Thermogenic Mechanisms and Their Hormonal Regulation

Silva, J. Enrique

doi:10.1152/physrev.00009.2005

Cited by 687Adipose Tissue and MetabolismPhysiological and biochemical adaptationsThermoregulation and physiological responses

Thermogenic Mechanisms and Their Hormonal Regulation

Silva, J. Enrique·2006·Physiological Reviews

DOI 10.1152/physrev.00009.2005

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Abstract

Increased heat generation from biological processes is inherent to homeothermy. Homeothermic species produce more heat from sustaining a more active metabolism as well as from reducing fuel efficiency. This article reviews the mechanisms used by homeothermic species to generate more heat and their regulation largely by thyroid hormone (TH) and the sympathetic nervous system (SNS). Thermogenic mechanisms antecede homeothermy, but in homeothermic species they are activated and regulated. Some of these mechanisms increase ATP utilization (same amount of heat per ATP), whereas others increase the heat resulting from aerobic ATP synthesis (more heat per ATP). Among the former, ATP utilization in the maintenance of ionic gradient through membranes seems quantitatively more important, particularly in birds. Regulated reduction of the proton-motive force to produce heat, originally believed specific to brown adipose tissue, is indeed an ancient thermogenic mechanism. A regulated proton leak has been described in the mitochondria of several tissues, but its precise mechanism remains undefined. This leak is more active in homeothermic species and is regulated by TH, explaining a significant fraction of its thermogenic effect. Homeothermic species generate additional heat, in a facultative manner, when obligatory thermogenesis and heat-saving mechanisms become limiting. Facultative thermogenesis is activated by the SNS but is modulated by TH. The type II iodothyronine deiodinase plays a critical role in modulating the amount of the active TH, T 3 , in BAT, thereby modulating the responses to SNS. Other hormones affect thermogenesis in an indirect or permissive manner, providing fuel and modulating thermogenesis depending on food availability, but they do not seem to have a primary role in temperature homeostasis. Thermogenesis has a very high energy cost. Cold adaptation and food availability may have been conflicting selection pressures accounting for the variability of thermogenesis in humans.

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Glucocorticoids do not directly increase thermogenesis, but they may have an important role in coordinating the thermogenic response to substrate and food availability.
“Glucocorticoids similarly do not directly increase thermogenesis, but they may have an important role in coordinating the thermogenic response to substrate and food availability 65.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [65]
Type 2 iodothyronine deiodinase plays a critical role in regulating the amount of active thyroid hormone, triiodothyronine, in brown fat, thereby modulating adaptive thermogenesis.
“Type 2 iodothyronine deiodinase plays a critical role in regulating the amount of active thyroid hormone, triiodothyronine, in brown fat, thereby modulating adaptive thermogenesis 64,65.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [65]

