Surviving winter on the Qinghai-Xizang Plateau: Extensive reversible protein phosphorylation plays a dominant role in regulating hypometabolism in hibernating <i>Nanorana parkeri</i>

Yong-Gang Niu; Deng-Bang Wei; Xue-Jing Zhang; Ti-Sen Xu; Xiang-Yong Li; Hai-Ying Zhang; Zhi-Fang An; Kenneth B. Storey; Qiang Chen

doi:10.24272/j.issn.2095-8137.2023.171

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Yong-Gang Niu, Deng-Bang Wei, Xue-Jing Zhang, Ti-Sen Xu, Xiang-Yong Li, Hai-Ying Zhang, Zhi-Fang An, Kenneth B. Storey, Qiang Chen. Surviving winter on the Qinghai-Xizang Plateau: Extensive reversible protein phosphorylation plays a dominant role in regulating hypometabolism in hibernating Nanorana parkeri. Zoological Research, 2024, 45(1): 1-12. doi: 10.24272/j.issn.2095-8137.2023.171

Citation:

Yong-Gang Niu, Deng-Bang Wei, Xue-Jing Zhang, Ti-Sen Xu, Xiang-Yong Li, Hai-Ying Zhang, Zhi-Fang An, Kenneth B. Storey, Qiang Chen. Surviving winter on the Qinghai-Xizang Plateau: Extensive reversible protein phosphorylation plays a dominant role in regulating hypometabolism in hibernating Nanorana parkeri. Zoological Research, 2024, 45(1): 1-12. doi: 10.24272/j.issn.2095-8137.2023.171

Citation:

Yong-Gang Niu, Deng-Bang Wei, Xue-Jing Zhang, Ti-Sen Xu, Xiang-Yong Li, Hai-Ying Zhang, Zhi-Fang An, Kenneth B. Storey, Qiang Chen. Surviving winter on the Qinghai-Xizang Plateau: Extensive reversible protein phosphorylation plays a dominant role in regulating hypometabolism in hibernating Nanorana parkeri. Zoological Research, 2024, 45(1): 1-12. doi: 10.24272/j.issn.2095-8137.2023.171

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Surviving winter on the Qinghai-Xizang Plateau: Extensive reversible protein phosphorylation plays a dominant role in regulating hypometabolism in hibernating Nanorana parkeri

doi: 10.24272/j.issn.2095-8137.2023.171

1.
Department of Life Sciences, Dezhou University, Dezhou, Shandong 253023, China
2.
State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, Qinghai 810016, China
3.
School of Life Sciences, Lanzhou University, Lanzhou, Gansu 730000, China
4.
Department of Biology, Carleton University, Ottawa, ON K1S 5B6, Canada

The mass spectrometry proteomic and phosphoproteomic data have been deposited in the ProteomeXchange Consortium via the PRIDE partner repository (dataset identifier PXD042165). The dataset is deposited in the Science Data Bank (https://www.scidb.cn/) under DOI: 10.57760/sciencedb.j00139.00079.
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
Y.G.N. and D.B.W. conceived and designed the project. Y.G.N., X.J.Z., T.S.X., X.Y.L., H.Y.Z., and Z.F.A. performed the experiments. Y.G.N. and X.J.Z. analyzed the data. T.S.X. and X.Y.L. collected the samples. Y.G.N. and X.J.Z. prepared the first draft of the manuscript. D.B.W., K.B.S., and Q.C. reviewed and edited the manuscript. All authors read and approved the final version of the manuscript.

Funds: This work was supported by the National Natural Science Foundation of China (32001110), Training Program for Cultivating High-level Talents by the China Scholarship Council (2021lxjjw01), and Open Project of State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University (2021-KF-004)

More Information

Corresponding author: E-mail: yonggangniu@126.com
Received Date: 2023-07-05
Accepted Date: 2023-07-19

Published Online: 2023-09-12

Abstract

Abstract

Changes in protein abundance and reversible protein phosphorylation (RPP) play important roles in regulating hypometabolism but have never been documented in overwintering frogs at high altitudes. To test the hypothesis that protein abundance and phosphorylation change in response to winter hibernation, we conducted a comprehensive and quantitative proteomic and phosphoproteomic analysis of the liver of the Xizang plateau frog, Nanorana parkeri, living on the Qinghai-Xizang (Tibet) Plateau (QTP). In total, 5 170 proteins and 5 695 phosphorylation sites in 1 938 proteins were quantified. Based on proteomic analysis, 674 differentially expressed proteins (438 up-regulated, 236 down-regulated) were screened in hibernating N. parkeri versus summer individuals. Functional enrichment analysis revealed that higher expressed proteins in winter were significantly enriched in immune-related signaling pathways, whereas lower expressed proteins were mainly involved in metabolic processes. A total of 4 251 modified sites (4 147 up-regulated, 104 down-regulated) belonging to 1 638 phosphoproteins (1 555 up-regulated, 83 down-regulated) were significantly changed in the liver. During hibernation, RPP regulated a diverse array of proteins involved in multiple functions, including metabolic enzymatic activity, ion transport, protein turnover, signal transduction, and alternative splicing. These changes contribute to enhancing protection, suppressing energy-consuming processes, and inducing metabolic depression. Moreover, the activities of phosphofructokinase, glutamate dehydrogenase, and ATPase were all significantly lower in winter compared to summer. In conclusion, our results support the hypothesis and demonstrate the importance of RPP as a regulatory mechanism when animals transition into a hypometabolic state.
- Nanorana parkeri,
- Proteomic,
- Phosphoproteomic,
- Hibernation,
- Reversible protein phosphorylation,
- Metabolism

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References(63)

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