Changes in calpains and calpastatin in the soleus muscle of Daurian ground squirrels during hibernation

Yang, Chenxi; He, Yue; Gao, Yunfang; Wang, Huiping; Goswami, Nandu

doi:10.1016/j.cbpa.2014.05.022

Cited by 38 publications

(44 citation statements)

References 32 publications

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“…Nevertheless, our enzyme activity data are supported by the observation that the activities of calpain 1 and 2 were also maintained in the soleus muscle of hibernating Daurian ground squirrels (Spermophilus dauricus) (Yang et al, 2014). In contrast to aestivators and hibernators, enzyme activity levels of calpain 1 and 2 have been shown to be increased during hindlimb suspension in rodents (Enns et al, 2007;Taillandier et al, 1996;Yang et al, 2014).…”

Section: Discussionsupporting

confidence: 75%

“…In agreement with our study, Lee et al (Lee et al, 2010) found no difference in the protein abundance of calpain 1 in pectoralis muscles of summer-active and 3-month hibernating Murina leucogaster bats, a species which also undergoes minimal loss in muscle mass despite inactivity during dormancy. Protein levels of both calpain 1 and 2 were also recently found to be unaffected by hibernation in squirrels (Yang et al, 2014). Cast immobilisation in typical rodent models has been shown to be associated with increased autolysis of calpain 1 and calpain 2 (Min et al, 2011;Talbert et al, 2013a;Talbert et al, 2013b;Vermaelen et al, 2007), highlighting the different response of C. alboguttata muscle to extended disuse.…”

Section: Discussionmentioning

confidence: 95%

“…In contrast to aestivators and hibernators, enzyme activity levels of calpain 1 and 2 have been shown to be increased during hindlimb suspension in rodents (Enns et al, 2007;Taillandier et al, 1996;Yang et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…However, calpastatin mRNA was unaffected by 4 months of aestivation (Table 4.3) suggesting it too is inactive during this time. Yang et al found that calpastatin protein abundance increased almost 200% in hibernating squirrels compared with control animals (Yang et al, 2014) and suggested this to be the most likely mechanism underpinning inhibition of disuse atrophy in dormant S.…”

Section: Discussionmentioning

confidence: 99%

“…higher in muscle of hibernating S. dauricus compared with control squirrels (Yang et al, 2014), indicating that this could be an important mechanism contributing to inhibition of disuse atrophy throughout dormancy. Aestivating C. alboguttata are also likely to have the capacity to tightly regulate cellular calcium homeostasis, which would prevent unwanted calpain proteolytic activity.…”

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

confidence: 94%

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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: Discussionsupporting

confidence: 75%

Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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

confidence: 94%

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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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Stress‐responsive microRNAs are involved in re‐programming of metabolic functions in hibernators

Arfat

Chang

Gao

2017

Journal Cellular Physiology

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Mammalian hibernation includes re-programing of metabolic capacities, partially, encouraged by microRNAs (miRNAs). Albeit much is known about the functions of miRNAs, we need learning on low temperature miRNAs target determination. As hibernators can withstand low body temperatures (TB) for a long time without anguish tissue damage, understanding the means and mechanisms that empower them to do as such are of restorative intrigue. Nonetheless, these mechanisms by which miRNAs and the hibernators react to stressful conditions are not much clear. It is evident from recent data that the gene expression and the translation of mRNA to protein are controlled by miRNAs. The miRNAs also influence regulation of major cellular processes. As the significance of miRNAs in stress conditions adaptation are getting clearer, this audit article abridges the key alterations in miRNA expression and the mechanism that facilitates stress survival.

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Unexpected regulation pattern of the IKKβ/NF‐κB/MuRF1 pathway with remarkable muscle plasticity in the Daurian ground squirrel (Spermophilus dauricus)

Wei¹,

Gong²,

Fu³

et al. 2018

Journal Cellular Physiology

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As a typical hibernator, the Daurian ground squirrel (Spermophilus dauricus) spends considerable time in a state of reduced activity with prolonged fasting. Despite this, they experience little muscle atrophy and have thus become an interesting anti-disuse muscle atrophy model. The IKKβ/NF-κB signaling pathway is significant to muscle atrophy due to the protein degradation resulting from the upregulation of the E3 ubiquitin ligase MuRF1. The current study showed that the IKKβ/NF-κB signaling pathway and MuRF1 maintained relatively steady mRNA and protein expression levels, with little muscle atrophy observed in the soleus (slow-twitch, SOL) or extensor digitorum longus (fast-twitch, EDL) during hibernation (HIB); however, mRNA expression significantly increased in the SOL and EDL muscle during interbout arousal (IBA), as did the MuRF1 mRNA level in the SOL and MuRF1 protein level in the EDL. Interestingly, the expressions of p50 and MuRF1 significantly increased during HIB in the gastrocnemius (mixed muscle, GAS) and showed moderate atrophy, but dramatically decreased during IBA. Elevated IKKβ and p50 mRNA and protein expression in the cardiac muscle (CM) during HIB did not accompany increased MuRF1 expression or muscle wasting. Importantly, almost all increased or decreased indicators in the tested tissues recovered to pre-hibernation levels after HIB. This is the first study to report on the unexpected regulation of the IKKβ/NF-κB/MuRF1 pathway with remarkable muscle plasticity in Daurian ground squirrels during hibernation. Furthermore, we found that different types of muscles exhibited different strategies to cope with prolonged hibernation-induced disuse muscle atrophy.

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Changes in calpains and calpastatin in the soleus muscle of Daurian ground squirrels during hibernation

Cited by 38 publications

References 32 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

Stress‐responsive microRNAs are involved in re‐programming of metabolic functions in hibernators

Unexpected regulation pattern of the IKKβ/NF‐κB/MuRF1 pathway with remarkable muscle plasticity in the Daurian ground squirrel (Spermophilus dauricus)

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