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. 2015 Mar 10;4(6):461-70.
doi: 10.1016/j.molmet.2015.03.001. eCollection 2015 Jun.

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

Gustavo Abreu-Vieira  1 , Cuiying Xiao  2 , Oksana Gavrilova  3 , Marc L Reitman  2
Affiliations

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

Gustavo Abreu-Vieira et al. Mol Metab. .

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.

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

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Figures

Figure 1
Figure 1
Tb is regulated by mainly by circadian phase and physical activity. A. Effect of circadian phase and Ta. Mean of the 18–28 °C data (the range where Tb is constant) during the dark (solid line) and light (dotted line) phases are indicated. Data are mean ± SEM, n = 11, chow-fed male C57BL/6J mice. B. Effect of circadian phase, activity, and Ta. The surfaces are calculated from the statistical model, detailed in Table S2.
Figure 2
Figure 2
Effect of environmental temperature and light–dark phase on physical activity and food intake. A,B. Components of energy expenditure as a function of environmental temperature. PAEE (green), TEF (red), CIT (blue), and BMR (black) are mean of daily average ± SEM of 11 chow-fed C57BL/6J mice, presented in kcal/h (A) or as a fraction of total daily energy expenditure (B). C. Example of calculation of PAEE in one mouse. PAEE (green) is the TEE minus the EE at rest (no activity), determined by quadratic regression of EE vs activity. TEF (red), CIT (blue), and BMR (black) are defined in the methods and results. Squares are 22 °C; circles are 33 °C. D. Physical activity during the dark and light phases. E. Food intake during the dark and light phases. Data in A,B,D,E are mean ± SEM, pooling 11 chow-fed male C57BL/6J mice from two independent experiments.
Figure 3
Figure 3
Energy cost of physical activity and of the dark phase. A. Energy cost of physical activity at various environmental temperatures during the light phase. PAEE = 0.0470 − (0.000973 * Ta) + (0.0000381 * activity); SE are 0.00272, 0.000111, and 0.000000730, respectively, adjusted R2 = 0.57. B. Mean light and dark phase apparent PAEE normalized for activity, illustrating the consistently higher normalized cost during the light phase and at Ta = 4 °C (*, p < 0.05; **, p < 0.01; ***, p < 0.001). C. Light and dark phase TEE. D. Cost of maintaining the warmer dark phase Tb. The Y axis is the difference in TEE of the dark and light phases, divided by the differences in mean Tb of the dark and light phases. The EE is attributed to PAEE (green), TEF (red), and residual (blue). Data are mean ± SEM, n = 11, chow-fed male C57BL/6J mice (in C the error bars fall within the symbols).
Figure 4
Figure 4
Heat conductance and energy expenditure. A. Energy expenditure as a function of environmental temperature during the light phase. TEE is total energy expenditure (open symbol, dashed line), TEE-PAEE is resting energy expenditure (black symbol, black line), and TEE-PAEE-TEF is basal energy expenditure (grey symbol, grey line). Regression lines were calculated using the 18–28 °C Ta range. The X intercept is the defended body temperature, dTb. The LCT is the Ta at which the regression line meets the thermoneutral metabolic rate. B. Effect of environmental temperature on heat conductance, calculated as EE/(Tb − Ta) during light phase. The LCT is the point above which the conductance increases. Data are mean ± SEM, n = 11, chow-fed male C57BL/6J mice (some error bars are within the symbols).
Figure 5
Figure 5
Effect of environmental temperature and light–dark phase on body temperature and energy homeostasis. A. Body composition. B. Energy expenditure as a function of environmental temperature during the light phase. Regression lines were calculated using the 18–28 °C Ta range. C. Energy expenditure as a function of environmental temperature during the light phase. Data as in B, but normalized with BMR set to 1. D. Effect of environmental temperature on the conductance, calculated as EE/(Tb − Ta) during light phase. E. Dependence of the heat conductance on lean and fat weight. Conductance = 0.0304 + (0.000884 * Fat) − (0.000339 * Lean); SE are 0.0114, 0.000191, and 0.000501, respectively, adjusted R2 = 0.71. F. Dependence of BMR on lean and fat weight. BMR = −0.00626 + (0.00113 * fat) + (0.00694 * lean); SE are 0.0682, 0.00114, and 0.00299, respectively, adjusted R2 = 0.58. In B-D, chow-fed data are circles and solid lines; HFD data are squares and dashed lines. Data are mean ± SEM of 6 chow-fed and 5 high-fat-fed male C57BL/6J mice (*, p < 0.05; ***, p < 0.001).
Figure 6
Figure 6
Contributors to insulation in mice. A. Heat conductance after death. Mice were euthanized by cervical dislocation, Tb was monitored by E-mitter, and the mean heat conductance from 6 to 35 min after death was calculated for each mouse. To obtain a range of body weights, male and female chow-fed C57BL/6J, male and female Mc3r−/−;Mc4r−/− (DKO, raw data from Ref. [71]), and male high fat diet-fed C57BL/6J mice were studied, as indicated. B. Heat conductance summary. Heat conductance during life (Control and dashed reference line, from Figure 5D), after death (Dead, from A, using a body weight of 29 g), and of shaved (Shaved) and nude (Nude) living mice, both approximated based on data in Ref. . The contribution of fur is the difference between the nude/shaved and control groups. The non-mechanical (“physiology’) component of insulation is the difference between the dead and nude/shaved groups.
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