Minimal Seasonal Alterations in the Skeletal Muscle of Captive Brown Bears

Hershey, John D.; Robbins, Charles T.; Nelson, O. Lynne; Lin, David C.

doi:10.1086/524391

Cited by 50 publications

(57 citation statements)

References 56 publications

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“…During mid-hibernation, bears will maintain a curled fetallike position to conserve energy and water, and they will change position as infrequently as once every 2days . Despite this prolonged inactivity, skeletal muscle atrophy is minimal in hibernating American black bears (Ursus americanus) and brown bears (Ursus arctos) (Tinker et al, 1998;Harlow et al, 2001;Lohuis et al, 2007;Hershey et al, 2008). Specifically, when comparing hibernation and non-hibernation muscle properties, there is no statistically significant change in muscle fiber size (Tinker et al, 1998;Hershey et al, 2008) and maximal force elicited by electrical stimulation decreases by only 23% (Harlow et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

“…Despite this prolonged inactivity, skeletal muscle atrophy is minimal in hibernating American black bears (Ursus americanus) and brown bears (Ursus arctos) (Tinker et al, 1998;Harlow et al, 2001;Lohuis et al, 2007;Hershey et al, 2008). Specifically, when comparing hibernation and non-hibernation muscle properties, there is no statistically significant change in muscle fiber size (Tinker et al, 1998;Hershey et al, 2008) and maximal force elicited by electrical stimulation decreases by only 23% (Harlow et al, 2001). This is in contrast to other mammals, for which weight-bearing activities are normally crucial to maintaining skeletal muscle mass, morphology and protein composition (Baldwin and Haddad, 2001).…”

Section: Introductionmentioning

confidence: 99%

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

Lin

Hershey

Mattoon

et al. 2012

Journal of Experimental Biology

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SUMMARYHibernating bears retain most of their skeletal muscle strength despite drastically reduced weight-bearing activity. Regular neural activation of muscles is a potential mechanism by which muscle atrophy could be limited. However, both mechanical loading and neural activity are usually necessary to maintain muscle size. An alternative mechanism is that the signaling pathways related to the regulation of muscle size could be altered so that neither mechanical nor neural inputs are needed for retaining strength. More specifically, we hypothesized that muscles in hibernating bears are resistant to a severe reduction in neural activation. To test this hypothesis, we unilaterally transected the common peroneal nerve, which innervates ankle flexor muscles, in hibernating and summer-active brown bears (Ursus arctos). In hibernating bears, the long digital extensor (LDE) and cranial tibial (CT) musculotendon masses on the denervated side decreased after 11weeks post-surgery by 18±11 and 25±10%, respectively, compared with those in the intact side. In contrast, decreases in musculotendon masses of summer-active bears after denervation were 61±4 and 58±5% in the LDE and CT, respectively, and significantly different from those of hibernating bears. The decrease due to denervation in summer-active bears was comparable to that occurring in other mammals. Whole-muscle cross-sectional areas (CSAs) measured from ultrasound images and myofiber CSAs measured from biopsies decreased similarly to musculotendon mass. Thus, hibernating bears alter skeletal muscle catabolic pathways regulated by neural activity, and exploration of these pathways may offer potential solutions for disuse atrophy of muscles.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Lin

Hershey

Mattoon

et al. 2012

Journal of Experimental Biology

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“…These findings suggest that Weddell seals may be physiologically "programmed" to withstand periods of reduced activity while maintaining muscle integrity. Wild animals may need to forage effectively and escape predation after such periods of reduced activities, and indeed, similar patterns of atrophy resistance have been observed in hibernating bats and rodents, and winter lethargy in bears (Lohuis et al 2007;Hershey et al 2008;Lee et al 2008;Nowell et al 2011). Despite being composed of primarily slow-oxidative fibers that are particularly vulnerable to atrophy, Weddell seal muscles maintained aerobic MHC profiles.…”

