Thyroid Hormone Regulation of Metabolism

Mullur, Rashmi; Liu, Yan-Yun; Brent, Gregory A.

doi:10.1152/physrev.00030.2013

Cited by 2,421Thyroid Disorders and TreatmentsAdipose Tissue and MetabolismRegulation of Appetite and Obesity

Thyroid Hormone Regulation of Metabolism

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Mullur, Rashmi, Liu, Yan-Yun, Brent, Gregory A.·2014·Physiological Reviews

DOI 10.1152/physrev.00030.2013PMC PMC4044302

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Abstract

Thyroid hormone (TH) is required for normal development as well as regulating metabolism in the adult. The thyroid hormone receptor (TR) isoforms, α and β, are differentially expressed in tissues and have distinct roles in TH signaling. Local activation of thyroxine (T 4 ), to the active form, triiodothyronine (T 3 ), by 5′-deiodinase type 2 (D2) is a key mechanism of TH regulation of metabolism. D2 is expressed in the hypothalamus, white fat, brown adipose tissue (BAT), and skeletal muscle and is required for adaptive thermogenesis. The thyroid gland is regulated by thyrotropin releasing hormone (TRH) and thyroid stimulating hormone (TSH). In addition to TRH/TSH regulation by TH feedback, there is central modulation by nutritional signals, such as leptin, as well as peptides regulating appetite. The nutrient status of the cell provides feedback on TH signaling pathways through epigentic modification of histones. Integration of TH signaling with the adrenergic nervous system occurs peripherally, in liver, white fat, and BAT, but also centrally, in the hypothalamus. TR regulates cholesterol and carbohydrate metabolism through direct actions on gene expression as well as cross-talk with other nuclear receptors, including peroxisome proliferator-activated receptor (PPAR), liver X receptor (LXR), and bile acid signaling pathways. TH modulates hepatic insulin sensitivity, especially important for the suppression of hepatic gluconeogenesis. The role of TH in regulating metabolic pathways has led to several new therapeutic targets for metabolic disorders. Understanding the mechanisms and interactions of the various TH signaling pathways in metabolism will improve our likelihood of identifying effective and selective targets.

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Thyroid hormone plays a critical role in determining energy expenditure, body mass, and body composition.
“LT4 suppression therapy may also affect metabolic function, since thyroid hormone plays a critical role in determining energy expenditure, body mass, and body composition (2).”
From Effects of levothyroxine replacement or suppressive therapy on energy expenditure and body composition (2016) · cites this paper as [2]

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FXR signaling in metabolic disease
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Reduction of hepatic steatosis in rats and mice after treatment with a liver-targeted thyroid hormone receptor agonist #
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Association Between a Novel Variant of the Human Type 2 Deiodinase Gene Thr92Ala and Insulin Resistance
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Regulation of the uncoupling protein gene expression
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Energy balance regulation by thyroid hormones at central level
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Mice deficient in MCT8 reveal a mechanism regulating thyroid hormone secretion
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Thyroid Hormone Effects on Mitochondrial Energetics
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Resting Energy Expenditure is Sensitive to Small Dose Changes in Patients on Chronic Thyroid Hormone Replacement
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A potent PPARα agonist stimulates mitochondrial fatty acid β-oxidation in liver and skeletal muscle
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Thyroid hormone transporters in health and disease
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Thyroid hormone excess and glucose intolerance
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“In the hyperthyroid state, skeletal muscle glucose uptake is increased to overcome a depletion in glycogen stores (62).”
