Advertisement
Research Article| Volume 13, ISSUE 3, P543-561, September 1993

Download started.

Ok

Molecular Mechanisms of Thyroid Hormone Action: A Physiologic Perspective

DOI:https://doi.org/10.1016/S0272-2712(18)30425-6
Molecular Mechanisms of Thyroid Hormone Action: A Physiologic Perspective
Previous ArticleMolecular Mechanisms of Thyroid Hormone Action
Next ArticleResistance to Thyroid Hormone
      This paper is only available as a PDF. To read, Please Download here.
      This article reviews the major action that thyroid hormone exerts at the nuclear level by regulating the level of mRNAs of specific genes. There are at least three thyroid hormone receptor isoforms that mediate hormonal effects at the tissue level. Recent studies have shown an unexpected degree of complexity in the nature of the association of the triiodothyronine (T3) receptors and the DNA of target genes. They have shown the multiple interactions possible between the T3-receptor complex and other proteins participating in the process of gene regulation.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.

      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Clinics in Laboratory Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Register: Create an account
      Institutional Access: Sign in to ScienceDirect

      References

        • Benbrook D.
        • Pfahl M.
        A novel thyroid hormone receptor encoded by a cDNA clone from a human testis library.
        Science. 1987; 238: 788
        • Bottger I.
        • Kriegei H.
        • Wieland O.
        Fluctuation of hepatic enzymes important in glucose metabolism in relation to thyroid function.
        Eur J Biochem. 1970; 13: 253
        • Braverman L.E.
        • Ingbar S.H.
        • Sterling K.
        Conversion of thyroxine to triiodothyronine in athyreotic human subjects.
        J Clin Invest. 1970; 49: 855
        • Brent G.
        • Dunn M.
        • Harney J.
        • et al.
        Thyroid hormone aporeceptor represses T3-inducible promoters and blocks activation of the retinoic acid receptor.
        New Biologist. 1989; 1: 329
        • Brent G.A.
        • Harney J.W.
        • Chen Y.
        • et al.
        Mutations of the rat growth hormone promoter which increase and decrease response to thyroid hormone define a consensus thyroid hormone response element.
        Mol Endocrinol. 1989; 3: 1996
        • Brent G.A.
        • Larsen P.R.
        • Harney J.W.
        • et al.
        Functional characterization of the rat growth hormone promoter elements required for induction by thyroid hormone with and without a co-transfected β type thyroid hormone receptor.
        J Biol Chem. 1989; 264: 178
        • Burmeister L.A.
        • Mariash C.N.
        Dietary sucrose enhances processing of mRNA-S14 nuclear precursor.
        J Biol Chem. 1991; 266: 22905
        • Burnside J.
        • Darling D.S.
        • Chin W.W.
        A nuclear factor that enhances binding of thyroid hormone receptors to thyroid hormone response elements.
        J Biol Chem. 1990; 265: 2500
        • Carlson D.J.
        • Strait K.A.
        • Schwartz H.L.
        • et al.
        Thyroid hormone receptor content in cultured astrocytes: /31 and al receptor in type II astrocytes and absence of al, al, and /31 receptors in type I astrocytes.
        Thyroid. 1992; 2: S-83
        • Carr F.E.
        • Bingham C.
        • Oppenheimer J.H.
        • et al.
        Quantitative investigation of hepatic genomic response to hormonal and pathophysiological stimuli by multivariate analysis of two-dimensional mRNA activity profiles.
        Proc Natl Acad Sci USA. 1984; 81: 974
        • Chatterjee V.K.K.
        • Lee J.K.
        • Rentoumis A.
        • et al.
        Negative regulation of the thyroid-stimulating hormone alpha gene by thyroid hormone: Receptor interaction adjacent to the TATA box.
