Skeletal muscle is protected from disuse in hibernating dauria ground squirrels

Gao, Yunfang; Wang, Jun; Wang, Huiping; Feng, Ban; Dang, Kai; Wang, Qi; Hinghofer‐Szalkay, Helmut

doi:10.1016/j.cbpa.2011.11.009

Cited by 55 publications

(70 citation statements)

References 25 publications

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“…Wickler et al, 1991;Tinker et al, 1998;Nowell et al, 2011). In contrast to other mammalian disuse models, hibernating ground squirrels preserve slower oxidative fibers (types I and IIx) relative to fast glycolytic type IIb (Egginton et al, 2001;Rourke et al, 2004;Rourke et al, 2006;Hershey et al, 2008;Nowell et al, 2011;Gao et al, 2012;Bodine, 2013;Xu et al, 2013). This response may be a mechanism to preserve oxidative ability in skeletal muscles and to support a shift to a lipid-based metabolism.…”

Section: Research Articlementioning

confidence: 91%

“…Multiple studies document muscle preservation or limited atrophy during hibernation in rodents (e.g. Wickler et al, 1987;Steffen et al, 1991;Cotton and Harlow, 2010;Nowell et al, 2011;Gao et al, 2012;Andres-Mateos et al, 2013), suggesting that some degree of protection against inactivity may exist and that its regulation is muscle-type specific (e.g. Reid et al, 1995;Nowell et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Prioritization of skeletal muscle growth for emergence from hibernation

Hindle

Otis

Epperson

et al. 2014

Journal of Experimental Biology

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Mammalian hibernators provide an extreme example of naturally occurring challenges to muscle homeostasis. The annual hibernation cycle is characterized by shifts between summer euthermy with tissue anabolism and accumulation of body fat reserves, and winter heterothermy with fasting and tissue catabolism. The circannual patterns of skeletal muscle remodeling must accommodate extended inactivity during winter torpor, the motor requirements of transient winter active periods, and sustained activity following spring emergence. Muscle volume in 13-lined ground squirrels (Ictidomys tridecemlineatus) calculated from MRI upper hindlimb images (n=6 squirrels, n=10 serial scans) declined from hibernation onset, reaching a nadir in early February. Paradoxically, mean muscle volume rose sharply after February despite ongoing hibernation, and continued total body mass decline until April. Correspondingly, the ratio of muscle volume to body mass was steady during winter atrophy (October-February) but increased (+70%) from February-May, which significantly outpaced changes in liver or kidney examined by the same method. Generally stable myocyte cross-sectional area and density indicated that muscle remodeling is well regulated in this hibernator despite vastly altered seasonal fuel and activity levels. Body composition analysis by ECHO MRI showed lean tissue preservation throughout hibernation amid declining fat mass by end of winter. Muscle protein synthesis was 66% depressed in early but not late winter compared to a summer fasted baseline, while no significant changes were observed in the heart, liver or intestine, providing evidence that could support a transition in skeletal muscle regulation between early and late winter, prior to spring emergence and re-feeding.

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Section: Research Articlementioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Prioritization of skeletal muscle growth for emergence from hibernation

Hindle

Otis

Epperson

et al. 2014

Journal of Experimental Biology

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“…The majority of studies conducted on hamsters (Deveci and Egginton, 2002b;James et al, 2011), ground squirrels (Cotton and Harlow, 2010;Gao et al, 2012;James et al, 2013;Nowell et al, 2011;Steffen et al, 1991;Yang et al, 2014) and bats (Kim et al, 2000;Lee et al, 2008;Yacoe, 1983a) have shown relatively minor changes in muscle mass and protein content during hibernation, with most reporting 5-30% decreases in mass and 5-15% decreases in protein (Table 1). There is, however, some variation depending on species, specific muscles and sampling period.…”

Section: Morphological Changes During Hibernationmentioning

confidence: 99%

“…Here again, hibernation typically results in relatively minor changes in fiber CSA, with most studies showing a reduction of only 0-10% (mean change of −4.4% for type I fibers and −2.4% for type II fibers) associated with hibernation (Andres- Cotton and Harlow, 2010;Deveci and Egginton, 2002a;Gao et al, 2012;Hershey et al, 2008;Lee et al, 2008Lee et al, , 2010Malatesta et al, 2009;Tinker et al, 1998). However, at the extremes, a few studies have shown reductions in fiber CSA of between −30% and −55% (Agostini et al, 1991;Steffen et al, 1991).…”

Section: Morphological Changes During Hibernationmentioning

confidence: 99%

“…However, a number of studies on hibernators have shown only a marginal loss of oxidative type I fibers and a retention of fiber ratio throughout the winter (Agostini et al, 1991;Cotton and Harlow, 2010;Deveci and Egginton, 2002a;Nowell et al, 2011;Rourke et al, 2004a;Tinker et al, 1998). Perhaps more surprising are the number of studies showing a moderate increase in type I slow oxidative fiber ratio during the hibernation season despite animals spending 90% of the winter season in an essentially immobile state (Agostini et al, 1991;Gao et al, 2012;Hershey et al, 2008;Lazareva et al, 2012;Malatesta et al, 2009;Nowell et al, 2011;Rourke et al, 2006Rourke et al, , 2004a. In fact, hibernators on average increase type I fiber ratio by 25% relative to fiber ratios during the summer active period (Table 1).…”

Section: Morphological Changes During Hibernationmentioning

confidence: 99%

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Skeletal muscle mass and composition during mammalian hibernation

Cotton

2016

Journal of Experimental Biology

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Hibernation is characterized by prolonged periods of inactivity with concomitantly low nutrient intake, conditions that would typically result in muscle atrophy combined with a loss of oxidative fibers. Yet, hibernators consistently emerge from winter with very little atrophy, frequently accompanied by a slight shift in fiber ratios to more oxidative fiber types. Preservation of muscle morphology is combined with downregulation of glycolytic pathways and increased reliance on lipid metabolism instead. Furthermore, while rates of protein synthesis are reduced during hibernation, balance is maintained by correspondingly low rates of protein degradation. Proposed mechanisms include a number of signaling pathways and transcription factors that lead to increased oxidative fiber expression, enhanced protein synthesis and reduced protein degradation, ultimately resulting in minimal loss of skeletal muscle protein and oxidative capacity. The functional significance of these outcomes is maintenance of skeletal muscle strength and fatigue resistance, which enables hibernating animals to resume active behaviors such as predator avoidance, foraging and mating immediately following terminal arousal in the spring.

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Metabolic Flexibility: Hibernation, Torpor, and Estivation

Staples

2016

Comprehensive Physiology

136

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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Skeletal muscle is protected from disuse in hibernating dauria ground squirrels

Cited by 55 publications

References 25 publications

Prioritization of skeletal muscle growth for emergence from hibernation

Prioritization of skeletal muscle growth for emergence from hibernation

Skeletal muscle mass and composition during mammalian hibernation

Metabolic Flexibility: Hibernation, Torpor, and Estivation

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