Molecular interaction of BMP-4, TGF-β, and estrogens in lactotrophs: Impact on the PRL promoter

Molecular Endocrinology

Volumn 23, Issue 7, 2009, Pages 1102-1114

  Giacomini, Damiana ^a   Páez Pereda, Marcelo ^b,c   Stalla, Johanna ^b   Stalla, Günter K ^b   Arzt, Eduardo ^a  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c Affectis Pharmaceutical AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; PROLACTIN; SMAD PROTEIN; SMAD1 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ESTROGEN RESPONSIVE ELEMENT; GENE MUTATION; HORMONE RELEASE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROLACTIN SECRETING CELL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; BINDING SITES; BONE MORPHOGENETIC PROTEIN 4; CELLS, CULTURED; ESTROGENS; LACTOTROPHS; PROLACTIN; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RATS; RECEPTOR CROSS-TALK; RECEPTORS, ESTROGEN; SMAD PROTEINS; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA;

EID: 67649628208     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2008-0425     Document Type: Article

References (71)

1. Goffin V, Bernichtein S, Touraine P, Kelly PA 2005 Development and potential clinical uses of human prolactin receptor antagonists. Endocr Rev 26:400-422 (Pubitemid 40686651)
2. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA 1998 Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19:225-268 (Pubitemid 29117815)
3. Freeman ME, Kanyicska B, Lerant A, Nagy G 2000 Prolactin: structure, function, and regulation of secretion. Physiol Rev 80:1523-1631 (Pubitemid 30764163)
4. De Paul AL, Pons P, Aoki A, Torres AI 1997 Heterogeneity of pituitary lactotrophs: immunocytochemical identification of functional subtypes. Acta Histochem 99:277-289 (Pubitemid 27396045)
5. Sasaki F, Sano M 1986 Roles of the arcuate nucleus and ovary in the maturation of growth hormone, prolactin, and nongranulated cells in the mouse adenohypophysis during postnatal development: a stereological morphometric study by electron microscopy. Endocrinology 119:1682-1689 (Pubitemid 17170537)
6. Chen CL, Meites J 1970 Effects of estrogen and progesterone on serum and pituitary prolactin levels in ovariectomized rats. Endocrinology 86:503-505
7. Burnstein KL, Cidlowski JA 1993 Multiple mechanisms for regulation of steroid hormone action. J Cell Biochem 51:130-134 (Pubitemid 23058568)
8. Waterman ML, Adler S, Nelson C, Greene GL, Evans RM, Rosenfeld MG 1988 A single domain of the estrogen receptor confers deoxyribonucleic acid binding and transcriptional activation of the rat prolactin gene. Mol Endocrinol 2:14-21 (Pubitemid 18052518)
9. Raymond V, Beaulieu M, Labrie F, Boissier J 1978 Potent antidopaminergic activity of estradiol at the pituitary level on prolactin release. Science 200:1173-1175 (Pubitemid 9087509)
10. Newton CJ, Arzt E, Stalla GK 1994 Involvement of the estrogen receptor in the growth response of pituitary tumor cells to interleukin-2. Biochem Biophys Res Commun 205:1930-1937
11. Gillam MP, Molitch ME, Lombardi G, Colao A 2006 Advances in the treatment of prolactinomas. Endocr Rev 27:485-534 (Pubitemid 44213229)
12. Garcia MM, Kapcala LP 1995 Growth of a microprolactinoma to a macroprolactinoma during estrogen therapy. J Endocrinol Invest 18:450-455
13. Heaney AP, Horwitz GA, Wang Z, Singson R, Melmed S 1999 Early involvement of estrogen-induced pituitary tumor transforming gene and fibroblast growth factor expression in prolactinoma pathogenesis. Nat Med 5:1317-1321 (Pubitemid 29535612)
14. Wiklund J, Wertz N, Gorski J 1981 A comparison of estrogen effects on uterine and pituitary growth and prolactin synthesis in F344 and Holtzman rats. Endocrinology 109:1700-1707 (Pubitemid 12197465)
15. Kelly MA, Rubinstein M, Asa SL, Zhang G, Saez C, Bunzow JR, Allen RG, Hnasko R, Ben-Jonathan N, Grandy DK, Low MJ 1997 Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2 receptor-deficient mice. Neuron 19:103-113 (Pubitemid 27332997)