Background
The role of thyroid hormones in the control of energy expenditure
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Triiodothyronine induces UCP-1 expression and mitochondrial biogenesis in human adipocytes
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The quantitative contributions of mitochondrial proton leak and ATP turnover reactions to the changed respiration rates of hepatocytes from rats of different thyroid status
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Thyroid hormone modulates glucose production via a sympathetic pathway from the hypothalamic paraventricular nucleus to the liver
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Brown Fat Activation Mediates Cold-Induced Thermogenesis in Adult Humans in Response to a Mild Decrease in Ambient Temperature
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The thermogenic effect of thyroid hormone and its clinical implications
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Catecholamine metabolism in thyroid disease. II. Norepinephrine secretion rate in hyperthyroidism and hypothyroidism
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Leptin Activates a Novel CNS Mechanism for Insulin-Independent Normalization of Severe Diabetic Hyperglycemia
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Modulation of RXR function through ligand design
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Thyroid Hormone as a Determinant of Metabolic and Contractile Phenotype of Skeletal Muscle
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A Thyroid Hormone Receptor α Gene Mutation (P398H) Is Associated with Visceral Adiposity and Impaired Catecholamine-stimulated Lipolysis in Mice
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Self-citation
Thyroid hormone-related regulation of gene expression in human fatty liver.
Pihlajamäki, J., Boes, T., Kim, E.-Y., Dearie, F., Kim, B. W., Schroeder, J., Mun, E., Nasser, I., Park, P. J., Bianco, A. C., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0212 · Cited by 164 · see citing works
Association of cocaine- and amphetamine-regulated transcript-immunoreactive elements with thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus and its role in the regulation of the hypothalamic-pituitary-thyroid axis during fasting
Fekete, C., Mihály, E., Luo, L.-G., Kelly, J., Clausen, J. T., Mao, Q., Rand, W. M., Moss, L. G., Kuhar, M., Emerson, C. H., et al. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09224.2000 · Cited by 163 · see citing works
Thyroid Hormone Induced Brown Adipose Tissue and Amelioration of Diabetes in a Patient with Extreme Insulin Resistance
Skarulis, M. C., Celi, F. S., Mueller, E., Zemskova, M., Malek, R., Hugendubler, L., Cochran, C. S., Solomon, J. M., Chen, C. C., & Görden, P. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0543 · Cited by 161 · see citing works
Coordination of hypothalamic and pituitary T3 production regulates TSH expression
Fonseca, T. L., Correa-Medina, M., Campos, M. P. O., Wittmann, G., Werneck-de-Castro, J. P., Arrojo e Drigo, R., Mora-Garzon, M., Ueta, C. B., Caicedo, A., Fekete, C., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci61231 · Cited by 155 · see citing works
Bile Acids and the Membrane Bile Acid Receptor TGR5—Connecting Nutrition and Metabolism
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Altered relationship between protonmotive force and respiration rate in non‐phosphorylating liver mitochondria isolated from rats of different thyroid hormone status
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Desiccated Thyroid Extract Compared With Levothyroxine in the Treatment of Hypothyroidism: A Randomized, Double-Blind, Crossover Study
