The ability of thyroid hormone receptors to sense T4 as an agonist depends on receptor isoform and on cellular cofactors

Molecular Endocrinology

Volumn 28, Issue 5, 2014, Pages 745-757

  Schroeder, Amy ^a   Jimenez, Robyn ^a   Young, Briana ^a   Privalsky, Martin L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GLUTATHIONE TRANSFERASE; LIOTHYRONINE; OLIGONUCLEOTIDE; PROTEINASE; STEROID RECEPTOR COACTIVATOR 1; SULFUR 35; THYROID HORMONE; THYROID HORMONE RECEPTOR; THYROXINE; ISOPROTEIN; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL TYPE; DNA PROBE; EXPRESSION VECTOR; GAS CHROMATOGRAPHY; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYPOTHALAMUS HYPOPHYSIS THYROID SYSTEM; IN VITRO STUDY; ISOTOPE LABELING; NONHUMAN; PRIORITY JOURNAL; THYROID GLAND; TWO HYBRID SYSTEM; 3T3 CELL LINE; AGONISTS; ANIMAL; CHO CELL LINE; CRICETULUS; HAMSTER; HEK293 CELL LINE; HELA CELL LINE; HEPG2 CELL LINE; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

3T3-L1 CELLS; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; HEK293 CELLS; HELA CELLS; HEP G2 CELLS; HUMANS; MICE; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONE RECEPTORS BETA; THYROXINE; TRANSCRIPTIONAL ACTIVATION; TRIIODOTHYRONINE;

EID: 84899733592     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2013-1335     Document Type: Article

References (64)

