A thyroid hormone receptor mutation that dissociates thyroid hormone regulation of gene expression in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 23, 2009, Pages 9441-9446

  Machado, Danielle S ^a   Sabet, Amin ^a   Santiago, Leticia A ^a,b   Sidhaye, Aniket R ^a   Chiamolera, Maria I ^a,c   Ortiga Carvalho, Tania M ^b   Wondisford, Fredric E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Corepressor; Homodimer; Negative regulation; Resistance to thyroid hormone

Indexed keywords

5' DEIODINASE I; GENE PRODUCT; GLUTATHIONE TRANSFERASE ALPHA; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; LIOTHYRONINE; MESSENGER RNA; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; PROTEIN SPOT14; THYROID HORMONE; THYROID HORMONE RECEPTOR; THYROID HORMONE RECEPTOR BETA; THYROTROPIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIMERIZATION; DIO1 GENE; DISSOCIATION; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE MUTATION; GENE REPRESSION; GH GENE; GPD1 GENE; HORMONE RESPONSIVE ELEMENT; HYPOTHALAMUS HYPOPHYSIS SYSTEM; HYPOTHYROIDISM; IN VIVO STUDY; KNOCKOUT MOUSE; LIGAND BINDING; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; THRSP GENE; THYROID HORMONE BLOOD LEVEL;

ANIMALS; GENE KNOCK-IN TECHNIQUES; HUMANS; MICE; MICE, TRANSGENIC; POINT MUTATION; REPRESSOR PROTEINS; THYROID HORMONE RECEPTORS BETA; THYROID HORMONE RESISTANCE SYNDROME; TRIIODOTHYRONINE;

ANIMALIA; MUS;

EID: 67249136626     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0903227106     Document Type: Article

References (61)

