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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“Mitochondria in the brown adipocytes express uncoupling protein-1 (UCP1) which uses lipids and carbohydrates to generate heat by uncoupling electron transport from oxidative phosphorylation [4].”
Background
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González‐García, I., Tena‐Sempere, M., & López, M. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-70178-3_15 · Cited by 35
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Nicholls, D. G. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.03.014 · Cited by 35
“In the intact brown adipocyte β-adrenergic stimulation of lipolysis delivers fatty acids to the mitochondrion (reviewed in [32]).”
BackgroundSelf-citation
Influence of environmental temperature on energy balance, diet-induced thermogenesis and brown fat activity in ‘cafeteria’-fed rats
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Bonet, M. L., Puigserver, P., Serra, F. A., Ribot, J., Vázquez, F., Picó, C., & Palou, A. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00274-3 · Cited by 35
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Uchida, Y., Tsukahara, F., Ohba, K., Ogawa, A., Irie, K., Fujii, E., Yoshimoto, T., Yoshioka, T., & Muraki, T. (1997) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)01181-3 · Cited by 35
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Expression of the mitochondrial uncoupling protein in brown adipocytes
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Lateral hypothalamic lesions and fenfluramine increase thermogenesis in brown adipose tissue
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“(4) Fed and fasting glucose was measured by OneTouch Ultra Glucose meter (LifeScan, Milpitas, CA).”
BackgroundMethod
Conjugated Linoleic Acid Induces Uncoupling Protein 1 in White Adipose Tissue of ob/ob Mice
Wendel, A. A., Purushotham, A., Liu, L., & Belury, M. A. (2009) · Lipids · doi:10.1007/s11745-009-3348-9 · Cited by 33
“Under normal physiological conditions, UCP1 is expressed almost exclusively in BAT, which, unlike white adipose tissue (WAT), is rich in mitochondria and has a high oxidative capacity, thereby contributing to energy expenditure [14, 15].”
Background
Interactions between the melanocortin system and the hypothalamo–pituitary–thyroid axis
Martin, N. M., Smith, K. L., Bloom, S. R., & Small, C. J. (2006) · Peptides · doi:10.1016/j.peptides.2005.01.028 · Cited by 34
Activation by retinoids of the uncoupling protein UCP1
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“[1]).”
Adenine Nucleotide Translocator as a Regulator of Mitochondrial Function: Implication in the Pathogenesis of Metabolic Syndrome
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“In the 1970s, a protein responsible for non-shivering thermogenesis was identified in the inner mitochondrial membrane of brown adipose tissue mitochondria, and was named as uncoupling protein (UCP1) [44].”
Background
The uncoupling protein 1 gene, UCP1, is expressed in mammalian islet cells and associated with acute insulin response to glucose in African American families from the IRAS Family Study
Sale, M. M., Hsu, F., Palmer, N. D., Gordon, C. J., Keene, K. L., Borgerink, H. M., Sharma, A. J., Bergman, R. N., Taylor, K. D., Saad, M. F., et al. (2007) · BMC Endocrine Disorders · doi:10.1186/1472-6823-7-1 · Cited by 34
“While UCP2 is expressed in a variety of tissues [36], UCP1 expression was believed to be largely restricted to brown adipose tissue (BAT) [36-38].”
Background
Molecular Screening of Uncoupling Protein 2 Gene in Patients with Noninsulin-Dependent Diabetes Mellitus or Obesity1
Kubota, T., Mori, H., Tamori, Y., Okazawa, H., FUKUDA, T., Miki, M., Ito, C., Fleury, C., Bouillaud, F., & Kasuga, M. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.8.4994 · Cited by 34
“Uncoupling protein 1 (UCP1), which is expressed exclusively in brown adipose tissue (BAT), contributes to energy expenditure by burning calories and generating heat (9, 10).”