Hoang, T. D., Olsen, C. H., Mai, V. Q., Clyde, P. W., & Shakir, M. K. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-4107 · Cited by 151 · see citing works
The nuclear corepressor, NCoR, regulates thyroid hormone action in vivo
Astapova, I. I., Lee, L. J., Morales, C., Tauber, S., Bilban, M., & Hollenberg, A. N. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804604105 · Cited by 149 · see citing works
SREBP-2 positively regulates transcription of the cholesterol efflux gene, ABCA1, by generating oxysterol ligands for LXR
Wong, J., Quinn, C. M., & Brown, A. J. (2006) · Biochemical Journal · doi:10.1042/bj20060914 · Cited by 148 · see citing works
Pathophysiological Importance of Thyroid Hormone Transporters
Heuer, H., & Visser, T. J. (2009) · Endocrinology · doi:10.1210/en.2008-1518 · Cited by 148 · see citing works
Activation of phosphatidylinositol 3-kinase signaling by a mutant thyroid hormone β receptor
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Thyroid Hormone Promotes Postnatal Rat Pancreatic β-Cell Development and Glucose-Responsive Insulin Secretion Through MAFA
Aguayo-Mazzucato, C., Zavacki, A., Marinelarena, A., Hollister-Lock, J., Khattabi, I. E., Marsili, A., Weir, G., Sharma, A. J., Larsen, P., & Bonner-Weir, S. (2013) · Diabetes · doi:10.2337/db12-0849 · Cited by 147 · see citing works
Reciprocal Regulation of Hepatic and Adipose Lipogenesis by Liver X Receptors in Obesity and Insulin Resistance
Beaven, S. W., Matveyenko, A. V., Wroblewski, K., Chao, L. C., Wilpitz, D. C., Hsu, T. W., Lentz, J., Drew, B. G., Hevener, A. L., & Tontonoz, P. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.04.021 · Cited by 146 · see citing works
Mild Cold Exposure Modulates Fibroblast Growth Factor 21 (FGF21) Diurnal Rhythm in Humans: Relationship between FGF21 Levels, Lipolysis, and Cold-Induced Thermogenesis
Lee, P., Brychta, R. J., Linderman, J. D., Smith, S., Chen, K. Y., & Celi, F. S. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3107 · Cited by 142 · see citing works
Thyroid Hormone Regulates Hepatic Expression of Fibroblast Growth Factor 21 in a PPARα-dependent Manner
Adams, A. C., Astapova, I. I., Fisher, F. M., Badman, M. K., Kurgansky, K. E., Flier, J. S., Hollenberg, A. N., & Maratos–Flier, E. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.c110.107375 · Cited by 141 · see citing works
Thyroid Hormone and Adipocyte Differentiation
Obregón, M.-J. (2008) · Thyroid · doi:10.1089/thy.2007.0254 · Cited by 140 · see citing works
Links between Thyroid Hormone Action, Oxidative Metabolism, and Diabetes Risk?
Crunkhorn, S., & Patti, M. (2008) · Thyroid · doi:10.1089/thy.2007.0249 · Cited by 139 · see citing works
Disruption of Thyroid Hormone Activation in Type 2 Deiodinase Knockout Mice Causes Obesity With Glucose Intolerance and Liver Steatosis Only at Thermoneutrality
Castillo, M., Hall, J. A., Correa-Medina, M., Ueta, C. B., Kang, H. W., Cohen, D. E., & Bianco, A. C. (2011) · Diabetes · doi:10.2337/db10-0758 · Cited by 138 · see citing works
The Role of the Thyrotropin-Releasing Hormone (TRH) Neuron as a Metabolic Sensor
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DOPAMINE IS A PHYSIOLOGICAL REGULATOR OF THYROTROPHIN (TSH) SECRETION IN NORMAL MAN
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Diiodothyropropionic acid (DITPA) in the treatment of MCT8 deficiency
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“Treatment with diiodothyropropionic acid (DITPA), in animal models and humans with inactivation or mutation in the MCT8 gene, results in reduction in serum TSH and serum T3, and an improvement in hypermetabolism with weight gain and reduced caloric needs (60, 262).”
