Thyroid hormone regulation of hepatic lipid and carbohydrate metabolism

Trends in Endocrinology and Metabolism

Volumn 25, Issue 10, 2014, Pages 538-545

  Sinha, Rohit A ^a   Singh, Brijesh K ^a   Yen, Paul M ^a,b  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Glucose metabolism; Lipid metabolism; Liver; Thyroid hormone

Indexed keywords

CHOLESTEROL; GLUCOSE; LIPID; THYROID HORMONE;

CARBOHYDRATE METABOLISM; CHOLESTEROL METABOLISM; GENE CONTROL; GLUCOSE METABOLISM; HORMONAL REGULATION; HUMAN; HYPERCHOLESTEROLEMIA; INSULIN RESISTANCE; LIPID METABOLISM; LIPOGENESIS; LIPOPHAGOCYTOSIS; METABOLIC REGULATION; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NONHUMAN; REVIEW; ANIMAL; HOMEOSTASIS; LIVER; LIVER DISEASE; METABOLISM; PHYSIOLOGY;

ANIMALS; CARBOHYDRATE METABOLISM; HOMEOSTASIS; HUMANS; LIPID METABOLISM; LIVER; LIVER DISEASES; THYROID HORMONES;

EID: 84908086702     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2014.07.001     Document Type: Review

References (100)