Background
Uncoupling Protein 2, but Not Uncoupling Protein 1, Is Expressed in the Female Mouse Reproductive Tract
Rousset, S., Alves‐Guerra, M., Ouadghiri-Bencherif, S., Kozak, L. P., Miroux, B., Richard, D., Bouillaud, F., Ricquier, D., & Cassard, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306980200 · Cited by 34
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“The thermogenic UCP1 uncouples the respiratory chain from ATP synthesis in brown adipose tissue (BAT) mitochondria (41), but the function of more recently discovered UCPs has not been resolved (40).”
Background
Adaptive thermogenesis: Turning on the heat
Lowell, B. B. (1998) · Current Biology · doi:10.1016/s0960-9822(07)00336-3 · Cited by 34
“This feature is largely due to their abundant mitochondria, which uniquely possess the ability to uncouple fuel oxidation from ATP production, thus generating heat.”
Influential
Mitochondrial respiration in muscle and liver from cold-acclimated hypothyroid rats
Zaninovich, Á. A., Rebagliati, I., Raı́ces, M., Ricci, C. R., & Hagmüller, K. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00363.2003 · Cited by 35
“Brown adipose tissue (BAT) is the main site for adaptive thermogenesis primarily because of the mitochondrial uncoupling protein-1 (UCP-1), which uncouples electron transport from the phosphorylation of ADP and appears to be the only protein able to respond to thermal challenge (31, 30).”
Background
Perindopril Effect on Uncoupling Protein and Energy Metabolism in Failing Rat Hearts
Murakami, K., Mizushige, K., Noma, T., Tsuji, T., Kimura, S., & Kohno, M. (2002) · Hypertension · doi:10.1161/01.hyp.0000029094.85023.01 · Cited by 34
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“Along these lines, Nicholls and Locke (49) established that the mitochondria of heat-adapted guinea-pigs maintain a significantly higher “energy potential” and are less sensitive to uncoupling events.”
Background
A High-Throughput Assay for Mitochondrial Membrane Potential in Permeabilized Yeast Cells
Farrelly, E. R., Amaral, M. C., Marshall, L., et al. (2001) · Analytical Biochemistry · doi:10.1006/abio.2001.5139 · Cited by 33
Effects of Continuous and Intermittent Cold (SART) Stress on Sympathoadrenal System Activity in Rats
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Short- and long-term effects of maternal perinatal undernutrition are lowered by cross-fostering during lactation in the male rat
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Iwai, M., Hell, N. S., & Shimazu, T. (1987) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00581894 · Cited by 33
Purinergic receptor stimulation increases membrane trafficking in brown adipocytes.
Pappone, P. A., & Lee, S. C. (1996) · The Journal of General Physiology · doi:10.1085/jgp.108.5.393 · Cited by 33
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Signaling pathways leading to ischemic mitochondrial neuroprotection
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“Uncoupling was originally thought to be an artifact of mitochondrial isolation, however the discovery of UCP1 (Nicholls and Locke 1984), UCP2 (Fleury et al. 1997) and UCP3 (Boss et al. 1997), as well as the closely related UCP4 (Mao et al. 1999) and 5 (also known as BMCP1) (Sanchis et al. 1998),…”
The Effects of High Fat Diet and Resveratrol on Mitochondrial Activity of Brown Adipocytes
Ku, C. R., Cho, Y. H., Hong, Z.-Y., Lee, H., Lee, S. J., Hong, S. S., & Lee, E. J. (2016) · Endocrinology and Metabolism · doi:10.3803/enm.2016.31.2.328 · Cited by 32
Evolutionary Genetics of Hypoxia and Cold Tolerance in Mammals
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“Consistently, coupling efficiency was lower in patient PBMCs mainly due to respiration associated with alternative proton conductance pathways in those cells, which generally results in heat production at the expense of ATP synthesis (31).”
Background
A critical assessment of the role of creatine in brown adipose tissue thermogenesis
Nicholls, D. G., & Brand, M. D. (2023) · Nature Metabolism · doi:10.1038/s42255-022-00718-2 · Cited by 32
Self-citation
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Metabolic Flux Analysis of Mitochondrial Uncoupling in 3T3-L1 Adipocytes
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Brown fat thermogenesis in cold-acclimated rats is not abolished by the suppression of thyroid function
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A new look at UCP 1
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The molecular and biochemical basis of nonshivering thermogenesis in an African endemic mammal, Elephantulus myurus
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“Furthermore, in rodents, UCP1 increases proton leak in the presence of free-fatty acids, in a GDPsensitive manner (32).”