        Proc Natl Acad Sei, USA. 1989; 86: 9114
        • Cook C.B.
        • Kakacska I.
        • Lechan R.M.
        • et al.
        Expression of thyroid hormone receptor /32 in rat hypothalamus.
        Endocrinol. 1992; 130: 1077
        • Danielson M.
        • Hinck L.
        • Ringold G.M.
        Two amino acids within the knuckle of the first zinc finger specify DNA response element activation by the glucocorticoid receptor.
        Cell. 1989; 57: 1131
        • Darling D.S.
        • Burnside J.
        • Chin W.W.
        Binding of thyroid hormone receptors to the rat thyrotropin-beta gene.
        Mol Endocrinol. 1989; 3: 1359
        • Dayton A.I.
        • Seiden J.R.
        • Laws G.
        • et al.
        A human c-erb-A oncogene homologue is closely proximal to the chromosome 17 breakpoint in acute promyelocytic leukemia.
        Proc Natl Acad Sci USA. 1984; 81: 4495
        • De Long G.R.
        • Stanbury J.B.
        • Fierro-Benitez R.
        Neurological signs in congenital iodine-deficiency disorder (endemic cretinism).
        Devel Med Child Neuro. 1985; 27: 317
        • Dozin B.
        • Magnuson M.A.
        • Nikodem V.M.
        Thyroid hormone regulation of malic enzyme synthesis.
        J Biol Chem. 1986; 261: 10290
        • Dozin B.
        • Rail J.E.
        • Nikodem V.M.
        Tissue-specific control of rat malic enzyme activity and messenger RNA levels by a high carbohydrate diet.
        Proc Natl Acad Sci USA. 1986; 83: 4705
        • Evans R.M.
        The steroid and thyroid hormone receptor superfamily.
        Science. 1988; 240: 889
        • Evans R.M.
        • Hollenberg S.M.
        Zinc fingers: Gilt by association.
        Cell. 1988; 52: 1
        • Farsetti A.
        • Desvergne B.
        • Hallenbeck P.
        • et al.
        Characterization of myelin basic protein thyroid hormone response element and its function in the context of native and heterologous promoter.
        J Biol Chem. 1992; 267: 15784
        • Forman B.A.
        • Samuels H.H.
        Mini-review: Interaction among a subfamily of nuclear hormone receptors.
        Mol Endocrinol. 1990; 4: 1293
        • Freake H.C.
        • Oppenheimer J.H.
        Stimulation of mRNA-S14 and lipogenesis in brown fat by hypothyroidism, cold exposure and cafeteria feeding: Evidence supporting a general role for S14 in lipogenesis and lipogenesis in the maintenance of thermogenesis.
        Proc Natl Acad Sci USA. 1987; 84: 3070
        • Freake H.C.
        • Schwartz H.L.
        • Oppenheimer J.H.
        The regulation of lipogenesis by thyroid hormone and its contribution to thermogenesis.
        Endocrinol. 1989; 125: 2868
        • Glass C.
        • Lipkin S.
        • Devary O.
        • et al.
        Positive and negative regulation of gene transcription by a retinoic-thyroid hormone receptor heterodimer.
        Cell. 1989; 59: 697
        • Glass C.K.
        • Franco R.
        • Weinberger C.
        • et al.
        A c-erbA binding site in rat growth hormone gene mediates trans-activation by thyroid hormone.
        Nature. 1987; 329: 738
        • Glass C.K.
        • Holloway J.M.
        • Devary O.J.
        • et al.
        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
        • Gudernatsch J.F.
        Feeding experiments on tadpoles: The influence of specific organs given as food on growth and differentiation. A contribution to the knowledge of organs of internal secretion.
        Wilhel Roux’ Arch Entwi Mech Org. 1912; 35: 457
        • Hermann T.
        • Hoffmann Zhang X.K.
        • Tran P.
        • et al.
        Heterodimeric receptor complexes determine 3,5,3′-triiodothyronine and retinoid signaling specificities.
        Mol Endocrinol. 1992; 6: 1153
        • Hodin R.A.
        • Lazar M.A.