1. Croyle ML, Maurer RA (1984) Thyroid hormone decreases thyrotropin subunit mRNA levels in rat anterior pituitary. DNA 3:231-236. (Pubitemid 14016008)
2. Shupnik MA, Chin WW, Habener JF, Ridgway EC (1985) Transcriptional regulation of the thyrotropin subunit genes by thyroid hormone. J Biol Chem 260:2900-2903. (Pubitemid 15141437)
3. Wondisford FE, et al. (1989) 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 264:14601-14604. (Pubitemid 19237269)
4. Wood WM, Kao MY, Gordon DF, Ridgway EC (1989) Thyroid hormone regulates the mouse thyrotropin beta-subunit gene promoter in transfected primary thyrotropes. J Biol Chem 264:14840-14847. (Pubitemid 19237305)
5. Chatterjee VK, Lee JK, Rentoumis A, Jameson JL (1989) Negative regulation of the thyroid-stimulating hormone alpha gene by thyroid hormone: Receptor interaction adjacent to the TATA box. Proc Natl Acad Sci USA 86:9114-9118. (Pubitemid 20010375)
6. Koller KJ, Wolff RS, Warden MK, Zoeller RT (1987) Thyroid hormones regulate levels of thyrotropin-releasing-hormone mRNA in the paraventricular nucleus. Proc Natl Acad Sci USA 84:7329-7333. (Pubitemid 18017339)
7. Segerson TP, et al. (1987) Thyroid hormone regulates TRH biosynthesis in the paraventricular nucleus of the rat hypothalamus. Science 238:78-80. (Pubitemid 17150486)
8. Lechan RM, Kakucska I (1992) Feedback regulation of thyrotropin-releasing hormone gene expression by thyroid hormone in the hypothalamic paraventricular nucleus. Ciba Found Symp 168:144-158; discussion 158-164.
9. Forrest D, Erway LC, Ng L, Altschuler R, Curran T (1996) Thyroid hormone receptor beta is essential for development of auditory function. Nat Genet 13:354-357. (Pubitemid 26230504)
10. Weiss RE, et al. (1997) Thyrotropin regulation by thyroid hormone in thyroid hormone receptor beta-deficient mice. Endocrinology 138:3624-3629. (Pubitemid 27351909)
11. Abel ED, et al. (1999) Divergent roles for thyroid hormone receptor beta isoforms in the endocrine axis and auditory system. J Clin Invest 104:291-300.
12. Abel ED, Ahima RS, Boers ME, Elmquist JK, Wondisford FE (2001) Critical role for thyroid hormone receptor beta2 in the regulation of paraventricular thyrotropin-releasing hormone neurons. J Clin Invest 107:1017-1023. (Pubitemid 32323411)
13. Gauthier K, et al. (1999) Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. EMBO J 18:623-631. (Pubitemid 29057247)
14. Lazar MA (2003) Thyroid hormone action: A binding contract. J Clin Invest 112:497-499. (Pubitemid 38056333)
15. Xu L, Glass CK, Rosenfeld MG (1999) Coactivator and corepressor complexes in nuclear receptor function. Curr Opin Genet Dev 9:140-147. (Pubitemid 29158546)
16. Hollenberg AN, et al. (1995) The human thyrotropin-releasing hormone gene is regulated by thyroid hormone through two distinct classes of negative thyroid hormone response elements. Mol Endocrinol 9:540-550.
17. Tagami T, Madison LD, Nagaya T, Jameson JL (1997) Nuclear receptor corepressors activate rather than suppress basal transcription of genes that are negatively regulated by thyroid hormone. Mol Cell Biol 17:2642-2648. (Pubitemid 27175146)
18. Weiss RE, et al. (1999) Mice deficient in the steroid receptor co-activator 1 (SRC-1) are resistant to thyroid hormone. EMBO J 18:1900-1904. (Pubitemid 29158533)
19. Ortiga-Carvalho TM, et al. (2005) Negative regulation by thyroid hormone receptor requires an intact coactivator-binding surface. J Clin Invest 115:2517-2523. (Pubitemid 41266214)
20. Usala SJ, et al. (1988) Tight linkage between the syndrome of generalized thyroid hormone resistance and the human c-erbA beta gene. Mol Endocrinol 2:1217-1220. (Pubitemid 19005932)
21. Sakurai A, et al. (1989) Generalized resistance to thyroid hormone associated with a mutation in the ligand-binding domain of the human thyroid hormone receptor beta. Proc Natl Acad Sci USA 86:8977-8981. (Pubitemid 20010349)
22. Usala SJ, et al. (1990) A base mutation of the C-erbA beta thyroid hormone receptor in a kindred with generalized thyroid hormone resistance. Molecular heterogeneity in two other kindreds. J Clin Invest 85:93-100. (Pubitemid 20030295)
