Integration of body temperature into the analysis of energy expenditure in the mouse.

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Abstract

We quantified the effect of environmental temperature on mouse energy homeostasis and body temperature.

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Nonshivering thermogenesis and its adequate measurement in metabolic studies.

Barbara Cannon, Jan Nedergaard (2011)

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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Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals.

Naresh Bal, Santosh Maurya, Danesh Sopariwala … (2012)

The role of skeletal muscle in nonshivering thermogenesis (NST) is not well understood. Here we show that sarcolipin (Sln), a newly identified regulator of the sarco/endoplasmic reticulum Ca(2+)-ATPase (Serca) pump, is necessary for muscle-based thermogenesis. When challenged to acute cold (4 °C), Sln(-/-) mice were not able to maintain their core body temperature (37 °C) and developed hypothermia. Surgical ablation of brown adipose tissue and functional knockdown of Ucp1 allowed us to highlight the role of muscle in NST. Overexpression of Sln in the Sln-null background fully restored muscle-based thermogenesis, suggesting that Sln is the basis for Serca-mediated heat production. We show that ryanodine receptor 1 (Ryr1)-mediated Ca(2+) leak is an important mechanism for Serca-activated heat generation. Here we present data to suggest that Sln can continue to interact with Serca in the presence of Ca(2+), which can promote uncoupling of the Serca pump and cause futile cycling. We further show that loss of Sln predisposes mice to diet-induced obesity, which suggests that Sln-mediated NST is recruited during metabolic overload. These data collectively suggest that SLN is an important mediator of muscle thermogenesis and whole-body energy metabolism.

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Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system.

Andrej Romanovsky (2006)

While summarizing the current understanding of how body temperature (T(b)) is regulated, this review discusses the recent progress in the following areas: central and peripheral thermosensitivity and temperature-activated transient receptor potential (TRP) channels; afferent neuronal pathways from peripheral thermosensors; and efferent thermoeffector pathways. It is proposed that activation of temperature-sensitive TRP channels is a mechanism of peripheral thermosensitivity. Special attention is paid to the functional architecture of the thermoregulatory system. The notion that deep T(b) is regulated by a unified system with a single controller is rejected. It is proposed that T(b) is regulated by independent thermoeffector loops, each having its own afferent and efferent branches. The activity of each thermoeffector is triggered by a unique combination of shell and core T(b)s. Temperature-dependent phase transitions in thermosensory neurons cause sequential activation of all neurons of the corresponding thermoeffector loop and eventually a thermoeffector response. No computation of an integrated T(b) or its comparison with an obvious or hidden set point of a unified system is necessary. Coordination between thermoeffectors is achieved through their common controlled variable, T(b). The described model incorporates Kobayashi's views, but Kobayashi's proposal to eliminate the term sensor is rejected. A case against the term set point is also made. Because this term is historically associated with a unified control system, it is more misleading than informative. The term balance point is proposed to designate the regulated level of T(b) and to attract attention to the multiple feedback, feedforward, and open-loop components that contribute to thermal balance.

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Author and article information

Journal

Journal ID (iso-abbrev): Mol Metab

Title: Molecular metabolism

Publisher: Elsevier BV

ISSN: 2212-8778

ISSN (Print): 2212-8778

Publication date (Electronic): Jun 2015

Volume: 4

Issue: 6

Affiliations

[1 ] Diabetes, Endocrinology, and Obesity Branch, National Institute of Diabetes and Digestive and Kidney Diseases, NIH, Bethesda, MD 20892, USA ; Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, 106 91 Stockholm, Sweden.

[2 ] Diabetes, Endocrinology, and Obesity Branch, National Institute of Diabetes and Digestive and Kidney Diseases, NIH, Bethesda, MD 20892, USA.

[3 ] Mouse Metabolism Core, National Institute of Diabetes and Digestive and Kidney Diseases, NIH, Bethesda, MD 20892, USA.

Article

Publisher Item ID: S2212-8778(15)00056-3

DOI: 10.1016/j.molmet.2015.03.001

PMC ID: 4443293

PubMed ID: 26042200

SO-VID: 32797f65-4daa-481a-a444-3ec902c3b6fc

History

Keywords: BMR, basal metabolic rate,Cold-induced thermogenesis,Heat conductance,dTb, defended body temperature,Body temperature,Tb, core body temperature,PAEE, physical activity energy expenditure,LCT, lower critical temperature,EE, energy expenditure,Ta, environmental temperature,RQ, respiratory quotient,Basal metabolic rate,Energy expenditure,CIT, cold-induced thermogenesis,TEF, thermic effect of food,TEE, total energy expenditure,HFD, high-fat diet,Thermoneutrality

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Keywords: BMR, basal metabolic rate, Cold-induced thermogenesis, Heat conductance, dTb, defended body temperature, Body temperature, Tb, core body temperature, PAEE, physical activity energy expenditure, LCT, lower critical temperature, EE, energy expenditure, Ta, environmental temperature, RQ, respiratory quotient, Basal metabolic rate, Energy expenditure, CIT, cold-induced thermogenesis, TEF, thermic effect of food, TEE, total energy expenditure, HFD, high-fat diet, Thermoneutrality

Integration of body temperature into the analysis of energy expenditure in the mouse.

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Most cited references 56

Nonshivering thermogenesis and its adequate measurement in metabolic studies.

Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals.

Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system.

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