Gonadotropin-releasing hormone-mediated phosphorylation of estrogen receptor-α contributes to fosB expression in mouse gonadotrophs

Endocrinology

Volumn 150, Issue 10, 2009, Pages 4583-4593

  Chen, Junling ^a   An, Beum Soo ^a   Cheng, Linan ^b   Hammond, Geoffrey L ^a   Leung, Peter C K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SHANGHAI INSTITUTE OF PLANNED PARENTHOOD RESEARCH   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; FOLLITROPIN; GONADORELIN; GONADORELIN RECEPTOR; GONADORELIN RECEPTOR 1; GONADORELIN RECEPTOR 2; HISTONE ACETYLTRANSFERASE PCAF; ITURELIX; LUCIFERASE; PROTEIN P300; SERINE DERIVATIVE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BETA CHAIN; CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION; CYTOPLASM; EARLY RESPONSE GENE; ESTROGEN RESPONSIVE ELEMENT; GENE ACTIVATION; GENE EXPRESSION; GONADOTROPIN SECRETING CELL; HYPOPHYSIS CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REPORTER GENE; TRANSCRIPTION INITIATION; UPREGULATION;

ANIMALS; CELL LINE; ESTROGEN RECEPTOR ALPHA; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GONADOTROPHS; GONADOTROPIN-RELEASING HORMONE; LUCIFERASES; MICE; P300-CBP TRANSCRIPTION FACTORS; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTO-ONCOGENE PROTEINS C-FOS; RESPONSE ELEMENTS;

EID: 70349307062     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-0455     Document Type: Article

References (56)

