Cited by 1,602Adipose Tissue and MetabolismLipid metabolism and biosynthesisPeroxisome Proliferator-Activated Receptors

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Thermogenic mechanisms in brown fat.

Nicholls, D G, Locke, R M·1984·Physiological Reviews

DOI 10.1152/physrev.1984.64.1.1

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“in [2]).”
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“…function Dissipating energy as heat production Storing energy as triglycerides Smith and Roberts (1964) Mitochondria Abundant Low Heaton (1972), Nicholls and Locke (1984) UCP1 High Nearly undetectable Virtanen et al. (2009), Svensson et al. (2011) Biomarkers UCP1, LHX8, and ZIC1, MPZL2, HOXC9,…”
Background
Incendiary Leptin
Seoane‐Collazo, P., Martínez‐Sánchez, N., Milbank, E., & Contreras, C. (2020) · Nutrients · doi:10.3390/nu12020472 · Cited by 61
“UCP1 provides an alternative way to return protons to the mitochondrial matrix, bypassing ATP synthase and producing heat via thermogenesis [17,23,24].”
Background
Gene expression, tissue distribution and potential physiological role of uncoupling protein in avian species
Dridi, S., Onagbesan, O. M., Swennen, Q., Buyse, J. G., Decuypere, E. M. P., & Taouis, M. (2004) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpb.2004.09.010 · Cited by 56
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“…and Rodents, Institute of Zoology, Chinese Academy of Sciences, 25 Beisihuan Xilu, Haidian Beijing 100080, China e-mail: wangdh@ioz.ac.cn J.-M. Wang Graduate School of the Chinese Academy of Sciences, Beijing 100049, China (Nicholls and Locke 1984; Cannon and Nedergaard 2004; Krauss et al. 2005).”
Background
Transformed but not normal hepatocytes express UCP2
Carretero, M. V., Torres, L., Latasa, M. U., García–Trevijano, E. R., Prìeto, J., Mato, J. M., & Avila, M. A. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01335-0 · Cited by 54
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Cold-induced changes in the energy coupling and the UCP3 level in rodent skeletal muscles
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Background
Activity of hepatic fatty acid oxidation enzymes in rats fed α-linolenic acid
Kabir, Y., & Ide, T. (1996) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/s0005-2760(96)00110-5 · Cited by 54
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Voltage-gated potassium channels in brown fat cells.
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Respiratory uncoupling by UCP1 and UCP2 and superoxide generation in endothelial cell mitochondria
Fink, B. D., Reszka, K. J., Herlein, J. A., Mathahs, M. M., & Sivitz, W. I. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00332.2004 · Cited by 53
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“UCPs were originally discovered as heat dissipation catalyzers involved in the thermogenic capacity of brown adipose tissue (Nicholls and Locke 1984).”
Background
Brown Adipose Tissue Ca2+-ATPase
MEIS, L. D. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m308280200 · Cited by 52
Mitochondrial proton leak in brown adipose tissue mitochondria of Ucp1 -deficient mice is GDP insensitive
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“These data were unexpected; 1 mM GDP is well known to inhibit the activity of UCP1 in BAT mitochondria (15, 36).”
Background
Effect of adenosine deaminase, N6-phenylisopropyladenosine and hypothyroidism on the responsiveness of rat brown adipocytes to noradrenaline
Woodward, J., & SAGGERSON, E. D. (1986) · Biochemical Journal · doi:10.1042/bj2380395 · Cited by 53
Evidence for masking of brown adipose tissue mitochondrial GDP-binding sites in response to fasting in rats made obese by dietary manipulation. Effects of reversion to standard diet
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Obesity research springs a proton leak
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Expression of UCP3 in CHO cells does not cause uncoupling, but controls mitochondrial activity in the presence of glucose
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The mitochondrial uncoupling protein: structural and genetic studies.
