Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet

Objective: Rodent models raised at environmental temperatures of 21–22 °C are increasingly switched to thermoneutral housing conditions in adulthood to better capture human physiology. We quantified the developmental effects of rearing mice at an ambient temperature of 22 °C vs. 30 °C on metabolic r...

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Main Authors: Daniele Neri, Angela M. Ramos-Lobo, Seoeun Lee, Alexandre Lafond, Lori M. Zeltser
Format: Article
Language:English
Published: Elsevier 2023-07-01
Series:Molecular Metabolism
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2212877823000741
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author Daniele Neri
Angela M. Ramos-Lobo
Seoeun Lee
Alexandre Lafond
Lori M. Zeltser
author_facet Daniele Neri
Angela M. Ramos-Lobo
Seoeun Lee
Alexandre Lafond
Lori M. Zeltser
author_sort Daniele Neri
collection DOAJ
description Objective: Rodent models raised at environmental temperatures of 21–22 °C are increasingly switched to thermoneutral housing conditions in adulthood to better capture human physiology. We quantified the developmental effects of rearing mice at an ambient temperature of 22 °C vs. 30 °C on metabolic responses to cold and high fat diet (HFD) in adulthood. Methods: Mice were reared from birth to 8 weeks of age at 22 °C or 30 °C, when they were acclimated to single housing at the same temperature for 2–3 weeks in indirect calorimetry cages. Energy expenditure attributable to basal metabolic rate, physical activity, thermic effect of food, and adaptive cold- or diet-induced thermogenesis was calculated. Responses to cooling were evaluated by decreasing the ambient temperature from 22 °C to 14 °C, while responses to HFD feeding were assessed at 30 °C. Influences of rearing temperature on thermogenic responses that emerge over hours, days and weeks were assessed by maintaining mice in the indirect calorimetry cages throughout the study. Results: At an ambient temperature of 22 °C, total energy expenditure (TEE) was 12–16% higher in mice reared at 22 °C as compared to 30 °C. Rearing temperature had no effect on responses in the first hours or week of the 14 °C challenge. Differences emerged in the third week, when TEE increased an additional 10% in mice reared at 22 °C, but mice reared at 30 °C could not sustain this level of cold-induced thermogenesis. Rearing temperature only affected responses to HFD during the first week, due to differences in the timing but not the strength of metabolic adaptations. Conclusion: Rearing at 22 °C does not have a lasting effect on metabolic adaptations to HFD at thermoneutrality, but it programs an enhanced capacity to respond to chronic cold challenges in adulthood. These findings highlight the need to consider rearing temperature when using mice to model cold-induced thermogenesis.
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spelling doaj.art-8d29bd847a4d403a98e1cb10655bf9f42023-06-24T05:16:25ZengElsevierMolecular Metabolism2212-87782023-07-0173101740Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat dietDaniele Neri0Angela M. Ramos-Lobo1Seoeun Lee2Alexandre Lafond3Lori M. Zeltser4Naomi Berrie Diabetes Center, Columbia University Irving Medical Center, New York, NY 10032, USANaomi Berrie Diabetes Center, Columbia University Irving Medical Center, New York, NY 10032, USANaomi Berrie Diabetes Center, Columbia University Irving Medical Center, New York, NY 10032, USANaomi Berrie Diabetes Center, Columbia University Irving Medical Center, New York, NY 10032, USANaomi Berrie Diabetes Center, Columbia University Irving Medical Center, New York, NY 10032, USA; Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, NY 10032, USA; Corresponding author. Naomi Berrie Diabetes Center, Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, NY 10032, USA.Objective: Rodent models raised at environmental temperatures of 21–22 °C are increasingly switched to thermoneutral housing conditions in adulthood to better capture human physiology. We quantified the developmental effects of rearing mice at an ambient temperature of 22 °C vs. 30 °C on metabolic responses to cold and high fat diet (HFD) in adulthood. Methods: Mice were reared from birth to 8 weeks of age at 22 °C or 30 °C, when they were acclimated to single housing at the same temperature for 2–3 weeks in indirect calorimetry cages. Energy expenditure attributable to basal metabolic rate, physical activity, thermic effect of food, and adaptive cold- or diet-induced thermogenesis was calculated. Responses to cooling were evaluated by decreasing the ambient temperature from 22 °C to 14 °C, while responses to HFD feeding were assessed at 30 °C. Influences of rearing temperature on thermogenic responses that emerge over hours, days and weeks were assessed by maintaining mice in the indirect calorimetry cages throughout the study. Results: At an ambient temperature of 22 °C, total energy expenditure (TEE) was 12–16% higher in mice reared at 22 °C as compared to 30 °C. Rearing temperature had no effect on responses in the first hours or week of the 14 °C challenge. Differences emerged in the third week, when TEE increased an additional 10% in mice reared at 22 °C, but mice reared at 30 °C could not sustain this level of cold-induced thermogenesis. Rearing temperature only affected responses to HFD during the first week, due to differences in the timing but not the strength of metabolic adaptations. Conclusion: Rearing at 22 °C does not have a lasting effect on metabolic adaptations to HFD at thermoneutrality, but it programs an enhanced capacity to respond to chronic cold challenges in adulthood. These findings highlight the need to consider rearing temperature when using mice to model cold-induced thermogenesis.http://www.sciencedirect.com/science/article/pii/S2212877823000741Rearing temperatureDevelopmental programmingThermoneutralityCold-induced thermogenesisDiet-induced thermogenesisEnergy expenditure
spellingShingle Daniele Neri
Angela M. Ramos-Lobo
Seoeun Lee
Alexandre Lafond
Lori M. Zeltser
Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet
Molecular Metabolism
Rearing temperature
Developmental programming
Thermoneutrality
Cold-induced thermogenesis
Diet-induced thermogenesis
Energy expenditure
title Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet
title_full Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet
title_fullStr Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet
title_full_unstemmed Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet
title_short Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet
title_sort rearing mice at 22°c programs increased capacity to respond to chronic exposure to cold but not high fat diet
topic Rearing temperature
Developmental programming
Thermoneutrality
Cold-induced thermogenesis
Diet-induced thermogenesis
Energy expenditure
url http://www.sciencedirect.com/science/article/pii/S2212877823000741
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