Brown Adipose Tissue: Function and Physiological Significance

CANNON, BARBARA; NEDERGAARD, JAN

doi:10.1152/physrev.00015.2003

Cited by 6,433Adipose Tissue and MetabolismLipid metabolism and biosynthesisAdipokines, Inflammation, and Metabolic Diseases

Brown Adipose Tissue: Function and Physiological Significance

CANNON, BARBARA, NEDERGAARD, JAN·2004·Physiological Reviews

DOI 10.1152/physrev.00015.2003

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Abstract

Cannon, Barbara, and Jan Nedergaard. Brown Adipose Tissue: Function and Physiological Significance. Physiol Rev 84: 277–359, 2004; 10.1152/physrev.00015.2003.—The function of brown adipose tissue is to transfer energy from food into heat; physiologically, both the heat produced and the resulting decrease in metabolic efficiency can be of significance. Both the acute activity of the tissue, i.e., the heat production, and the recruitment process in the tissue (that results in a higher thermogenic capacity) are under the control of norepinephrine released from sympathetic nerves. In thermoregulatory thermogenesis, brown adipose tissue is essential for classical nonshivering thermogen-esis (this phenomenon does not exist in the absence of functional brown adipose tissue), as well as for the cold acclimation-recruited norepinephrine-induced thermogenesis. Heat production from brown adipose tissue is activated whenever the organism is in need of extra heat, e.g., postnatally, during entry into a febrile state, and during arousal from hibernation, and the rate of thermogenesis is centrally controlled via a pathway initiated in the hypothalamus. Feeding as such also results in activation of brown adipose tissue; a series of diets, apparently all characterized by being low in protein, result in a leptin-dependent recruitment of the tissue; this metaboloregulatory thermogenesis is also under hypothalamic control. When the tissue is active, high amounts of lipids and glucose are combusted in the tissue. The development of brown adipose tissue with its characteristic protein, uncoupling protein-1 (UCP1), was probably determinative for the evolutionary success of mammals, as its thermogenesis enhances neonatal survival and allows for active life even in cold surroundings.

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Acting via the sympathetic nervous system, the hypothalamus is a key effector of CNS influence on adipose tissue, including response to cold.
“Acting via the sympathetic nervous system32,43,44. the hypothalamus is a key effector of CNS influence on adipose tissue, including response to cold.”
From IDOL regulates systemic energy balance through control of neuronal VLDLR expression (2019) · cites this paper as [32]
BAT burning power intensely clears and oxidizes circulating lipids and glucose to generate heat.
“Thus, BAT burning power intensely clears and oxidizes circulating lipids and glucose to generate heat ([17](#B17)).”
From Mitochondrial fatty acid oxidation in obesity (2013) · cites this paper as [17]
In response to cold exposure or overfeeding, norepinephrine released from the SNS regulates brown adipocytes at multiple levels: it promotes proliferation and differentiation of brown preadipocytes, directly regulates the thermogenic program of BAT by activation of UCP1 gene, and protects brown adipocytes from TNFα-induced apoptosis.
“In response to cold exposure or overfeeding, norepinephrine released from the SNS regulates brown adipocytes at multiple levels: it promotes proliferation and differentiation of brown preadipocytes, directly regulates the thermogenic program of BAT by activation of UCP1 gene, and protects brown adipocytes from TNFα-induced apoptosis 63.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [63]
Mammals have BAT, a highly specialized tissue that functions to produce heat.
“Mammals have BAT, a highly specialized tissue that functions to produce heat 73.”
From Inter‐organ communication: a gatekeeper for metabolic health (2019) · cites this paper as [73]
Free fatty acids resulting from lipolysis are used both as energy substrates and as activators of UCP1 to uncouple ATP production from mitochondrial respiration into heat.
“Free fatty acids, resulting from lipolysis, are used both as energy substrates and as activators of UCP1 to uncouple ATP production from mitochondrial respiration into heat 73, 85.”
From Inter‐organ communication: a gatekeeper for metabolic health (2019) · cites this paper as [73]