        • Chin W.W.
        Differential and tissue-specific regulation of the multiple rat c-erbA messenger RNA species by thyroid hormone.
        J Clin Invest. 1990; 85: 101
        • Hodin R.A.
        • Lazar M.A.
        • Wintman B.I.
        • et al.
        Identification of a thyroid hormone receptor that is pituitary-specific.
        Science. 1989; 244: 76
        • Hollenberg S.M.
        • Evans R.M.
        Multiple and cooperative trans-activation domains of the human glucocorticoid receptor.
        Cell. 1988; 55: 899
        • Hollenberg S.M.
        • Weinberger C.
        • Ong E.S.
        • et al.
        Primary structure and expression of a functional glucocorticoid receptor cDNA.
        Nature. 1985; 318: 635
        • Izumo S.
        • Mahdavi V.
        Thyroid hormone receptor a isoforms generated by alternative splicing differentially activate myosin HC gene transcription.
        Nature. 1988; 334: 539
        • Izumo S.
        • Nadal-Ginard B.
        • Mahdavi V.
        All members of the myosin heavy chain multigene family respond to thyroid hormone in a highly tissue specific manner.
        Science. 1986; 231: 597
        • Jump D.B.
        • Bell A.
        • Santiago V.
        Thyroid hormone and dietary carbohydrate interact to regulate rat liver S14 gene transcription and chromatin structure.
        J Biol Chem. 1990; 265: 3474
        • Jump D.B.
        • Narayan P.
        • Towle H.
        • et al.
        Rapid effects of triiodothyronine on hepatic gene expression: Hybridization analysis of tissue specific T3-regulation of mRNA-S14.
        J Biol Chem. 1984; 259: 2789
        • Kinlaw W.B.
        Unexpected nuclear localization and hepatic zonation of spot 14 (S14) protein revealed by anti-fusion protein antiserum.
        Thyroid. 1992; 2: S-85
        • Kinlaw W.B.
        • Ling N.C.
        • Oppenheimer J.H.
        Identification of rat S14 protein and comparison of its regulation with that of mRNA S14 employing synthetic peptide antisera.
        J Biol Chem. 1989; 264: 19779
        • Kinlaw W.B.
        • Schwartz H.L.
        • Oppenheimer J.H.
        Rapid antagonistic effects of triiodothyronine (T3) and glucagon on rat hepatic S14 gene transcription.
        Endocrinol. 1988; 125: 2255
        • Klein I.
        Thyroid hormone and the cardiovascular system.
        Am J Med. 1990; 88: 631
        • Koenig R.J.
        • Brent G.A.
        • Warne R.L.
        • et al.
        Thyroid hormone receptor binds to a site in the rat growth hormone promoter required for induction by thyroid hormone.
        Proc Natl Acad Sci USA. 1987; 84: 5670
        • Koenig R.J.
        • Lazar M.A.
        • Hodin R.A.
        • et al.
        Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternate mRNA splicing.
        Nature. 1989; 337: 659
        • Koenig R.J.
        • Warne R.L.
        • Brent G.A.
        • et al.
        Isolation of a cDNA clone encoding a biologically active thyroid hormone receptor.
        Proc Natl Acad Sci USA. 1988; 85: 5031
        • Krane I.M.
        • Spindel E.R.
        • Chin W.W.
        Thyroid hormone decreases the stability and the poly (A) tract length of rat thyrotropin /3-subunit messenger RNA.
        Mol Endocrinol. 1991; 5: 469
        • Kumar V.
        • Green S.
        • Stack G.
        • et al.
        Functional domains of the human estrogen receptor.
        Cell. 1987; 51: 941
        • Lardy H.A.
        • Malley G.F.
        Metabolic effects of thyroid hormones in vitro.
        Rec Prog Horm Res. 1954; 10: 129
        • Lazar M.A.
        • Berrodin T.J.
        Thyroid hormone receptors form distinct nuclear protein-dependent and independent complexes with a thyroid hormone response element.
        Mol Endocrinol. 1990; 4: 1627
        • Lazar M.A.
        • Chin W.W.