Background
Endocrine manifestations of eating disorders
Warren, M. P. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2304 · Cited by 134 · see citing works
Plasma catecholamine concentrations in hyperthyroidism and hypothyroidism
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Expression of Uncoupling Protein 1 in Mouse Brown Adipose Tissue Is Thyroid Hormone Receptor-β Isoform Specific and Required for Adaptive Thermogenesis
Ribeiro, M. O., Bianco, S. D. C., Kaneshige, M., Schultz, J. J., Cheng, S. Y., Bianco, A. C., & Brent, G. A. (2009) · Endocrinology · doi:10.1210/en.2009-0667 · Cited by 132 · see citing works
Self-citation
Cytosolic Action of Thyroid Hormone Leads to Induction of Hypoxia-Inducible Factor-1α and Glycolytic Genes
Moeller, L. C., Dumitrescu, A. M., & Refetoff, S. (2005) · Molecular Endocrinology · doi:10.1210/me.2004-0542 · Cited by 131 · see citing works
Molecular aspects of thyroid hormone transporters, including MCT8, MCT10, and OATPs, and the effects of genetic variation in these transporters
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Clinical Application of Thyrotropin-Releasing Hormone
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Activation of the hepatic LDL receptor promoter by thyroid hormone
Lopez, D., Abisambra, J. F., Bedi, M., & Ness, G. C. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2007.05.001 · Cited by 126 · see citing works
Thyronamines—Past, Present, and Future
Piehl, S., Hoefig, C. S., Scanlan, T. S., & Köhrle, J. (2011) · Endocrine Reviews · doi:10.1210/er.2009-0040 · Cited by 126 · see citing works
Metabolic Effects of Liothyronine Therapy in Hypothyroidism: A Randomized, Double-Blind, Crossover Trial of Liothyronine <i>Versus</i> Levothyroxine
Celi, F. S., Zemskova, M., Linderman, J. D., Smith, S., Drinkard, B., Sachdev, V., Skarulis, M. C., Kozlosky, M., Csako, G., Costello, R., et al. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1329 · Cited by 125 · see citing works
3-Iodothyronamine: a novel hormone controlling the balance between glucose and lipid utilisation
Braulke, L. J., Klingenspor, M., DeBarber, A. E., Tobias, S. C., Grandy, D. K., Scanlan, T. S., & Heldmaier, G. (2007) · Journal of Comparative Physiology B · doi:10.1007/s00360-007-0208-x · Cited by 125 · see citing works
Prevalence of Thyroid Dysfunction in Patients with Type 2 Diabetes
Díez, J. J., Sánchez, P. P., & Iglesias, P. (2011) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0031-1271691 · Cited by 121 · see citing works
Effects of Thyroid Hormone on GLUT4 Glucose Transporter Gene Expression and NIDDM in Rats
Torrance, C. J., DeVente, J., Jones, J. P., & Dohm, G. L. (1997) · Endocrinology · doi:10.1210/endo.138.3.4981 · Cited by 120 · see citing works
Thyroid Hormone Receptor β-Deficient Mice Show Complete Loss of the Normal Cholesterol 7α-Hydroxylase (CYP7A) Response to Thyroid Hormone but Display Enhanced Resistance to Dietary Cholesterol
Gullberg, H., Rudling, M., Forrest, D., Angelin, B., & Vennström, B. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.11.0548 · Cited by 119 · see citing works
Triiodothyronine‐mediated upregulation of UCP2 and UCP3 mRNA expression in human skeletal muscle without coordinated induction of mitochondrial respiratory chain genes
Barbe, P., Larrouy, D., Boulanger, C., Chevillotte, E., Viguerie, N., Thalamas, C., Oliva Trastoy, M., Roques, M., Vidal, H., & Langin, D. (2001) · The FASEB Journal · doi:10.1096/fj.00-0502fje · Cited by 118 · see citing works
Tissue-Specific Actions of Thyroid Hormone: Insights From Animal Models
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Self-citation
DITPA (3,5-Diiodothyropropionic Acid), a Thyroid Hormone Analog to Treat Heart Failure: Phase II Trial Veterans Affairs Cooperative Study
Goldman, S., McCarren, M., Morkin, E., Ladenson, P. W., Edson, R., Warren, S., Ohm, J., Thai, H., Churby, L., Barnhill, J., et al. (2009) · Circulation · doi:10.1161/circulationaha.108.834424 · Cited by 117 · see citing works
Prevalence of abnormal thyrotropin concentrations measured by a sensitive assay in patients with type 2 diabetes mellitus.