Background
A threshold membrane potential accounts for controversial effects of fatty acids on mitochondrial oxidative phosphorylation
Köhnke, D., Ludwig, B., & Kadenbach, B. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)81616-8 · Cited by 32
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UCP2 muscle gene transfer modifies mitochondrial membrane potential
Martí, A., Larrarte, E., Novo, F. J., Garcia‐Fernandez, M. I., & Martínez, J. (2001) · International Journal of Obesity · doi:10.1038/sj.ijo.0801484 · Cited by 32
Leptin does not reduce body fat content but augments cold defense abilities in thermoneutrally reared rat pups
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Identification of specific pathways of communication between the CNS and NK cell system
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Partial purification and functional reconstitution of GDP sensitive brown adipose tissue mitochondria uncoupling protein using octyl glucoside
Strieleman, P. J., Schalinske, K. L., & Shrago, E. S. (1985) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(85)80189-3 · Cited by 32
The effects of thyroid hormones on brown adipose tissue in humans: a PET‐CT study
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“Brown adipose tissue (BAT), which specializes in combustion of lipids and releasing energy as heat, is related to energy expenditure in lower mammals [1,2].”
Background
Gene expression survey of mitochondrial uncoupling proteins (UCP1/UCP3) in gilthead sea bream (Sparus aurata L.)
Bermejo-Nogales, A., Calduch-Giner, J. À., & Pérez‐Sánchez, J. (2010) · Journal of Comparative Physiology B · doi:10.1007/s00360-009-0441-6 · Cited by 31
“1978), and has a well-documented role in non-shivering thermogenesis (Nicholls and Locke 1984).”
Background
The Environmental Pollutants Perfluorooctane Sulfonate and Perfluorooctanoic Acid Upregulate Uncoupling Protein 1 (UCP1) in Brown-Fat Mitochondria Through a UCP1-Dependent Reduction in Food Intake
Shabalina, I. G., Kramarova, T. V., Mattsson, C. L., Petrovič, N., Qazi, M. R., Csikasz, R. I., Chang, S., Butenhoff, J. L., DePierre, J. W., Cannon, B., et al. (2015) · Toxicological Sciences · doi:10.1093/toxsci/kfv098 · Cited by 31
Mitochondrial Kinases and the Role of Mitochondrial Protein Phosphorylation in Health and Disease
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Increased locomotor and thermogenic activity in mice with targeted ablation of the GHRH gene
Leone, S., Chiavaroli, A., Shohreh, R., et al. (2015) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2014.12.007 · Cited by 31
“The released free fatty acids are oxidized in mitochondria to serve as an energy source of thermogenesis [6,23].”
Background
Mitochondrial uncoupling protein 1 expression in thymocytes
Adams, A. E., Carroll, A. M., Fallon, P. G., & Porter, R. K. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.04.020 · Cited by 31
Genomic organization and promoter function of the mouse uncoupling protein 2 (UCP2) gene
Yamada, M., Hashida, T., Shibusawa, N., Iwasaki, T., Murakami, M., Monden, T., Satoh, T., & Mori, M. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00835-7 · Cited by 31
The Guanosine Monophosphate Reductase Gene Is Conserved in Rats and Its Expression Increases Rapidly in Brown Adipose Tissue during Cold Exposure
Salvatore, D., Bartha, T., & Larsen, P. R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.47.31092 · Cited by 31
Hypnogenic center theory of sleep: no support from metabolic mapping in monkeys
Nakamura, R., Kennedy, C., Gillin, J. C., Suda, S., Ito, M., Storch, F. I., Mendelson, W. B., Sokoloff, L., & Mishkin, M. (1983) · Brain Research · doi:10.1016/0006-8993(83)90507-3 · Cited by 31
Brown Adipose Tissue Thermogenesis during Pregnancy in Mice
Andrews, J. F., Richard, D., Jennings, G., & Trayhurn, P. (1986) · Annals of Nutrition and Metabolism · doi:10.1159/000177180 · Cited by 31
Atrial natriuretic peptide receptors are present in brown adipose tissue
Okamura, H., Kelly, P. A., Chabot, J. ‐., et al. (1988) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(88)80943-4 · Cited by 31
Uncoupling Protein 1 Does Not Produce Heat without Activation
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“UCP1, the central mechanistic component of brown fat-mediated non-shivering thermogenesis, is itself a regulatory center inhibited by purine nucleotides (GDP, GTP, ADP, ATP) [109].”
