Molecular mechanisms of crosstalk between thyroid hormones and estrogens

Current Opinion in Endocrinology and Diabetes

Volumn 12, Issue 5, 2005, Pages 381-388

  Vasudevan, Nandini ^a   Pfaff, Donald ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Consensus estrogen response; Consensus estrogen response element; Estrogen response element; Isoforms; Kinases; Nongenomic; Phosphorylation; Squelching

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; THYROID HORMONE; THYROID HORMONE RECEPTOR;

CELL TYPE; GENETIC TRANSCRIPTION; HORMONE RESPONSIVE ELEMENT; HUMAN; MOLECULAR RECOGNITION; NERVE GROWTH; NERVE REGENERATION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION;

EID: 26444484232     PISSN: 10683097     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.med.0000178273.09365.22     Document Type: Review

References (89)

1. Zhu YS, Dellovade TL, Plaff DW. Interactions between hormonal and environmental signals on hypothalamic neurons: molecular mechanisms signaling environmental events. Trends Endocrinol Metab 1997; 8:111-115.
2. Shupnik MA. Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene 2004; 23:7979-7989. Although crosstalk between growth factors and steroid hormone receptors has been explored previously by the use of estrogen receptor knockout mice, this review gives a molecular perspective to the interactions between members of the nuclear receptor superfamily, that is, estrogen receptor, progesterone receptor, and the receptor tyrosine kinases (growth factor receptors).
3. Dupont J, Le Roith D. Insulin-like growth factor 1 and oestradiol promote cell proliferation of MCF-7 breast cancer cells: new insights into their synergistic effects. Mol Pathol 2001; 54:149-154.
4. Evans RM. The steroid and thyroid hormone receptor superfamily. Science 1988; 240:889-895.
5. Mangelsdorf DJ, Thummel C, Beato M, et al. Overview: the nuclear receptor superfamily: the second decade. Cell 1995; 83:835-840.
6. Nilsson S, Makela S, Treuter E, et al. Mechanisms of estrogen action. Physiol Rev 2001; 81:1535-1565.
7. Lazar M. Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev 1993; 14:184-193.
8. Wu Y, Koenig RJ. Gene regulation by thyroid hormone. Trends Endocrinol Metab 2000; 11:207-211.
9. Lazar MA. Thyroid hormone action: a binding contract. J Clin Invest 2003; 112:497-499.
10. Zhang J, Lazar MA. The mechanism of action of thyroid hormones. Annu Rev Physiol 2000; 62:439-466.
11. Oberste-Berghaus C, Zanger K, Hashimoto K, et al. Thyroid hormone-independent interaction between the thyroid hormone receptor beta2 amino terminus and coactivators. J Biol Chem 2000; 275:1787-1792.
12. Hollenberg AN, Monden T, Madura JP, et al. Function of nuclear co-repressor protein on thyroid hormone response elements is regulated by the receptor A/B domain. J Biol Chem 1996; 271:28516-28520.
13. Safer JD, Langlois MF, Cohen R, et al. Isoform variable action among thyroid hormone receptor mutants provides insight into pituitary resistance to thyroid hormone. Mol Endocrinol 1997; 11:16-26.
14. Langlois MF, Zanger K, Monden T, et al. A unique role of the beta-2 thyroid hormone receptor isoform in negative regulation by thyroid hormone: mapping of a novel amino-terminal domain important for ligand-independent activation. J Biol Chem 1997; 272:24927-24933.
15. Knobil E, Neill J. The physiology of reproduction. 2nd ed. New York: Raven; 1994.
16. Lubahn DB, Moyer JS, Golding TS, et al. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 1993; 90:11162-11166.
17. Ogawa S, Eng V, Taylor J, et al. Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in female mice. Endocrinology 1998; 139:5070-5081.
18. Knobil E, Neill J. Encyclopedia of reproduction. San Diego: Academic Press; 1999.
19. Robinson JE, Karsch FJ. Refractoriness to inductive day lengths terminates the breeding season of the Suffolk ewe. Biol Reprod 1984; 3:656-663.
