The T3 receptor β1 isoform regulates UCP1 and D2 deiodinase in rat brown adipocytes

Endocrinology

Volumn 151, Issue 10, 2010, Pages 5074-5083

  Martinez De Mena, Raquel ^a,b   Scanlan, Thomas S ^c   Obregon, Maria Jesus ^a,b  

^a CSIC   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CO 23; CYCLIC AMP; GC 1; HORMONE INHIBITOR; LIOTHYRONINE RECEPTOR; LIOTHYRONINE RECEPTOR ALPHA; LIOTHYRONINE RECEPTOR BETA; MESSENGER RNA; OXIDOREDUCTASE; THYROID HORMONE; TYPE 2 DEIODINASE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; 5 (3,5 DIIODO 4 (3 ISOPROPYL 4 HYDROXYPHENOXY)BENZYL)IMIDAZOLIDINE 2,4 DIONE; 5-(3,5-DIIODO-4-(3-ISOPROPYL-4-HYDROXYPHENOXY)BENZYL)IMIDAZOLIDINE-2,4-DIONE; ACETIC ACID DERIVATIVE; ADRENERGIC RECEPTOR STIMULATING AGENT; GC 1 COMPOUND; HYDANTOIN DERIVATIVE; IODIDE PEROXIDASE; IODOTHYRONINE DEIODINASE TYPE II; ION CHANNEL; ISOPROTEIN; LIOTHYRONINE; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; NORADRENALIN; PHENOL DERIVATIVE; THYROID HORMONE RECEPTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BROWN ADIPOSE TISSUE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG ACTIVITY; ENZYME ACTIVITY; ENZYME DEGRADATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT; ANIMAL; CELL CULTURE; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; SPRAGUE DAWLEY RAT;

ACETIC ACIDS; ADIPOSE TISSUE, BROWN; ADRENERGIC AGENTS; ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; HYDANTOINS; IODIDE PEROXIDASE; ION CHANNELS; MITOCHONDRIAL PROTEINS; NOREPINEPHRINE; PHENOLS; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; THYROID HORMONE RECEPTORS BETA; TRIIODOTHYRONINE;

EID: 77957279363     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0533     Document Type: Article

References (57)