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confidence: 65%

Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities

2015

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β-hydroxyacyl CoA dehydrogenase) were likewise maintained across the year. The preservation of aerobic capacity is likely critical to foraging capabilities, so that following the molt Weddell seals can rapidly regain body mass at the start of winter foraging. In contrast, muscle lactate dehydrogenase activity, a marker of anaerobic metabolism, exhibited seasonal plasticity in this diving top predator and was lowest after the summer period of reduced activity. Total body oxygen stores Abstract Adult Weddell seals (Leptonychotes weddellii) haul-out on the ice in October/November (austral spring) for the breeding season and reduce foraging activities for ~4 months until their molt in the austral fall (January/February). After these periods, animals are at their leanest and resume actively foraging for the austral winter. In mammals, decreased exercise and hypoxia exposure typically lead to decreased production of O 2 -carrying proteins and muscle wasting, while endurance training increases aerobic potential. To test whether similar effects were present in marine mammals, this study compared the physiology of 53 post-molt female Weddell seals in the austral fall to 47 pre-breeding females during the spring in McMurdo Sound, Antarctica. Once body mass and condition (lipid) were controlled for, there were no seasonal changes in total body oxygen (TBO 2 ) stores. Within each season, hematocrit and hemoglobin values were negatively correlated with animal size, and larger animals had lower mass-specific TBO 2 stores. But because larger seals had lower mass-specific metabolic rates, their calculated aerobic dive limit was similar to smaller seals. Indicators of muscular efficiency, myosin heavy chain composition, myoglobin concentrations, and aerobic enzyme activities (citrate synthase and Keywords

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“…After five months of hibernation, the average cross-sectional areas of fast and slow fibres remained unchanged from summer to winter, while muscle protein concentration decreased by only 8% (Hershey et al, 2008). Like squirrels, the magnitude of muscle wasting in bears is dependent on the type of muscle studied.…”

Section: Hibernating Mammals As Models Of Muscle Disuse Atrophymentioning

confidence: 92%

“…A recent study examined the biceps femoris muscle of summer active and winter hibernating brown bears (Ursus arctos) (Hershey et al, 2008).…”

Section: Hibernating Mammals As Models Of Muscle Disuse Atrophymentioning

confidence: 99%

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

Reilly¹

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In most mammals, extended inactivity or immobilisation of skeletal muscle (e.g. bedrest, limb-casting or hindlimb unloading) results in muscle disuse atrophy, a process which is characterised by the loss of skeletal muscle mass and function. In stark contrast, animals that experience natural bouts of prolonged muscle inactivity, such as hibernating mammals and aestivating frogs, consistently exhibit limited or no change in either skeletal muscle size or contractile performance. While many of the factors regulating skeletal muscle mass are known, little information exists as to what mechanisms protect against muscle atrophy in some species.Green-striped burrowing frogs (Cyclorana alboguttata) survive in arid environments by burrowing underground and entering into a deep, prolonged metabolic depression known as aestivation. Throughout aestivation, C. alboguttata is immobilised within a cast-like cocoon of shed skin and ceases feeding and moving. Remarkably, these frogs exhibit very little muscle atrophy despite extended disuse and fasting. The overall aim of the current research study was to gain a better understanding of the physiological, cellular and molecular basis underlying resistance to muscle disuse atrophy in C. alboguttata.The first aim of this study was to develop a genomic resource for C. alboguttata by sequencing and functionally characterising its skeletal muscle transcriptome, and to conduct gene expression profiling to identify transcriptional pathways associated with metabolic depression and maintenance of muscle function in aestivating burrowing frogs. A transcriptome was assembled using next-generation short read sequencing followed by a comparison of gene expression patterns between active and four-month aestivating C.alboguttata. This identified a complex suite of gene expression changes that occur in muscle during aestivation and provides evidence that aestivation in burrowing frogs involves transcriptional regulation of genes associated with cytoskeletal remodelling, avoidance of oxidative stress, energy metabolism, the cell stress response, cell death and survival and epigenetic modification. In particular, the expression levels of genes encoding cell cycle regulatory-, pro-survival and chromatin remodelling proteins, such as serine/threonine-protein kinase Chk1, cell division protein kinase 2, survivin, vesicular overexpressed in cancer prosurvival protein 1 and histone-binding protein RBBP4, were upregulated in aestivators.The second aim of this study was to examine the potential role of mitochondrial ROS in the regulation of muscle mass and function during aestivation in C. alboguttata. In III mammals, muscle disuse atrophy has been associated with oxidative damage due to increased mitochondrial ROS production. C. alboguttata reduced skeletal muscle mitochondrial respiration by approximately 50% following four months of aestivation, while mitochondrial ROS production was more than 80% lower in aestivating skeletal muscle relative to controls when mitochondrial substrates were pre...

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Minimal Seasonal Alterations in the Skeletal Muscle of Captive Brown Bears

Cited by 50 publications

References 56 publications

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

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

Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities

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

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