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“Literature related to brown fat metabolism is voluminous (Nicholls 1983; Nicholls and Locke 1984; Himms-Hagen 1985, 1989; Smith et al. 2004) and is briefly summarised here.”
Background
Brown adipose tissue dynamics in wild-type and UCP1-knockout mice: in vivo insights with magnetic resonance
Grimpo, K., Völker, M. N., Heppe, E. N., Braun, S., Heverhagen, J. T., & Heldmaier, G. (2013) · Journal of Lipid Research · doi:10.1194/jlr.m042895 · Cited by 52
The Mitochondrial Uncoupling Protein UCP1: A Gated Pore
Aréchaga, I., Ledesma, A., & Rial, E. (2001) · IUBMB Life · doi:10.1080/15216540152845966 · Cited by 51
“Its activity is regulated by purine nucleotides (inhibitors) and non-esterified fatty acids (activators) (1).”
BackgroundInfluential
Functional characterization of UCP1 in mammalian HEK293 cells excludes mitochondrial uncoupling artefacts and reveals no contribution to basal proton leak
Jastroch, M., Hirschberg, V., & Klingenspor, M. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.05.014 · Cited by 53
Perilipin regulates the thermogenic actions of norepinephrine in brown adipose tissue
Souza, S. C., Christoffolete, M. A., Ribeiro, M. O., Miyoshi, H., Strissel, K. J., Stancheva, Z. S., Rogers, N. H., D'Eon, T. M., Perfield, J. W., Imachi, H., et al. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m700047-jlr200 · Cited by 52
Quantifying and Localizing the Mitochondrial Proteome Across Five Tissues in A Mouse Population
Williams, E. G., Wu, Y., Wolski, W., Kim, J. Y., Lan, J., Hasan, M., Halter, C., Jha, P., Ryu, D., Auwerx, J. H., et al. (2018) · Molecular & Cellular Proteomics · doi:10.1074/mcp.ra118.000554 · Cited by 51
“This aligns to function, as BAT predominantly uses the ETC for mitochondrial uncoupling to generate heat (27), bypassing CV.”
Background
Perinatal thermogenesis
Gunn, T. R., & Gluckman, P. D. (1995) · Early Human Development · doi:10.1016/0378-3782(95)01647-l · Cited by 51
Brown Fat UCP1 Is Specifically Expressed in Uterine Longitudinal Smooth Muscle Cells
Nibbelink, M. M., Moulin, K., Arnaud, E., Duval, C., Pénicaud, L., & Casteilla, L. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105658200 · Cited by 52
Activation by ATP of a proton‐conducting pathway in yeast mitochondria
Prieto, S., Bouillaud, F., Ricquier, D., & Rial, E. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb17212.x · Cited by 52
Factors affecting brown adipose tissue activity in animals and man
Ricquier, D., & Mory, G. (1984) · Clinics in Endocrinology and Metabolism · doi:10.1016/s0300-595x(84)80035-3 · Cited by 52
Choosing an Adipose Tissue Depot for Sampling
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Hyperthermic Syndromes Induced by Toxins
Rusyniak, D. E., & Sprague, J. E. (2006) · Clinics in Laboratory Medicine · doi:10.1016/j.cll.2006.01.007 · Cited by 51
Nonshivering Thermogenesis in Marsupials: Absence of Thermogenic Response to β3-Adrenergic Agonists
Nicol, S. C., Pavlides, D., & Andersen, N. A. (1997) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/s0300-9629(96)00357-x · Cited by 51
Genetic suppression of ghrelin receptors activates brown adipocyte function and decreases fat storage in rats
Mano‐Otagiri, A., Iwasaki-Sekino, A., Nemoto, T., Ohata, H., Shuto, Y., Nakabayashi, H., Sugihara, H., Oikawa, S., & Shibasaki, T. (2009) · Regulatory Peptides · doi:10.1016/j.regpep.2009.11.010 · Cited by 51
Participation of ATP/ADP antiporter in oleate- and oleate hydroperoxide-induced uncoupling suppressed by GDP and carboxyatractylate
Khailova, L. S., Prikhodko, E. A., Dedukhova, V. I., MOKHOVA, E. N., Popov, V. N., & Skulachev, V. P. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.04.024 · Cited by 51
“It is well established that proton conductance induced byUCP1 in the presence of fatty acids is suppressed by GDP, GTP, ADP, and ATP (for reviews, see [3,4]).”