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Resistance to thyroid hormone is associated with raised energy expenditure, muscle mitochondrial uncoupling, and hyperphagia
Mitchell, C. S., Savage, D. B., Dufour, S., Schoenmakers, N. A., Murgatroyd, P. R., Befroy, D. E., Halsall, D. J., Northcott, S., Raymond‐Barker, P., Curran, S., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci38793 · Cited by 116 · see citing works
Hypothyroidism and Thyroiditis
Brent, G. A., & Davies, T. F. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4377-0324-5.00013-4 · Cited by 115 · see citing works
Self-citation
Role of the Iodothyronine Deiodinases in the Physiology and Pathophysiology of Thyroid Hormone Action
Larsen, P. R., & Zavacki, A. M. (2012) · European Thyroid Journal · doi:10.1159/000343922 · Cited by 114 · see citing works
Novel Thyroxine Derivatives, Thyronamine and 3-iodothyronamine, Induce Transient Hypothermia and Marked Neuroprotection Against Stroke Injury
Doyle, K. P., Suchland, K. L., Ciesielski, T., Lessov, N. S., Grandy, D. K., Scanlan, T. S., & Stenzel‐Poore, M. P. (2007) · Stroke · doi:10.1161/strokeaha.106.480277 · Cited by 112 · see citing works
Mechanism of Thyroid-Hormone Regulated Expression of the SERCA Genes in Skeletal Muscle: Implications for Thermogenesis
Simonides, W. S., Thelen, M., van der Linden, C. G., Muller, A., & van Hardeveld, C. (2001) · Bioscience Reports · doi:10.1023/a:1013692023449 · Cited by 112 · see citing works
Activation of PPARα lowers synthesis and concentration of cholesterol by reduction of nuclear SREBP-2
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Thyroid hormone receptor-β agonists prevent hepatic steatosis in fat-fed rats but impair insulin sensitivity via discrete pathways
Vatner, D. F., Weismann, D., Beddow, S. A., Kumashiro, N., Erion, D. M., Liao, X.-H., Grover, G. J., Webb, P., Phillips, K. J., Weiss, R. E., et al. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00573.2012 · Cited by 110 · see citing works
A Thyroid Hormone Analog with Reduced Dependence on the Monocarboxylate Transporter 8 for Tissue Transport
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Regulation of in vivo TSH secretion by leptin
Seoane, L. M., Carro, E., Tovar, S., Casanueva, F. F., & Dieguez, C. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(00)00145-2 · Cited by 109 · see citing works
Clinical Phenotype of a New Type of Thyroid Hormone Resistance Caused by a Mutation of the TRα1 Receptor: Consequences of LT4 Treatment
van Mullem, A. A., Chrysis, D., Eythimiadou, A., Chroni, E., Tsatsoulis, A. A., de Rijke, Y. B., Visser, W. E., Visser, T. J., & Peeters, R. P. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1050 · Cited by 107 · see citing works
Distinct Dysregulation of Lipid Metabolism by Unliganded Thyroid Hormone Receptor Isoforms
Araki, O., Ying, H., Zhu, X., Willingham, M. C., & Cheng, S.-Y. (2009) · Molecular Endocrinology · doi:10.1210/me.2008-0311 · Cited by 105 · see citing works
Peroxisomal Proliferator-activated Receptor-γ Coactivator-1α (PGC-1α) Enhances the Thyroid Hormone Induction of Carnitine Palmitoyltransferase I (CPT-Iα)
Zhang, Y., Ma, K., Song, S., Elam, M. B., Cook, G. A., & Park, E. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406028200 · Cited by 105 · see citing works
Weight Loss after Therapy of Hypothyroidism Is Mainly Caused by Excretion of Excess Body Water Associated with Myxoedema
Karmisholt, J., Andersen, S., & Laurberg, P. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1521 · Cited by 103 · see citing works
Peripheral Metabolism of Thyroid Hormone and Glucose Homeostasis
Chidakel, A. R., Mentuccia, D., & Celi, F. S. (2005) · Thyroid · doi:10.1089/thy.2005.15.899 · Cited by 103 · see citing works
Ubiquitination-induced conformational change within the deiodinase dimer is a switch regulating enzyme activity
