Thyroid hormone inhibits the human prolactin gene promoter by interfering with activating protein-1 and estrogen stimulations

Pernasetti, Flavia; Caccavelli, L.; Van de Weerdt, Cécile; Martial, Joseph; Muller, Marc

doi:10.1210/mend.11.7.9945

Article (Scientific journals)

Thyroid hormone inhibits the human prolactin gene promoter by interfering with activating protein-1 and estrogen stimulations

Pernasetti, Flavia; Caccavelli, L.; Van de Weerdt, Cécile et al.

1997 • In Molecular Endocrinology, 11 (7), p. 986-96

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/31657

DOI
10.1210/mend.11.7.9945

PubMed
9178758

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Keywords :

Animals; Base Sequence; Cell Line; DNA-Binding Proteins/metabolism; Estradiol/*pharmacology; Forskolin/pharmacology; Gene Expression/drug effects; Hela Cells; Humans; Pituitary Gland/cytology/drug effects/*metabolism; Prolactin/drug effects/*genetics; Promoter Regions, Genetic/*drug effects/genetics; Rats; Sensitivity and Specificity; Transcription Factor AP-1/drug effects/*genetics/metabolism; Transcription Factor Pit-1; Transcription Factors/metabolism; Triiodothyronine/*pharmacology

Abstract :

[en] Transcription of the human PRL (hPRL) gene in the pituitary is subject to tissue-specific and multihormonal regulation involving two main regulatory regions, a proximal promoter and a distal enhancer. In this report we show that thyroid hormone inhibits the expression of the hPRL gene in rat pituitary cells. Transient expression experiments show that thyroid hormone regulation involves a strong inhibitory element, located in the proximal (-164/-35) promoter, which is modulated by a more distal stimulatory response control region. Gel retardation experiments reveal that the thyroid hormone receptor does not bind to the proximal negative element. We show the existence of an activating protein-1 (AP-1) response element located at positions -61 to -54 of the proximal promoter, conferring AP-1 stimulation to the hPRL promoter. This AP-1 induction is abolished when hormone-bound thyroid hormone receptor is present, indicating that there is an interference between the thyroid hormone receptor and AP-1 regulatory pathways. Furthermore, using the complete hPRL upstream region, we show that estrogen induction is abolished by simultaneous thyroid hormone treatment.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Pernasetti, Flavia; Université de Liège - ULiège

Caccavelli, L.; Université de Liège - ULiège

Van de Weerdt, Cécile ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Martial, Joseph ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Muller, Marc ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Language :

English

Title :

Thyroid hormone inhibits the human prolactin gene promoter by interfering with activating protein-1 and estrogen stimulations

Publication date :

1997

Journal title :

Molecular Endocrinology

ISSN :

0888-8809

eISSN :

1944-9917

Publisher :

Endocrine Society, Chevy Chase, United States - Maryland

Volume :

Issue :

Pages :

986-96

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6T3G-3RM6VK0-6&_user=532038&_rdoc=1&_fmt=&_orig=search&_sort=d&view=c&_acct=C000026659&_version=1&_urlVersion=0&_userid=532038&md5=821bf23156aa046426e8ee41a0fbd8e7#fn1

Commentary :