1. Schally AV, Arimura A, Baba Y, Nair RM, Matsuo H, Redding TW, Debeljuk L 1971 Isolation and properties of the FSH and LH-releasing hormone. Biochem Biophys Res Commun 43:393-399
2. Matsuo H, Baba Y, Nair RM, Arimura A, Schally AV 1971 Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem Biophys Res Commun 43:1334-1339
3. Baba Y, Matsuo H, Schally AV 1971 Structure of the porcine LHand FSH-releasing hormone. II. Confirmation of the proposed structure by conventional sequential analyses. Biochem Biophys Res Commun 44:459-463
4. Guillemin R 1967 The adenohypophysis and its hypothalamic control. Annu Rev Physiol 29:313-348
5. Kang SK, Choi KC, Yang HS, Leung PC 2003 Potential role of gonadotrophin-releasing hormone (GnRH)-I and GnRH-II in the ovary and ovarian cancer. Endocr Relat Cancer 10:169-177
6. Cheng CK, Leung PC 2005 Molecular biology of gonadotropin-releasing hormone (GnRH)-I, GnRH-II, and their receptors in humans. Endocr Rev 26:283-306
7. Pawson AJ, Morgan K, Maudsley SR, Millar RP 2003 Type II gonadotrophin-releasing hormone (GnRH-II) in reproductive biology. Reproduction 126:271-278 (Pubitemid 37185227)
8. Weck J, Fallest PC, Pitt LK, Shupnik MA 1998 Differential gonadotropin-releasing hormone stimulation of rat luteinizing hormone subunit gene transcription by calcium influx and mitogen-activated protein kinase-signaling pathways. Mol Endocrinol 12:451-457 (Pubitemid 30666274)
9. Halvorson LM, Kaiser UB, Chin WW 1999 The protein kinase C system acts through the early growth response protein 1 to increase LHβ gene expression in synergy with steroidogenic factor-1. Mol Endocrinol 13:106-116
10. Fowkes RC, King P, Burrin JM 2002 Regulation of human glycoprotein hormone α-subunit gene transcription in LβT2 gonadotropes by protein kinase C and extracellular signal-regulated kinase 1/2. Biol Reprod 67:725-734 (Pubitemid 34925188)
11. Vasilyev VV, Lawson MA, Dipaolo D, Webster NJ, Mellon PL 2002 Different signaling pathways control acute induction versus long-term repression of LHβ transcription by GnRH. Endocrinology 143:3414-3426 (Pubitemid 34925716)
12. Haisenleder DJ, Ferris HA, Shupnik MA 2003 The calcium component of gonadotropin-releasing hormone-stimulated luteinizing hormone subunit gene transcription is mediated by calcium/calmodulin-dependent protein kinase type II. Endocrinology 144:2409-2416
13. Bonfil D, Chuderland D, Kraus S, Shahbazian D, Friedberg I, Seger R, Naor Z 2004 Extracellular signal-regulated kinase, Jun N-terminal kinase, p38, and c-Src are involved in gonadotropin-releasing hormone-stimulated activity of the glycoprotein hormone follicle-stimulating hormone β-subunit promoter. Endocrinology 145:2228-2244 (Pubitemid 38535052)
14. Mutiara S, Kanasaki H, Harada T, Oride A, Miyazaki K 2008 The involvement of phosphatidylinositol 3-kinase in gonadotropin-releasing hormone-induced gonadotropin α- and FSHβ-subunit genes expression in clonal gonadotroph LβT2 cells. Mol Cell Endocrinol 283:1-11
15. Coss D, Jacobs SB, Bender CE, Mellon PL 2004 A novel AP-1 site is critical for maximal induction of the follicle-stimulating hormone β gene by gonadotropin-releasing hormone. J Biol Chem 279:152-162 (Pubitemid 38044810)
16. Coss D, Hand CM, Yaphockun KK, Ely HA, Mellon PL 2007 p38 mitogen-activated protein kinase is critical for synergistic induction of the FSHβ gene by gonadotropin-releasing hormone and activin through augmentation of c-Fos induction and Smad phosphorylation. Mol Endocrinol 21:3071-3086 (Pubitemid 350223516)
17. Wang Y, Fortin J, Lamba P, Bonomi M, Persani L, Roberson MS, Bernard DJ 2008 AP-1 and Smad proteins synergistically regulate human follicle-stimulating hormone β promoter activity. Endocrinology 149:5577-5591
18. Strahl BD, Huang HJ, Sebastian J, Ghosh BR, Miller WL 1998 Transcriptional activation of the ovine follicle-stimulating hormone β-subunit gene by gonadotropin-releasing hormone: involvement of two activating protein-1-binding sites and protein kinase C. Endocrinology 139:4455-4465 (Pubitemid 28487759)
19. Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA 2001 Mechanisms of estrogen action. Physiol Rev 81:1535-1565
20. Hall JM, Couse JF, Korach KS 2001 The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 276:36869-36872 (Pubitemid 37384094)
21. Klinge CM 2001 Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res 29:2905-2919 (Pubitemid 32685217)
22. McKenna NJ, Lanz RB, O'Malley BW 1999 Nuclear receptor co-regulators: cellular and molecular biology. Endocr Rev 20:321-344 (Pubitemid 30649811)
23. McKenna NJ, O'Malley BW 2002 Minireview: nuclear receptor coactivators-an update. Endocrinology 143:2461-2465
24. Aronica SM, Katzenellenbogen BS 1993 Stimulation of estrogen receptor-mediated transcription and alteration in the phosphorylation state of the rat uterine estrogen receptor by estrogen, cyclic adenosine monophosphate, and insulin-like growth factor-I. Mol Endocrinol 7:743-752 (Pubitemid 23207377)
25. Bunone G, Briand PA, 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 (Pubitemid 26141134)
26. Demay F, De Monti M, Tiffoche C, Vaillant C, Thieulant ML 2001 Steroid-independent activation of ER by GnRH in gonadotrope pituitary cells. Endocrinology 142:3340-3347 (Pubitemid 32681738)
27. Arnold SF, Obourn JD, Jaffe H, Notides AC 1995 Phosphorylation of the human estrogen receptor by mitogen-activated protein kinase and casein kinase II: consequence on DNA binding. J Steroid Biochem Mol Biol 55:163-172