Sagar, G. D. V., Gereben, B., Callebaut, I., Mornon, J.-P., Zeöld, A., da Silva, W. S., Luongo, C., Dentice, M., Tente, S. M., Freitas, B. C. G., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00283-07 · Cited by 103 · see citing works
Mice with a Targeted Deletion of the Type 2 Deiodinase Are Insulin Resistant and Susceptible to Diet Induced Obesity
Marsili, A., Aguayo‐Mazzucato, C., Chen, T., Kumar, A., Chung, M., Lunsford, E. P., Harney, J. W., Van-Tran, T., Gianetti, E., Ramadan, W., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020832 · Cited by 102 · see citing works
Sterol Regulatory Element-binding Protein-2- and Liver X Receptor-driven Dual Promoter Regulation of Hepatic ABC Transporter A1 Gene Expression
Tamehiro, N., Shigemoto‐Mogami, Y., Kakeya, T., Okuhira, K., Suzuki, K., Sato, R., Nagao, T., & Nishimaki‐Mogami, T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701228200 · Cited by 101 · see citing works
Thyroid hormone is required for hypothalamic neurons regulating cardiovascular functions
Mittag, J., Lyons, D. J., Sällström, J., Vujović, M., Dudazy-Gralla, S., Warner, A., Wallis, K., Alkemade, A., Nordström, K., Monyer, H., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci65252 · Cited by 101 · see citing works
Thyroid hormone receptors: The challenge of elucidating isotype-specific functions and cell-specific response
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Thyroid Thermogenesis and Active Sodium Transport
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Potential therapeutic applications of thyroid hormone analogs
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SREBP-1 integrates the actions of thyroid hormone, insulin, cAMP, and medium-chain fatty acids on ACCα transcription in hepatocytes
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Multigenic control of thyroid hormone functions in the nervous system
Nunez, J., Celi, F. S., Ng, L., & Forrest, D. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.03.006 · Cited by 96 · see citing works
Circulating Levels of FGF-21 in Obese Youth: Associations With Liver Fat Content and Markers of Liver Damage
Giannini, C., Feldstein, A. E., Santoro, N., Kim, G. J., Kursawe, R., Pierpont, B. M., & Caprio, S. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1250 · Cited by 95 · see citing works
A Thyroid Hormone Response Unit Formed between the Promoter and First Intron of the Carnitine Palmitoyltransferase-Iα Gene Mediates the Liver-specific Induction by Thyroid Hormone
Jackson‐Hayes, L., Song, S., Lavrentyev, E. N., Jansen, M. S., Hillgartner, F. B., Tian, L., Wood, P. A., Cook, G. A., & Park, E. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211062200 · Cited by 94 · see citing works
Type 2 deiodinase at the crossroads of thyroid hormone action
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Central Role of Brown Adipose Tissue Thyroxine 5′-Deiodinase on Thyroid Hormone-Dependent Thermogenic Response to Cold*
Carvalho, S. D., Kimura, E. T., Bianco, A. C., & Silva, J. E. (1991) · Endocrinology · doi:10.1210/endo-128-4-2149 · Cited by 93 · see citing works
The in vivo role of nuclear receptor corepressors in thyroid hormone action
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Regulation of thyrotropin-releasing hormone-expressing neurons in paraventricular nucleus of the hypothalamus by signals of adiposity
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Thyroid hormone receptor subtype specificity for hormone-dependent neurogenesis in Xenopus laevis
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The Nuclear Receptor Corepressor (NCoR) Controls Thyroid Hormone Sensitivity and the Set Point of the Hypothalamic-Pituitary-Thyroid Axis
