Maintenance of slow type I myosin protein and mRNA expression in overwintering prairie dogs (Cynomys leucurus and ludovicianus) and black bears (Ursus americanus)

Abstract

Hibernating mammals have the remarkable ability to withstand long periods of fasting and reduced activity with dramatic maintenance of skeletal muscle function and protein composition. We investigated several hindlimb muscles of white-tailed prairie dogs (Cynomys leucurus) and black bears (Ursus americanus), two very different hibernators who are dormant and fasting during winter. The black-tailed prairie dog (C. ludovicianus) remains active during winter, but suffers minor skeletal muscle atrophy; nevertheless, they also demonstrate apparent skeletal muscle adaptations. Using SDS-PAGE, we measured myosin protein isoform profiles before and after the hibernation season. All species maintained or increased levels of slow myosin, despite the collective physiological challenges of hypophagia and reduced activity. This contrasts markedly with standard mammalian models of skeletal muscle inactivity and atrophy predicting significant loss of slow myosin. A mechanism for changes in myosin isoforms was investigated using reverse-transcription PCR, following partial sequencing of the adult MHC isoforms in C. leucurus and U. americanus. However, mRNA expression was not well correlated with changes in MHC protein isoforms, and other synthesis and degradation pathways may be involved besides transcriptional control. The muscles of hibernating mammals demonstrate surprising and varied physiological responses to inactivity and atrophy with respect to slow MHC expression.

Daily torpor reduces mass and changes stress and power output of soleus and EDL muscles in the Djungarian hamster, Phodopus sungorus

“…Recent studies assessing the relative expression of myosin isoforms in hibernating mammals have demonstrated either a fast to slow muscle fibre type transition or no change in fibre type. There were fast to slow shifts in proportional expression of myosin heavy chain in gastrocnemius and plantaris muscle in ground squirrels (Rourke et al, 2004;Nowell et al, 2011), and soleus in white tailed prairie dogs and biceps femoris in black bears (Rourke et al, 2006). However, there were no changes in myosin heavy chain expression in the soleus or diaphragm muscle in ground squirrels (Rourke et al, 2004), pectoral muscle in bats (Lee et al, 2008), gastrocnemius in black bears (Rourke et al, 2006) or biceps femoris in captive brown bears (Hershey et al, 2008).…”

“…There were fast to slow shifts in proportional expression of myosin heavy chain in gastrocnemius and plantaris muscle in ground squirrels (Rourke et al, 2004;Nowell et al, 2011), and soleus in white tailed prairie dogs and biceps femoris in black bears (Rourke et al, 2006). However, there were no changes in myosin heavy chain expression in the soleus or diaphragm muscle in ground squirrels (Rourke et al, 2004), pectoral muscle in bats (Lee et al, 2008), gastrocnemius in black bears (Rourke et al, 2006) or biceps femoris in captive brown bears (Hershey et al, 2008). Where significant changes in myosin heavy chain expression occur, we would expect concomitant alterations in the contractile rate of skeletal muscle (Harridge, 2007;Canepari et al, 2010).…”

Skeletal muscles of hibernating brown bears are unusually resistant to effects of denervation

“…Namely, shivering in hibernating bears has been reported (Harlow et al, 2004;Toien et al, 2011), and this activity has been implicated in helping retard muscle atrophy during hibernation (Harlow et al, 2004;Rourke et al, 2006;Lohuis et al, 2007). However, the drastic reduction in weight-bearing activities implies that both the amounts of physiological mechanical loading and neural activation of the muscle are abnormally small.…”

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

“…It is conceivable that burrowing frogs might remodel and preserve existing muscle contractile proteins in the early stages of aestivation, precluding the requirement to transcribe actin and myosin genes in the middle and latter stages of dormancy. These findings are consistent with other studies of various species' of hibernating mammal which have shown that myosin heavy chain protein expression is often maintained despite prolonged muscle inactivity (Rourke et al, 2006;Rourke et al, 2004). While muscle contractile activity ceases during dormancy, skeletal muscle is also challenged to retain structural integrity despite disuse and starvation.…”