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Integrated transcriptomics and metabolomics reveal protective effects on heart of hibernating Daurian ground squirrels

迟钝 转录组 生物 代谢组学 磷酸戊糖途径 谷胱甘肽 氧化应激 休眠(计算) 生物化学 细胞生物学 糖酵解 内分泌学 基因表达 新陈代谢 生物信息学 基因 温度调节 国家(计算机科学) 计算机科学 算法
作者
Yingyu Yang,Ziwei Hao,Ning An,Yuting Han,Weilan Miao,Kenneth B. Storey,Étienne Lefai,Xiaoxuan Liu,Junshu Wang,Shuo Liu,Man‐Jiang Xie,Hui Chang
出处
期刊:Journal of Cellular Physiology [Wiley]
卷期号:238 (11): 2724-2748 被引量:5
标识
DOI:10.1002/jcp.31123
摘要

Abstract Hibernating mammals are natural models of resistance to ischemia, hypoxia‐reperfusion injury, and hypothermia. Daurian ground squirrels ( spermophilus dauricus ) can adapt to endure multiple torpor‐arousal cycles without sustaining cardiac damage. However, the molecular regulatory mechanisms that underlie this adaptive response are not yet fully understood. This study investigates morphological, functional, genetic, and metabolic changes that occur in the heart of ground squirrels in three groups: summer active (SA), late torpor (LT), and interbout arousal (IBA). Morphological and functional changes in the heart were measured using hematoxylin‐eosin (HE) staining, Masson staining, echocardiography, and enzyme‐linked immunosorbent assay (ELISA). Results showed significant changes in cardiac function in the LT group as compared with SA or IBA groups, but no irreversible damage occurred. To understand the molecular mechanisms underlying these phenotypic changes, transcriptomic and metabolomic analyses were conducted to assess differential changes in gene expression and metabolite levels in the three groups of ground squirrels, with a focus on GO and KEGG pathway analysis. Transcriptomic analysis showed that differentially expressed genes were involved in the remodeling of cytoskeletal proteins, reduction in protein synthesis, and downregulation of the ubiquitin‐proteasome pathway during hibernation (including LT and IBA groups), as compared with the SA group. Metabolomic analysis revealed increased free amino acids, activation of the glutathione antioxidant system, altered cardiac fatty acid metabolic preferences, and enhanced pentose phosphate pathway activity during hibernation as compared with the SA group. Combining the transcriptomic and metabolomic data, active mitochondrial oxidative phosphorylation and creatine‐phosphocreatine energy shuttle systems were observed, as well as inhibition of ferroptosis signaling pathways during hibernation as compared with the SA group. In conclusion, these results provide new insights into cardio‐protection in hibernators from the perspective of gene and metabolite changes and deepen our understanding of adaptive cardio‐protection mechanisms in mammalian hibernators.
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