Astapova, I. I., Vella, K. R., Ramadoss, P., Holtz, K. A., Rodwin, B. A., Liao, X.-H., Weiss, R. E., Rosenberg, M. A., Rosenzweig, A., & Hollenberg, A. N. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0462 · Cited by 88 · see citing works
Lipoprotein Alterations, Hepatic Lipase Activity, and Insulin Sensitivity in Subclinical Hypothyroidism: Response to L-T 4 Treatment
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Physiological importance and control of non-shivering facultative thermogenesis
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Body Weight and Body Composition Changes after Treatment of Hyperthyroidism1
Lönn, L., Stenlöf, K., Ottosson, M., Lindroos, A., Nyström, E., & Sjöström, L. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.12.5338 · Cited by 83 · see citing works
The effect of peroxisome-proliferator-activated receptor-α on the activity of the cholesterol 7α-hydroxylase gene
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Thyroid Hormone Increases Muscle/Fat Glucose Transporter Gene Expression in Rat Skeletal Muscle*
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Thyroid Hormone Responsive Genes in Cultured Human Fibroblasts
Moeller, L. C., Dumitrescu, A. M., Walker, R. L., Meltzer, P. S., & Refetoff, S. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1768 · Cited by 82 · see citing works
Dietary Cholesterol Fails to Stimulate the Human Cholesterol 7α-Hydroxylase Gene (CYP7A1) in Transgenic Mice
Agellon, L. B., Drover, V. A. B., Cheema, S. K., Gbaguidi, F. G., & Walsh, A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c200105200 · Cited by 80 · see citing works
Maintenance of the thyroid axis during diet-induced obesity in rodents is controlled at the central level
Perello, M., Çakir, I., Cyr, N. E., Romero, A., Stuart, R. C., Chiappini, F., Hollenberg, A. N., & Nillni, E. A. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00448.2010 · Cited by 80 · see citing works
Novel neural pathways for metabolic effects of thyroid hormone
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Thyroid hormone reduces cholesterol via a non-LDL receptor-mediated pathway
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Thyroid hormone induces cardiac myocyte hypertrophy in a thyroid hormone receptor α1-specific manner that requires TAK1 and p38 mitogen-activated protein kinase
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A Mutant Thyroid Hormone Receptor α Antagonizes Peroxisome Proliferator-Activated Receptor α Signaling in Vivo and Impairs Fatty Acid Oxidation
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Self-citation
Impact of Early Nutrient Restriction During Critical Illness on the Nonthyroidal Illness Syndrome and Its Relation With Outcome: A Randomized, Controlled Clinical Study
Langouche, L., Vander Perre, S., Marques, M., Boelen, A., Wouters, P. J., Casaer, M. P., & Van den Berghe, G. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2809 · Cited by 79 · see citing works
MECHANISMS OF THYROID HORMONE ACTION
Motomura, K., & Brent, G. A. (1998) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(05)70294-2 · Cited by 74 · see citing works
Self-citation
Catecholamines Metabolism in Thyroid Diseases. I. Epinephrine Secretion Rate in Hyperthyroidism and Hypothyroidism
COULOMBE, P., DUSSAULT, J. H., LETARTE, J., & SIMARD, S. J. (1976) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-42-1-125 · Cited by 74 · cited 1× · see citing works
“Direct measurement of epinephrine secretion shows no difference in hyperthyroid or hypothyroid patients (47).”
Background
Total sleep deprivation and the thyroid axis: effects of sleep and waking activity.
Gary, K. A., Winokur, A., Douglas, S. D., Kapoor, S. C., Zaugg, L., & Dinges, D. F. (1996) · PubMed · Cited by 73 · see citing works
3-Iodothyronamine (T1AM): A New Player on the Thyroid Endocrine Team?