1. Cannon B, Nedergaard J 2004 Brown adipose tissue: function and physiological significance. Physiol Rev 84:277-359
2. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J 2009 UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9:203-209
3. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ 2009 Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500-1508
4. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerbäck S, Nuutila P 2009 Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518-1525
5. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR 2009 Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509-1517
6. Jacobsson A, Nedergaard J, Cannon B 1986 α- And β-adrenergic control of thermogenin mRNA expression in brown adipose tissue. Biosci Rep 6:621-631
7. Rehnmark S, Néchad M, Herron D, Cannon B, Nedergaard J 1990 α- And β-adrenergic induction of the expression of the uncoupling protein thermogenin in brown adipocytes differentiated in culture. J Biol Chem 265:16464-16471
8. Bianco AC, Silva JE 1987 Intracellular conversion of thyroxine to triiodothyronine is required for the optimal thermogenic function of brown adipose tissue. J Clin Invest 79:295-300
9. Silva JE, Matthews PS 1988 Full expression of uncoupling protein gene requires the concurrence of norepinephrine and triiodothyronine. Mol Endocrinol 2:706-713
10. Bianco AC, Sheng XY, Silva JE 1988 Triiodothyronine amplifies norepinephrine stimulation of uncoupling protein gene transcription by a mechanism not requiring protein synthesis. J Biol Chem 263:18168-18175
11. Hernández A, Obregón MJ 2000 Triiodothyronine amplifies the adrenergic stimulation of uncoupling protein expression in rat brown adipocytes. Am J Physiol Endocrinol Metab 278:E769-E777
12. Guerra C, Roncero C, Porras A, Fernández M, Benito M 1996 Triiodothyronine induces the transcription of the uncoupling protein gene and stabilizes its mRNA in fetal rat brown adipocyte primary cultures. J Biol Chem 271:2076-2081
13. Rehnmark S, Bianco AC, Kieffer JD, Silva JE 1992 Transcriptional and posttranscriptional mechanisms in uncoupling protein mRNA response to cold. Am J Physiol 262:E58-E67
14. Rabelo R, Schifman A, Rubio A, Sheng X, Silva JE 1995 Delineation of thyroid hormone-responsive sequences within a critical enhancer in the rat uncoupling protein gene. Endocrinology 136:1003-1013
15. Bianco AC, Silva JE 1987 Nuclear 3,5,3′-triiodothyronine (T3) in brown adipose tissue: receptor occupancy and sources of T3 as determined by in vitro techniques. Endocrinology 120:55-62
16. Silva JE, Rabelo R 1997 Regulation of the uncoupling protein gene expression. Eur J Endocrinol 136:251-264
17. de Jesus LA, Carvalho SD, Ribeiro MO, Schneider M, Kim SW, Harney JW, Larsen PR, Bianco AC 2001 The type 2 iodothyronine deiodinase is essential for adaptive thermogenesis in brown adipose tissue. J Clin Invest 108:1379-1385
18. Christoffolete MA, Linardi CC, de Jesus L, Ebina KN, Carvalho SD, Ribeiro MO, Rabelo R, Curcio C, Martins L, Kimura ET, Bianco AC 2004 Mice with targeted disruption of the Dio2 gene have cold-induced overexpression of the uncoupling protein 1 gene but fail to increase brown adipose tissue lipogenesis and adaptive thermogenesis. Diabetes 53:577-584
19. Obregon MJ 2008 Thyroid hormones and adipocyte differentiation. Thyroid 18:18595
20. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR 2002 Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 23:38-89
21. Martinez-deMena R, Hernández A, Obregón MJ 2002 Triiodothyronine is required for the stimulation of type II 5′-deiodinase mRNA in rat brown adipocytes. Am J Physiol Endocrinol Metab 282:E1119-E1127
22. Yen PM 2001 Physiological and molecular basis of thyroid hormone action. Physiol Rev 81:1097-1142
23. Brent GA 2000 Tissue-specific actions of thyroid hormone: insights from animal models. Rev Endocr Metab Disord 1:27-33
24. Wu Y, Koenig RJ 2000 Gene regulation by thyroid hormone. Trends Endocrinol Metab 11:207-211
25. Baxter JD, Webb P, Grover G, Scanlan TS 2004 Selective activation of thyroid hormone signaling pathways by GC-1: a new approach to controlling cholesterol and body weight. Trends Endocrinol Metab 15:154-157
26. Hernández A, Obregón MJ 1996 Presence and mRNA expression of T3 receptors in differentiating rat brown adipocytes. Mol Cell Endocrinol 121:37-46
27. Scanlan TS 2010 Sobetirome: a case history of bench-to-clinic drug discovery and development. Heart Fail Rev 15:177-182
28. Trost SU, Swanson E, Gloss B, Wang-Iverson DB, Zhang H, Volodarsky T, Grover GJ, Baxter JD, Chiellini G, Scanlan TS, Dillmann WH 2000 The thyroid hormone receptor-β-selective agonist GC-1 differentially affects plasma lipids and cardiac activity. Endocrinology 141:3057-3064
29. Grover GJ, Mellström K, Ye L, Malm J, Li YL, Bladh LG, Sleph PG, Smith MA, George R, Vennström B, Mookhtiar K, Horvath R, Speelman J, Egan D, Baxter JD 2003 Selective thyroid hormone receptor-β activation: a strategy for reduction of weight, cholesterol, and lipoprotein (a) with reduced cardiovascular liability. Proc Natl Acad Sci USA 100:10067-10072