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Development of brown fat cells in monolayer culture
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Structure and Expression of a Novel Member, FGF-16, of the Fibroblast Growth Factor Family
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Dissociation of leptin secretion and adiposity during prehibernatory fattening in little brown bats
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Targeted Disruption of Histamine H1-Receptor Attenuates Regulatory Effects of Leptin on Feeding, Adiposity, and UCP Family in Mice
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Tumor necrosis factor α mediates apoptosis of brown adipocytes and defective brown adipocyte function in obesity
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Adipose Tissue as an Endocrine Organ
Kershaw, E. E., & Flier, J. S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0395 · Cited by 5,522 · see citing works
Identification and Importance of Brown Adipose Tissue in Adult Humans
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Functional Brown Adipose Tissue in Healthy Adults
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Thyroid Hormone Regulation of Metabolism
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What we talk about when we talk about fat
Rosen, E. D., & Spiegelman, B. M. (2014) · Cell · doi:10.1016/j.cell.2013.12.012 · Cited by 2,373 · see citing works
PRDM16 controls a brown fat/skeletal muscle switch
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Brown and beige fat: Development, function and therapeutic potential
Harms, M., & Seale, P. (2013) · Nature Medicine · doi:10.1038/nm.3361 · Cited by 2,328 · see citing works
PPARγ signaling and metabolism: the good, the bad and the future
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High Incidence of Metabolically Active Brown Adipose Tissue in Healthy Adult Humans
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Unexpected evidence for active brown adipose tissue in adult humans
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Transcriptional paradigms in mammalian mitochondrial biogenesis and function
Scarpulla, R. C. (2008) · Physiological Reviews · doi:10.1152/physrev.00025.2007 · Cited by 1,666 · see citing works
Brown adipose tissue activity controls triglyceride clearance
Bartelt, A., Bruns, O. T., Reimer, R., Hohenberg, H., Ittrich, H., Peldschus, K., Kaul, M. G., Tromsdorf, U. I., Weller, H., Waurisch, C., et al. (2011) · Nature Medicine · doi:10.1038/nm.2297 · Cited by 1,608 · see citing works
Adipose tissue distribution, inflammation and its metabolic consequences, including diabetes and cardiovascular disease
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Developmental Origin of Fat: Tracking Obesity to Its Source
Gesta, S., Tseng, Y.-H., & Kahn, C. R. (2007) · Cell · doi:10.1016/j.cell.2007.10.004 · Cited by 1,508 · see citing works
Mitochondrial electron transport chain: Oxidative phosphorylation, oxidant production, and methods of measurement
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Mitochondrial Dynamics in the Regulation of Nutrient Utilization and Energy Expenditure
Liesa, M., & Shirihai, O. S. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.03.002 · Cited by 1,341 · see citing works
UCP1 Ablation Induces Obesity and Abolishes Diet-Induced Thermogenesis in Mice Exempt from Thermal Stress by Living at Thermoneutrality
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Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network
Scarpulla, R. C. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.09.019 · Cited by 1,281 · see citing works
Mitochondrial Oxidative Stress: Implications for Cell Death
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Fever and the thermal regulation of immunity: the immune system feels the heat
Evans, S. S., Repasky, E. A., & Fisher, D. T. (2015) · Nature reviews. Immunology · doi:10.1038/nri3843 · Cited by 1,267 · see citing works
Chronic Peroxisome Proliferator-activated Receptor γ (PPARγ) Activation of Epididymally Derived White Adipocyte Cultures Reveals a Population of Thermogenically Competent, UCP1-containing Adipocytes Molecularly Distinct from Classic Brown Adipocytes
Petrovic, N., Walden, T. B., Shabalina, I. G., Timmons, J. A., Cannon, B., & Nedergaard, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.053942 · Cited by 1,263 · see citing works
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Adipose tissue browning and metabolic health
Bartelt, A., & Heeren, J. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.204 · Cited by 1,177 · see citing works