16. Asa SL, Kelly MA, Grandy DK, Low MJ 1999 Pituitary lactotroph adenomas develop after prolonged lactotroph hyperplasia in dopamine D2 receptor-deficient mice. Endocrinology 140:5348-5355 (Pubitemid 30687146)
17. Saiardi A, Bozzi Y, Baik JH, Borrelli E 1997 Antiproliferative role of dopamine: loss of D2 receptors causes hormonal dysfunction and pituitary hyperplasia. Neuron 19:115-126 (Pubitemid 27332998)
18. Sarkar DK, Kim KH, Minami S 1992 Transforming growth factor-β1 messenger RNA and protein expression in the pituitary gland: its action on prolactin secretion and lactotropic growth. Mol Endocrinol 6:1825-1833
19. Delidow BC, Billis WM, Agarwal P, White BA 1991 Inhibition of prolactin gene transcription by transforming growth factor-β in GH3 cells. Mol Endocrinol 5:1716-1722
20. Lacerte A, Lee EH, Reynaud R, Canaff L, De Guise C, Devost D, Ali S, Hendy GN, Lebrun JJ 2004 Activin inhibits pituitary prolactin expression and cell growth through Smads, Pit-1 and menin. Mol Endocrinol 18:1558-1569 (Pubitemid 38692190)
21. Ramsdell JS 1991 Transforming growth factor-α and -β are potent and effective inhibitors of GH4 pituitary tumor cell proliferation. Endocrinology 128:1981-1990
22. Coya R, Alvarez CV, Perez F, Gianzo C, Diéguez C 1999 Effects of TGF-β1 on prolactin synthesis and secretion: an in-vitro study. J Neuroendocrinol 11:351-360 (Pubitemid 29199693)
23. Pastorcic M, De A, Boyadjieva N, Vale W, Sarkar DK 1995 Reduction in the expression and action of transforming growth factor β1 on lactotropes during estrogen-induced tumorigenesis in the anterior pituitary. Cancer Res 55:4892-4898
24. Burns G, Sarkar DK 1993 Transforming growth factor β1-like immunoreactivity in the pituitary gland of the rat: effect of estrogen. Endocrinology 133:1444-1449 (Pubitemid 23267804)
25. Hentges S, Pastorcic M, De A, Boyadjieva N, Sarkar DK 2000 Opposing actions of two transforming growth factor-β isoforms on pituitary lactotropic cell proliferation. Endocrinology 141:1528-1535 (Pubitemid 32269122)
26. Scully KM, Rosenfeld MG 2002 Pituitary development: regulatory codes in mammalian organogenesis. Science 295:2231-2235 (Pubitemid 34258830)
27. Davis SW, Camper SA 2007 Noggin regulates Bmp4 activity during pituitary induction. Dev Biol 305:145-160 (Pubitemid 46591909)
28. Paez-Pereda M, Giacomini D, Refojo D, Nagashima AC, Hopfner U, Grubler Y, Chervin A, Goldberg V, Goya R, Hentges ST, Low MJ, Holsboer F, Stalla GK, Arzt E 2003 Involvement of bone morphogenetic protein 4 (BMP-4) in pituitary prolactinoma pathogenesis through a Smad/estrogen receptor crosstalk. Proc Natl Acad Sci USA 100:1034-1039 (Pubitemid 36183950)
29. Day RN, Maurer RA 1989 The distal enhancer region of the rat prolactin gene contains elements conferring response to multiple hormones. Mol Endocrinol 3:3-9 (Pubitemid 19045667)
30. Kim KE, Day RN, Maurer RA 1988 Functional analysis of the interaction of a tissue-specific factor with an upstream enhancer element of the rat prolactin gene. Mol Endocrinol 2:1374-1381 (Pubitemid 19005950)
31. Gutierrez-Hartmann A, Siddiqui S, Loukin S 1987 Selective transcription and DNase I protection of the rat prolactin gene by GH3 pituitary cell-free extracts. Proc Natl Acad Sci USA 84:5211-5215
32. Nelson C, Crenshaw 3rd EB, Franco R, Lira SA, Albert VR, Evans RM, Rosenfeld MG 1986 Discrete cis-active genomic sequences dictate the pituitary cell type-specific expression of rat prolactin and growth hormone genes. Nature 322:557-562
33. Maurer RA 1985 Selective binding of the estradiol receptor to a region at least one kilobase upstream from the rat prolactin gene. DNA 4:1-9 (Pubitemid 15172205)
34. Simmons DM, Voss JW, Ingraham HA, Holloway JM, Broide RS, Rosenfeld MG, Swanson LW 1990 Pituitary cell phenotypes involve cell-specific Pit-1 mRNA translation and synergistic interactions with other classes of transcription factors. Genes Dev 4:695-711 (Pubitemid 20175515)
