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

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          Abstract

          Objectives

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

          Methods

          The effect of environmental temperature (4–33 °C) on body temperature, energy expenditure, physical activity, and food intake in various mice (chow diet, high-fat diet, Brs3 -/y , lipodystrophic) was measured using continuous monitoring.

          Results

          Body temperature depended most on circadian phase and physical activity, but also on environmental temperature. The amounts of energy expenditure due to basal metabolic rate (calculated via a novel method), thermic effect of food, physical activity, and cold-induced thermogenesis were determined as a function of environmental temperature. The measured resting defended body temperature matched that calculated from the energy expenditure using Fourier's law of heat conduction. Mice defended a higher body temperature during physical activity. The cost of the warmer body temperature during the active phase is 4–16% of total daily energy expenditure. Parameters measured in diet-induced obese and Brs3 -/y mice were similar to controls. The high post-mortem heat conductance demonstrates that most insulation in mice is via physiological mechanisms.

          Conclusions

          At 22 °C, cold-induced thermogenesis is ∼120% of basal metabolic rate. The higher body temperature during physical activity is due to a higher set point, not simply increased heat generation during exercise. Most insulation in mice is via physiological mechanisms, with little from fur or fat. Our analysis suggests that the definition of the upper limit of the thermoneutral zone should be re-considered. Measuring body temperature informs interpretation of energy expenditure data and improves the predictiveness and utility of the mouse to model human energy homeostasis.

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          Most cited references56

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          Nonshivering thermogenesis and its adequate measurement in metabolic studies.

          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.

            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.

              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

                Contributors
                Journal
                Mol Metab
                Mol Metab
                Molecular Metabolism
                Elsevier
                2212-8778
                10 March 2015
                June 2015
                10 March 2015
                : 4
                : 6
                : 461-470
                Affiliations
                [1 ]Diabetes, Endocrinology, and Obesity Branch, National Institute of Diabetes and Digestive and Kidney Diseases, NIH, Bethesda, MD 20892, USA
                [2 ]Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, 106 91 Stockholm, Sweden
                [3 ]Mouse Metabolism Core, National Institute of Diabetes and Digestive and Kidney Diseases, NIH, Bethesda, MD 20892, USA
                Author notes
                []Corresponding author. National Institute of Diabetes and Digestive and Kidney Diseases, NIH, Building 10-CRC, Room 5-5940, 10 Center Drive, Bethesda, MD 20982, USA. Tel.: +1 301 496 6442. marc.reitman@ 123456nih.gov
                Article
                S2212-8778(15)00056-3
                10.1016/j.molmet.2015.03.001
                4443293
                26042200
                32797f65-4daa-481a-a444-3ec902c3b6fc
                History
                : 17 February 2015
                : 26 February 2015
                : 3 March 2015
                Categories
                Original Article

                thermoneutrality,basal metabolic rate,cold-induced thermogenesis,body temperature,energy expenditure,heat conductance,ta, environmental temperature,tb, core body temperature,dtb, defended body temperature,ee, energy expenditure,tee, total energy expenditure,paee, physical activity energy expenditure,tef, thermic effect of food,bmr, basal metabolic rate,cit, cold-induced thermogenesis,rq, respiratory quotient,lct, lower critical temperature,hfd, high-fat diet

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