        Regulation of two c-erb A messenger ribonucleic acids in rat GH3 cells by thyroid hormone.
        Mol Endocrinol. 1988; 2: 479
        • Liaw C.
        • Seelig S.
        • Mariash C.N.
        • et al.
        Interactions of thyroid hormone, growth hormone, and high carbohydrate, fat-free diet in regulating several rat liver messenger ribonucleic acid species.
        Biochem. 1983; 22: 213
        • Liaw C.W.
        • Towle H.C.
        Characterization of a thyroid hormone-responsive gene from rat.
        J Biol Chem. 1984; 259: 7253
        • Mariash C.N.
        • Kaiser F.E.
        • Schwartz H.L.
        • et al.
        Synergism of thyroid hormone and high carbohydrate diet in the induction of lipogenic enzymes in the rat: mechanisms and implications.
        J Clin Invest. 1980; 65: 1126
        • Mariash C.N.
        • McSwigan C.R.
        • Towle H.C.
        • et al.
        Glucose and triiodothyronine both induce malic enzyme in the rat hepatocyte culture.
        J Clin Invest. 1981; 68: 1485
        • Mariash C.N.
        • Oppenheimer J.H.
        Stimulation of malic enzyme formation in hepatocyte culture by metabolites: evidence favoring a nonglycolytic metabolite as the proximate signal.
        Metabolism. 1983; 33: 545
        • Mariash C.N.
        • Oppenheimer J.H.
        Thyroid hormone-carbohydrate interaction.
        in: Oppenheimer JH Samuels H.H. Molecular Basis of Thyroid Hormone Action. Academic Press, San Diego1983: 265
        • Mariash C.N.
        • Seelig S.
        • Schwartz H.L.
        • et al.
        Rapid synergistic interaction between thyroid hormone and carbohydrate on mRNA S14 induction.
        J Biol Chem 2. 1986; 61: 9583
        • Martial J.A.
        • Seeburg P.H.
        • Guenzi D.
        • et al.
        Regulation of growth hormone gene expression: Synergistic effects of thyroid and glucocorticoid hormones.
        J Biol Chem. 1977; 74: 4293
        • Mitsuhashi T.
        • Tennyson G.E.
        • Nikodem V.M.
        Alternative splicing generates messages encoding rat c-erbA proteins that do not bind thyroid hormone.
        Proc Natl Acad Sci USA. 1988; 85: 5804
        • Muller M.J.
        • Seitz H.J.
        Thyroid hormone action on intermediary metabolism. II. Lipid metabolism in hypo-and hyperthyroidism.
        Klin Wochensch. 1984; 62: 49
        • Murray M.B.
        • Towle H.C.
        Identification of nuclear factors that enhance binding of the thyroid hormone receptor to a thyroid hormone response element.
        Mol Endocrinol. 1989; 3: 1434
        • Murray M.B.
        • Zilz N.D.
        • McCreary N.L.
        • et al.
        Isolation and characterization of rat cDNA clones for two distinct thyroid hormone receptors.
        J Biol Chem. 1988; 263: 12770
        • Naar A.M.
        • Boutin J.M.
        • Lipkin S.M.
        • et al.
        The orientation and spacing of core DNA-binding motifs dictate selective transcriptional responses to three nuclear receptors.
        Cell. 1991; 65: 1267
        • Nakai A.
        • Sakurai A.
        • Macchia E.
        • et al.
        The roles of three forms of human thyroid hormone receptor in gene regulation.
        Mol Cell Endocrinol. 1990; 72: 143
        • Narayan P.
        • Liaw C.W.
        • Towle H.C.
        Rapid induction of a specific nuclear mRNA precursor by thyroid hormone.
        Proc Natl Acad Sri USA. 1984; 81: 4687
        • Nordquist D.T.
        • Kozak C.A.
        • Orr H.T.
        cDNA cloning and characterization of three genes uniquely expressed in cerebellum by Purkinje cells.
        J Neurosci. 1988; 8: 223
        • Nyborg J.K.
        • Nguyen A.P.
        • Spindler S.R.
        Relationship between thyroid and glucocorticoid hormone receptor occupancy, growth hormone gene transcription, and mRNA accumulation.