20. Karsch FJ, Robinson JE, Woodfill CJI, Brown MB. Circannual cycles of luteinizing hormone and prolactin secretion in ewes during prolonged exposure to a fixed photoperiod: evidence for an endogenous reproductive rhythm. Biol Reprod 1989; 41:1034-1046.
21. Robinson JE, Karsch FJ. Timing of the breeding season of the ewe: what is the role of daylength? Reprod Nutr Dev 1988; 28:365-374.
22. Moenter SM, Woodfill CJI, Karsch FJ. Role of the thyroid gland in seasonal reproduction: thyroidectomy blocks seasonal suppression of reproductive neuroendocrine activity in ewes. Endocrinology 1991; 128:1337-1344.
23. Viguie C, Battaglia DF, Krasa HB, et al. Thyroid hormones act primarily within the brain to promote the seasonal inhibition of luteinizing hormone secretion in the ewe. Endocrinology 1999; 140:1111-1117.
24. Freeman ME, LaRochelle FT, Moore RB. Effect of thyroid status on spontaneous and induced surges of luteinizing hormone. Endocrinology 1976; 99: 713-719.
25. Jansen HT, Lubbers LS, Macchia E, et al. Thyroid hormone receptor (alpha) distribution in hamster and sheep brain: colocalisation in gonadotropin- releasing hormone and other identified neurons. Endocrinology 1997; 138: 5039-5047.
26. Webster JR, Moenter SM, Woodfill CJI, Karsch JF. Role of the thyroid gland in seasonal reproduction: II. Thyroxine allows a season-specific suppression of gonadotropin secretion in sheep. Endocrinology 1991; 129:176-183.
27. Webster JR, Moenter SJ, Barrell GK, et al. Role of the thyroid gland in seasonal reproduction: III. Thyroidectomy blocks seasonal suppression of gonadotropin- releasing hormone secretion in sheep. Endocrinology 1991; 129:1635-1643.
28. Dellovade TL, Zhu YS, Krey L, Pfaff DW. Thyroid hormone and estrogen interact to regulate behavior. Proc Natl Acad Sci USA 1996; 93:12581-12586.
29. Morgan MA, Dellovade TL, Pfaff DW. Effect of thyroid hormone administration on estrogen-induced sex behavior in female mice. Horm Behav 2000; 37:15-22.
30. Dellovade TL, Chan J, Vennstrom B, et al. The two thyroid hormone receptor genes have opposite effects on estrogen stimulated sex behaviors. Nat Neurosci 2000; 3:472-475.
31. Kirkland J, Gardner R, Mukku V, et al. Hormonal control of uterine growth: the effect of hypothyroidism on estrogen-stimulated cell division. Endocrinology 1981; 108:2346-2351.
32. Franklyn J, Betteridge J, Holder R, et al. Bone mineral density in thyroxine treated females with or without a previous history of thyrotoxicosis. Clin Endocrinol (Oxf) 1994; 41:425-432.
33. Pfaff DW, Kow LM, Zhu YS, et al. Hypothalamic cellular and molecular mechanisms helping to satisfy axiomatic requirements for reproduction. J Neuroendocrinol 1996; 8:325-336.
34. Quinones-Jenab V, Jenab S, Ogawa S, et al. Effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the uterus, pituitary, and forebrain of the female rat. Neuroendocrinology 1997; 65:9-17.
35. Nishimori K, Young LJ, Guo Q, et al. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci USA 1996; 93:11699-11704.
36. Fahrbach SE, Morrell JI, Pfaff DW. Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 1985; 40: 526-532.
37. Fahrbach S, Morrell J, Pfaff D. Effect of varying the duration of pre-test cage habituation on oxytocin induction of short-latency maternal behavior. Physiol Behav 1986; 37:135-139.
38. Arletti R, Bertolini A. Oxytocin stimulates lordosis behavior in female rats. Neuropeptides 1985; 6:247-253.
39. Arletti R, Benelli A, Bertolini A. Oxytocin involvement in male and female sexual behavior. Ann N Y Acad Sci 1992; 652:180-193.
40. Bale TL, Davis AM, Auger AP, et al. CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J Neurosci 2001; 21:2546-2552.