Background
Housing-temperature reveals energy intake counter-balances energy expenditure in normal-weight, but not diet-induced obese, male mice
John, L. M., Petersen, N., Gerstenberg, M. K., Torz, L., Pedersen, K., Christoffersen, B. Ø., & Kuhre, R. E. (2022) · Communications Biology · doi:10.1038/s42003-022-03895-8 · Cited by 31
Images of mitochondrial UCP 1 in mouse thymocytes using confocal microscopy
Adams, A. E., Hanrahan, O., Nolan, D. P., Voorheis, H. P., Fallon, P. G., & Porter, R. K. (2007) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2007.10.003 · Cited by 30
Dynamic regulation of mitochondrial respiratory chain efficiency in Saccharomyces cerevisiae
Postmus, J., Tüzün, I., Bekker, M., Müller, W. H., de Mattos, M. J. T., Brul, S., & Smits, G. J. (2011) · Microbiology · doi:10.1099/mic.0.050039-0 · Cited by 29
“Incomplete coupling is thought to be important in reducing the production of reactive oxygen species (ROS) (Boveris & Chance, 1973; Brookes, 2005; Turrens & Boveris, 1980) in thermogenesis (Nicholls & Locke, 1984) and metabolic regulation (Rolfe & Brand, 1997).”
Background
Fatty acid activation of the uncoupling proteins requires the presence of the central matrix loop from UCP1
Jiménez-Jiménez, J., Ledesma, A., Zaragoza, P., González‐Barroso, M. M., & Rial, E. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.05.027 · Cited by 33
“We have long defended that UCP1 has a unique fatty acid sensitivity that directly correlates with its physiological regulation [3,4,8,11].”
Background
Fasting-induced selective mobilization of brown adipose tissue fatty acids
Groscolas, R., & Herzberg, G. R. (1997) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)37436-8 · Cited by 30
Involvement of orexin neurons in fasting- and central adenosine-induced hypothermia
Futatsuki, T., Yamashita, A., Ikbar, K. N., Yamanaka, A., Arita, K., Kakihana, Y., & Kuwaki, T. (2018) · Scientific Reports · doi:10.1038/s41598-018-21252-w · Cited by 29
In vivo morphometry and functional morphology of brown adipose tissue by magnetic resonance imaging
Sbarbati, A., Baldassarri, A. M., Zancanaro, C., Boicelli, A. C., & Osculati, F. (1991) · The Anatomical Record · doi:10.1002/ar.1092310302 · Cited by 30
The effect of mild cold exposure on UCP3 mRNA expression and UCP3 protein content in humans
Schrauwen, P., Westerterp‐Plantenga, M. S., Moonen‐Kornips, E., Schaart, G., & Lichtenbelt, W. D. V. M. (2002) · International Journal of Obesity · doi:10.1038/sj.ijo.0801943 · Cited by 30
Postnatal appearance of uncoupling protein and formation of thermogenic mitochondria in hamster brown adipose tissue
Houštěk, J., Janíková, D., Bednář, J., Kopecký, J., Šebestián, J., & Soukup, T. (1990) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(90)90077-h · Cited by 30
Loss of brown adipose tissue uncoupling protein mRNA on deacclimation of cold-exposed rats
Reichling, S., Ridley, R. G., Patel, H. V., Harley, C. B., & Freeman, K. B. (1987) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(87)91470-7 · Cited by 30
Differential interaction of fatty acids and fatty acyl CoA esters with the purified/reconstituted brown adipose tissue mitochondrial uncoupling protein
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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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