Autophagy and Akt-mTOR signaling display periodic oscillations during torpor-arousal cycles in oxidative skeletal muscle of Daurian ground squirrels (Spermophilus dauricus)

Chang, Hui; Peng, Xin; Xia, Yan; Zhang, Jie; Xu, Shenhui; Wang, Huiping; Wang, Zhe; Ma, Xiufeng; Gao, Yunfang

doi:10.1007/s00360-019-01245-5

Cited by 17 publications

(13 citation statements)

References 49 publications

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“…The consensus finding is that Akt activity is highly suppressed during torpor. The evidence supporting this includes a significant reduction in the phosphorylation state of the Akt activating residue Ser-473 [ 16 , 34 , 35 , 36 , 37 ]. Enzymatic assays have also shown that Akt purified from tissue of hibernating ground squirrels is significantly less active as compared to the enzyme from euthermic control ground squirrels [ 34 , 38 ].…”

Section: Mtorc1 Control Of Cell Growth Under Metabolic Stressmentioning

confidence: 99%

mTOR Signaling in Metabolic Stress Adaptation

Storey

2021

Biomolecules

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The mechanistic target of rapamycin (mTOR) is a central regulator of cellular homeostasis that integrates environmental and nutrient signals to control cell growth and survival. Over the past two decades, extensive studies of mTOR have implicated the importance of this protein complex in regulating a broad range of metabolic functions, as well as its role in the progression of various human diseases. Recently, mTOR has emerged as a key signaling molecule in regulating animal entry into a hypometabolic state as a survival strategy in response to environmental stress. Here, we review current knowledge of the role that mTOR plays in contributing to natural hypometabolic states such as hibernation, estivation, hypoxia/anoxia tolerance, and dauer diapause. Studies across a diverse range of animal species reveal that mTOR exhibits unique regulatory patterns in an environmental stressor-dependent manner. We discuss how key signaling proteins within the mTOR signaling pathways are regulated in different animal models of stress, and describe how each of these regulations uniquely contribute to promoting animal survival in a hypometabolic state.

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Section: Mtorc1 Control Of Cell Growth Under Metabolic Stressmentioning

confidence: 99%

mTOR Signaling in Metabolic Stress Adaptation

Storey

2021

Biomolecules

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“…Troponin T plays an important role in regulating the protein system and can bind to tropomyosin to form a complex (Perry, 1998). Furthermore, various stress conditions (including fasting, oxidative stress and hypoxia) can induce autophagy as an adaptive physiological response to restore cell metabolism (Chang et al., 2020). Increased autophagy is a survival‐promoting mechanism rather than a death‐promoting mechanism and is an important prosurvival mechanism in myocardial hibernation.…”

Section: Introductionmentioning

confidence: 99%

“…The autophagy protein B‐cell lymphoma 2 interacting protein 1 (Beclin1) is necessary for the formation and maturation of autophagosomes (Choubey et al., 2014). Microtubule‐associated protein 1 light chain 3 (LC3) is a key marker of autophagy, which is downstream of the autophagic pathway and involved in the formation of autophagosomes (Chang et al., 2020; Klionsky et al., 2012). When phosphatidylethanolamine attaches to the cytosolic LC3‐I, LC3‐II is formed, which is then recruited to the autophagosome membrane (Jiang et al., 2010).…”

Section: Introductionmentioning

confidence: 99%

Differential protein metabolism and regeneration in hypertrophic diaphragm and atrophic gastrocnemius muscles in hibernating Daurian ground squirrels

Xia

Gao

Niu

et al. 2021

Experimental Physiology

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Are differences in the regulation of protein metabolism and regeneration involved in the different phenotypic adaptation mechanisms of muscle hypertrophy and atrophy in hibernators? Two fast-type muscles (diaphragm and gastrocnemius) in summer active and hibernating Daurian ground squirrels were selected to detect changes in crosssectional area (CSA) and protein expression indicative of protein synthesis metabolism (protein expression of P-Akt, P-mTORC1, P-S6K1 and P-4E-BP1), protein degradation metabolism (MuRF1, atrogin-1, calpain-1, calpain-2, calpastatin, desmin, troponin T, Beclin1 and LC3-II) and muscle regeneration (MyoD, myogenin and myostatin). In the hibernation group compared with the summer active group, the CSA of the diaphragm muscle increased significantly by 26.1%, whereas the CSA of the gastrocnemius muscle decreased significantly by 20.4%. Our study also indicated that increased protein synthesis, decreased protein degradation and increased muscle regenerative potential contributed to diaphragm muscle hypertrophy, whereas decreased protein synthesis, increased protein degradation and decreased muscle regenerative potential contributed to gastrocnemius muscle atrophy. In conclusion, the differences in muscle regeneration and regulatory pattern of protein metabolism might contribute to the different adaptive changes observed in the diaphragm and gastrocnemius muscles of ground squirrels.

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“…Intriguingly, skeletal muscle mass and strength are preserved during hibernation as well as the fiber size despite long periods of immobilization, contrary to what happens in non-hibernating mammals [11][12][13]. Protective mechanisms apparently take place in skeletal muscle during hibernation, which most likely involve, among others, inhibition of proteolysis, a decrease in autophagy and increased oxidative capacity [14,15]. The preservation of muscle mass during hibernation could also involve SC activation; however, the role of SCs in the prevention of atrophy has barely been investigated [16,17].…”

Section: Introductionmentioning

confidence: 99%

Satellite Cells in Skeletal Muscle of the Hibernating Dormouse, a Natural Model of Quiescence and Re-Activation: Focus on the Cell Nucleus

Malatesta

Costanzo

Cisterna

et al. 2020

Cells

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Satellite cells (SCs) participate in skeletal muscle plasticity/regeneration. Activation of SCs implies that nuclear changes underpin a new functional status. In hibernating mammals, periods of reduced metabolic activity alternate with arousals and resumption of bodily functions, thereby leading to repeated cell deactivation and reactivation. In hibernation, muscle fibers are preserved despite long periods of immobilization. The structural and functional characteristics of SC nuclei during hibernation have not been investigated yet. Using ultrastructural and immunocytochemical analysis, we found that the SCs of the hibernating edible dormouse, Glis glis, did not show apoptosis or necrosis. Moreover, their nuclei were typical of quiescent cells, showing similar amounts and distributions of heterochromatin, pre-mRNA transcription and processing factors, as well as paired box protein 7 (Pax7) and the myogenic differentiation transcription factor D (MyoD), as in euthermia. However, the finding of accumulated perichromatin granules (i.e., sites of storage/transport of spliced pre-mRNA) in SC nuclei of hibernating dormice suggested slowing down of the nucleus-to-cytoplasm transport. We conclude that during hibernation, SC nuclei maintain similar transcription and splicing activity as in euthermia, indicating an unmodified status during immobilization and hypometabolism. Skeletal muscle preservation during hibernation is presumably not due to SC activation, but rather to the maintenance of some functional activity in myofibers that is able to counteract muscle wasting.

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Autophagy and Akt-mTOR signaling display periodic oscillations during torpor-arousal cycles in oxidative skeletal muscle of Daurian ground squirrels (Spermophilus dauricus)

Cited by 17 publications

References 49 publications

mTOR Signaling in Metabolic Stress Adaptation

mTOR Signaling in Metabolic Stress Adaptation

Differential protein metabolism and regeneration in hypertrophic diaphragm and atrophic gastrocnemius muscles in hibernating Daurian ground squirrels

Satellite Cells in Skeletal Muscle of the Hibernating Dormouse, a Natural Model of Quiescence and Re-Activation: Focus on the Cell Nucleus

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