1. Mullur R., et al. Thyroid hormone regulation of metabolism. Physiol. Rev. 2014, 94:355-382.
2. Arrojo E.D.R., et al. Role of the type 2 iodothyronine deiodinase (D2) in the control of thyroid hormone signaling. Biochim. Biophys. Acta 2013, 1830:3956-3964.
3. Schwartz H.L., et al. Quantitation of rat tissue thyroid hormone binding receptor isoforms by immunoprecipitation of nuclear triiodothyronine binding capacity. J. Biol. Chem. 1992, 267:11794-11799.
4. 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.
5. Chung G.E., et al. Non-alcoholic fatty liver disease across the spectrum of hypothyroidism. J. Hepatol. 2012, 57:150-156.
6. Bellentani S., et al. Epidemiology of non-alcoholic fatty liver disease. Dig. Dis. 2010, 28:155-161.
7. Liangpunsakul S., Chalasani N. Is hypothyroidism a risk factor for non-alcoholic steatohepatitis?. J. Clin. Gastroenterol. 2003, 37:340-343.
8. Pihlajamaki J., et al. Thyroid hormone-related regulation of gene expression in human fatty liver. J. Clin. Endocrinol. Metab. 2009, 94:3521-3529.
9. Klein I., Danzi S. Thyroid disease and the heart. Circulation 2007, 116:1725-1735.
10. Duntas L.H., Wartofsky L. Cardiovascular risk and subclinical hypothyroidism: focus on lipids and new emerging risk factors. What is the evidence?. Thyroid 2007, 17:1075-1084.
11. Brent G.A. Clinical practice. Graves' disease. N. Engl. J. Med. 2008, 358:2594-2605.
12. Venditti P., Di Meo S. Thyroid hormone-induced oxidative stress. Cell. Mol. Life Sci. 2006, 63:414-434.
13. Kumar A., et al. Hyperthyroidism induces apoptosis in rat liver through activation of death receptor-mediated pathways. J. Hepatol. 2007, 46:888-898.
14. Gierach M., et al. Insulin resistance and thyroid disorders. Endokrynol. Pol. 2014, 65:70-76.
15. Kazantzis M., Stahl A. Fatty acid transport proteins, implications in physiology and disease. Biochim. Biophys. Acta 2012, 1821:852-857.
16. Koonen D.P., et al. Increased hepatic CD36 expression contributes to dyslipidemia associated with diet-induced obesity. Diabetes 2007, 56:2863-2871.
17. Newberry E.P., et al. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J. Biol. Chem. 2003, 278:51664-51672.
18. Chen A., et al. Liver fatty acid binding protein (L-Fabp) modulates murine stellate cell activation and diet-induced nonalcoholic fatty liver disease. Hepatology 2013, 57:2202-2212.
19. Wierzbicki M., et al. Differential effects of in vivo PPAR alpha and gamma activation on fatty acid transport proteins expression and lipid content in rat liver. J. Physiol. Pharmacol. 2009, 60:99-106.
20. Klieverik L.P., et al. Thyroid hormone effects on whole-body energy homeostasis and tissue-specific fatty acid uptake in vivo. Endocrinology 2009, 150:5639-5648.
21. Santana-Farre R., et al. Influence of neonatal hypothyroidism on hepatic gene expression and lipid metabolism in adulthood. PLoS ONE 2012, 7:e37386.
22. Hashimoto K., et al. Mouse sterol response element binding protein-1c gene expression is negatively regulated by thyroid hormone. Endocrinology 2006, 147:4292-4302.
23. Hashimoto K., et al. Liver X receptor-alpha gene expression is positively regulated by thyroid hormone. Endocrinology 2007, 148:4667-4675.
24. Hashimoto K., et al. Carbohydrate response element binding protein gene expression is positively regulated by thyroid hormone. Endocrinology 2009, 150:3417-3424.
25. Liu Y.Y., Brent G.A. Thyroid hormone crosstalk with nuclear receptor signaling in metabolic regulation. Trends Endocrinol. Metab. 2010, 21:166-173.
26. Hashimoto K., et al. Human stearoyl-CoA desaturase 1 (SCD-1) gene expression is negatively regulated by thyroid hormone without direct binding of thyroid hormone receptor to the gene promoter. Endocrinology 2013, 154:537-549.
27. Araki O., et al. Distinct dysregulation of lipid metabolism by unliganded thyroid hormone receptor isoforms. Mol. Endocrinol. 2009, 23:308-315.
28. Fozzatti L., et al. Differential recruitment of nuclear coregulators directs the isoform-dependent action of mutant thyroid hormone receptors. Mol. Endocrinol. 2011, 25:908-921.