23. Refetoff S, Weiss RE, Usala SJ (1993) The syndromes of resistance to thyroid hormone. Endocr Rev 14:348-399. (Pubitemid 23168055)
24. Yen PM (2003) Molecular basis of resistance to thyroid hormone. Trends Endocrinol Metab 14:327-333. (Pubitemid 37093130)
25. Chatterjee VK, et al. (1991) Thyroid hormone resistance syndrome. Inhibition of normal receptor function by mutant thyroid hormone receptors. J Clin Invest 87:1977-1984.
26. Yen PM, et al. (1992) Triiodothyronine (T3) decreases binding to DNA by T3-receptor homodimers but not receptor-auxiliary protein heterodimers. J Biol Chem 267:3565-3568.
27. Nagaya T, Eberhardt NL, Jameson JL (1993) Thyroid hormone resistance syndrome: Correlation of dominant negative activity and location of mutations. J Clin Endocrinol Metab 77:982-990. (Pubitemid 23301474)
28. Zavacki AM, Harney JW, Brent GA, Larsen PR (1993) Dominant negative inhibition by mutant thyroid hormone receptors is thyroid hormone response element and receptor isoform specific. Mol Endocrinol 7:1319-1330. (Pubitemid 23319115)
29. Gershengorn MC, Weintraub BD (1975) Thyrotropin-induced hyperthyroidism caused by selective pituitary resistance to thyroid hormone. A new syndrome of "inappropriate secretion of TSH". J Clin Invest 56:633-642.
30. Brucker-Davis F, et al. (1995) Genetic and clinical features of 42 kindreds with resistance to thyroid hormone. The National Institutes of Health Prospective Study. Ann Intern Med 123:572-583.
31. Adams M, et al. (1994) Genetic analysis of 29 kindreds with generalized and pituitary resistance to thyroid hormone. Identification of thirteen novel mutations in the thyroid hormone receptor beta gene. J Clin Invest 94:506-515. (Pubitemid 24978970)
32. Flynn TR, et al. (1994) A novel C-terminal domain in the thyroid hormone receptor selectively mediates thyroid hormone inhibition. J Biol Chem 269:32713-32716.
33. Wan W, Farboud B, Privalsky ML (2005) Pituitary resistance to thyroid hormone syndrome is associated with T3 receptor mutants that selectively impair beta2 isoform function. Mol Endocrinol 19:1529-1542. (Pubitemid 41002983)
34. Hayashi Y, et al. (1995) Do clinical manifestations of resistance to thyroid hormone correlate with the functional alteration of the corresponding mutant thyroid hormone- beta receptors? J Clin Endocrinol Metab 80:3246-3256.
35. Cohen RN, Wondisford FE, Hollenberg AN (1998) Two separate NCoR (nuclear receptor corepressor) interaction domains mediate corepressor action on thyroid hormone response elements. Mol Endocrinol 12:1567-1581. (Pubitemid 30663439)
36. Wagner RL, et al. (1995) A structural role for hormone in the thyroid hormone receptor. Nature 378:690-697. (Pubitemid 3009997)
37. Au-Fliegner M, Helmer E, Casanova J, Raaka BM, Samuels HH (1993) The conserved ninth C-terminal heptad in thyroid hormone and retinoic acid receptors mediates diverse responses by affecting heterodimer but not homodimer formation. Mol Cell Biol 13:5725-5737. (Pubitemid 23260674)
38. Nagaya T, Jameson JL (1993) Thyroid hormone receptor dimerization is required for dominant negative inhibition by mutations that cause thyroid hormone resistance. J Biol Chem 268:15766-15771. (Pubitemid 23222078)
39. Yen PM, Wilcox EC, Hayashi Y, Refetoff S, Chin WW (1995) Studies on the repression of basal transcription (silencing) by artificial and natural human thyroid hormone receptor- beta mutants. Endocrinology 136:2845-2851.
40. Monden T, et al. (2003) Leucine at codon 428 in the ninth heptad of thyroid hormone receptor beta1 is necessary for interactions with the transcriptional cofactors and functions regardless of dimer formations. Thyroid 13:427-435. (Pubitemid 36750552)
41. Astapova I, et al. (2008) The nuclear corepressor, NCoR, regulates thyroid hormone action in vivo. Proc Natl Acad Sci USA 105:19544-19549.
42. Clifton-Bligh RJ, et al. (1998) A novel TR beta mutation (R383H) in resistance to thyroid hormone syndrome predominantly impairs corepressor release and negative transcriptional regulation. Mol Endocrinol 12:609-621. (Pubitemid 30659063)