Background
Regulation of the uncoupling protein in brown adipose tissue.
LaNoue, K. F., Strzelecki, T., Strzelecka, D., & Koch, C. D. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42469-0 · Cited by 51
Pathophysiology of Childhood Obesity
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Effects of forced uncoupling protein 1 expression in 3T3–L1 cells on mitochondrial function and lipid metabolism.
Si, Y., Palani, S., Jayaraman, A., & Lee, K. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m600343-jlr200 · Cited by 50
“Zucker diabetic fatty rats injected with an adenoviral vector carrying rat leptin cDNA exhibited mitochondrial biogenesis and increased expression of peroxisome proliferator-activated receptor g coactivator-1a, UCP1, and UCP2 in the WAT (17).”
BackgroundInfluential
Browning Epicardial Adipose Tissue: Friend or Foe?
Doukbi, E., Soghomonian, A., Sengenès, C., Ahmed, S., Ancel, P., Dutour, A., & Gaborit, B. (2022) · Cells · doi:10.3390/cells11060991 · Cited by 60
“This protein inserted in the inner membrane of the mitochondria can be activated by cold exposure or food intake and acts as a proton channel that dissipates the electrochemical gradient produced by the oxidative phosphorylation without allowing the synthesis of ATP, the energy is then released as heat [122,123].”
Background
Deletion of Inducible Nitric-Oxide Synthase in Leptin-Deficient Mice Improves Brown Adipose Tissue Function
Becerril, S., Rodrı́guez, A., Catalán, V., Sáinź, N., Ramírez, B., Collantes, M., Peñuelas, I., Gómez‐Ambrosi, J., & Frühbeck, G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010962 · Cited by 50
“The activation of BAT has been evidenced to play an important role in energy expenditure [47].”
Background
Control and Physiological Determinants of Sympathetically Mediated Brown Adipose Tissue Thermogenesis
Richard, D., Monge-Roffarello, B., Chechi, K., Labbé, S. M., & Turcotte, É. E. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00036 · Cited by 51
“…February 2012 | Volume 3 | Article 36 | 1 UCP1 is a mitochondrial inner membrane protein that is capable of uncoupling mitochondrial oxidation from ATP synthesis, in a process that triggers heat production through enhanced cellular respiration (Nicholls and Locke, 1984).”
BackgroundInfluential
Contrast-Enhanced Ultrasound: A Novel Noninvasive, Nonionizing Method for the Detection of Brown Adipose Tissue in Humans
Flynn, A. W., Li, Q., Panagia, M., Abdelbaky, A., MacNabb, M. H., Samir, A. E., Cypess, A. M., Weyman, A. E., Tawakol, A. A., & Scherrer‐Crosbie, M. (2015) · Journal of the American Society of Echocardiography · doi:10.1016/j.echo.2015.06.014 · Cited by 50
Regulation of UCP1 and UCP3 in arctic ground squirrels and relation with mitochondrial proton leak
Barger, J. L., Barnes, B. M., & Boyer, B. B. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01260.2005 · Cited by 49
“UCP1 is a transmembrane protein located in the mitochondrial inner membrane, which, on activation by the sympathetic nervous system, allows for protons to reenter the mitochondrial matrix without passing through ATP synthase.”