29. Oppenheimer J.H., et al. Functional relationship of thyroid hormone-induced lipogenesis, lipolysis, and thermogenesis in the rat. J. Clin. Invest. 1991, 87:125-132.
30. Nozaki S., et al. Stimulation of the activity and mRNA level of hepatic triacylglycerol lipase by triiodothyronine in HepG2 cells. Biochim. Biophys. Acta 1992, 1127:298-302.
31. Simo R., et al. Thyroid hormone upregulates zinc-alpha2-glycoprotein production in the liver but not in adipose tissue. PLoS ONE 2014, 9:e85753.
32. Zechner R., et al. FAT SIGNALS-lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 2012, 15:279-291.
33. Liu K., Czaja M.J. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ. 2013, 20:3-11.
34. Sinha R.A., et al. Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. J. Clin. Invest. 2012, 122:2428-2438.
35. Jackson-Hayes L., et al. A thyroid hormone response unit formed between the promoter and first intron of the carnitine palmitoyltransferase-Ialpha gene mediates the liver-specific induction by thyroid hormone. J. Biol. Chem. 2003, 278:7964-7972.
36. Thakran S., et al. Role of sirtuin 1 in the regulation of hepatic gene expression by thyroid hormone. J. Biol. Chem. 2013, 288:807-818.
37. Chang H.C., Guarente L. SIRT1 and other sirtuins in metabolism. Trends Endocrinol. Metab. 2014, 25:138-145.
38. Adams A.C., et al. Thyroid hormone regulates hepatic expression of fibroblast growth factor 21 in a PPARalpha-dependent manner. J. Biol. Chem. 2010, 285:14078-14082.
39. Emanuelli B., et al. Interplay between FGF21 and insulin action in the liver regulates metabolism. J. Clin. Invest. 2014, 124:515-527.
40. Domouzoglou E.M., et al. Fibroblast growth factor 21 and thyroid hormone show mutual regulatory dependency but have independent actions in vivo. Endocrinology 2014, 155:2031-2040.
41. Cioffi F., et al. Thyroid hormones and mitochondria: with a brief look at derivatives and analogues. Mol. Cell. Endocrinol. 2013, 379:51-61.
42. Ness G.C. Thyroid hormone. Basis for its hypocholesterolemic effect. J. Fla. Med. Assoc. 1991, 78:383-385.
43. Lopez D., et al. Activation of the hepatic LDL receptor promoter by thyroid hormone. Biochim. Biophys. Acta 2007, 1771:1216-1225.
44. Shin D.J., Osborne T.F. Thyroid hormone regulation and cholesterol metabolism are connected through sterol regulatory element-binding protein-2 (SREBP-2). J. Biol. Chem. 2003, 278:34114-34118.
45. Moon J.H., et al. Decreased expression of hepatic low-density lipoprotein receptor-related protein 1 in hypothyroidism: a novel mechanism of atherogenic dyslipidemia in hypothyroidism. Thyroid 2013, 23:1057-1065.
46. Bilic-Komarica E., et al. Effects of treatment with L-thyroxin on glucose regulation in patients with subclinical hypothyroidism. Med. Arch. 2012, 66:364-368.
47. Lammel Lindemann J.A., et al. Thyroid hormone induction of human cholesterol 7 alpha-hydroxylase (Cyp7a1) in vitro. Mol. Cell. Endocrinol. 2014, 388:32-40.
48. Bonde Y., et al. Stimulation of murine biliary cholesterol secretion by thyroid hormone is dependent on a functional ABCG5/G8 complex. Hepatology 2012, 56:1828-1837.
49. Yap C.S., et al. Thyroid hormone negatively regulates CDX2 and SOAT2 mRNA expression via induction of miRNA-181d in hepatic cells. Biochem. Biophys. Res. Commun. 2013, 440:635-639.
50. Hashimoto K., Mori M. Crosstalk of thyroid hormone receptor and liver X receptor in lipid metabolism and beyond [Review]. Endocr. J. 2011, 58:921-930.
51. Liu Y.Y., et al. A mutant thyroid hormone receptor alpha antagonizes peroxisome proliferator-activated receptor alpha signaling in vivo and impairs fatty acid oxidation. Endocrinology 2007, 148:1206-1217.
52. Christoffolete M.A., et al. Regulation of thyroid hormone activation via the liver X-receptor/retinoid X-receptor pathway. J. Endocrinol. 2010, 205:179-186.
53. Fang S., et al. Corepressor SMRT promotes oxidative phosphorylation in adipose tissue and protects against diet-induced obesity and insulin resistance. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3412-3417.