http://endo.endojournals.org/

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since 04 December 2009

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Bibliography

De Groot LJ, Larsen PR, Refetoff S, Stambury JB 1984 The Thyroid and its Diseases, ed 5. Wiley and Sons, New York
Evans RM 1988 The steroid and thyroid hormone receptor super-family. Science 240:889-895
Beato M 1989 Gene regulation by steroid hormones. Cell 56:335-344
Brent GA, Harney JW, Chen JW, Warne R, Moore RL, Larsen PR 1989 Mutations of the rat growth hormone promoter which increase and decrease response to thyroid hormone define a consensus thyroid hormone response element. Mol Endocrinol 3:1996-2004
Naar AM, Boutin JM, Lipkin SM, YUVC, Holloway JM, Glass CK, Rosenfeld MG 1991 The orientation and spacing of core DNA-binding motifs dictate selective transcriptional responses to three nuclear receptors. Cell 65:1267-1279
Glass CK, Holloway JM, Devary OV, Rosenfeld MG 1988 The thyroid hormone receptor binds with opposite transcriptional effects to a common sequence motif in thyroid hormone and estrogen response elements. Cell 54:313-323
Baniahmad AC, Steiner C, Kohne AC, Renkavitz R 1990 Modular structure of a chicken lysosyme silencer: involvement of an unusual thyroid hormone receptor binding site. Cell 61:505-514
Umesono K, Murakami KK, Thompson CC, Evans RM 1991 Direct repeats as selective response elements for thyroid hormone, retinoic acid, and vitamin D 3 receptors. Cell 65:1255-1266
Carr FE, Wong NCW 1994 Characteristics of a negative thyroid hormone response element. J Biol Chem 269:4175-4179
Cato ACB, Heitlinger E, Ponta H, Klein-Hitpass L, Ryffel GU, Bailly A, Rauch C, Milgrom E 1988 Estrogen and progesterone receptor-binding sites on the chicken vitellogenin II gene: synergism of steroid hormone action. Mol Cell Biol 8:5323-5330
Cato ACB, Ponta H 1989 Different regions of the estrogen receptor are required for synergistic action with the glucocorticoid and progesterone receptors. Mol Cell Biol 9:5324-5330
Meyer M-E, Gronemeyer H, Turcotte B, Bocquel M-T, Tasset D, Chambon P 1989 Steroid receptors compete for factors that mediate their enhancer function. Cell 57:433-442
Schule R, Muller M, Kaltschmidt C, Renkawitz R 1988 Many transcription factors interact synergistically with steroid receptors. Science 242:1416-1420
Voz ML, Peers B, Wiedig MJ, Jacquemin P, Belayew A, Martial JA 1992 Transcriptional regulation by triiodothyronine requires synergistic action of the thyroid receptor with another trans-acting factor. Mol Cell Biol 12:3991-3997
Zhang X-K, Wills KN, Husmann M, Hermann T, Pfahl M 1991 Novel pathway for thyroid hormone receptor action through interaction with jun and fos oncogene activities. Mol Cell Biol 11:6016-6025
Schuele R, Rangarajan P, Kliewer S, Ransone LJ, Bolado J, Yang N, Verma IM, Evans RM 1990 Functional antagonism between oncoprotein c-jun and the glucocorticoid receptor. Cell 62:1217-1226
Schuele R, Rangarajan P, Yang N, Kliewer S, Ransone LJ, Bolado J, Verma IM, Evans RM 1991 Retinoic acid is a negative regulator of AP-1-responsive genes. Biochemistry 88:6092-6096
Desbois C, Aubert D, Legrand C, Pain B, Samarut J 1991 A Novel mechanism of action for v-erbA: abrogation of the inactivation of the transcription factor AP-1 by retinoic acid and thyroid hormone receptors. Cell 67:731-740
Schmidt EDL, Cramer SJ, Offringa R 1993 The thyroid hormone receptor interferes with transcriptional activation via the AP-1 complex. Biochem Biophys Res Commun 192:151-160
Wondisford FE, Steinfelder HJ, Nations M, Radovick S 1993 AP-1 antagonizes thyroid hormone receptor action on the thyrotropin a subunit gene. J Biol Chem 268:2749-2754
Savouret J-F, Rauch M, Redeuilh G, Sar S, Chauchereau A, Woodruff K, Parker MG, Milgrom E 1994 Interplay between estrogens, progestins, retinoid acid and AP-1 on a single regulatory site in the progesterone receptor gene. J Biol Chem 269:28955-28962
Herrlich P, Ponta H 1994 Mutual cross-modulation of steroid/retinoid acid receptor and AP-1 transcription factor activities. A novel property with practical implications. Trends Endocrinol Metab 5:341-346
Vogt PK, Bos TJ 1990 jun: oncogene and transcription factor. Adv Cancer Res 55:1-35
Karin M 1990 The AP-1 complex and its role in transcriptional control by protein kinase C. In: Cohen P, Foulkes G (eds) Molecular Aspects of Cellular Regulation. Elsevier, Amsterdam, vol 6:143-161
Ingraham HA, Chen R, Mangalam HJ, Elsholtz HP, Flynn SE, Lin CR, Simmons DM, Swanson L, Rosenfeld MG 1988 A tissue-specific transcription factor containing a homeodomain specifies a pituitary phenotype. Cell 55:519-529
Mangalam HJ, Albert VR, Ingraham HA, Kapiloff M, Wilson L, Nelson C, Elsholtz H, Rosenfeld MG 1989 A pituitary POU domain protein, Pit-1, activates both growth hormone and prolactin promoters transcriptionally. Genes Dev 3:946-958
Bodner M, Castrillo J-L, Theill LE, Deerinck T, Ellisman M, Karin M 1988 The pituitary-specific transcription factor GHF-1 is a homeobox-containing protein. Cell 55:505-518
Nelson C, Albert VR, Elsholtz HP, Lu LI-W, Rosenfeld MG 1988 Activation of cell-specific expression of rat growth hormone and prolactin genes by common transcription factor. Science 239:1400-1405