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Thyroid hormone (T3) rapidly activates p38 and AMPK in skeletal muscle in vivo
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Thyroid Hormone Receptor α and Regulation of Type 3 Deiodinase
Barca‐Mayo, O., Liao, X.-H., Alonso‐Sampedro, M., Cosmo, C. D., Hernández, A., Refetoff, S., & Weiss, R. E. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0213 · Cited by 73 · see citing works
Acute exogenous TSH administration stimulates leptin secretion in vivo
Santini, F., Galli, G., Maffei, M., Fierabracci, P., Pelosini, C., Marsili, A., Giannetti, M., Castagna, M. G., Checchi, S., Molinaro, E., et al. (2010) · European Journal of Endocrinology · doi:10.1530/eje-10-0138 · Cited by 73 · see citing works

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Identification of region-specific astrocyte subtypes at single cell resolution
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Impaired Sensitivity to Thyroid Hormones Is Associated With Diabetes and Metabolic Syndrome
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Assessing the human health risks of perfluorooctane sulfonate by in vivo and in vitro studies
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Thyroid hormone regulation of hepatic lipid and carbohydrate metabolism
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Hypothalamic AMPK-ER Stress-JNK1 Axis Mediates the Central Actions of Thyroid Hormones on Energy Balance
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Thyroid Hormone Transporters
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Chemistry and Biology in the Biosynthesis and Action of Thyroid Hormones
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Low energy availability: history, definition and evidence of its endocrine, metabolic and physiological effects in prospective studies in females and males
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Thyroid disruption by triphenyl phosphate, an organophosphate flame retardant, in zebrafish (Danio rerio) embryos/larvae, and in GH3 and FRTL-5 cell lines
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Chemical Hybridization of Glucagon and Thyroid Hormone Optimizes Therapeutic Impact for Metabolic Disease
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Thyroid hormone signaling and the liver
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Metabolic Effects of the Intracellular Regulation of Thyroid Hormone: Old Players, New Concepts
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Interplay between gut microbiome, host genetic and epigenetic modifications in MASLD and MASLD-related hepatocellular carcinoma
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Obesity and Thyroid Axis
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Perfluoroalkyl substances and changes in body weight and resting metabolic rate in response to weight-loss diets: A prospective study
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Adipose tissues and thyroid hormones
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Effect of the plastic pollutant bisphenol A on the biology of aquatic organisms: A meta‐analysis
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Euthyroid Sick Syndrome
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Reactive Oxygen Species and Oxidative Stress in the Pathogenesis of MAFLD
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Roles of Regulatory T Cells in Tissue Pathophysiology and Metabolism
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The microbiota–gut–brain interaction in regulating host metabolic adaptation to cold in male Brandt’s voles (Lasiopodomys brandtii)
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Virus Infections and Host Metabolism—Can We Manage the Interactions?
Sumbria, D., Berber, E., Mathayan, M., & Rouse, B. T. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.594963 · Cited by 141 · see citing works
Deiodinases and the Three Types of Thyroid Hormone Deiodination Reactions
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“For example, thyroid hormones T4 and its active form, T3, as well as type 2 deiodinase (D2), an essential enzyme activating T4 to T3, are required for adaptive thermogenesis in BAT (de Jesus et al , 2001; Mullur et al , 2014).”

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Authors: Mullur, R., Liu, Y.-Y., & Brent, G. A.
Affiliations: University of California, Los Angeles (US)
Corresponding author: Brent, Gregory A.
ORCID: Mullur, Rashmi
Liu, Yan-Yun
Brent, Gregory A.
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2014-04
Volume: 94
Issue: 2
Pages: 355-382
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00030.2013
PMC: PMC4044302
OpenAlex: W1966824338
Cited by: 2,421
References: 292
Citations by year: 2026: 223 · 2025: 273 · 2024: 300 · 2023: 273 · 2022: 269 · 2021: 237 · 2020: 254 · 2019: 163 · 2018: 132 · 2017: 118 · 2016: 90 · 2015: 60 · 2014: 27
FWCI: 15.61
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Physiological Reviews (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (F32CA090073)
National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK98576, R01DK098576)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: thyroid hormones, thyroid hormone receptor, triiodothyronine, adaptive thermogenesis, brown adipose tissue, hypothalamus, thyrotropin-releasing hormone, thyroid-stimulating hormone, leptin, appetite regulation, adrenergic system, peroxisome proliferator-activated receptors, liver X receptor, bile acid signaling, hepatic insulin sensitivity, hepatic gluconeogenesis, cholesterol metabolism, carbohydrate metabolism, metabolic disorders
MeSH terms: Animals, Body Weight, Cholesterol, Energy Metabolism, Humans, Thyroid Gland, Thyroid Hormones, Triglycerides, Signal Transduction, Thermogenesis, Carbohydrate Metabolism

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Thyroid Hormone Regulation of Metabolism

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