54. Astapova I., Hollenberg A.N. The in vivo role of nuclear receptor corepressors in thyroid hormone action. Biochim. Biophys. Acta 2013, 1830:3876-3881.
55. Astapova I., et al. Hepatic nuclear corepressor 1 regulates cholesterol absorption through a TRbeta1-governed pathway. J. Clin. Invest. 2014, 124:1976-1986.
56. Cordeiro A., et al. Thyroid hormone regulation of Sirtuin 1 expression and implications to integrated responses in fasted mice. J. Endocrinol. 2013, 216:181-193.
57. Grasselli E., et al. Non-receptor-mediated actions are responsible for the lipid-lowering effects of iodothyronines in FaO rat hepatoma cells. J. Endocrinol. 2011, 210:59-69.
58. Gnoni G.V., et al. 3,5,3'triiodo-L-thyronine induces SREBP-1 expression by non-genomic actions in human HEP G2 cells. J. Cell. Physiol. 2012, 227:2388-2397.
59. Yamauchi M., et al. Thyroid hormone activates adenosine 5'-monophosphate-activated protein kinase via intracellular calcium mobilization and activation of calcium/calmodulin-dependent protein kinase kinase-beta. Mol. Endocrinol. 2008, 22:893-903.
60. Potenza M., et al. Excess thyroid hormone and carbohydrate metabolism. Endocr. Pract. 2009, 15:254-262.
61. Klieverik L.P., et al. Effects of thyrotoxicosis and selective hepatic autonomic denervation on hepatic glucose metabolism in rats. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E513-E520.
62. Lopez M., et al. Energy balance regulation by thyroid hormones at central level. Trends Mol. Med. 2013, 19:418-427.
63. Park E.A., et al. Role of CCAAT enhancer-binding protein beta in the thyroid hormone and cAMP induction of phosphoenolpyruvate carboxykinase gene transcription. J. Biol. Chem. 1999, 274:211-217.
64. Suh J.H., et al. SIRT1 is a direct coactivator of thyroid hormone receptor beta1 with gene-specific actions. PLoS ONE 2013, 8:e70097.
65. Singh B.K., et al. FoxO1 deacetylation regulates thyroid hormone-induced transcription of key hepatic gluconeogenic genes. J. Biol. Chem. 2013, 288:30365-30372.
66. Sargis R.M. The hijacking of cellular signaling and the diabetes epidemic: mechanisms of environmental disruption of insulin action and glucose homeostasis. Diabetes Metab. J. 2014, 38:13-24.
67. Dube S., et al. Assessment of insulin action on carbohydrate metabolism: physiological and non-physiological methods. Diabet. Med. 2013, 30:664-670.
68. Poupeau A., Postic C. Cross-regulation of hepatic glucose metabolism via ChREBP and nuclear receptors. Biochim. Biophys. Acta 2011, 1812:995-1006.
69. Huang Y.Y., et al. Cross-talk between the thyroid and liver: a new target for nonalcoholic fatty liver disease treatment. World J. Gastroenterol. 2013, 19:8238-8246.
70. Deetman P.E., et al. The relationship of the anti-oxidant bilirubin with free thyroxine is modified by insulin resistance in euthyroid subjects. PLoS ONE 2014, 9:e90886.
71. Vatner D.F., et al. Thyroid hormone receptor-beta agonists prevent hepatic steatosis in fat-fed rats but impair insulin sensitivity via discrete pathways. Am. J. Physiol. Endocrinol. Metab. 2013, 305:E89-E100.
72. Flamant F., et al. Thyroid hormones signaling is getting more complex: STORMs are coming. Mol. Endocrinol. 2007, 21:321-333.
73. Baxter J.D., Webb P. Thyroid hormone mimetics: potential applications in atherosclerosis, obesity and type 2 diabetes. Nat. Rev. Drug Discov. 2009, 8:308-320.
74. van der Valk F., et al. The effect of a diiodothyronine mimetic on insulin sensitivity in male cardiometabolic patients: a double-blind randomized controlled trial. PLoS ONE 2014, 9:e86890.
75. Erion M.D., et al. Targeting thyroid hormone receptor-beta agonists to the liver reduces cholesterol and triglycerides and improves the therapeutic index. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15490-15495.
76. Grover G.J., et al. Selective thyroid hormone receptor-beta activation: a strategy for reduction of weight, cholesterol, and lipoprotein (a) with reduced cardiovascular liability. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10067-10072.