1. Larsen PR, Davies TF, Schlumberger MJ, Hay ID. Thyroid physiology and diagnostic evaluation of patients with thyroid disorders. In: Larsen PR, Kronenberg HM, Melmed S, Polonsky KS, eds. Williams Textbook of Endocrinology. 10th ed. Philadelphia: Saunders; 2003: 331-373.
2. Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev. 2001; 81: 1097-1142.
3. Cheng SY, Leonard JL, Davis PJ. Molecular aspects of thyroid hormone actions. Endocr Rev. 2010; 31: 139-170.
4. Flamant F, Baxter JD, Forrest D, et al. International Union of Pharmacology. LIX. The pharmacology and classification of the nuclear receptor superfamily: thyroid hormone receptors. Pharmacol Rev. 2006; 58: 705-711.
5. Wu Y, Koenig RJ. Gene regulation by thyroid hormone. Trends Endocrinol Metab. 2000; 11: 207-211.
6. Zhang J, Lazar MA. The mechanism of action of thyroid hormones. Annu Rev Physiol. 2000; 62: 439-466.
7. Privalsky ML. The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu Rev Physiol. 2004; 66: 315-360.
8. Rosen MD, Privalsky ML. Thyroid hormone receptor mutations in cancer and resistance to thyroid hormone: perspective and prognosis. J Thyroid Res. 2011; 2011: 361304.
9. Wondisford FE. Thyroid hormone action: insight from transgenic mouse models. J Investig Med. 2003; 51: 215-220.
10. Chan IH, Privalsky ML. Isoform-specific transcriptional activity of overlapping target genes that respond to thyroid hormone receptors α1 and β1. Mol Endocrinol. 2009; 23: 1758-1775.
11. Chatonnet F, Guyot R, Benoît G, Flamant F. Genome-wide analysis of thyroid hormone receptors shared and specific functions in neural cells. Proc Natl Acad Sci USA. 2013; 110: E766-E775.
12. Flamant F, Gauthier K. Thyroid hormone receptors: the challenge of elucidating isotype-specific functions and cell-specific response. Biochim Biophys Acta. 2013; 1830: 3900-3907.
13. Forrest D, Vennstrom B. Functions of thyroid hormone receptors in mice. Thyroid. 2000; 10: 41-52.
14. Gil-Ibañez P, Morte B, Bernal J. Role of thyroid hormone receptor subtypes alpha and beta on gene expression in the cerebral cortex and striatum of postnatal mice. Endocrinology. 2013; 154: 1940-1947.
15. Murata Y. Multiple isoforms of thyroid hormone receptor: an analysis of their relative contribution in mediating thyroid hormone action. Nagoya J Med Sci. 1998; 61: 103-115.
16. Samuels HH, Tsai JS, Casanova J, Stanley F. Thyroid hormone action: in vitro characterization of solubilized nuclear receptors from rat liver and cultured GH1 cells. J Clin Invest. 1974; 54: 853-865.
17. Köhrle J. The selenoenzyme family of deiodinase isozymes controls local thyroid hormone availability. Rev Endocr Metab Disord. 2000; 1: 49-58.
18. Maia AL, Goemann IM, Meyer EL, Wajner SM. Deiodinases: the balance of thyroid hormone: type 1 iodothyronine deiodinase in human physiology and disease. J Endocrinol. 2011; 209: 283-297.
19. St Germain DL, Galton VA. The deiodinase family of selenoproteins. Thyroid. 1997; 7: 655-668.
20. Williams GR, Bassett JH. Deiodinases: the balance of thyroid hormone: local control of thyroid hormone action: role of type 2 deiodinase. J Endocrinol. 2011; 209: 261-272.
21. Galton VA. The role of 3, 5, 3β-triiodothyronine in the physiological action of thyroxine in the premetamorphic tadpole. Endocrinology. 1989; 124: 2427-2433.
22. Apriletti JW, Ribeiro RC, Wagner RL, et al. Molecular and structural biology of thyroid hormone receptors. Clin Exp Pharmacol Physiol Suppl. 1998; 25: S2-S11.
23. Ribeiro RC, Apriletti JW, Wagner RL, et al. Mechanisms of thyroid hormone action: insights from X-ray crystallographic and functional studies. Recent Progr Horm Res. 1998; 53: 351-392; discussion 392-354.
24. Ribeiro RC, Apriletti JW, Wagner RL, et al. X-ray crystallographic and functional studies of thyroid hormone receptor. J Steroid Biochem Mol Biol. 1998; 65: 133-141.
25. Galton VA, Schneider MJ, Clark AS, St Germain DL. Life without thyroxine to 3, 5, 3β-triiodothyronine conversion: studies in mice devoid of the 5-deiodinases. Endocrinology. 2009; 150: 2957-2963.
26. Ito M, Roeder RG. The TRAP/SMCC/mediator complex and thyroid hormone receptor function. Trends Endocrinol Metab. 2001; 12: 127-134.
27. Spencer TE, Jenster G, Burcin MM, et al. Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 1997; 389: 194-198.
28. Goodson M, Jonas BA, Privalsky MA. Corepressors: custom tailoring and alterations while you wait. Nucl Recept Signal. 2005; 3: e003.
29. Hahm JB, Privalsky ML. Research resource: identification of novel coregulators specific for thyroid hormone receptor-beta2. Mol Endocrinol. 2013; 27: 840-859.
30. Rosen MD, Privalsky ML. Thyroid hormone receptor mutations found in renal clear cell carcinomas alter corepressor release and reveal helix 12 as key determinant of corepressor specificity. Mol Endocrinol. 2009; 23: 1183-1192.
31. Goodson ML, Jonas BA, Privalsky ML. Alternative mRNA splicing of SMRT creates functional diversity by generating corepressor isoforms with different affinities for different nuclear receptors. J Biol Chem. 2005; 280: 7493-7503.
32. Lee S, Privalsky ML. Heterodimers of retinoic acid receptors and thyroid hormone receptors display unique combinatorial regulatory properties. Mol Endocrinol. 2005; 19: 863-878.
33. Lee S, Young BM, Wan W, Chan IH, Privalsky ML. A mechanism for pituitary-resistance to thyroid hormone (PRTH) syndrome: a loss in cooperative coactivator contacts by thyroid hormone receptor (TR)β2. Mol Endocrinol. 2011; 25: 1111-1125.