35. Day RN, Koike S, Sakai M, Muramatsu M, Maurer RA 1990 Both Pit-1 and the estrogen receptor are required for estrogen responsiveness of the rat prolactin gene. Mol Endocrinol 4:1964-1971
36. Howard PW, Maurer RA 1995 A composite Ets/Pit-1 binding site in the prolactin gene can mediate transcriptional responses to multiple signal transduction pathways. J Biol Chem 270:20930-20936
37. Bradford AP, Conrad KE, Tran PH, Ostrowski MC, Gutierrez-Hartmann A 1996 GHF-1/Pit-1 functions as a cell-specific integrator of Ras signaling by targeting the Ras pathway to a composite Ets-1/GHF-1 response element. J Biol Chem 271:24639-24648 (Pubitemid 26333206)
38. Bradford AP, Conrad KE, Wasylyk C, Wasylyk B, Gutierrez-Hartmann A 1995 Functional interaction of c-Ets-1 and GHF-1/Pit-1 mediates Ras activation of pituitary-specific gene expression: mapping of the essential c-Ets-1 domain. Mol Cell Biol 15:2849-2857
39. Diamond SE, Gutierrez-Hartmann A 1996 A 26-amino acid insertion domain defines a functional transcription switch motif in Pit-1β. J Biol Chem 271:28925-28932 (Pubitemid 26382594)
40. Bradford AP, Brodsky KS, Diamond SE, Kuhn LC, Liu Y, Gutierrez-Hartmann A 2000 The Pit-1 homeodomain and β-domain interact with Ets-1 and modulate synergistic activation of the rat prolactin promoter. J Biol Chem 275:3100-3106 (Pubitemid 30083006)
41. Adamson AD, Friedrichsen S, Semprini S, Harper CV, Mullins JJ, White MR, Davis JR 2008 Human prolactin gene promoter regulation by estrogen: convergence with tumor necrosis factor-α signaling. Endocrinology 149:687-694 (Pubitemid 351159349)
42. Murdoch FE, Byrne LM, Ariazi EA, Furlow JD, Meier DA, Gorski J 1995 Estrogen receptor binding to DNA: affinity for nonpalindromic elements from the rat prolactin gene. Biochemistry 34:9144-9150
43. Berwaer M, Monget P, Peers B, Mathy-Hartert M, Bellefroid E, Davis JR, Belayew A, Martial JA 1991 Multihormonal regulation of the human prolactin gene expression from 5000 bp of its upstream sequence. Mol Cell Endocrinol 80:53-64
44. Farrow KN, Gutierrez-Hartmann A 1999 Transforming growth factor-β1 inhibits rat prolactin promoter activity in GH4 neuroendocrine cells. DNA Cell Biol 18:863-873
45. Komolov IS, Perez-Arce JA, Fedotov VP 1980 The effects of estradiol on prolactin and growth hormone secretion in cultured pituitary cells from intact and ovariectomized rats. Endokrinologie 75:278-284 (Pubitemid 10024128)
46. Miyoshi T, Otsuka F, Otani H, Inagaki K, Goto J, Yamashita M, Ogura T, Iwasaki Y, Makino H 2008 Involvement of bone morphogenetic protein-4 in GH regulation by octreotide and bromocriptine in rat pituitary GH3 cells. J Endocrinol 197:159-169 (Pubitemid 351566935)
47. Yanagisawa J, Yanagi Y, Masuhiro Y, Suzawa M, Watanabe M, Kashiwagi K, Toriyabe T, Kawabata M, Miyazono K, Kato S 1999 Convergence of transforming growth factor-β and vitamin D signaling pathways on SMAD transcriptional coactivators. Science 283:1317-1321 (Pubitemid 129507216)
48. Kang HY, Lin HK, Hu YC, Yeh S, Huang KE, Chang C 2001 From transforming growth factor-β signaling to androgen action: identification of Smad3 as an androgen receptor coregulator in prostate cancer cells. Proc Natl Acad Sci USA 98:3018-3023 (Pubitemid 32220792)
49. Hayes SA, Zarnegar M, Sharma M, Yang F, Peehl DM, ten Dijke P, Sun Z 2001 SMAD3 represses androgen receptor-mediated transcription. Cancer Res 61:2112-2118
50. Song CZ, Tian X, Gelehrter TD 1999 Glucocorticoid receptor inhibits transforming growth factor-β signaling by directly targeting the transcriptional activation function of Smad3. Proc Natl Acad Sci USA 96:11776-11781 (Pubitemid 29502808)
51. Giacomini D, Páez-Pereda M, Theodoropoulou M, Labeur M, Refojo D, Gerez J, Chervin A, Berner S, Losa M, Buchfelder M, Renner U, Stalla GK, Arzt E 2006 Bone morphogenetic protein-4 inhibits corticotroph tumor cells: involvement in the retinoic acid inhibitory action. Endocrinology 147:247-256 (Pubitemid 43004278)
52. Matsuda T, Yamamoto T, Muraguchi A, Saatcioglu F 2001 Cross-talk between transforming growth factor-β and estrogen receptor signaling through Smad3. J Biol Chem 276:42908-42914 (Pubitemid 37370969)