41. Romano GJ, Mobbs CB, Raff DW. Estrogen regulation of proenkephalin gene expression in the ventromedial hypothalamus of the rat: temporal qualities and synergism with progesterone. Brain Res Mol Brain Res 1989; 5: 51-58.
42. Romano GJ, Mobbs CV, Lauber A, et al. Differential regulation of proenkephalin gene expression by estrogen in the ventromedial hypothalamus of male and female rats: implications for the molecular basis of a sexually differentiated behavior. Brain Res Mol Brain Res 1990; 536:63-68.
43. Lauber AH, Romano GJ, Mobbs CV, et al. Estradiol induction of proenkephalin messenger RNA in hypothalamus: dose-response and relation to reproductive behavior in the female rat. Brain Res Mol Brain Res 1990; 8:47-54.
44. Romano GJ, Harlan RE, Shivers BD, et al. Estrogen increases proenkephalin messenger ribonucleic acid levels in the ventromedial hypothalamus of the rat. Mol Endocrinol 1988; 2:1320-1328.
45. McCarthy MM, Kleopoulos SP, Mobbs CV, Pfaff DW. Infusion of antisense oligodeoxynucleotides to the oxytocin receptor in the ventromedial hypothalamus reduces estrogen induced sexual receptivity and oxytocin receptor binding in the female rat. Neuroendocrinology 1994; 59:432-440.
46. Nicot A, Ogawa S, Berman Y, et al. Effects of an intrahypothalamic injection of antisense oligonucleotides for preproenkephalin mRNA in female rats: evidence for opioid involvement in lordosis reflex. Brain Res 1997; 777:60-68.
47. Dellovade TL, Zhu YS, Pfaff DW. Thyroid hormones and estrogen effect oxytocin gene expression in hypothalamic neurons. J Neuroendocrinol 1999; 11: 1-10.
48. Dellovade TL, Kia HK, Zhu Y-S, Pfaff DW. Thyroid hormone coadministration inhibits the estrogen-stimulated elevation of preproenkephalin mRNA in female rat hypothalamic neurons. Neuroendocrinology 1999; 70:168-174.
49. Ridgway EC, Longcope C, Maloof F. Metabolic clearance and blood production rates of estradiol in hyperthyroidism. J Clin Endocrinol Metab 1975; 41: 491-497.
50. Bourget C, Femino A, Franz C, et al. The effects of I-thyroxine and dexamethasone on steroid dynamics in male cynomologous monkeys. J Steroid Biochem 1987; 28:575-579.
51. Peczely P. The role of thyroid and adrenal cortical hormones in the modulation of the gonadal function in birds. Acta Biol Hung 1985; 36:45-70.
52. Mazer NA. Interaction of estrogen therapy and thyroid hormone replacement in postmenopausal women. Thyroid 2004; 14(Suppl 1):S27-S34.
53. Alarid ET, Bakopoulos N, Solodin N. Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol Endocrinol 1999; 13:1522-1534.
54. Preisler-Mashek MT, Solodin N, Stark BL, et al. Ligand-specific regulation of proteasome-mediated proteolysis of estrogen receptor-alpha. Am J Physiol Endocrinol Metab 2002; 282:E891-E898.
55. Valley CC, Metivier R, Solodin NM, et al. Differential regulation of estrogen-inducible proteolysis and transcription by the estrogen receptor {alpha} N terminus. Mol Cell Biol 2005; 25:5417-5428. This paper builds on previous work done by this group on ERα degradation. They have advanced the idea that the proteolysis of this receptor is important in autoregulation and is needed for optimal transcription, possibly by way of the serine residue at position 118 in the AF-1 N terminal domain. This was the first paper to pinpoint a role for the AF-1 domain in proteolytic degradation of the receptor.
56. Alarid ET, Preisler-Mashek MT, Solodin NM. Thyroid hormone is an inhibitor of estrogen-induced degradation of estrogen receptor-alpha protein: estrogen-dependent proteolysis is not essential for receptor transactivation function in the pituitary. Endocrinology 2003; 144:3469-3476.
57. Glass CK, Holloway J, Devary OV, Rosenfeld MG. The thyroid hormone receptor binds with opposite transcriptional effects to a common sequence motif in thyroid hormone and estrogen response elements. Cell 1988; 54: 313-323.
