The effects of hibernation on the contractile and biochemical properties of skeletal muscles in the thirteen-lined ground squirrel, <i>Ictidomys tridecemlineatus</i>

James, Rob S.; Staples, James F.; Brown, Jason C. L.; Tessier, Shannon N.; Storey, Kenneth B.

doi:10.1242/jeb.080663

Cited by 44 publications

(58 citation statements)

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“…Similar to aestivating C. alboguttata, total antioxidant capacity was found to be elevated in the gastrocnemius muscle of torpid thirteen-lined ground squirrels relative to active animals (James et al, 2013). These results demonstrate that increases in skeletal muscle antioxidants occur during metabolic depression, which could explain decreased rates of mitochondrial ROS production.…”

Section: Effect Of Aestivation On Ros Production and Calpains In C Amentioning

confidence: 89%

“…Though many studies have investigated muscle antioxidant levels during dormancy and/or arousal in aestivators and hibernators (Allan and Storey, 2012;Hudson et al, 2006;James et al, 2013;Ramos-Vasconcelos and Hermes-Lima, 2003;Young et al, 2013), little is known about changes in mitochondrial ROS production and this has only recently received experimental attention in natural models of muscle disuse (Brown et al, 2012). Additionally, relatively few physiological studies examine mitochondrial function using permeabilised fibres, tissues or cells.…”

Section: Discussionmentioning

confidence: 99%

“…However, the amount of muscle tissue loss can vary in hibernating squirrels depending on the type of muscle examined. James et al (James et al, 2013) reported no loss of mass or tension in soleus muscle of S. tridecemlineatus following three months of hibernation, whereas a 14% loss was found in the gastrocnemius and 43% loss in the semitendinous muscles of the golden-mantled ground squirrel (Spermophilus lateralis) (Wickler et al, 1991). Muscle atrophy develops early on in hibernating S. lateralis but does not advance in the final 3 months (Nowell et al, 2011), a result which is similar to that which occurs during prolonged bed rest in humans (Adams et al, 2003;Phillips et al, 2009).…”

Section: Hibernating Mammals As Models Of Muscle Disuse Atrophymentioning

confidence: 99%

“…Although mechanistic links between ROS and both proteolysis and protein synthesis have been demonstrated in clinical models of muscle disuse atrophy (Powers et al, 2011), almost nothing is known about the effects of ROS signalling during dormancy. However, one study did report an increase in antioxidant capacity in hibernating muscle which might protect cells by scavenging ROS (James et al, 2013). This is important given that throughout dormancy the capacity to replace ROS-damaged molecules is compromised as a consequence of drastically reduced rates of transcription and translation .…”

Section: Hibernating Mammals As Models Of Muscle Disuse Atrophymentioning

confidence: 99%

“…We note there was particularly high variation in ROS production among control frogs at higher, saturating substrate concentrations, precluding a statistically-significant difference between aestivators and controls in this latter part of the experiment. In a recent study, Brown et al (Brown et al, 2013) suggested that sub-saturating mitochondrial substrate (succinate) concentrations are more physiologically-relevant in vivo. Indeed, the concentration of succinate in many mammalian tissues is considered to be low, in the 0.2-0.5 mM range (Starkov, 2008).…”

Section: Ros (H2o2) Productionmentioning

confidence: 99%

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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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Section: Effect Of Aestivation On Ros Production and Calpains In C Amentioning

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: Hibernating Mammals As Models Of Muscle Disuse Atrophymentioning

confidence: 99%

Section: Hibernating Mammals As Models Of Muscle Disuse Atrophymentioning

confidence: 99%

Section: Ros (H2o2) Productionmentioning

confidence: 99%

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

Reilly¹

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Metabolic Flexibility: Hibernation, Torpor, and Estivation

Staples

2016

Comprehensive Physiology

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127

116

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Many environmental conditions can constrain the ability of animals to obtain sufficient food energy, or transform that food energy into useful chemical forms. To survive extended periods under such conditions animals must suppress metabolic rate to conserve energy, water, or oxygen. Amongst small endotherms, this metabolic suppression is accompanied by and, in some cases, facilitated by a decrease in core body temperature-hibernation or daily torpor-though significant metabolic suppression can be achieved even with only modest cooling. Within some ectotherms, winter metabolic suppression exceeds the passive effects of cooling. During dry seasons, estivating ectotherms can reduce metabolism without changes in body temperature, conserving energy reserves, and reducing gas exchange and its inevitable loss of water vapor. This overview explores the similarities and differences of metabolic suppression among these states within adult animals (excluding developmental diapause), and integrates levels of organization from the whole animal to the genome, where possible. Several similarities among these states are highlighted, including patterns and regulation of metabolic balance, fuel use, and mitochondrial metabolism. Differences among models are also apparent, particularly in whether the metabolic suppression is intrinsic to the tissue or depends on the whole-animal response. While in these hypometabolic states, tissues from many animals are tolerant of hypoxia/anoxia, ischemia/reperfusion, and disuse. These natural models may, therefore, serve as valuable and instructive models for biomedical research.

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Integrative Physiology of Fasting

Secor

Carey

2016

Comprehensive Physiology

132

144

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Extended bouts of fasting are ingrained in the ecology of many organisms, characterizing aspects of reproduction, development, hibernation, estivation, migration, and infrequent feeding habits. The challenge of long fasting episodes is the need to maintain physiological homeostasis while relying solely on endogenous resources. To meet that challenge, animals utilize an integrated repertoire of behavioral, physiological, and biochemical responses that reduce metabolic rates, maintain tissue structure and function, and thus enhance survival. We have synthesized in this review the integrative physiological, morphological, and biochemical responses, and their stages, that characterize natural fasting bouts. Underlying the capacity to survive extended fasts are behaviors and mechanisms that reduce metabolic expenditure and shift the dependency to lipid utilization. Hormonal regulation and immune capacity are altered by fasting; hormones that trigger digestion, elevate metabolism, and support immune performance become depressed, whereas hormones that enhance the utilization of endogenous substrates are elevated. The negative energy budget that accompanies fasting leads to the loss of body mass as fat stores are depleted and tissues undergo atrophy (i.e., loss of mass). Absolute rates of body mass loss scale allometrically among vertebrates. Tissues and organs vary in the degree of atrophy and downregulation of function, depending on the degree to which they are used during the fast. Fasting affects the population dynamics and activities of the gut microbiota, an interplay that impacts the host's fasting biology. Fasting-induced gene expression programs underlie the broad spectrum of integrated physiological mechanisms responsible for an animal's ability to survive long episodes of natural fasting.

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The effects of hibernation on the contractile and biochemical properties of skeletal muscles in the thirteen-lined ground squirrel, Ictidomys tridecemlineatus

Cited by 44 publications

References 46 publications

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

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

Metabolic Flexibility: Hibernation, Torpor, and Estivation

Integrative Physiology of Fasting

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