Chronic Cold Exposure Increases Skeletal Muscle Oxidative Structure and Function inMonodelphis domestica, a Marsupial Lacking Brown Adipose Tissue

Abstract

Monodelphis domestica (Marsupialia: Didelphidae) was used as a model animal to investigate and compare muscle adaptation to exercise training and cold exposure. The experimental treatment consisted of four groups of animals: either warm or cold acclimation temperature and with or without endurance exercise training. Maximal aerobic capacity during a running VO2max test in the warm-exercised or cold-exposed (with or without exercise) groups was about 130 mL O(2)/kg/min, significantly higher than the warm-acclimated controls at 113.5 mL O(2)/kg/min. Similarly, during an acute cold challenge (VO2summit), maximal aerobic capacity was higher in these three experimental groups at approximately 95 mL O(2)/kg/min compared with 80.4 mL O(2)/kg/min in warm-acclimated controls. Respiratory exchange ratio was significantly lower (0.89-0.68), whereas relative heart mass (0.52%-0.73%) and whole-body muscle mitochondrial volume density (2.59 to 3.04 cm(3)) were significantly higher following cold exposure. Chronic cold exposure was a stronger stimulus than endurance exercise training for tissue-specific adaptations. Although chronic cold exposure and endurance exercise are distinct challenges, physiological adaptations to each overlap such that the capacities for aerobic performance in response to both cold exposure and running are increased by either or both treatments.

Regulatory role of PGC-1alpha/PPARs signaling in skeletal muscle metabolic recruitment during cold acclimation

“…In contrast to the clear role of skeletal muscle shivering thermogenesis in thermoregulation early in cold acclimation, its role during prolonged cold exposure, when nonshivering is activated, is not clear. Recent data showed that sustained cold exposure in animals with brown adipose tissue causes metabolic and structural changes in skeletal muscle that indicate their shivering activity (Meyer et al, 2010;Mineo et al, 2012), similar to those observed following endurance exercise training (Schaeffer et al, 2003). It is known that shivering-related metabolic recruitment, in terms of fuel selection, can be achieved in three ways: (1) by recruitment of specific subpopulations of fibers within the same muscle; (2) by recruitment of muscles varying in fiber composition; and (3) by recruitment of different metabolic pathways within the same fibers.…”

Muscle mitochondrial volume and aerobic capacity in a small marsupial (Sminthopsis crassicaudata) match those of 'athletic' placentals, reflecting flexible links between energy-use levels in mammals generally.

“…A clear supporting framework for these abilities is apparent in other species so far examined. As in 'athletic' placentals (Weibel et al, 2004;Weibel and Hoppeler, 2005), the peak aerobic demands associated with maximum energy output by muscle are met via the commensurate, matched oxygen supply system from the lungs to the muscle mitochondria via the expanded Sminthopsis crassicaudata data are from the present study; B. penicillata, M. rufus and M. domestica data are from previous studies Kram and Dawson, 1998;Schaeffer et al, 2003). Placental data are from Weibel et al (Weibel et al, 2004).…”

“…The volume of muscle, its total mitochondrial content and its overall vascular supply were essentially identical in the Macropodiformes to values seen in 'athletic' placental mammals. Haim et al (1995), other data from Hoppeler et al (1984); rat-kangaroo (Bettongia penicillata) data from Dawson (2003, 2012); short-tailed opossum (Monodelphis domestica), BMR from Dawson and Olson (1988), other data from Schaeffer et al (2003).…”

“…Available information is equivocal in regard to this question. The only marsupial for which comparable information is also available on MMR and on muscle and muscle mitochondria volumes (Table4) is the grey short-tailed opossum (Monodelphis domestica, Family: Didelphidae) (Schaeffer et al, 2003). The MMR of M. domestica is relatively low (Table4, Fig.1) and falls in line with those of the 'sedentary' placentals, not with 'athletic' small mammals such as the placental A. sylvaticus and the marsupials, S. crassicaudata and B. penicillata.…”

“…The only other marsupial for which comparable data are available is a South American opossum, Monodelphis domestica (Family: Didephidae) (M b ≈90g). It also has a comparatively large fAS (Dawson and Olson, 1988;Schaeffer et al, 2003) but its MMR does not reach an 'athletic' level, though the mitochondrial volume densities of its skeletal muscles are not lower than generally seen in similar sized placentals (Schaeffer et al, 2003). However, there is support for relatively high aerobic capabilities extending to smaller marsupials.…”