Berwaer M, Monget P, Peers B, Mathy-Hartert M, Bellefroid E, Davis JRE, 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
Peers B, Voz ML, Monget P, Mathy-Hartert M, Berwaer M, Belayew A, Martial JA 1990 Regulatory elements controlling pituitary-specific expression of the human prolactin gene. Mol Cell Biol 10:4690-4700
Berwaer M, Peers B, Nalda AM, Monget P, Davis JRE, Belayew A, Martial JA 1993 Thyrotropin-releasing hormone and epidermial growth factor induce human prolactin expression via identical multiple cis elements. Mol Cell Endocrinol 10:4690-4700
Peers B, Monget P, Nalda MA, Voz ML, Berwaer M, Belayew A, Martial JA 1991 Transcriptional induction of the human prolactin gene by cAMP requires two cis-acting elements and at least the pituitary-specific factor Pit-1. J Biol Chem 266:18127-18134
Peers B, Nalda MA, Monget P, Voz ML, Belayew A, Martial JA 1992 Binding of a 100 kDa ubiquitous factor to the human prolactin promoter is required for its basal and hormone-regulated activity. Eur J Biochem 210:53-58
Gellersen B, Kempf R, Telgmann R, DiMatttia G 1995 Pituitary-type transcription of the human prolactin gene in the absence of Pit-1. Mol Endocrinol 9:887-901
Maurer RA 1982 Thyroid hormone specifically inhibts prolactin synthesis and decreases prolactin messenger ribonucleic acid levels in cultured pituitary cells. Endocrinology 110:1507-1514,
Stanley F, Samuels HH 1982 n-Butyrate affects thyroid stimulation of prolactin production and m RNA levels in GH1 cells. J Biol Chem 259:9768-9775
Forman BM, Yang C-r, Stanley F, Casanova J, Samuels HH 1988 c-erbA protooncogenes mediate thyroid hormone-dependent and -independent regulation of the rat growth hormone and prolactin genes. Mol Endocrinol 2:902-911
Stanley F 1989 Transcriptional regulation of prolactin gene expression by thyroid hormone-alternate supression and stimulation in different GH cell lines. Mol Endocrinol 3:1627-1633
Day RN, Maurer RA 1989 Thyroid hormone-responsive elements of the prolactin gene: evidence for both positive and negative regulation. Mol Endocrinol 3:931-938
Watanabe H, Sasaki S 1995 Effect of thyroid status on the prolactin-releasing action of vasoactive intestinal peptide in humans: comparison with the action of thyrotropin-releasing hormone. Neuroendocrinology 61:207-212
Chomczynski P, Soszynski PA, Frohman LA 1993 Stimulatory effect of thyroid hormone on growth hormone gene expression in a human pituitary cell line. J Clin Endocrinol Metab 77:281-285
Sanchez-Pacheco A, Palomino T, Aranda A 1995 Negative regulation of expression of the pituitary specific transcription factor GHF-1/Pit-1 by thyroid hormone through interference with promoter enhancer elements. Mol Cell Biol 15:6322-6330
Franklyn JA, Gammage MD, Sheppard MC 1987 Amiodarone and thyroid hormone effects on anterior pituitary hormone gene expression. Clin Endocrinol (Oxf) 27:373-382
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
Cullen KE, Kladde MP, Seyfred MA 1993 Interaction between transcription regulatory regions of prolactin chromatin. Science 261:203-206
Gothard LQ, Hibbard JC, Seyfred MA 1996 estrogen-mediated induction of the rat prolactin gene transcription requires the formation of a chromatin loop between the distal enhancer and the proximal promoter regions. Mol Endocrinol 10:185-195
Luckow B, Schutz G 1987 CAT constructions with multiple unique restriction sites for the functional analysis of eukariotic promoters and regulatory elements. Nucleic Acids Res 15:5490
Nordeen SK 1988 Luciferase reporter gene vectors for analysis of promoters and enhancers. BioTechniques 6:454-456
MacGregor GR, Mogg AE, Burke JF, Caskey CT 1987 Histochemical staining of clonal mammalian cell lines expressing E. coli □β-galactosidase indicates heterogeneous expression of bacterial gene. Somat Cell Mol Genet 13:253-265
Pernasetti F, Wera S, Belayew A, Martial JA 1996 Cloning of a human GHF-1/Pit-1 cDNA variant. Nucleic Acids Res 21:3584
Angel P, Imagawa M, Chiu R, Stein B, Imbra RJ, Rahmsdorf HJ, Jonat C, Herrlich P, Karin M 1987 Phorbol ester-inducible genes contain a common cis element recognised by TPA modulated trans-acting factor. Cell 49:729-739
Samuels HH, Stanley F, Casanova J 1979 Depletion of L-3,5,3′-triiodothyronine and L-thyroxine in euthyroid calf serum for use in cell culture studies of the action of thyroid hormone. Endocrinology 105:80-85
Baniahmad A, Muller M, Steiner Ch, Renkawitz R 1987 Activity of two different silencer elements of the chicken lysozyme gene can be compensated by enhancer elements. EMBO J 6:2297-2303
Sekkali B, Belayew A, Martial JA 1994 A comparative study of reporter gene activities in fish cells and embryos. Mol Marine Biol Biotechnol 3:30-34
Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW 1990 Use of T 7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185:60-89
Martin B, Renkawitz R, Muller M 1994 Two silencing sub-domains of v-erbA synergize with each other, but not with RXR. Nucleic Acids Res 22:4898-4905
Truong AT, Duez C, Belayew A, Renard A, Pictet R, Bell GI, Martial JA 1984 Isolation and characterisation of the human prolactin gene. EMBO J 3:429-437