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Epinephrine mediates facultative carbohydrate-induced thermogenesis in human skeletal muscle
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GDP binding to rat brown fat mitochondria: effects of thyroxine at different ambient temperatures
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Thyroid hormone and norepinephrine signaling in brown adipose tissue. II: Differential effects of thyroid hormone on beta 3-adrenergic receptors in brown and white adipose tissue.
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Cloning and functional characterization of an uncoupling protein homolog in hummingbirds
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Concomitant interindividual variation in body temperature and metabolic rate
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Changes in energy metabolism in response to 48 h of overfeeding and fasting in Caucasians and Pima Indians
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“The responses are genetically determined (33, 252), and in general there is correlation between the increase in energy expenditure with overfeeding and its reduction in fasting, defining a range from spend-thrift to thrifty phenotypes (252).”
Background
Malignant Hyperthermia: A Pharmacogenetic Disease of Ca++ Regulating Proteins
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Thyroid Thermogenesis
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The Uncoupling Protein UCP1 Does Not Increase the Proton Conductance of the Inner Mitochondrial Membrane by Functioning as a Fatty Acid Anion Transporter
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Interrelationships among thyroxine, growth hormone, and the sympathetic nervous system in the regulation of 5'-iodothyronine deiodinase in rat brown adipose tissue.
Silva, J. E., & Larsen, P. R. (1986) · Journal of Clinical Investigation · doi:10.1172/jci112424 · Cited by 84 · see citing works
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Influence of thyroid hormone status on expression of genes encoding G protein subunits in the rat heart.
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Stimulation of glucose transport by insulin and norepinephrine in isolated rat brown adipocytes
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The role of thyroid hormone in amphibian metamorphosis
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Normal Thyroid Thermogenesis but Reduced Viability and Adiposity in Mice Lacking the Mitochondrial Glycerol Phosphate Dehydrogenase
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Sequence and tissue-dependent RNA expression of mouse FAD-linked glycerol-3-phosphate dehydrogenase
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“In the mouse, skeletal muscle ranks second, next to BAT in mGPD abundance, followed by brain, kidney, and liver (136), which we have just confirmed (3).”
Background
Effects of thyroid hormone on norepinephrine signaling in brown adipose tissue. I. Beta 1- and beta 2-adrenergic receptors and cyclic adenosine 3',5'-monophosphate generation
Rubio, A., Raasmaja, A., Maia, A. L., Kim, K. R., & Silva, J. E. (1995) · Endocrinology · doi:10.1210/endo.136.8.7628360 · Cited by 75 · see citing works
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Thyroid Hormones Regulate G-protein β-Subunit mRNA Expression in Vivo
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Mouse Lacking NAD+-Linked Glycerol Phosphate Dehydrogenase Has Normal Pancreatic Beta Cell Function But Abnormal Metabolite Pattern in Skeletal Muscle
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Cardiovascular hemodynamics and exercise tolerance in thyroid disease
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Expression of an uncoupling protein gene homolog in chickens
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Elevated Regional Lipolysis in Hyperthyroidism
Riis, A. L., Gravholt, C. H., Djurhuus, C., Nørrelund, H., Jørgensen, J. O. L., Weeke, J., & Møller, N. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020174 · Cited by 72 · see citing works
Glucagon in physiological concentrations stimulates brown fat thermogenesis in vivo
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3,5,3′-Triiodothyronine actively stimulates UCP in brown fat under minimal sympathetic activity
Branco, M., Ribeiro, M. O., Negrão, N., & Bianco, A. C. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.276.1.e179 · Cited by 70 · see citing works
α1- and β-Adrenergic Agents Cause Synergistic Stimulation of the Iodothyronine Deiodinase in Rat Brown Adipocytes*
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Feedback regulation of thyrotropin-releasing hormone (TRH): mechanisms for the non-thyroidal illness syndrome.
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Interactions among receptors, thyroid hormone response elements, and ligands in the regulation of the rat uncoupling protein gene expression by thyroid hormone
Rabelo, R., Reyes, C., Schifman, A. L., & Silva, J. E. (1996) · Endocrinology · doi:10.1210/endo.137.8.8754777 · Cited by 68 · see citing works
Self-citation
Hormonal regulation of iodothyronine 5'-deiodinase in rat brown adipose tissue
