrosine phosphorylation. Cancer Cell 10:309-319
31. Kraus S, Gioeli D, Vomastek T, Gordon V, Weber MJ 2006 Receptor for activated C kinase 1 (RACK1) and Src regulate the tyrosine phosphorylation and function of the androgen receptor. Cancer Res 66:11047-11054
32. 530 facilitates hormone-dependent transcriptional activation of the chicken progesterone receptor. Mol Endocrinol 8:1465-1473
33. Cui Y, Zhang M, Pestell R, Curran EM, Welshons WV, Fuqua SA 2004 Phosphorylation of estrogen receptor α blocks its acetylation and regulates estrogen sensitivity. Cancer Res 64:9199-9208
34. Fuqua SAW, Wiltschke C, Zhang QX, Borg A, Castles CG, Friedrichs WE, Hopp T, Hilsenbeck S, Mohsin S, O'Connell P, Allred DC 2000 A hypersensitive estrogen receptor-α mutation in premalignant breast lesions. Cancer Res 60:4026-4029
35. Likhite VS, Stossi F, Kim K, Katzenellenbogen BS, Katzenellenbogen JA 2006 Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Mol Endocrinol 20:3120-3132
36. Webster JC, Jewell CM, Bodwell J, Munck A, Madhabananda S, Cidlowski JA 1997 Mouse glucocorticoid receptor phosphorylation status influences multiple functions of the receptor protein. J Biol Chem 272:9287-9293
37. Ismaili N, Blind R, Garabedian MJ 2005 Stabilization of the unliganded glucocorticoid receptor by TSG101. J Biol Chem 280:11120-11126
38. Lange CA, Shen T, Horwitz KB 2000 Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc Natl Acad Sci USA 97:1032-1037
39. Cheng X, Cole RN, Zaia J, Hart GW 2000 Alternative O-glycosylation/O- phosphorylation of the murine estrogen receptor β. Biochemistry 39:11609-11620
40. Murphy LC, Weitsman GE, Skliris GP, Teh EM, Li L, Peng B, Davie JR, Ung K, Niu YL, Troup S, Tomes L, Watson PH 2006 Potential role of estrogen receptor α (ERα) phosphorylated at Serine118 in human breast cancer in vivo. J Steroid Biochem Mol Biol 102:139-146
41. Valley CC, Metivier R, Solodin NM, Fowler AM, Mashek MT, Hill L, Alarid ET 2005 Differential regulation of estrogen-inducible proteolysis and transcription by the estrogen receptor α N terminus. Mol Cell Biol 25:5417-5428
42. Chen S, Xu Y, Yuan X, Bubley GJ, Balk SP 2006 Androgen receptor phosphorylation and stabilization in prostate cancer by cyclin-dependent kinase 1. Proc Natl Acad Sci USA 103:15969-15974
43. Mellinghoff IK, Vivanco I, Kwon A, Tran C, Wongvipat J, Sawyers CL 2004 HER2/neu kinase-dependent modulation of androgen receptor function through effects on DNA binding and stability. Cancer Cell 6:517-527
44. Castano E, Vorojeikina DP, Notides AC 1997 Phosphorylation of serine-167 on the human oestrogen receptor is important for oestrogen response element binding and transcriptional activation. Biochem J 326:149-157
45. Tzeng DZ, Klinge CM 1996 Phosphorylation of purified estradiol-liganded estrogen receptor by casein kinase II increases estrogen response element binding but does not alter ligand stability. Biochem Biophys Res Commun 223:554-560
46. Shah YM, Rowan BG 2005 The Src kinase pathway promotes tamoxifen agonist action in Ishikawa endometrial cells through phosphorylation-dependent stabilization of estrogen receptor α promoter interaction and elevated steroid receptor coactivator 1 activity. Mol Endocrinol 19:732-748
47. Chen D, Pace PE, Coombes RC, Ali S 1999 Phosphorylation of human estrogen receptor α by protein kinase A regulates dimerization. Mol Cell Biol 19:1002-1015
48. Qiu M, Olsen A, Faivre E, Horwitz KB, Lange CA 2003 Mitogen activated protein kinase regulates nuclear association of human progesterone receptors. Mol Endocrinol 17:628-642
49. Gioeli D, Black BE, Gordon V, Spencer A, Kesler CT, Eblen ST, Paschal BM, Weber MJ 2006 Stress kinase signaling regulates androgen receptor phosphorylation, transcription, and localization. Mol Endocrinol 20:503-515
50. Itoh M, Adachi M, Yasui H, Takekawa M, Tanaka H, Imai K 2002 Nuclear export of glucocorticoid receptor is enhanced by c-Jun N-terminal kinase-mediated phosphorylation. Mol Endocrinol 16:2382-2392
51. Liu J, DeFranco DB 2000 Protracted nuclear export of glucocorticoid receptor limits its turnover and does not require the exportin 1/CRM1-directed nuclear export pathway. Mol Endocrinol 14:40-51
