Four‐week cold acclimation in adult humans shifts uncoupling thermogenesis from skeletal muscles to brown adipose tissue

• Published in: The Journal of physiology 2017-03, Vol.595 (6), p.2099-2113
• Main Authors: Blondin, Denis P., Daoud, Amani, Taylor, Taryn, Tingelstad, Hans C., Bézaire, Véronic, Richard, Denis, Carpentier, André C., Taylor, Albert W., Harper, Mary‐Ellen, Aguer, Céline, Haman, François
• Format: Article
• Language: English
• Subjects: Acclimatization - physiology; Adipose Tissue, Brown - physiology; Adult; Body fat; Cold Temperature; cold‐acclimation; energy metabolism; Humans; Integrative; Integrative Physiology; Male; Muscle, Skeletal - physiology; Myosin Heavy Chains - metabolism; non‐shivering thermogenesis; Oxygen Consumption; proton leak; Research Paper; shivering; Skeletal Muscle; Thermogenesis - physiology; Thermoregulation; uncoupling; Young Adult
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/JP273395

Key points 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