        J Biol Chem. 1984; 259: 12377
        • O’Donnell A.L.
        Mutational analysis identifies a new functional domain of the thyroid hormone receptor.
        Mol Endocrinol. 1990; 4: 715
        • O’Donnell A.L.
        • Rosen E.D.
        • Darling D.S.
        • et al.
        Thyroid hormone receptor mutations that interfere with transcriptional activation also interfere with receptor interaction with a nuclear protein.
        Mol Endocrinol. 1991; 5: 94
        • O’Malley B.
        The steroid receptor superfamily: More excitement predicted for the future.
        Mol Endocrinol. 1990; 4: 363
        • Oppenheimer J.H.
        The nuclear receptor-thyroid hormone complex: Relationship to thyroid hormone distribution, metabolism, and biologic action.
        in: Oppenheimer J.H. Samuels H.H. Molecular Basis of Thyroid Hormone Action. Academic Press, San Diego1983: 1
        • Oppenheimer J.H.
        • Koerner D.
        • Schwartz H.L.
        • et al.
        Specific nuclear triiodothyronine binding sites in rat liver and kidney.
        J Clin Endocrinol Metab. 1972; 35: 330
        • Oppenheimer J.H.
        • Schwartz H.L.
        • Lane J.T.
        • et al.
        Functional relationship of thyroid hormone-induced lipogenesis, lipolysis, and thermogenesis in the rat.
        J Clin Invest. 1991; 87: 125
        • Oppenheimer J.H.
        • Schwartz H.L.
        • Mariash C.N.
        • et al.
        Advances in our understanding of thyroid hormone action at the cellular level.
        Endocr Rev. 1987; 8: 288
        • Oppenheimer J.H.
        • Schwartz H.L.
        • Surks M.I.
        Propylthiouracil inhibits the conversion of L-thyroxine to L-triiodothyronine. An explanation of the antithyroxine effect of propylthiouracil and evidence supporting the concept that triiodothyronine is the active thyroid hormone.
        J Clin Invest. 1972; 51: 2493
        • Oppenheimer J.H.
        • Schwartz H.L.
        • Surks M.I.
        Tissue differences in the concentration of triiodothyronine nuclear binding sites in the rat: liver, kidney, pituitary, heart, brain, spleen, and testis.
        Endocrinol. 1974; 95: 897
        • Pascual A.
        • Casanova J.
        • Samuels H.H.
        Photoaffinity labeling of thyroid hormone receptors in intact cells.
        J Biol Chem. 1982; 257: 9640
        • Perez-Castillo A.
        • Schwartz H.L.
        • Oppenheimer J.H.
        Rat hepatic mRNA-S14 and lipogenic enzymes during weaning: role for S14 in lipogenesis.
        Am J Physiol. 1987; 253: E536
        • Petty K.J.
        • Desvergne B.
        • Mitsuhashi T.
        • et al.
        Identification of a thyroid hormone response element in the malic enzyme gene.
        J Biol Chem. 1990; 265: 7395
        • Petty K.J.
        • Morioka H.
        • Mitsuhashi T.
        • et al.
        Thyroid hormone regulation of transcription factors involved in malic enzyme gene expression.
        J Biol Chem. 1989; 264: 11483
        • Pitt-Rivers R.
        • Tata J.
        Physiological actions of thyroid hormone.
        in: The Thyroid Hormones. Pergamon Press, New York1959: 59
        • Rentoumis A.
        • Krishna V.
        • Chatterjee K.
        • et al.
        Negative and positive transcriptional regulation by thyroid hormone receptor isoforms.
        Mol Endocrinol. 1990; 4: 1522
        • Rodd C.
        • Schwartz H.L.
        • Strait K.A.
        • et al.
        Ontogeny of hepatic nuclear triiodothyronine receptor isoforms in the rat.
        Endocrinol. 1992; 131: 2559
        • Rodriguez R.
        • Weigel N.L.
        • O’Malley B.W.
        • et al.
        Dimerization of the chicken progesterone receptor in vitro can occur in the absence of hormone and DNA.
        Mol Endocrinol. 1990; 4: 1782
        • Rohrer D.K.
        • Hartong R.
        • Dillmann W.H.