BackgroundInfluential
Transformation of Skeletal Muscle from Fast- to Slow-Twitch during Acquisition of Cold Tolerance in the Chick
Hirabayashi, M., Ijiri, D., Kamei, Y., Tajima, A., & KANAI, Y. (2004) · Endocrinology · doi:10.1210/en.2004-0723 · Cited by 50
Iron, Thermoregulation, and Metabolic Rate
Rosenzweig, P. H., & Volpe, S. L. (1999) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408399908500491 · Cited by 50
Abnormal mitochondrial bioenergetics and heart rate dysfunction in mice lacking very-long-chain acyl-CoA dehydrogenase
Exil, V. J., Gardner, C. D., Rottman, J. N., et al. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00811.2005 · Cited by 50
The effects of l -arginine and l -NAME supplementation on redox-regulation and thermogenesis in interscapular brown adipose tissue
Otašević, V., Korać, A., Buzadžić, B., & Korać, B. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01895 · Cited by 50
“Thermogenesis in brown adipocytes is related to the presence of a specific mitochondrial protein, UCP1 (uncoupling protein 1; Nicholls and Locke, 1984).”
Background
Induction of Uncoupling Protein Expression in Brown and White Adipose Tissue by Leptin
Commins, S. P. (1999) · Endocrinology · doi:10.1210/en.140.1.292 · Cited by 50
Membrane responses to norepinephrine in cultured brown fat cells.
Lucero, M. T., & Pappone, P. A. (1990) · The Journal of General Physiology · doi:10.1085/jgp.95.3.523 · Cited by 50
Topogenesis of mitochondrial inner membrane uncoupling protein. Rerouting transmembrane segments to the soluble matrix compartment.
Liu, X. J., Bell, A. W., Freeman, K. B., et al. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.107.2.503 · Cited by 50
Adipose tissue plasticity and the pleiotropic roles of BMP signaling
Qian, S., Tang, Y., & Tang, Q. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100678 · Cited by 56
Pleiotropic effects of apolipoprotein C3 on HDL functionality and adipose tissue metabolic activity
Zvintzou, E., Lhomme, M., Chasapi, S., Filou, S., Theodoropoulos, V., Xapapadaki, E., Kontush, A., Spyroulias, G. A., Tellis, C. C., Tselepis, A. D., et al. (2017) · Journal of Lipid Research · doi:10.1194/jlr.m077925 · Cited by 48
“ylation is uncoupled from respiration (66).”
ATP-induced unspecific channel in yeast mitochondria.
Guérin, B., Bunoust, O., Rouqueys, V., et al. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47264-x · Cited by 49
Fundamental mechanisms of thermogenesis
Ricquier, D. (2006) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2005.10.010 · Cited by 47
“Newborn humans exposed to cold are incapable of shivering, and the thermogenic activity of BAT maintains the body temperature [5–8].”
BackgroundInfluential
Effects of magnesium and nucleotides on the proton conductance of rat skeletal-muscle mitochondria
Cadenas, S., & Brand, M. D. (2000) · Biochemical Journal · doi:10.1042/bj3480209 · Cited by 50
Obesity in Insulin Receptor Substrate‐2–Deficient Mice: Disrupted Control of Arcuate Nucleus Neuropeptides
Masaki, T., Chiba, S., Noguchi, H., Yasuda, T., Tobe, K., Suzuki, R., Kadowaki, T., & Yoshimatsu, H. (2004) · Obesity Research · doi:10.1038/oby.2004.106 · Cited by 49
Cold-Induced Changes in Gene Expression in Brown Adipose Tissue: Implications for the Activation of Thermogenesis
Watanabe, M., Yamamoto, T., Mori, C., Okada, N., Yamazaki, N., Kajimoto, K., Kataoka, M., & Shinohara, Y. (2008) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.31.775 · Cited by 46
The Potential Use of Piglets as Human Pediatric Surrogate for Preclinical Pharmacokinetic and Pharmacodynamic Drug Testing
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Mitochondrial bioenergetics and redox dysfunctions in hypercholesterolemia and atherosclerosis
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The Murine Misty Mutation: Phenotypic Effects on Melanocytes, Platelets and Brown Fat
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A 211-bp enhancer of the rat uncoupling protein-1 (UCP-1) gene controls specific and regulated expression in brown adipose tissue
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Acute Central Infusion of Leptin Modulates Fatty Acid Mobilization by Affecting Lipolysis and mRNA Expression for Uncoupling Proteins
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Mitochondrial Uncoupling Proteins: New Perspectives for Evolutionary Ecologists
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“In the mid-1980s, the coupling of oxidative phosphorylation was found to be impaired by a speciﬁc transporter in the brown adipose tissue (BAT) of rodents, the uncoupling protein 1 (UCP1; Nicholls and Locke 1984; Aquila et al. 1985; Bouillaud et al. 1986).”