Transcriptional Control of Brown Fat Determination by PRDM16
Seale, P., Kajimura, S., Yang, W., Chin, S., Rohas, L. M., Uldry, M., Tavernier, G., Langin, D., & Spiegelman, B. M. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.06.001 · Cited by 1,174 · see citing works
Adipose-tissue plasticity in health and disease
Sakers, A. P., Siqueira, M. K. D., Seale, P., & Villanueva, C. J. (2022) · Cell · doi:10.1016/j.cell.2021.12.016 · Cited by 1,061 · see citing works
Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis
Nguyen, K. D., Qiu, Y., Cui, X., Goh, Y. P. S., Mwangi, J., David, T., Mukundan, L., Brombacher, F., Locksley, R. M., & Chawla, A. (2011) · Nature · doi:10.1038/nature10653 · Cited by 1,038 · see citing works
Anti-obesity drug discovery: advances and challenges
Müller, T. D., Blüher, M., Tschöp, M. H., & DiMarchi, R. D. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00337-8 · Cited by 1,021 · see citing works
Brown and Beige Fat: Physiological Roles beyond Heat Generation
Kajimura, S., Spiegelman, B. M., & Seale, P. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.09.007 · Cited by 1,004 · see citing works
Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans
Ouellet, V., Labbé, S. M., Blondin, D. P., Phoenix, S., Guérin, B., Haman, F., Turcotte, É. E., Richard, D., & Carpentier, A. C. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60433 · Cited by 985 · see citing works
Mechanism of Fatty-Acid-Dependent UCP1 Uncoupling in Brown Fat Mitochondria
Fedorenko, A., Lishko, P. V., & Kirichok, Y. (2012) · Cell · doi:10.1016/j.cell.2012.09.010 · Cited by 968 · see citing works
Recruited brown adipose tissue as an antiobesity agent in humans
Yoneshiro, T., Aita, S., Matsushita, M., Kayahara, T., Kameya, T., Kawai, Y., Iwanaga, T., & Saito, M. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67803 · Cited by 957 · see citing works
Body size, energy metabolism and lifespan
Speakman, J. R. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01556 · Cited by 914 · see citing works
Hypoxia and Adipose Tissue Function and Dysfunction in Obesity
Trayhurn, P. (2013) · Physiological Reviews · doi:10.1152/physrev.00017.2012 · Cited by 884 · see citing works
Chemerin, a Novel Adipokine That Regulates Adipogenesis and Adipocyte Metabolism
Goralski, K. B., McCarthy, T. C., Hanniman, E. A., Zabel, B. A., Butcher, E. C., Parlee, S. D., Muruganandan, S., & Sinal, C. J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700793200 · Cited by 851 · see citing works
Cold acclimation recruits human brown fat and increases nonshivering thermogenesis
van der Lans, A. A. J. J., Joris Hoeks, J., Brans, B. T., Vijgen, G. H. E. J., Visser, M. G. W., Vosselman, M. J., Hansen, J., Jörgensen, J. A., Wu, J., Mottaghy, F. M., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci68993 · Cited by 841 · see citing works
Mitochondrial proton and electron leaks
Jastroch, M., Divakaruni, A. S., Mookerjee, S., Treberg, J. R., & Brand, M. D. (2010) · Essays in Biochemistry · doi:10.1042/bse0470053 · Cited by 829 · see citing works
Gut Microbiota Orchestrates Energy Homeostasis during Cold
Chevalier, C., Stojanović, O., Colin, D. J., Suarez-Zamorano, N., Tarallo, V., Veyrat-Durebex, C., Rigo, D., Fabbiano, S., Stevanović, A., Hagemann, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.11.004 · Cited by 829 · see citing works
Adaptive thermogenesis in adipocytes: Is beige the new brown?
Wu, J., Cohen, P., & Spiegelman, B. M. (2013) · Genes & Development · doi:10.1101/gad.211649.112 · Cited by 828 · see citing works
Transcriptional integration of mitochondrial biogenesis
Scarpulla, R. C., Vega, R. B., & Kelly, D. P. (2012) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2012.06.006 · Cited by 798 · see citing works
Nitric oxide signalling in cardiovascular health and disease
Farah, C., Michel, L. Y. M., & Balligand, J.-L. (2018) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.224 · Cited by 779 · see citing works
PPARs in Obesity-Induced T2DM, Dyslipidaemia and NAFLD
Gross, B., Pawlak, M., Lefebvre, P., & Staels, B. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.135 · Cited by 778 · see citing works
Bi-directional interconversion of brite and white adipocytes
Rosenwald, M., Perdikari, A., Rülicke, T., & Wolfrum, C. (2013) · Nature Cell Biology · doi:10.1038/ncb2740 · Cited by 792 · see citing works
Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans
Lee, P., Linderman, J. D., Smith, S., Brychta, R. J., Wang, J., Idelson, C., Perron, R. M., Werner, C. D., Phan, G. Q., Kammula, U. S., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2013.12.017 · Cited by 802 · see citing works
Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice
Liu, J., Divoux, A., Sun, J., Zhang, J., Clément, K., Glickman, J. N., Sukhova, G. K., Wolters, P. J., Du, J., Gorgun, C. Z., et al. (2009) · Nature Medicine · doi:10.1038/nm.1994 · Cited by 796 · see citing works
SIRT3 Opposes Reprogramming of Cancer Cell Metabolism through HIF1α Destabilization
Finley, L. W. S., Carracedo, A., Lee, J., Souza, A., Egia, A., Zhang, J., Teruya-Feldstein, J., Moreira, P. I., Cardoso, S. M., Clish, C. B., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.02.014 · Cited by 782 · see citing works
The physiological costs of reproduction in small mammals
Speakman, J. R. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2145 · Cited by 791 · see citing works
Brown Adipose Tissue Improves Whole-Body Glucose Homeostasis and Insulin Sensitivity in Humans
Chondronikola, M., Volpi, E., Børsheim, E., Porter, C. C., Annamalai, P., Enerbäck, S., Lidell, M. E., Saraf, M. K., Labbé, S. M., Hurren, N. M., et al. (2014) · Diabetes · doi:10.2337/db14-0746 · Cited by 789 · see citing works
A Creatine-Driven Substrate Cycle Enhances Energy Expenditure and Thermogenesis in Beige Fat
Kazak, L., Chouchani, E. T., Jedrychowski, M. P., Erickson, B. K., Shinoda, K., Cohen, P., Vetrivelan, R., Lu, G. Z., Laznik-Bogoslavski, D., Hasenfuss, S. C., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.035 · Cited by 787 · see citing works
Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system
Romanovsky, A. A. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00668.2006 · Cited by 786 · see citing works
Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3
Brand, M. D., & Esteves, T. C. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.06.002 · Cited by 785 · see citing works
The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation
Barbatelli, G., Murano, I., Madsen, L., Hao, Q., Jimenez, M., Kristiansen, K., Giacobino, J., Matteis, R. D., & Cinti, S. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00600.2009 · Cited by 751 · see citing works
A Switch from White to Brown Fat Increases Energy Expenditure in Cancer-Associated Cachexia
Petruzzelli, M., Schweiger, M., Schreiber, R., Campos‐Olivas, R., Tsoli, M., Allen, J., Swarbrick, M. M., Rose‐John, S., Rincón, M., Robertson, G. R., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.06.011 · Cited by 752 · see citing works
Irisin Stimulates Browning of White Adipocytes Through Mitogen-Activated Protein Kinase p38 MAP Kinase and ERK MAP Kinase Signaling
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“, triglycerides), whereas brown adipocytes consume energy (5,6).”
Protection from obesity and diabetes by blockade of TGF-β/smad3 signaling
Yadav, H., Quijano, C., Kamaraju, A. K., Gavrilova, O., Malek, R., Chen, W., Zerfas, P., Zhigang, D., Wright, E. C., Stuelten, C., et al. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.04.013 · Cited by 709 · see citing works
Obesity Pathogenesis: An Endocrine Society Scientific Statement
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Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages
Timmons, J. A., Wennmalm, K., Larsson, O., Walden, T. B., Lassmann, T., Petrovic, N., Hamilton, D. L., Gimeno, R. E., Wahlestedt, C., Baar, K., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610615104 · Cited by 732 · see citing works
Self-citation
The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue
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Authors: CANNON, B., & NEDERGAARD, J.
Affiliations: Stockholm University (SE)
ORCID: CANNON, BARBARA
NEDERGAARD, JAN
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2004-01
Volume: 84
Issue: 1
Pages: 277-359
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00015.2003
OpenAlex: W2132358997
Cited by: 6,433
References: 924
Citations by year: 2026: 243 · 2025: 301 · 2024: 317 · 2023: 379 · 2022: 371 · 2021: 440 · 2020: 424 · 2019: 413 · 2018: 444 · 2017: 407 · 2016: 400 · 2015: 338 · 2014: 335 · 2013: 318 · 2012: 262
FWCI: 13.31
Type: journal article
Language: en
Open access: closed
Locations: Physiological Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Keywords: brown adipose tissue, thermogenesis, non-shivering thermogenesis, cold acclimation, norepinephrine, sympathetic nervous system, hypothalamic thermoregulation, leptin, UCP1, energy expenditure, neonatal survival, mammalian evolution
MeSH terms: Animals, Adipose Tissue, Brown, Humans, Norepinephrine, Signal Transduction, Thermogenesis

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Brown Adipose Tissue: Function and Physiological Significance

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