        Influence of thyroid hormone and retinoic acid on slow sarcoplasmic reticulum Ca2+ATPase and myosin heavy chain a gene expression in cardiac myocytes.
        J Biol Chem. 1991; 266: 8638
        • Ruegamer W.R.
        • Newman G.H.
        • Richert D.A.
        • et al.
        Specificity of the a-glycerophosphate dehydrogenase and malic enzyme response to thyroxine.
        Endocrinol. 1965; 77: 707
        • Samuels H.H.
        Identification and characterization of thyroid hormone receptors and action using cell culture techniques.
        in: Oppenheimer J.H. Samuels H.H. Molecular Basis of Thyroid Hormone Action. Academic Press, San Diego1983: 36
        • Samuels H.H.
        • Stanley F.
        • Shapiro L.
        Dose-dependent depletion of nuclear receptors by L-triiodothyronine: Evidence for a role in induction of growth hormone synthesis in cultured GH1 cells.
        Proc Natl Acad Sci USA. 1976; 73: 3877
        • Sap J.
        • Munoz A.
        • Damm K.
        • et al.
        The c-erb-A protein is a high affinity receptor for thyroid hormone.
        Nature. 1986; 324: 635
        • Schueler P.A.
        • Schwartz H.L.
        • Strait K.A.
        • et al.
        Binding of 3,5,3′-triiodothyronine (T3) and its analogues to the in vitro translational products of c-erbA proto-oncogenes: Differences in the affinity of the α and β forms for the acetic acid analogues and failure of the human testis and kidney α-2 products to bind T3.
        Mol Endocrinol. 1990; 4: 227
        • Schwartz H.L.
        Effect of thyroid hormone in growth and development.
        in: Oppenheimer J.H. Samuels H.H. Molecular Basis of Thyroid Hormone Action. Academic Press, San Diego1983: 413
        • Schwartz H.L.
        • Strait K.A.
        • Oppenheimer J.H.
        • et al.
        Immunoprecipitation of T3-binding proteins in rat tissue nuclear extracts by specifically directed antisera.
        J Biol Chem. 1992; 267: 11794
        • Schwartz H.L.
        • Surks M.I.
        • Oppenheimer J.H.
        Quantitation of extra thyroidal conversion of L-thyroxine to 3,5,3′-triiodo-l-thyronine in the rat.
        J Clin Invest. 1971; 50: 1124
        • Shupnik M.A.
        • Ridgway E.C.
        • Chin W.W.
        Molecular biology of thyrotropin.
        Endocr Rev. 1989; 10: 459
        • Song M.-K.H.
        • Dozin B.
        • Grieco D.
        • et al.
        Transcriptional activation and stabilization of malic enzyme mRNA precursor by thyroid hormone.
        J Biol Chem. 1988; 263: 17970
        • Stapleton S.R.
        • Mitchell D.A.
        • Salati L.M.
        • et al.
        Triiodothyronine stimulates transcription of the fatty acid synthase gene in chick embryo hepatocytes in culture. Insulin and insulin-like growth factor amplify that effect.
        J Biol Chem. 1990; 265: 18442
        • Stassart J.
        • Schwartz H.
        • Strait K.
        • et al.
        TR-al is the predominant thyroid hormone receptor in rat fetal brain: Malic enzyme as a potential gene target.
        Clin Res. 1992; 40: 711
        • Strait K.A.
        • Schwartz H.L.
        • Perez-Castillo A.
        • et al.
        Quantitation of erb A α and β expression in developing and adult rat tissues under the influence of thyroidal status and comparison with nuclear binding capacity.
        J Biol Chem. 1990; 265: 10514
        • Strait K.A.
        • Schwartz H.L.
        • Seybold V.S.
        • et al.
        Immunofluorescent localization of thyroid hormone receptor protein β1 and variant α1 in selected tissues: Cerebellar Purkinje cells as a model for β1 receptor mediated developmental effects of thyroid hormone in brain.
        Proc Natl Acad Sci USA. 1991; 88: 3887
        • Strait K.A.
        • Zou L.
        • Oppenheimer J.H.
