Cited by 679Adipose Tissue and MetabolismPhysiological and biochemical adaptationsRegulation of Appetite and Obesity

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Nonshivering thermogenesis and its adequate measurement in metabolic studies

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Cannon, Barbara, Nedergaard, Jan·2011·Journal of Experimental Biology

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Abstract

Alterations in nonshivering thermogenesis are presently discussed as being both potentially causative of and able to counteract obesity. However, the necessity for mammals to defend their body temperature means that the ambient temperature profoundly affects the outcome and interpretation of metabolic experiments. An adequate understanding and assessment of nonshivering thermogenesis is therefore paramount for metabolic studies. Classical nonshivering thermogenesis is facultative, i.e. it is only activated when an animal acutely requires extra heat (switched on in minutes), and adaptive, i.e. it takes weeks for an increase in capacity to develop. Nonshivering thermogenesis is fully due to brown adipose tissue activity; adaptation corresponds to the recruitment of this tissue. Diet-induced thermogenesis is probably also facultative and adaptive and due to brown adipose tissue activity. Although all mammals respond to injected/infused norepinephrine (noradrenaline) with an increase in metabolism, in non-adapted mammals this increase mainly represents the response of organs not involved in nonshivering thermogenesis; only the increase after adaptation represents nonshivering thermogenesis. Thermogenesis (metabolism) should be expressed per animal, and not per body mass [not even to any power (0.75 or 0.66)]. A 'cold tolerance test' does not examine nonshivering thermogenesis capacity; rather it tests shivering capacity and endurance. For mice, normal animal house temperatures are markedly below thermoneutrality, and the mice therefore have a metabolic rate and food consumption about 1.5 times higher than their intrinsic requirements. Housing and examining mice at normal house temperatures carries a high risk of identifying false positives for intrinsic metabolic changes; in particular, mutations/treatments that affect the animal's insulation (fur, skin) may lead to such problems. Correspondingly, true alterations in intrinsic metabolic rate remain undetected when metabolism is examined at temperatures below thermoneutrality. Thus, experiments with animals kept and examined at thermoneutrality are likely to yield an improved possibility of identifying agents and genes important for human energy balance.