34. Yang Z, Privalsky ML. Isoform-specific transcriptional regulation by thyroid hormone receptors: hormone-independent activation operates through a steroid receptor mode of co-activator interaction. Mol Endocrinol. 2001; 15: 1170-1185.
35. Mengeling BJ, Pan F, Privalsky ML. Novel mode of deoxyribonucleic acid recognition by thyroid hormone receptors: thyroid hormone receptor beta-isoforms can bind as trimers to natural response elements comprised of reiterated half-sites. Mol Endocrinol. 2005; 19: 35-51.
36. Phan TQ, Jow MM, Privalsky ML. DNA recognition by thyroid hormone and retinoic acid receptors: 3, 4, 5 rule modified. Mol Cell Endocrinol. 2010; 319: 88-98.
37. Goodson ML, Farboud B, Privalsky ML. An improved high throughput protein-protein interaction assay for nuclear hormone receptors. Nucl Recept Signal. 2007; 5: e002.
38. Goodson ML, Farboud B, Privalsky ML. High throughput analysis of nuclear receptor-cofactor interactions. Methods Mol Biol. 2009; 505: 157-169.
39. Mengeling BJ, Phan TQ, Goodson ML, Privalsky ML. Aberrant corepressor interactions implicated in PML-RAR(alpha) and PLZF-RAR(alpha) leukemogenesis reflect an altered recruitment and release of specific NCoR and SMRT splice variants. J Biol Chem. 2011; 286: 4236-4247.
40. Chan IH, Privalsky ML. Thyroid hormone receptors mutated in liver cancer function as distorted antimorphs. Oncogene. 2006; 25: 3576-3588.
41. Farboud B, Hauksdottir H, Wu Y, Privalsky ML. Isotype-restricted corepressor recruitment: a constitutively closed helix 12 conformation in retinoic acid receptors beta and gamma interferes with corepressor recruitment and prevents transcriptional repression. Mol Cell Biol. 2003; 23: 2844-2858.
42. Yoh SM, Privalsky ML. Molecular analysis of human resistance to thyroid hormone syndrome. Methods Mol Biol. 2002; 202: 129-152.
43. Jonas BA, Privalsky ML. SMRT and N-CoR corepressors are regulated by distinct kinase signaling pathways. J Biol Chem. 2004; 279: 54676-54686.
44. Jonas BA, Varlakhanova N, Hayakawa F, Goodson M, Privalsky ML. Response of SMRT (silencing mediator of retinoic acid and thyroid hormone receptor) and N-CoR (nuclear receptor corepressor) corepressors to mitogen-activated protein kinase kinase kinase cascades is determined by alternative mRNA splicing. Mol Endocrinol. 2007; 21: 1924-1939.
45. Sandler B, Webb P, Apriletti JW, et al. Thyroxine-thyroid hormone receptor interactions. J Biol Chem. 2004; 279: 55801-55808.
46. Steinsapir J, Bianco AC, Buettner C, Harney J, Larsen PR. Substrate-induced down-regulation of human type 2 deiodinase (hD2) is mediated through proteasomal degradation and requires interaction with the enzyme's active center. Endocrinology. 2000; 141: 1127-1135.
47. Visser WE, Friesema EC, Visser TJ. Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol Endocrinol. 2011; 25: 1-14.
48. Warner GJ, Berry MJ, Moustafa ME, Carlson BA, Hatfield DL, Faust JR. Inhibition of selenoprotein synthesis by selenocysteine tRNA[Ser]Sec lacking isopentenyladenosine. J Biol Chem. 2000; 275: 28110-28119.
49. Ikeda M, Rhee M, ChinWW. Thyroid hormone receptor monomer, homodimer, and heterodimer (with retinoid-X receptor) contact different nucleotide sequences in thyroid hormone response elements. Endocrinology. 1994; 135: 1628-1638.
50. Izumo S, Mahdavi V. Thyroid hormone receptor alpha isoforms generated by alternative splicing differentially activate myosin HC gene transcription. Nature. 1988; 334: 539-542.
51. Baniahmad A, Steiner C, Köhne AC, Renkawitz R. Modular structure of a chicken lysozyme silencer: involvement of an unusual thyroid hormone receptor binding site. Cell. 1990; 61: 505-514.
52. Leo C, Chen JD. The SRC family of nuclear receptor coactivators. Gene. 2000; 245: 1-11.
53. Friesema EC, Ganguly S, Abdalla A, Manning Fox JE, Halestrap AP, Visser TJ. Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J Biol Chem. 2003; 278: 40128-40135.
54. O'Shea PJ, Williams GR. Insight into the physiological actions of thyroid hormone receptors from genetically modified mice. J Endocrinol. 2002; 175: 553-570.
55. St Germain DL, Galton VA, Hernandez A. Minireview: Defining the roles of the iodothyronine deiodinases: current concepts and challenges. Endocrinology. 2009; 150: 1097-1107.
56. Williams RH, Larsen PR, eds. Williams Textbook of Endocrinology. 10th ed. Philadelphia: Saunders; 2003.
57. Edwards DP. The role of coactivators and corepressors in the biology and mechanism of action of steroid hormone receptors. J Mammary Gland Biol Neoplasia. 2000; 5: 307-324.
58. Jenster G. Coactivators and corepressors as mediators of nuclear receptor function: an update. Mol Cell Endocrinol. 1998; 143: 1-7.
59. Wang Q, Blackford JA Jr, Song LN, Huang Y, Cho S, Simons SS Jr. Equilibrium interactions of corepressors and coactivators with agonist and antagonist complexes of glucocorticoid receptors. Mol Endocrinol. 2004; 18: 1376-1395.
60. Zhang J, Guenther MG, Carthew RW, Lazar MA. Proteasomal regulation of nuclear receptor corepressor-mediated repression. Genes Dev. 1998; 12: 1775-1780.
61. Zhou Y, Gross W, Hong SH, Privalsky ML. The SMRT corepressor is a target of phosphorylation by protein kinase CK2 (casein kinase II). Mol Cell Biochem. 2001; 220: 1-13.
62. McIver B, Gorman CA. Euthyroid sick syndrome: an overview. Thyroid. 1997; 7: 125-132.
63. Stathatos N, Wartofsky L. The euthyroid sick syndrome: is there a physiologic rationale for thyroid hormone treatment? J Endocrinol Invest. 2003; 26: 1174-1179.
64. Freitas J, Cano P, Craig-Veit C, Goodson ML, Furlow JD, Murk AJ. Detection of thyroid hormone receptor disruptors by a novel stable in vitro reporter gene assay. Toxicol In Vitro. 2011; 25: 257-266.