58. Adan RA, Cox JJ, Van Kats JP, Burbach JP. Thyroid hormone regulates the oxytocin gene. J Biol Chem 1992; 267:3771-3777.
59. Yen PM, Wilcox EC, Chin WW. Steroid hormone receptors selectively affect transcriptional activation but not basal repression by thyroid hormone receptors. Endocrinology 1995; 136:440-445.
60. Yarwood NJ, Gurr JA, Sheppard MC, Franklyn JA. Estradiol modulates thyroid hormone regulation of the human glycoprotein hormone alpha subunit gene. J Biol Chem 1993; 268:21984-21989.
61. Vasudevan N, Zhu YS, Daniel S, et al. Crosstalk between estrogen receptors and thyroid hormone receptor isoforms results in differential regulation of the preproenkephalin gene. J Neuroendocrinol 2001; 13:779-790.
62. Vasudevan N, Davidkova G, Zhu YS, et al. Differential interaction of estrogen receptor and thyroid hormone receptor isoforms on the rat oxytocin receptor promoter leads to differences in transcriptional regulation. Neuroendocrinology 2001; 74:309-324.
63. Vasudevan N, Koibuchi N, Chin WW, Pfaff DW. Differential crosstalk between estrogen receptor (ER) alpha and ER beta and the thyroid hormone receptor isoforms results in flexible regulation of the consensus ERE. Brain Res Mol Brain Res 2001; 95:9-17.
64. Joshi J, Sabol SL. Proenkephalin gene expression in C6 rat glioma cells: potentiation of cyclic adenosine 3′,5′-monophosphate-dependent transcription by glucocorticoids. Mol Endocrinol 1991; 5:1069-1080.
65. Bale TL, Dorsa DM. Cloning, novel promoter sequence, and estrogen regulation of a rat oxytocin receptor gene. Endocrinology 1997; 138:1151-1158.
66. Zhu YS, Yen PM, Chin WW, Pfaff DW. Estrogen and thyroid hormone interaction on regulation of gene expression. Proc Natl Acad Sci USA 1996; 93: 12587-12592.
67. Yen PM, Ikeda M, Wilcox EC, et al. Half-site arrangement of hybrid glucocorticoid and thyroid hormone response elements specifies thyroid hormone receptor complex binding to DNA and transcriptional activity. J Biol Chem 1994; 269:12704-12709.
68. Lopez GN, Webb P, Shinsako JH, et al. Titration by estrogen receptor activation function-2 of targets that are downstream from coactivators. Mol Endocrinol 1999; 13:897-909.
69. Rabelo EM, Tata JR. Thyroid hormone potentiates estrogen activation of vitellogenin genes and autoinduction of estrogen receptor in adult Xenopus hepatocytes. Mol Cell Endocrinol 1993; 96:37-44.
70. Fitts JM, Klein RM, Powers AC. Estrogen and tamoxifen interplay with T3 in male rats: pharmacologically distinct classes of estrogen responses affecting growth, bone, and lipid metabolism, and their relation to serum GH and IGF-1. Endocrinology 2001; 142:4223-4235.
71. Davis PJ, Tillmann HC, Davis FB, Wehling M. Comparison of the mechanisms of nongenomic actions of thyroid hormone and steroid hormones. J Endocrinol Invest 2002; 25:377-388.
72. Cao X, Kambe F, Moeller LC, et al. Thyroid hormone induces rapid activation of Akt/protein kinase B-mammalian target of rapamycin-p70S6K cascade through phosphatidylinositol 3-kinase in human fibroblasts. Mol Endocrinol 2005; 19:102-112. Most of the work on thyroid hormone has focused on its genomic actions. Here, the authors show a rapid activation of PI3K and subsequent phosphorylation of mammalian target of rapamycin by way of liganded Tβ1. Because rapid actions of thyroid hormone have also been thought to be mediated by way of novel membrane receptors for thyroid hormone, this study demonstrates the involvement of TRβ itself.
73. Cato AC, Nestl A, Mink S. Rapid actions of steroid receptors in cellular signaling pathways. Sci STKE 2002; 2002:RE9.