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Background
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Background
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Background
Mitochondrial DNA Variation Dictates Expressivity and Progression of Nuclear DNA Mutations Causing Cardiomyopathy
McManus, M. J., Picard, M. A., Chen, H.-W., de Haas, H. J., Potluri, P., Leipzig, J. N., Towheed, A., Angelin, A., Sengupta, P. P., Morrow, R. M., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.08.002 · Cited by 84
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Modeling insulin resistance in rodents by alterations in diet: What have high-fat and high-calorie diets revealed?
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BackgroundInfluential
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Heart Failure With Preserved Ejection Fraction Induces Beiging in Adipose Tissue
Valero‐Muñoz, M., Li, S. J., Wilson, R. M., Hulsmans, M., Aprahamian, T. R., Fuster, J. J., Nahrendorf, M., Scherer, P. E., & Sam, F. (2015) · Circulation Heart Failure · doi:10.1161/circheartfailure.115.002724 · Cited by 77
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Self-citation
Refinement of Animal Models of Sepsis and Septic Shock
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“Mammals and birds are endotherms and can regulate their body temperature via their metabolism (81).”
Background
Characterization of cold‐induced remodelling reveals depot‐specific differences across and within brown and white adipose tissues in mice
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The metabolic stress response: Adaptation to acute-, repeated- and chronic challenges in mice
Kuti, D., Winkler, Z., Horváth, K., Juhász, B., Szilvásy-Szabó, A., Fekete, C., Ferenczi, S., & Kovács, K. J. (2022) · iScience · doi:10.1016/j.isci.2022.104693 · Cited by 77
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Estimation of Activity Related Energy Expenditure and Resting Metabolic Rate in Freely Moving Mice from Indirect Calorimetry Data
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Feeding circuit development and early-life influences on future feeding behaviour
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Metabolic Dysfunction and Altered Mitochondrial Dynamics in the Utrophin-Dystrophin Deficient Mouse Model of Duchenne Muscular Dystrophy
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The Gustatory Signaling Pathway and Bitter Taste Receptors Affect the Development of Obesity and Adipocyte Metabolism in Mice
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Intermittent hypoxia-induced glucose intolerance is abolished by α-adrenergic blockade or adrenal medullectomy
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Circadian lipid synthesis in brown fat maintains murine body temperature during chronic cold
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Method
Growth Differentiation Factor-5 Promotes Brown Adipogenesis in Systemic Energy Expenditure
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Method
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The Complex Roles of Mechanistic Target of Rapamycin in Adipocytes and Beyond
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Sympathetic nerve innervation is required for beigeing in white fat
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Background
Brown Adipogenic Reprogramming Induced by a Small Molecule
Nie, B., Nie, T., Hui, X. H., Gu, P., Mao, L., Li, K., Yuan, R., Zheng, J., Wang, H., Li, K., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.062 · Cited by 64
“…metabolic energy output is contributed from both non-shivering thermogenesis of BAT and shivering thermogenesis of skeletal muscles, whereas measuring the response to sympathetic nervous system activation in awake animals tends to show higher inter-animal variability (Cannon and Nedergaard, 2011).”
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Caloric Restriction Promotes Structural and Metabolic Changes in the Skin
Forni, M. F., Peloggia, J., Braga, T. T., Chinchilla, J. E. O., Shinohara, J. S., Navas, C. A., Câmara, N. O. S., & Kowaltowski, A. J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.052 · Cited by 64
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ADRA1A–Gαq signalling potentiates adipocyte thermogenesis through CKB and TNAP
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Ambient Temperature and Obesity
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mTORC1 in AGRP neurons integrates exteroceptive and interoceptive food-related cues in the modulation of adaptive energy expenditure in mice
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Sympathetic inputs regulate adaptive thermogenesis in brown adipose tissue through cAMP-Salt inducible kinase axis
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Deem, J. D., Faber, C. L., Pedersen, C. E., Phan, B. A., Larsen, S. A., Ogimoto, K., Nelson, J. T., Damian, V. M., Tran, M. A., Palmiter, R. D., et al. (2020) · eLife · doi:10.7554/elife.58764 · Cited by 58
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Background
The use of infrared thermography in the measurement and characterization of brown adipose tissue activation
Law, J., Chalmers, J., Morris, D. E., Robinson, L., Budge, H., & Symonds, M. E. (2017) · Temperature · doi:10.1080/23328940.2017.1397085 · Cited by 65
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Background
Glucocorticoid-Induced Obesity Develops Independently of UCP1
Luijten, I. H. N., Brooks, K., Boulet, N., Shabalina, I. G., Jaiprakash, A., Carlsson, B., Fischer, A. W., Cannon, B., & Nedergaard, J. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.041 · Cited by 59
Self-citation
Energy Reallocation to Breeding Performance through Improved Nest Building in Laboratory Mice
Gaskill, B. N., Pritchett‐Corning, K. R., Gordon, C. J., Pajor, E. A., Lucas, J. R., Davis, J. K., & Garner, J. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074153 · Cited by 58
“Mice in laboratory conditions must therefore use additional energy to stay warm [9].”
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A hot lunch for herbivores: physiological effects of elevated temperatures on mammalian feeding ecology
Beale, P. K., Marsh, K. J., Foley, W. J., & Moore, B. D. (2017) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12364 · Cited by 62
“This means that there is a smaller margin before the limits of survival are reached at high ambient temperatures compared to cold (Cannon & Nedergaard, 2011).”
Background
Functional Significance of the Mitochondrial Membrane Potential
Zorova, L. D., Popkov, V. A., Plotnikov, E. Y., Silachev, D. N., Pevzner, I. B., Jankauskas, S. S., Zorov, S. D., Babenko, V. А., & Zorov, D. B. (2018) · Biochemistry (Moscow) Supplement Series A Membrane and Cell Biology · doi:10.1134/s1990747818010129 · Cited by 59
“At the same time, non-shivering thermogenesis has been demonstrated [14] and it was caused by the uncoupling of oxidative phosphorylation [15, 16], resulting in that the mitochondrial transmembrane potential is consumed directly to generate heat, bypassing the step of ATP synthesis or significantly reducing its produc…”
Crosstalk between Drp1 phosphorylation sites during mitochondrial remodeling and their impact on metabolic adaptation
Valera‐Alberni, M., Joffraud, M., Miró, J., Capellades, J., Junza, A., Dayon, L., Galindo, A. N., Sanchez-Garcia, J. L., Valsesia, A., Cercillieux, A., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109565 · Cited by 61
Physiology and relevance of human adaptive thermogenesis response
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Brown adipose tissue in humans: Therapeutic potential to combat obesity
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Adipose HIF-1α causes obesity by suppressing brown adipose tissue thermogenesis
Jun, J. C., Devera, R., Unnikrishnan, D. C., Shin, M., Bevans‐Fonti, S., Yao, Q., Rathore, A., Younas, H., Halberg, N., Scherer, P. E., et al. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1480-6 · Cited by 58
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The C-terminal fibrinogen-like domain of angiopoietin-like 4 stimulates adipose tissue lipolysis and promotes energy expenditure
McQueen, A. E., Kanamaluru, D., Yan, K., Gray, N. E., Wu, L., Li, M.-L., Chang, A., Hasan, A., Stifler, D., Koliwad, S. K., et al. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.803973 · Cited by 56
“After establishing the ability of FLD to stimulate energy expenditure at room temperature (22–23 °C), which prior studies indicate is cold enough to stimulate reactive thermogenesis in mice (25), we examined Ad-FLD mice at thermoneutrality to eliminate any such thermogenic stress.”
Background
Coordinated targeting of cold and nicotinic receptors synergistically improves obesity and type 2 diabetes
Clemmensen, C., Jall, S., Kleinert, M., Quarta, C., Gruber, T., Reber, J., Sachs, S., Fischer, K., Feuchtinger, A., Karlas, A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06769-y · Cited by 56
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Cholinergic neurons in the dorsomedial hypothalamus regulate mouse brown adipose tissue metabolism
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“For instance, animals have the ability to increase endogenous heat production through shivering thermogenesis on cold exposure [41].”
Background
Adipose tissue insulin resistance due to loss of PI3K p110α leads to decreased energy expenditure and obesity
Nelson, V. L., Jiang, Y., Dickman, K. G., Ballou, L. M., & Lin, R. Z. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00625.2013 · Cited by 55
“where V̇CO2 is the volume of CO2 produced and V̇O2 is the volume of O2 consumed (12).”
Background
No insulating effect of obesity
Fischer, A. W., Csikasz, R. I., von Essen, G., Cannon, B., & Nedergaard, J. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00093.2016 · Cited by 60
Self-citation
Common and distinct regulation of human and mouse brown and beige adipose tissues: a promising therapeutic target for obesity
Liu, X., Cervantes, C., & Liu, F. (2017) · Protein & Cell · doi:10.1007/s13238-017-0378-6 · Cited by 59
“Adult hBAT, which is dispersed mainly in the supraclavicular, para-aortic, and suprarenal regions and is densely innervated, could be activated by cold through the sympathetic nervous system (Cannon and Nedergaard, 2011; Lowell and Spiegelman, 2000).”
Background