53. Yamamoto T, Saatcioglu F, Matsuda T 2002 Cross-talk between bone morphogenic proteins and estrogen receptor signaling. Endocrinology 143:2635-2642 (Pubitemid 34701327)
54. Sarkar DK, Pastorcic M, De A, Engel M, Moses H, Ghasemzadeh MB 1998 Role of transforming growth factor (TGF)-β type I and TGF-β type II receptors in the TGF-β1-regulated gene expression in pituitary prolactin-secreting lactotropes. Endocrinology 139:3620-3628 (Pubitemid 28512322)
55. Kusanagi K, Inoue H, Ishidou Y, Mishima HK, Kawabata M, Miyazono K 2000 Characterization of a bone morphogenetic protein-responsive Smad-binding element. Mol Biol Cell 11:555-565 (Pubitemid 30112165)
56. Massagué J 2000 How cells read TGF-β signals. Nat Rev Mol Cell Biol 1:169-178
57. Massagué J, Blain SW, Lo RS 2000 TGFβ signaling in growth control, cancer, and heritable disorders. Cell 103:295-309
58. Chen CR, Kang Y, Siegel PM, Massagué J 2002 E2F4/5 and p107 as Smad cofactors linking the TGFβ receptor to c-myc repression. Cell 110:19-32 (Pubitemid 34874603)
59. Arzt E, Buric R, Stelzer G, Stalla J, Sauer J, Renner U, Stalla GK 1993 Interleukin involvement in anterior pituitary cell growth regulation: effects of interleukin-2 (IL-2) and IL-6. Endocrinology 132:459-467 (Pubitemid 23019537)
60. Berthois Y, Katzenellenbogen JA, Ktzenellenbogen BS 1986 Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture. Proc Natl Acad Sci USA 83:2496-2500 (Pubitemid 16026909)
61. Farrow KN, Manning N, Schaufele F, Gutierrez-Hartmann A 1996 The c-Jun δ-domain inhibits neuroendocrine promoter activity in a DNA sequence and pituitary-specific manner. J Biol Chem 271:17139-17146 (Pubitemid 26244264)
62. Zschocke J, Manthey D, Bayatti N, van der Burg B, Goodenough S, Behl C 2002 Estrogen receptor α-mediated silencing of caveolin gene expression in neuronal cells. J Biol Chem 277:38772-38780 (Pubitemid 35154740)
63. Korchynskyi O, ten Dijke P 2002 Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277:4883-4891
64. Spinella-Jaegle S, Roman-Roman S, Faucheu C, Dunn F, Kawai S, Galléa S, Stiot V, Blanchet AM, Courtois B, Baron R, Rawadi G 2001 Opposite effects of bone morphogenetic protein-2 and transforming growth factor-β1 on osteoblast differentiation. Bone 29:323-330 (Pubitemid 32930058)
65. Norris JD, Fan D, Kerner SA, McDonnell DP 1997 Identification of a third autonomous activation domain within the human estrogen receptor. Mol Endocrinol 11:747-754 (Pubitemid 27225302)
66. Carbia-Nagashima A, Gerez J, Perez-Castro C, Paez-Pereda M, Silberstein S, Stalla GK, Holsboer F, Arzt E 2007 RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1α during hypoxia. Cell 131:309-323 (Pubitemid 47592916)
67. Maurer RA, Notides AC 1987 Identification of an estrogen-responsive element from the 5′-flanking region of the rat prolactin gene. Mol Cell Biol 7:4247-4254 (Pubitemid 17166403)
68. Stopa M, Anhuf D, Terstegen L, Gatsios P, Gressner AM, Dooley S 2000 Participation of Smad2, Smad3, and Smad4 in transforming growth factor β (TGF-β)-induced activation of Smad7. The TGF-β response element of the promoter requires functional Smad binding element and E-box sequences for transcriptional regulation. J Biol Chem 275:29308-29317 (Pubitemid 32043801)
69. Li W, Chen F, Nagarajan RP, Liu X, Chen Y 2001 Characterization of the DNA-binding property of Smad5. Biochem Biophys Res Commun 286:1163-1169 (Pubitemid 32924892)
70. Páez-Pereda M, Kovalovsky D, Hopfner U, Theodoropoulou M, Pagotto U, Uhl E, Losa M, Stalla J, Grübler Y, Missale C, Arzt E, Stalla G 2001 Retinoic acid prevents experimental Cushing syndrome. J Clin Invest 108:1123-1131 (Pubitemid 32995370)
71. Liberman AC, Refojo D, Druker J, Toscano M, Rein T, Holsboer F, Arzt E 2007 The activated glucocorticoid receptor inhibits the transcription factor T-bet by direct protein-protein interaction. FASEB J 21:1177-1188 (Pubitemid 46495707)