74. Farach-Carson MC, Davis PJ. Steroid hormone interactions with target cells: cross talk between membrane and nuclear pathways. J Pharmacol Exp Ther 2003; 307:839-845.
75. Bjornstrom L, Sjoberg M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 2005; 19:833-842. This timely review attempts to couple the nongenomic actions of estrogens to transcription from genes that do not contain estrogen response elements. This has long been held as a mechanism by which estrogens activate genes with Sp1 or AP1 sites.
76. Vasudevan N, Kow LM, Pfaff DW. Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line. Proc Natl Acad Sci USA 2001; 98:12267-12271.
77. Tang HY, Lin HY, Zhang S, et al. Thyroid hormone causes mitogen-activated protein kinase-dependent phosphorylation of the nuclear estrogen receptor. Endocrinology 2004; 145:3265-3272. In the past few years, nongenomic actions of estrogens have been extensively studied, but far less is known about the nongenomic actions of other hormones and their physiologic relevance. This is one of the few complete studies to show that thyroxine, the genomically less active form of thyroid hormone, can rapidly activate MAPK, which in turn can phosphorylate the ERα.
78. Zhao X, Lorenc H, Stephenson H, et al. Thyroid hormone can increase estrogen-mediated transcription from a consensus estrogen response element in neuroblastoma cells. Proc Natl Acad Sci USA 2005; 102:4890-4895. This was the first paper to show that nongenomic actions of triiodothyronine, by way of mitogen-activated protein-erk kinase, can activate transcription from a consensus ERE. The authors used a novel two-pulse paradigm designed previously to show that phosphorylation of the ERα is a key step in coupling nongenomic kinase cascades to transcription.
79. Bergh JJ, Lin HY, Lansing L, et al. Integrin {alpha}V{beta}3 Contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 2005; 146:2864-2871. This was the first report of a membrane thyroid hormone receptor. Previous studies by this group implicated a G protein coupled receptor; however, this study shows that the integrinαvβ3 receptor can bind thyroxine with high affinity.
80. Davis PJ, Shih A, Lin HY, et al. Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J Biol Chem 2000; 275:38032-38039.
81. Lin HY, Davis FB, Gordinier JK, et al. Thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells. Am J Physiol 1999; 276: C1014-C1024.
82. Zhu XG, Hanover JA, Hager GL, Cheng SY. Hormone-induced translocation of thyroid hormone receptors in living cells visualized using a receptor green fluorescent protein chimera. J Biol Chem 1998; 273:27058-27063.
83. Chen D, Pace PE, Coombes RC, Ali S. Phosphorylation of human estrogen receptor alpha by protein kinase A regulates dimerization. Mol Cell Biol 1999; 19:1002-1015.
84. Lavinsky RM, Jepsen K, Heinzet T, et al. Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc Natl Acad Sci USA 1998; 95:2920-2925.
85. Tremblay A, Tremblay GB, Labrie F, Giguere V. Ligand-independent recruitment of SRC-1 to estrogen receptor beta through phosphorylation of activation function AF-1. Mol Cell 1999; 3:513-519.
86. Cui Y, Zhang M, Pestell R, et al. Phosphorylation of estrogen receptor alpha blocks its acetylation and regulates estrogen sensitivity. Cancer Res 2004; 64:9199-9208. The functional relevance of ERα phosphorylation is incompletely understood. This paper offers insight into the relevance of PKA phosphorylation of S305 in breast cancers. Such phosphorylation serves to enhance transcription by blocking acetylation at the nearby K303 site.
87. Fuqua SA, Cui Y, Lee AV, et al. Insights into the role of progesterone receptors in breast cancer. J Clin Oncol 2005; 23:931-932; author reply 932-933.
88. Fuqua SA, Cui Y. Estrogen and progesterone receptor isoforms: clinical significance in breast cancer. Breast Cancer Res Treat 2004; 87(Suppl 1):S3-10.
89. Pfaff D, Kia H, Zhu Y-S. Cold stress and its implications for thyroid and reproductive physiology: molecular and behavioral data. In: Yamashita H, Funder J, Verbalis J, et al. Control mechanisms of stress and emotion: neuroendocrine-based studies. Amsterdam: Elsevier; 1999:29-32.