28. Le Goff 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 (Pubitemid 24237814)
29. Windle JJ, Weiner RI, Mellon PL 1990 Cell lines of the pituitary gonadotrope lineage derived by targeted oncogenesis in transgenic mice. Mol Endocrinol 4:597-603 (Pubitemid 20156991)
30. Alarid ET, Windle JJ, Whyte DB, Mellon PL 1996 Immortalization of pituitary cells at discrete stages of development by directed oncogenesis in transgenic mice. Development 122:3319-3329
31. Pernasetti F, Vasilyev VV, Rosenberg SB, Bailey JS, Huang HJ, Miller WL, Mellon PL 2001 Cell-specific transcriptional regulation of follicle-stimulating hormone-β by activin and gonadotropin-releasing hormone in the LβT2 pituitary gonadotrope cell model. Endocrinology 142:2284-2295 (Pubitemid 32473082)
32. Bourdeau V, Deschênes J, Métivier R, Nagai Y, Nguyen D, Bretschneider N, Gannon F, White JH, Mader S 2004 Genome-wide identification of high-affinity estrogen response elements in human and mouse. Mol Endocrinol 18:1411-1427 (Pubitemid 38692179)
33. Ali S, Metzger D, Bornert JM, Chambon P 1993 Modulation of transcriptional activation by ligand-dependent phosphorylation of the human oestrogen receptor A/B region. EMBO J 12:1153-1160 (Pubitemid 23095864)
34. Kakar SS, Winters SJ, Zacharias W, Miller DM, Flynn S 2003 Identification of distinct gene expression profiles associated with treatment of LβT2 cells with gonadotropin-releasing hormone agonist using microarray analysis. Gene 308:67-77 (Pubitemid 36597824)
35. Burger LL, Dalkin AC, Aylor KW, Haisenleder DJ, Marshall JC 2002 GnRH pulse frequency modulation of gonadotropin subunit gene transcription in normal gonadotropes-assessment by primary transcript assay provides evidence for roles of GnRH and follistatin. Endocrinology 143:3243-3249
36. Schreihofer DA, Resnick EM, Lin VY, Shupnik MA 2001 Ligand-independent activation of pituitary ER: dependence on PKA-stimulated pathways. Endocrinology 142:3361-3368
37. Okada Y, Murota-Kawano A, Kakar SS, Winters SJ 2003 Evidence that gonadotropin-releasing hormone (GnRH) II stimulates luteinizing hormone and follicle-stimulating hormone secretion from monkey pituitary cultures by activating the GnRH I receptor. Biol Reprod 69:1356-1361 (Pubitemid 37173872)
38. Millar RP 2003 GnRH II and type II GnRH receptors. Trends Endocrinol Metab 14:35-43
39. Al-Dhaheri MH, Rowan BG 2007 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
40. Ortí E, Bodwell JE, Munck A 1992 Phosphorylation of steroid hormone receptors. Endocr Rev 13:105-128
41. Lannigan DA 2003 Estrogen receptor phosphorylation. Steroids 68:1-9
42. El-Tanani MK, Green CD 1997 Two separate mechanisms for ligand-independent activation of the estrogen receptor. Mol Endocrinol 11:928-937
43. 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 (Pubitemid 29046844)
44. Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, Masushige S, Gotoh Y, Nishida E, Kawashima H, Metzger D, Chambon P 1995 Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270:1491-1494
45. Tremblay GB, Tremblay A, Copeland NG, Gilbert DJ, Jenkins NA, Labrie F, Giguère V 1997 Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. Mol Endocrinol 11:353-365 (Pubitemid 27106331)
46. 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 (Pubitemid 29292608)
47. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H 2001 Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor α: a new model for anti-estrogen resistance. J Biol Chem 276:9817-9824 (Pubitemid 37391881)
48. Hsieh KP, Martin TF 1992 Thyrotropin-releasing hormone and gonadotropin-releasing hormone receptors activate phospholipase C by coupling to the guanosine triphosphate-binding proteins Gq and G11. Mol Endocrinol 6:1673-1681
49. Sundaresan S, Colin IM, Pestell RG, Jameson JL 1996 Stimulation of mitogen-activated protein kinase by gonadotropin-releasing hormone: evidence for the involvement of protein kinase C. Endocrinology 137:304-311 (Pubitemid 26005005)
50. Lavinsky RM, Jepsen K, Heinzel T, Torchia J, Mullen TM, Schiff R, Del-Rio AL, Ricote M, Ngo S, Gemsch J, Hilsenbeck SG, Osborne CK, Glass CK, Rosenfeld MG, Rose DW 1998 Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc Natl Acad Sci USA 95:2920-2925 (Pubitemid 28135830)
51. Spencer TE, Jenster G, Burcin MM, Allis CD, Zhou J, Mizzen CA, McKenna NJ, Onate SA, Tsai SY, Tsai MJ, O'Malley BW 1997 Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389:194-198 (Pubitemid 27400603)
52. An BS, Selva DM, Hammond GL, Rivero-Muller A, Rahman N, Leung PC 2006 Steroid receptor coactivator-3 is required for progesterone receptor trans-activation of target genes in response to gonadotropin-releasing hormone treatment of pituitary cells. J Biol Chem 281:20817-20824
53. Blanco JC, Minucci S, Lu J, Yang XJ, Walker KK, Chen H, Evans RM, Nakatani Y, Ozato K 1998 The histone acetylase PCAF is a nuclear receptor coactivator. Genes Dev 12:1638-1651 (Pubitemid 28299515)
54. Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y, Evans RM 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 (Pubitemid 27347246)
55. Shaulian E, Karin M 2001 AP-1 in cell proliferation and survival. Oncogene 20:2390-2400
56. Kaminska B, Pyrzynska B, Ciechomska I, Wisniewska M 2000 Modulation of the composition of AP-1 complex and its impact on transcriptional activity. Acta Neurobiol Exp (Wars) 60:395-402 (Pubitemid 30659916)