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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)

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Abstract

Whether hibernation accelerates or suppresses autophagy is still unknown. In the current study, we examined changes in autophagy in oxidative soleus (SOL) muscle in summer active (SA), pre-hibernation (PRE), torpor (TOR), interbout arousal (IBA), and post-hibernation groups of Daurian ground squirrels (Spermophilus dauricus). Here, the SOL muscle showed no significant atrophy during hibernation in regard to muscle wet weight, fiber cross-sectional area, or MuRF1 protein level. Autophagy-related proteins beclin1 and Atg7 increased significantly, whereas LC3-II decreased significantly in the PRE group compared with the SA group. However, neither the expression nor activity of cathepsin L showed any differences between the SA and PRE groups. In addition, beclin1, LC3-II, and the LC3-II/LC3-I ratio increased, p62 decreased, LC3 puncta increased, p62 puncta decreased, and cathepsin L activity increased in the TOR group compared with the PRE group. In contrast, beclin1, LC3-II, and the LC3-II/LC3-I ratio decreased, p62 increased, LC3 puncta decreased, p62 puncta increased, and cathepsin L activity declined in the IBA group compared with the TOR group. Moreover, the phosphorylation of Akt (Ser473) and mTOR (Ser2448) changed significantly during hibernation and showed an inverse relationship with autophagy changes. In conclusion, autophagy proteins displayed periodic oscillation in the torpor-arousal cycle, which may be advantageous in maintaining SOL muscle mass during the entire hibernation period. Furthermore, the Akt-mTOR signaling was decreased in TOR and increased in IBA group in the SOL muscle of Daurian ground squirrels during hibernation.

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Abbreviations

SA:

Summer active

PRE:

Pre-hibernation

TOR:

Torpor

IBA:

Interbout arousals

POST:

Post-hibernation

SOL:

Soleus muscle

CSA:

Cross-sectional area

MuRF1:

Muscle RING finger 1

beclin1:

Autophagy-related-6

LC3:

Microtubule-associated protein 1 light chain 3

p62:

SQSTM1/sequestosome 1

Atg7:

Autophagy-related-7

Akt:

Protein kinase B

mTOR:

Mammalian target of rapamycin

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Acknowledgements

This work was supported by funds from the National Natural Science Foundation of China (Grant Nos. 31640072 and 31772459).

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  1. Hui Chang, Xin Peng and Xia Yan are equal contributors.

Authors and Affiliations

  1. Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi’an, 710069, People’s Republic of China

    Hui Chang, Huiping Wang & Yunfang Gao

  2. Key Laboratory of Resource Biology and Biotechnology in Western China, College of Life Sciences, Northwest University, Ministry of Education, 229# North Taibai Road, Xi’an, 710069, People’s Republic of China

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

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  1. Hui Chang
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Contributions

HC and YG conceived and designed the experiments. XP, HC, XY, JZ, SX, HW, ZW and XM performed the experiments. XP and HC analyzed the data. HC wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Yunfang Gao.

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The authors declare that they have no competing interests.

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All procedures were approved by the animal care committee of the Wildlife Protection Society of China (SL-2012-42) and the Northwest University Ethics Committee.

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Communicated by H.V. Carey.

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Chang, H., Peng, X., Yan, X. et al. Autophagy and Akt-mTOR signaling display periodic oscillations during torpor-arousal cycles in oxidative skeletal muscle of Daurian ground squirrels (Spermophilus dauricus). J Comp Physiol B 190, 113–123 (2020). https://doi.org/10.1007/s00360-019-01245-5

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