30. Ribeiro MO, Carvalho SD, Schultz JJ, Chiellini G, Scanlan TS, Bianco AC, Brent GA 2001 Thyroid hormone-sympathetic interaction and adaptive thermogenesis are thyroid hormone receptor isoform-specific. J Clin Invest 108:97-105
31. Ocasio CA, Scanlan TS 2006 Design and characterization of a thyroid hormone receptor α (TRα)-specific agonist. ACS Chem Biol 1:585-593
32. Néchad M, Kuusela P, Carneheim C, Björntorp P, Nedergaard J, Cannon B 1983 Development of brown fat cells in monolayer culture. I. Morphological and biochemical distinction from white fat cells in culture. Exp Cell Res 149:105-118
33. 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 action of thyroid hormone. Endocrinology 105:80-85
34. Morreale de Escobar G, Pastor R, Obregon MJ, Escobar del Rey F 1985 Effects of maternal hypothyroidism on the weight and thyroid hormone content of rat embryonic tissues. Endocrinology 117:1890-1900
35. Hernández A, Obregón MJ 1996 T3 potentiates the adrenergic stimulation of type II 5′-deiodinase in cultured rat brown adipocytes. Am J Physiol 271:E15-E23
36. Obregón MJ, Ruiz de Oña C, Hernandez A, Calvo R, Escobar del Rey F, Morreale de Escobar G 1989 Thyroid hormones and 5′-deiodinase in rat brown adipose tissue during fetal life. Am J Physiol 257:E625-E631
37. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ 1951 Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
38. Bouillaud F, Weissenbach J, Ricquier D 1986 Complete cDNA-derived amino acid sequence of rat brown fat uncoupling protein. J Biol Chem 261:1487-1490
39. Hernández A, Obregón MJ 1995 Presence of growth factors-induced type III iodothyronine 5-deiodinase in cultured rat brown adipocytes. Endocrinology 136:4543-4550
40. Snedecor GW, Cochran WG 1980 Statistical methods. 7th ed. Ames, IA: Iowa State University Press
41. Martinez-deMena R, Obregón MJ 2005 Insulin increases the adrenergic stimulation of 5′ deiodinase activity and mRNA expression in rat brown adipocytes; role of MAPK and PI3K. J Mol Endocrinol 34:139-151
42. Forrest D, Vennström B 2000 Functions of thyroid hormone receptors in mice. Thyroid 10:41-52
43. Baxter JD, Webb P 2009 Thyroid hormone mimetics: potential applications in atherosclerosis, obesity and type 2 diabetes. Nat Rev Drug Discov 8:308-320
44. Ribeiro MO, Bianco SD, Kaneshige M, Schultz JJ, Cheng SY, Bianco AC, Brent GA 2010 Expression of uncoupling protein 1 in mouse brown adipose tissue is thyroid hormone receptor-β isoform specific and required for adaptive thermogenesis. Endocrinology151:432-440
45. Golozoubova V, Gullberg H, Matthias A, Cannon B, Vennström B, Nedergaard J 2004 Depressed thermogenesis but competent brown adipose tissue recruitment in mice devoid of all hormone-binding thyroid hormone receptors. Mol Endocrinol 18:384-401
46. Medina-Gomez G, Hernàndez A, Calvo RM, Martin E, Obregón MJ 2003 Potent thermogenic action of triiodothyroacetic acid in brown adipocytes. Cell Mol Life Sci 60:1957-1967
47. Silva JE 2006 Thermogenic mechanisms and their hormonal regulation. Physiol Rev 86:435-464
48. Medina-Gomez G, Calvo RM, Obregon MJ 2008 Thermogenic effect of triiodothyroacetic acid at low doses in rat adipose tissue without adverse side effects in the thyroid axis. Am J Physiol Endocrinol Metab 294:E688-E697
49. Hernandez A, Garcia B, Obregon MJ 2007 Gene expression from the imprinted Dio3 locus is associated with cell proliferation of cultured brown adipocytes. Endocrinology 148:3968-3976
50. Steinsapir J, Harney J, Larsen PR 1998 Type 2 iodothyronine deiodinase in rat pituitary tumor cells is inactivated in proteasomes. J Clin Invest 102:1895-1899
51. Gereben B, Goncalves C, Harney JW, Larsen PR, Bianco AC 2000 Selective proteolysis of human type 2 deiodinase: a novel ubiquitin-proteasomal mediated mechanism for regulation of hormone activation. Mol Endocrinol 14:1697-1708
52. Curcio-Morelli C, Zavacki AM, Christofollete M, Gereben B, de Freitas BC, Harney JW, Li Z, Wu G, Bianco AC 2003 Deubiquitination of type 2 iodothyronine deiodinase by von Hippel-Lindau protein-interacting deubiquitinating enzymes regulates thyroid hormone activation. J Clin Invest 112:189-196
53. Sagar GD, Gereben B, Callebaut I, Mornon JP, Zeöld A, da Silva WS, Luongo C, Dentice M, Tente SM, Freitas BC, Harney JW, Zavacki AM, Bianco AC 2007 Ubiquitination-induced conformational change within the deiodinase dimer is a switch regulating enzyme activity. Mol Cell Biol 27:4774-4783
54. Silva JE, Larsen PR 1985 Potential of brown adipose tissue type II thyroxine 5′-deiodinase as a local and systemic source of triiodothyronine in rats. J Clin Invest 76:2296-2305
55. Silva JE, Bianco SD 2008 Thyroid-adrenergic interactions: physiological and clinical implications. Thyroid 18:157-165
56. Amorim BS, Ueta CB, Freitas BC, Nassif RJ, Gouveia CH, Christoffolete MA, Moriscot AS, Lancelloti CL, Llimona F, Barbeiro HV, de Souza HP, Catanozi S, Passarelli M, Aoki MS, Bianco AC, Ribeiro MO 2009 A TRβ-selective agonist confers resistance to diet-induced obesity. J Endocrinol 203:291-299
57. Castillo M, Freitas BC, Rosene ML, Drigo RA, Grozovsky R, Maciel RM, Patti ME, Ribeiro MO, Bianco AC 2010 Impaired metabolic effects of a thyroid hormone receptor β-selective agonist in a mouse model of diet-induced obesity. Thyroid 20:545-553