Shivering and nonshivering thermogenesis in exercised cold-deacclimated rats

Abstract

Norepinephrine (NE)-induced increase in oxygen consumption (VO2) and colonic temperature (Tc) was greater in cold-acclimated rats housed at 4 degrees C for 4 weeks (CA) than warm-acclimated controls housed at 24 degrees C for 4 weeks (WA). On the other hand, shivering activity measured at 4 degrees C was less in CA than in WA, while propranolol administration eliminated the difference between these two groups by enhancing shivering in CA. Wet weight and protein content of interscapular brown adipose tissue (IBAT) were greater in CA than in WA. Following cold acclimation, CA were deacclimated at 24 degrees C for 5 weeks. During deacclimation, half of this latter group were forced to run (15 m.min-1 for 1 h) every day (CD-T) while the remaining rats remained sedentary (CD-S). Shivering activity assessed at 4 degrees C 4 weeks after commencing cold deacclimation was significantly less in CD-T than in CD-S and the difference disappeared following propranolol injection. VO2 and Tc responses to NE injection measured 1, 2 and 5 weeks after commencing cold deacclimation did not differ between CD-S and CD-T. Although IBAT weight was lighter in CD-T than in CD-S, its total protein content was not different between the latter two groups of rats. These results suggest that a greater degree of NE-independent nonshivering thermogenesis (NST) is retained in rats that are exercised during the process of deacclimation as compared with animals that are sedentary. This difference in NST would not seem to be directly related to BAT thermogenic capacity.

Browning of the white adipose tissue regulation: new insights into nutritional and metabolic relevance in health and diseases

“…Both ATs play various physiological roles, including energy storage, endocrine regulation, and thermogenesis. As a means of adapting, mammalians developed a mechanism to maintain their body temperatures under unfavorable climates [ 2 ]. This process, called adaptative thermogenesis, occurs due to the elevated plasticity of ATs, which allows reversible changes in their morphology and functions [ 3 ].…”

“…The occurrence of these events maintains proper body temperature under adverse thermal acclimation. Once shivering thermogenesis is decreased in cold acclimation (around 4 °C), non-shivering thermogenesis is the major way to produce heat in this context [ 2 , 4 ]. The detection of the thermal changes begins with the capture of sensory stimuli by cutaneous thermoreceptors, which promote the sensitization of afferent nerves.…”

Adipose tissue browning and thermogenesis under physiologically energetic challenges: a remodelled thermogenic system

“…Despite the anatomical, functional and fat content differences between rodents and human, there remains a reciprocal relationship between NST and ST. Adipose-specific mTORC2 knockout mice reduced total UCP1 expression levels and the thermogenic capacity in BAT and iWAT upon cold exposure, but the compensatory increase in ST resulted in unaltered total energy expenditure (Castro et al, 2021). On cold acclimation at 4°C for 4 weeks, NA-induced NST was elevated in rats, as expected with a significant decrease in shivering activity, whereas treatment with propanolol, a β-AR blocker, enhanced ST and eliminated differences in thermogenesis (Moriya et al, 1988).…”

“…Similarly, detraining increased adipocyte size and lipid accumulation, but exercise in early childhood efficiently mitigated BAT whitening and decreased food consumption until adulthood (Nguyen et al., 2022). In an earlier study, exercise rescued the regression of cold‐induced NST irrespective of BAT thermogenesis, implying that exercise might protect the thermogenic capacity of beige adipocytes and prevent their return to white adipocytes (Moriya et al., 1988). These results suggest a role of long‐term exercise in maintaining adipose tissue browning and thermogenic capacity, but the molecular mechanisms remain largely obscure stemming from limited data about the effects of exercise on adipose tissue whitening.…”

“…Nevertheless, only circumstantial evidence is available, as J Physiol 602.1 the pressing challenge lies in how to precisely measure the thermogenic cost of NST and ST. During the course of evolution, it is possible there was more reliance on NST or lower shivering intensity to establish a more economical thermogenic system, which is conducive to conserving energy in the context of high energetic metabolism (Blondin et al, 2014;Hohtola, 1981). This could explain the observations in many studies that a characteristic of cold adaptation is manifested in increased NST and decreased ST, or reduced shivering intensity (Barre et al, 1985;Gordon et al, 2019;Griggio, 1988;Moriya et al, 1988;Teulier et al, 2010). Consistent with the finding that cold transferred the hub of thermogenesis to BAT (Blondin, Daoud, et al, 2017), Brazaitis et al (2014) reported that cold acclimation elicited a thermo-regulatory shift from ST to NST, as well as from periphery to centre to centralize thermoregulation.…”