77. Ladenson P.W., et al. Use of the thyroid hormone analogue eprotirome in statin-treated dyslipidemia. N. Engl. J. Med. 2010, 362:906-916.
78. Taylor A.H., et al. Beneficial effects of a novel thyromimetic on lipoprotein metabolism. Mol. Pharmacol. 1997, 52:542-547.
79. Johansson L., et al. Selective thyroid receptor modulation by GC-1 reduces serum lipids and stimulates steps of reverse cholesterol transport in euthyroid mice. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:10297-10302.
80. Berkenstam A., et al. The thyroid hormone mimetic compound KB2115 lowers plasma LDL cholesterol and stimulates bile acid synthesis without cardiac effects in humans. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:663-667.
81. Tancevski I., et al. The liver-selective thyromimetic T-0681 influences reverse cholesterol transport and atherosclerosis development in mice. PLoS ONE 2010, 5:e8722.
82. Pedrelli M., et al. Thyroid hormones and thyroid hormone receptors: effects of thyromimetics on reverse cholesterol transport. World J. Gastroenterol. 2010, 16:5958-5964.
83. Shoemaker T.J., et al. Thyroid hormone analogues for the treatment of metabolic disorders: new potential for unmet clinical needs?. Endocr. Pract. 2012, 18:954-964.
84. Mork L.M., et al. The thyroid receptor modulator KB3495 reduces atherosclerosis independently of total cholesterol in the circulation in ApoE deficient mice. PLoS ONE 2013, 8:e78534.
85. Jornayvaz F.R., et al. Thyroid hormone receptor-alpha gene knockout mice are protected from diet-induced hepatic insulin resistance. Endocrinology 2012, 153:583-591.
86. Vujovic M., et al. Interference of a mutant thyroid hormone receptor alpha1 with hepatic glucose metabolism. Endocrinology 2009, 150:2940-2947.
87. Liu Y.Y., et al. A thyroid hormone receptor alpha gene mutation (P398H) is associated with visceral adiposity and impaired catecholamine-stimulated lipolysis in mice. J. Biol. Chem. 2003, 278:38913-38920.
88. Bochukova E., et al. A mutation in the thyroid hormone receptor alpha gene. N. Engl. J. Med. 2012, 366:243-249.
89. van Mullem A.A., et al. Clinical Consequences of Mutations in Thyroid Hormone Receptor-alpha1. Eur. Thyroid J. 2014, 3:17-24.
90. Koo S.H. Nonalcoholic fatty liver disease: molecular mechanisms for the hepatic steatosis. Clin. Mol. Hepatol. 2013, 19:210-215.
91. Schwenger K.J., Allard J.P. Clinical approaches to non-alcoholic fatty liver disease. World J. Gastroenterol. 2014, 20:1712-1723.
92. Pagadala M.R., et al. Prevalence of hypothyroidism in nonalcoholic fatty liver disease. Dig. Dis. Sci. 2012, 57:528-534.
93. Erdogan M., et al. Metabolic syndrome prevalence in subclinic and overt hypothyroid patients and the relation among metabolic syndrome parameters. J. Endocrinol. Invest. 2011, 34:488-492.
94. Perra A., et al. Thyroid hormone (T3) and TRbeta agonist GC-1 inhibit/reverse nonalcoholic fatty liver in rats. FASEB J. 2008, 22:2981-2989.
95. Cable E.E., et al. Reduction of hepatic steatosis in rats and mice after treatment with a liver-targeted thyroid hormone receptor agonist. Hepatology 2009, 49:407-417.
96. Yehuda-Shnaidman E., et al. Thyroid hormone, thyromimetics, and metabolic efficiency. Endocr. Rev. 2014, 35:35-58.
97. Mollica M.P., et al. 3,5-diiodo-l-thyronine, by modulating mitochondrial functions, reverses hepatic fat accumulation in rats fed a high-fat diet. J. Hepatol. 2009, 51:363-370.
98. Grasselli E., et al. 3,5-Diiodo-L-thyronine modulates the expression of genes of lipid metabolism in a rat model of fatty liver. J. Endocrinol. 2012, 212:149-158.
99. Cavallo A., et al. 3,5-Diiodo-L-thyronine administration to hypothyroid rats rapidly enhances fatty acid oxidation rate and bioenergetic parameters in liver cells. PLoS ONE 2013, 8:e52328.
100. Astapova I., et al. The nuclear corepressor, NCoR, regulates thyroid hormone action in vivo. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:19544-19549.