Thyroxine 5'-Deiodination Mediates Norepinephrine-Induced Lipogenesis in Dispersed Brown Adipocytes
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“Based on published values for BAT lipogenesis (2) and oxygen consumption of animals acclimated at room temperature (9), it has been estimated that the caloric cost of BAT lipogenesis is ;10% of the total BAT oxygen consumption, a figure that is expected to rise during cold stimulation.”
Background
Energy restriction with high-fat diet enriched with coconut oil gives higher UCP1 and lower white fat in rats
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“Brown adipocytes are highly oxidative cells that release energy as heat (10, 11) thanks to their high mitochondrial content and to the expression of UCP1.”
Background
Adipose tissue insulin receptor knockdown via a new primate-derived hybrid recombinant AAV serotype
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Identification of a Ca2+-ATPase in Brown Adipose Tissue Mitochondria
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The effects of endurance training and exhaustive exercise on mitochondrial enzymes in tissues of the rat (Rattus norvegicus)
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Dramatic enhancement of the specific expression of the heart‐type fatty acid binding protein in rat brown adipose tissue by cold exposure
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Prevention of cold-induced increase in blood pressure of rats by captopril.
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Mitochondrial energetic metabolism—some general principles
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“In the case of UCP1, which is mainly expressed in brown adipose tissue, the Hþ transport function is well-established and highly regulated by guanosine triphosphate (GTP) (inhibition) and fatty acids (stimulation) (16).”
Background

Authors: Nicholls, D. G., & Locke, R. M.
ORCID: Nicholls, D G
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 1984-01
Volume: 64
Issue: 1
Pages: 1-64
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.1984.64.1.1
OpenAlex: W1900866157
Cited by: 1,602
References: 0
Citations by year: 2026: 10 · 2025: 14 · 2024: 24 · 2023: 21 · 2022: 33 · 2021: 28 · 2020: 36 · 2019: 34 · 2018: 40 · 2017: 36 · 2016: 45 · 2015: 35 · 2014: 42 · 2013: 38 · 2012: 34
FWCI: 44.71
Type: journal article
Language: en
Open access: closed
Locations: Physiological Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
Keywords: brown adipose tissue, thermogenesis, non-shivering thermogenesis, UCP1, mitochondrial respiration, energy expenditure
MeSH terms: Adaptation, Physiological, Cyclic AMP, Adenosine Triphosphate, Animals, Biomechanical Phenomena, Body Temperature Regulation, Adipose Tissue, Brown, Carrier Proteins, Cyclic AMP Receptor Protein, Cell Physiological Phenomena, Central Nervous System, Chlorides, Cytosol, Diet, Fatty Acids, Cricetinae, Hibernation, Hydrogen-Ion Concentration, Insulin, Lipolysis, Mitochondria, Obesity, Oxidation-Reduction, Permeability, Protein Kinases, Proteins, Protons, Receptors, Adrenergic, beta, Respiratory Physiological Phenomena, Sympathetic Nervous System, Thyroid Hormones, Time Factors, Mice, Rats

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