43. Wu SY, et al. (2006) A novel thyroid hormone receptor-beta mutation that fails to bind nuclear receptor corepressor in a patient as an apparent cause of severe, predominantly pituitary resistance to thyroid hormone. J Clin Endocrinol Metab 91:1887-1895.
44. Makowski A, Brzostek S, Cohen RN, Hollenberg AN (2003) Determination of nuclear receptor corepressor interactions with the thyroid hormone receptor. Mol Endocrinol 17:273-286. (Pubitemid 36183150)
45. Cohen RN, Putney A, Wondisford FE, Hollenberg AN (2000) The nuclear corepressors recognize distinct nuclear receptor complexes. Mol Endocrinol 14:900-914. (Pubitemid 32260502)
46. Meier CA, et al. (1992) Variable transcriptional activity and ligand binding of mutant beta 1 3,5,3′-triiodothyronine receptors from four families with generalized resistance to thyroid hormone. Mol Endocrinol 6:248-258.
47. Yoh SM, Chatterjee VK, Privalsky ML (1997) Thyroid hormone resistance syndrome manifests as an aberrant interaction between mutant T3 receptors and transcriptional corepressors. Mol Endocrinol 11:470-480. (Pubitemid 27147015)
48. Yoh SM, Privalsky ML (2000) Resistance to thyroid hormone (RTH) syndrome reveals novel determinants regulating interaction of T3 receptor with corepressor. Mol Cell Endocrinol 159:109-124. (Pubitemid 30067645)
49. Tagami T, Jameson JL (1998) Nuclear corepressors enhance the dominant negative activity of mutant receptors that cause resistance to thyroid hormone. Endocrinology 139:640-650. (Pubitemid 28513214)
50. Safer JD, Cohen RN, Hollenberg AN, Wondisford FE (1998) Defective release of corepressor by hinge mutants of the thyroid hormone receptor found in patients with resistance to thyroid hormone. J Biol Chem 273:30175-30182. (Pubitemid 28545480)
51. Nagaya T, Fujieda M, Seo H (1998) Requirement of corepressor binding of thyroid hormone receptor mutants for dominant negative inhibition. Biochem Biophys Res Commun 247:620-623. (Pubitemid 28418441)
52. Collingwood TN, et al. (1998) A role for helix 3 of the TRbeta ligand-binding domain in coactivator recruitment identified by characterization of a third cluster of mutations in resistance to thyroid hormone. EMBO J 17:4760-4770. (Pubitemid 28377176)
53. Liu Y, Takeshita A, Misiti S, Chin WW, Yen PM (1998) Lack of coactivator interaction can be amechanism for dominant negative activity by mutant thyroid hormone receptors. Endocrinology 139:4197-4204. (Pubitemid 28513706)
54. Hollenberg AN, Monden T, Madura JP, Lee K, Wondisford FE (1996) Function of nuclear co-repressor protein on thyroid hormone response elements is regulated by the receptor A/B domain. J Biol Chem 271:28516-28520. (Pubitemid 26374674)
55. Abel ED, et al. (1999) Novel insight from transgenic mice into thyroid hormone resistance and the regulation of thyrotropin. J Clin Invest 103:271-279. (Pubitemid 29053145)
56. Takeshita A, et al. (1998) Thyroid hormone response elements differentially modulate the interactions of thyroid hormone receptors with two receptor binding domains in the steroid receptor coactivator-1. J Biol Chem 273:21554-21562. (Pubitemid 28405324)
57. Shibusawa N, et al. (2003) Thyroid hormone action in the absence of thyroid hormone receptor DNA-binding in vivo. J Clin Invest 112:588-597. (Pubitemid 38056343)
58. Shibusawa N, Hollenberg AN, Wondisford FE (2003) Thyroid hormone receptor DNA binding is required for both positive and negative gene regulation. J Biol Chem 278:732-738. (Pubitemid 36790743)
59. Hashimoto K, et al. (2001) An unliganded thyroid hormone receptor causes severe neurological dysfunction. Proc Natl Acad Sci USA 98:3998-4003. (Pubitemid 32249887)
60. Kaneshige M, et al. (2000) Mice with a targeted mutation in the thyroid hormone beta receptor gene exhibit impaired growth and resistance to thyroid hormone. Proc Natl Acad Sci USA 97:13209-13214.
61. Zhu XG, Yu CL, McPhie P, Wong R, Cheng SY (1996) Understanding the molecular mechanism of dominant negative action of mutant thyroid hormone beta1-receptors: The important role of the wild-type/mutant receptor heterodimer. Endocrinology 137:712-721. (Pubitemid 126423652)