Authors: Cannon, B., & Nedergaard, J.
Affiliations: Stockholm University (SE)
Corresponding author: Cannon, Barbara
ORCID: Cannon, Barbara
Nedergaard, Jan
Venue: Journal of Experimental Biology
Publisher: The Company of Biologists
Published: 2011-01-15
Volume: 214
Issue: 2
Pages: 242-253
ISSN: 0022-0949 (ISSN-L)
1477-9145
DOI: 10.1242/jeb.050989
OpenAlex: W2148400263
Cited by: 677
References: 99
Citations by year: 2026: 20 · 2025: 31 · 2024: 32 · 2023: 45 · 2022: 42 · 2021: 55 · 2020: 53 · 2019: 42 · 2018: 69 · 2017: 48 · 2016: 47 · 2015: 42 · 2014: 48 · 2013: 48 · 2012: 41
FWCI: 3.31
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: other-oa
Locations: Journal of Experimental Biology (publishedVersion, other-oa)
PubMed (publishedVersion)
RVC Research Online (Royal Veterinary College) (submittedVersion, cc-by)
Funders: Vetenskapsrådet
Topics: Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: non-shivering thermogenesis, brown adipose tissue, thermoneutrality, ambient temperature, metabolic rate measurement, norepinephrine, shivering, diet-induced thermogenesis, obesity, energy balance, mice, fur insulation
MeSH terms: Acclimatization, Animals, Adipose Tissue, Brown, Cold Temperature, Humans, Norepinephrine, Thermogenesis

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Nonshivering thermogenesis and its adequate measurement in metabolic studies

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