        131 isoform-specific regulation of a triiodothyronine-induced gene during cerebellar development.
        Mol Endocrinol. 1992; 6: 1874
        • Tapley D.F.
        • Cooper C.
        • Lehninger A.L.
        The action of thyroxine on mitochondria and oxidative phosphorylation.
        Biochim Biophys Acta. 1955; 18: 597
        • Tata J.R.
        • Widnell C.C.
        Ribonucleic acid synthesis during the early action of thyroid hormones.
        Biochem J. 1966; 98: 604
        • Tepperman H.L.
        • Tepperman J.
        Patterns of dietary and hormonal induction of certain NADP-linked liver enzymes.
        Am J Physiol. 1964; 206: 357
        • Thompson C.C.
        • Evans R.M.
        Trans-activation by thyroid hormone receptors: Functional parallels with steroid hormone receptors.
        Proc Natl Acad Sci USA. 1989; 86: 3494
        • Thompson C.C.
        • Weinberger C.
        • Lebo R.
        • et al.
        Identification of a novel thyroid hormone receptor expressed in the mammalian central nervous system.
        Science. 1987; 237: 1610
        • Towle H.C.
        • Mariash C.N.
        • Oppenheimer J.H.
        Changes in hepatic levels of messenger ribonucleic acid for malic enzyme during induction by thyroid hormone or diet.
        Biochem. 1980; 19: 579
        • Umesono K.
        • Evans R.M.
        Determinants of target gene specificity for steroid/thyroid hormone receptors.
        Cell. 1989; 57: 1139
        • Umesono K.
        • Murakami K.K.
        • Thompson C.C.
        • et al.
        Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors.
        Cell. 1991; 65: 1255
        • Wahlstrom G.M.
        • Sjoberg M.
        • Andersson M.
        • et al.
        Binding characteristics of the thyroid hormone receptors homo-and heterodimers to consensus AGGTCA repeat motifs.
        Mol Endocrinol. 1992; 6: 1013
        • Weinberger C.
        • Thompson C.C.
        • Ong E.S.
        • et al.
        The c-erb-A gene encodes a thyroid hormone receptor.
        Nature. 1986; 324: 641
        • Weirich R.T.
        • Schwartz H.L.
        • Oppenheimer J.H.
        An analysis of the interrelationship of nuclear and plasma triiodothyronine in the sea lamprey eel, lake trout, and the rat: Evolutionary considerations.
        Endocrinol. 1987; 120: 664
        • Wondisford F.E.
        • Farr E.A.
        • Radovic S.
        • et al.
        Thyroid hormone inhibition of human thyrotropin beta-subunit gene expression is mediated by a cis-acting element located in the first exon.
        J Biol Chem. 1989; 261: 14601
        • Yu V.C.
        • Delsert C.
        • Andersen B.
        • et al.
        RXR/3: A coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements.
        Cell. 1991; 67: 1251
        • Zhang X.
        • Hoffman B.
        • Tran P.B.
        • et al.
        Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors.
        Nature. 1992; 355: 441
        • Zilz N.
        • Murray M.
        • Towle H.
        Identification of multiple thyroid hormone response elements located far upstream from the rat S14 promoter.
        J Biol Chem. 1990; 265: 8131

      Article info

      Footnotes

      This work was supported by Grant No. DK19812 and DK07203-14 (JHO) from the National Institutes of Health.

      Identification

      DOI: https://doi.org/10.1016/S0272-2712(18)30425-6

      Copyright

      © 1993 Elsevier Inc. Published by Elsevier Inc. All rights reserved.

      ScienceDirect

      Access this article on ScienceDirect

      The content on this site is intended for healthcare professionals.


      We use cookies to help provide and enhance our service and tailor content. To update your cookie settings, please visit the Cookie Preference Center for this site.
      Copyright © 2023 Elsevier Inc. except certain content provided by third parties.


      RELX