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The multiple contributions of thyroid hormone to heat production
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The Regulation of Lipogenesis by Thyroid Hormone and Its Contribution to Thermogenesis*
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Thyroid calorigenesis in isolated, perfused rat liver: minor role of active sodium‐potassium transport.
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Temperature Homeostasis in Transgenic Mice Lacking Thyroid Hormone Receptor-α Gene Products
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X-Linked Glycerol Kinase Deficiency in the Mouse Leads to Growth Retardation, Altered Fat Metabolism, Autonomous Glucocorticoid Secretion and Neonatal Death
Huq, A. H. M. M., Lovell, R. S., Ou, C. N., Beaudet, A. L., & Craigen, W. J. (1997) · Human Molecular Genetics · doi:10.1093/hmg/6.11.1803 · Cited by 66 · see citing works
The multiple contributions of thyroid hormone to heat production
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Role of the Sarcoplasmic Reticulum Ca2+-ATPase on Heat Production and Thermogenesis
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Mitochondrial uncoupling proteins in mammals and plants
Borecký, J., Maia, I. G., & Arruda, P. (2001) · Bioscience Reports · doi:10.1023/a:1013604526175 · Cited by 63 · see citing works
Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans)
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An Analysis of the Interrelationship of Nuclear and Plasma Triiodothyronine in the Sea Lamprey, Lake Trout, and Rat: Evolutionary Considerations*
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EFFECTS OF HYPOTHYROIDISM ON THE BROWN ADIPOSE TISSUE OF ADULT RATS: COMPARISON WITH THE EFFECTS OF ADAPTATION TO COLD
Mory, G., Ricquier, D., Pesquiès, P., & Hemon, P. (1981) · Journal of Endocrinology · doi:10.1677/joe.0.0910515 · Cited by 62 · see citing works
Adrenaline: a physiological metabolic regulatory hormone in humans?
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Corticosterone inhibits uncoupling protein gene expression in brown adipose tissue
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Thyroid Hormones and Thermogenesis
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Life without UCP1: mitochondrial, cellular and organismal characteristics of the UCP1-ablated mice
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Impaired metabolic response to nerve stimulation in brown adipose tissue of hypothyroid rats
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Control of energy fluxes by the sarcoplasmic reticulum Ca2+‐ATPase: ATP hydrolysis, ATP synthesis and heat production
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Evidence for a Compensated Thermogenic Defect in Transgenic Mice Lacking the Mitochondrial Glycerol-3-Phosphate Dehydrogenase Gene
Eichler, R. A. D. S., Alfadda, A. A., Eto, K., Kadowaki, T., & Silva, J. E. (2003) · Endocrinology · doi:10.1210/en.2003-0687 · Cited by 58 · see citing works
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Thyroid Hormone Regulation of Metabolism
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Self-citation
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Acute sleep deprivation increases portion size and affects food choice in young men
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“Substrate cycles may account for a significant fraction of ATP consumption, and modulation of their activity may increase heat production and energy expenditure (88,106).”
Background
Expression of mitochondrial biogenesis-signaling factors in brown adipocytes is influenced specifically by 17β-estradiol, testosterone, and progesterone
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Moderate weight loss is sufficient to affect thyroid hormone homeostasis and inhibit its peripheral conversion
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Authors: Silva, J. E.
Affiliations: Tufts University (US)
Corresponding author: Silva, J. Enrique
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2006-04
Volume: 86
Issue: 2
Pages: 435-464
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00009.2005
OpenAlex: W2138100786
Semantic Scholar: 00ce1a7b56e3ef95245359effdc4ed7029d78779
Cited by: 687
References: 259
Citations by year: 2026: 19 · 2025: 34 · 2024: 28 · 2023: 32 · 2022: 37 · 2021: 34 · 2020: 32 · 2019: 32 · 2018: 23 · 2017: 35 · 2016: 39 · 2015: 25 · 2014: 46 · 2013: 42 · 2012: 47
FWCI: 3.95
Type: journal article
Language: en
Open access: closed
Locations: Physiological Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Health Sciences › Medicine › Physiology › Thermoregulation and physiological responses
Keywords: thermogenesis, homeothermy, thyroid hormones, sympathetic nervous system, proton leak, brown adipose tissue, iodothyronine deiodinase, type 2 deiodinase, ATP consumption, proton motive force, cold adaptation, food availability, temperature homeostasis, birds
MeSH terms: Animals, Homeostasis, Hormones, Humans, Sympathetic Nervous System, Thyroid Hormones, Thermogenesis

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Thermogenic Mechanisms and Their Hormonal Regulation

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