52. DeFranco DB, Qi M, Borror KC, Garabedian MJ, Brautigan DL 1991 Protein phosphatases types 1 and/or 2A regulate nucleocytoplasmic shuttling of glucocorticoid receptors. Mol Endocrinol 5:1215-1228
53. Walther RF, Atlas E, Carrigan A, Rouleau Y, Edgecombe A, Visentin L, Lamprecht C, Addicks GC, Hache RJ, Lefebvre YA 2005 A serine/threonine-rich motif is one of three nuclear localization signals that determine unidirectional transport of the mineralocorticoid receptor to the nucleus. J Biol Chem 280:17549-17561
54. 211 in the chicken progesterone receptor modulates its transcriptional activity. J Biol Chem 271:12801-12806
55. Takimoto GS, Hovland AR, Tasset DM, Melville MY, Tung L, Horwitz KB 1997 Role of phosphorylation on DNA binding and transcriptional functions of human progesterone receptors. J Biol Chem 271:13308-13316
56. Bunone G, Briand P-A, Miksicek RJ, Picard D 1996 Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J 15:2174-2183
57. Rogatsky I, Trowbridge JM, Garabedian MJ 1999 Potentiation of human estrogen receptor α transcriptional activation through phosphorylation of serines 104 and 106 by the cyclin A-CDK2 complex. J Biol Chem 274:22296-22302
58. Shen T, Horwitz KB, Lange CA 2001 Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-activated protein kinase-dependent phosphorylation of serine 294. Mol Cell Biol 21:6122-6131
59. Rogatsky I, Logan SK, Garabedian MJ 1998 Antagonism of glucocorticoid receptor transcriptional activation by the c-Jun N-terminal kinase. Proc Natl Acad Sci USA 95:2050-2055
60. Miller AL, Webb MS, Copp AJ, Wang Y, Johnson BH, Kumar R, Thompson EB 2005 p38 mitogen-activated protein kinase (MAPK) is a key mediator in glucocorticoid-induced apoptosis of lymphoid cells: correlation between p38 MAPK activation and site-specific phosphorylation of the human glucocorticoid receptor at serine 211. Mol Endocrinol 19:1569-1583
61. Daniel AR, Qiu M, Faivre EJ, Ostrander JH, Skildum A, Lange CA 2007 Linkage of progestin and epidermal growth factor signaling: phosphorylation of progesterone receptors mediates transcriptional hypersensitivity and increased ligand-independent breast cancer cell growth. Steroids 72:188-201
62. Masuhiro Y, Mezaki Y, Sakari M, Takeyama K, Yoshida T, Inoue K, Yanagisawa J, Hanazawa S, O'Malley BW, Kato S 2005 Splicing potentiation by growth factor signals via estrogen receptor phosphorylation. Proc Natl Acad Sci USA 102:8126-8131
63. Gburcik V, Bot N, Maggiolini M, Picard D 2005 SPBP is a phosphoserine-specific repressor of estrogen receptor α. Mol Cell Biol 25:3421-3430
64. Tremblay A, Tremblay GB, Labrie F, Giguère V 1999 Ligand-independent recruitment of SRC-1 to estrogen receptor β through phosphorylation of activation function AF-1. Mol Cell 3:513-519
65. Sanchez M, Sauve K, Picard N, Tremblay A 2007 The hormonal response of estrogen receptor β is decreased by the phosphatidylinositol 3-kinase/Akt pathway via a phosphorylation-dependent release of CREB-binding protein. J Biol Chem 282:4830-4840
66. Wu R-C, Qin J, Yi P, Wong J, Tsai SY, Tsai MJ, O'Malley BW 2004 Selective phosphorylations of the SRC-3/AIBI coactivator integrate genomic responses to multiple cellular signaling pathways. Mol Cell 15:937-949
67. Wu R-C, Smith CL, O'Malley BW 2005 Transcriptional regulation by steroid receptor coactivator phosphorylation. Endocr Rev 26:393-399
68. Gregory CW, Fei X, Ponguta LA, He B, Bill HM, French FS, Wilson EM 2004 Epidermal growth factor increases coactivation of the androgen receptor in recurrent prostate cancer. J Biol Chem 279:7119-7130
69. Ueda T, Mawji NR, Bruchovsky N, Sadar MD 2002 Ligand-independent activation of the androgen receptor by interleukin-6 and the role of steroid receptor coactivator-1 in prostate cancer cells. J Biol Chem 277:38087-38094
70. Rowan BG, Garrison N, Weigel NL, O'Malley BW 2000 8-bromo-cyclic AMP induces phosphorylation of two sites in SRC-1 that facilitate ligand-independent activation of the chicken progesterone receptor and are critical for functional cooperation between SRC-1 and CREB binding protein. Mol Cell Biol 20:8720-8730
71. Narayanan R, Adigun AA, Edwards DP, Weigel NL 2005 Cyclin-dependent kinase activity is required for progesterone receptor function: novel role for cyclin A/Cdk2 as a progesterone receptor coactivator. Mol Cell Biol 25:264-277