title: Four-week cold acclimation in adult humans shifts uncoupling thermogenesis from skeletal muscles to brown adipose tissue.
abstract: Muscle-derived thermogenesis during acute cold exposure in humans consists of a combination of cold-induced increases in skeletal muscle proton leak and shivering. Daily cold exposure results in an increase in brown adipose tissue oxidative capacity coupled with a decrease in the cold-induced skeletal muscle proton leak and shivering intensity. Improved coupling between electromyography-determined muscle activity and whole-body heat production following cold acclimation suggests a maintenance of ATPase-dependent thermogenesis and decrease in skeletal muscle ATPase independent thermogenesis. Although daily cold exposure did not change the fibre composition of the vastus lateralis, the fibre composition was a strong predictor of the shivering pattern evoked during acute cold exposure.
  
  
  
  We previously showed that 4 weeks of daily cold exposure in humans can increase brown adipose tissue (BAT) volume by 45% and oxidative metabolism by 182%. Surprisingly, we did not find a reciprocal reduction in shivering intensity when exposed to a mild cold (18°C). The present study aimed to determine whether changes in skeletal muscle oxidative metabolism or shivering activity could account for these unexpected findings. Nine men participated in a 4 week cold acclimation intervention (10°C water circulating in liquid-conditioned suit, 2 h day-1, 5 days week-1). Shivering intensity and pattern were measured continuously during controlled cold exposure (150 min at 4 °C) before and after the acclimation. Muscle biopsies from the m. vastus lateralis were obtained to measure oxygen consumption rate and proton leak of permeabilized muscle fibres. Cold acclimation elicited a modest 21% (P < 0.05) decrease in whole-body and m. vastus lateralis shivering intensity. Furthermore, cold acclimation abolished the acute cold-induced increase in proton leak. Although daily cold exposure did not change the fibre composition of the m. vastus lateralis, fibre composition was a strong predictor of the shivering pattern evoked during acute cold. We conclude that muscle-derived thermogenesis during acute cold exposure in humans is not only limited to shivering, but also includes cold-induced increases in proton leak. The efficiency of muscle oxidative phosphorylation improves with cold acclimation, suggesting that reduced muscle thermogenesis occurs through decreased proton leak, in addition to decreased shivering intensity as BAT capacity and activity increase. These changes occur with no net difference in whole-body thermogenesis.
authors.affiliation: Department of Medicine, Centre de recherche du Centre hospitalier universitaire de Sherbrooke, Université de Sherbrooke, Sherbrooke, Canada.
authors.forename: Denis P
authors.initials: DP
authors.lastname: Blondin
authors.affiliation: Faculty of Science, University of Ottawa, Ottawa, Canada.|Institut de recherche de l'Hôpital Montfort, Ottawa, Canada.
authors.forename: Amani
authors.initials: A
authors.lastname: Daoud
authors.affiliation: Carleton Sports Medicine Clinic, Carleton University, Ottawa, Canada.
authors.forename: Taryn
authors.initials: T
authors.lastname: Taylor
authors.affiliation: Faculty of Health Sciences, University of Ottawa, Ottawa, Canada.
authors.forename: Hans C
authors.initials: HC
authors.lastname: Tingelstad
authors.affiliation: Department of Chemistry, Carleton University, Ottawa, Canada.
authors.forename: Véronic
authors.initials: V
authors.lastname: Bézaire
authors.affiliation: Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.
authors.forename: Denis
authors.initials: D
authors.lastname: Richard
authors.affiliation: Department of Medicine, Centre de recherche du Centre hospitalier universitaire de Sherbrooke, Université de Sherbrooke, Sherbrooke, Canada.
authors.forename: André C
authors.initials: AC
authors.lastname: Carpentier
authors.affiliation: Faculty of Health Sciences, University of Western Ontario, London, Canada.
authors.forename: Albert W
authors.initials: AW
authors.lastname: Taylor
authors.affiliation: Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Canada.
authors.forename: Mary-Ellen
authors.identifier: 0000-0003-3864-5886
authors.initials: ME
authors.lastname: Harper
authors.affiliation: Institut de recherche de l'Hôpital Montfort, Ottawa, Canada.|Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Canada.
authors.forename: Céline
authors.initials: C
authors.lastname: Aguer
authors.affiliation: Faculty of Health Sciences, University of Ottawa, Ottawa, Canada.
authors.forename: François
authors.identifier: 0000-0002-3728-1665
authors.initials: F
authors.lastname: Haman
mesh_terms: D000064:Acclimatization / Q000502:physiology*; D002001:Adipose Tissue, Brown / Q000502:physiology*; D000328:Adult; D003080:Cold Temperature; D006801:Humans; D008297:Male; D018482:Muscle, Skeletal / Q000502:physiology*; D018995:Myosin Heavy Chains / Q000378:metabolism; D010101:Oxygen Consumption; D022722:Thermogenesis / Q000502:physiology*; D055815:Young Adult
chemical_list: D018995:Myosin Heavy Chains
keywords: cold-acclimation; energy metabolism; non-shivering thermogenesis; proton leak; shivering; uncoupling