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A Temporal Examination of Cytoplasmic Ca2 + Levels, Sarcoplasmic Reticulum Ca2 + Levels, and Ca2 + -Handling-Related Proteins in Different Skeletal Muscles of Hibernating Daurian Ground Squirrels.

ABSTRACT: To explore the possible mechanism of the sarcoplasmic reticulum (SR) in the maintenance of cytoplasmic calcium (Ca2+) homeostasis, we studied changes in cytoplasmic Ca2+, SR Ca2+, and Ca2+-handling proteins of slow-twitch muscle (soleus, SOL), fast-twitch muscle (extensor digitorum longus, EDL), and mixed muscle (gastrocnemius, GAS) in different stages in hibernating Daurian ground squirrels (Spermophilus dauricus). Results showed that the level of cytoplasmic Ca2+ increased and SR Ca2+ decreased in skeletal muscle fiber during late torpor (LT) and inter-bout arousal (IBA), but both returned to summer active levels when the animals aroused from and re-entered into torpor (early torpor, ET), suggesting that intracellular Ca2+ is dynamic during hibernation. The protein expression of ryanodine receptor1 (RyR1) increased in the LT, IBA, and ET groups, whereas the co-localization of calsequestrin1 (CSQ1) and RyR1 in GAS muscle decreased in the LT and ET groups, which may increase the possibility of RyR1 channel-mediated Ca2+ release. Furthermore, calcium pump (SR Ca2+-ATPase 1, SERCA1) protein expression increased in the LT, IBA, and ET groups, and the signaling pathway-related factors of SERCA activity [i.e., ?-adrenergic receptor2 protein expression (in GAS), phosphorylation levels of phospholamban (in GAS), and calmodulin kinase2 (in SOL)] all increased, suggesting that these factors may be involved in the up-regulation of SERCA1 activity in different groups. The increased protein expression of Ca2+-binding proteins CSQ1 and calmodulin (CaM) indicated that intracellular free Ca2+-binding ability also increased in the LT, IBA, ET, and POST groups. In brief, changes in cytoplasmic and SR Ca2+ concentrations, SR RyR1 and SERCA1 protein expression levels, and major RyR1 and SERCA1 signaling pathway-related factors were unexpectedly active in the torpor stage when metabolic functions were highly inhibited.

SUBMITTER: Wang Z

PROVIDER: S-EPMC7609816 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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A Temporal Examination of Cytoplasmic Ca2 + Levels, Sarcoplasmic Reticulum Ca2 + Levels, and Ca2 + -Handling-Related Proteins in Different Skeletal Muscles of Hibernating Daurian Ground Squirrels.

Wang Zhe Z Zhang Jie J Ma Xiu-Feng XF Chang Hui H Peng Xin X Xu Shen-Hui SH Wang Hui-Ping HP Gao Yun-Fang YF

Frontiers in physiology 20201021

To explore the possible mechanism of the sarcoplasmic reticulum (SR) in the maintenance of cytoplasmic calcium (Ca2+) homeostasis, we studied changes in cytoplasmic Ca2+, SR Ca2+, and Ca2+-handling proteins of slow-twitch muscle (soleus, SOL), fast-twitch muscle (extensor digitorum longus, EDL), and mixed muscle (gastrocnemius, GAS) in different stages in hibernating Daurian ground squirrels (Spermophilus dauricus). Results showed that the level ...[more]

PMID: 33192559

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Project description:Mammalian hibernators experience repeated hypoxic ischaemia and reperfusion during the torpor-arousal cycle. We investigated levels of oxidative stress, antioxidant capacity, and the underlying mechanism in heart, liver, brain and kidney tissue as well as plasma during different periods of hibernation in Daurian ground squirrels (Spermophilus dauricus). Our data showed that the levels of hydrogen peroxide significantly increased in the heart and brain during late torpor (LT) compared with levels during the summer active (SA) state. The content of malondialdehyde (MDA) was significantly lower during interbout arousal (IBA) and early torpor (ET) than that during SA or pre-hibernation (PRE), and MDA levels in the LT brain were significantly higher than the levels in other states. Superoxide dismutase 2 protein levels increased markedly in the heart throughout the entire torpor-arousal cycle. Catalase expression remained at an elevated level in the liver during the hibernation cycle. Superoxide dismutase 1 and glutathione peroxidase 1 (GPx1) expression increased considerably in all tissues during the IBA and ET states. In addition, the activities of the various antioxidant enzymes were higher in all tissues during IBA and ET than during LT; however, GPx activity in plasma decreased significantly during the hibernation season. The expression of p-Nrf2 decreased in all tissue types during IBA, but significantly increased during LT, especially in liver tissue. Interestingly, most changed indicators recovered to SA or PRE levels in post-hibernation (POST). These results suggest that increased reactive oxygen species during LT may activate the Nrf2/Keap1 antioxidant pathway and may contribute to the decreased MDA levels found during the IBA and ET states, thereby protecting organisms from oxidative damage over the torpor-arousal cycle of hibernation. This is the first report on the remarkable controllability of oxidative stress and tissue specificity in major oxidative tissues of a hibernator.

Project description:Hibernating mammals experience conditions of extreme oxidative stress, such as fasting, muscle disuse, and repeated hypoxic ischemia-reperfusion, during the torpor-arousal cycle. Despite this, they experience little oxidative injury and are thus an interesting model of anti-oxidative damage. Thus, in the current study, we explored the levels and underlying mechanism of oxidative stress and antioxidant capacity in three skeletal muscles [slow-twitch soleus (SOL), fast-twitch extensor digitorum longus (EDL), and mixed gastrocnemius (GAS)] of Daurian ground squirrels (Spermophilus dauricus) during hibernation. Results showed that hydrogen peroxide content in the EDL and GAS decreased significantly during pre-hibernation (PRE) and late torpor (LT) compared to levels in the summer active (SA) group. Furthermore, relative to SA levels, malondialdehyde content decreased significantly during interbout arousal (IBA) and early torpor (ET) in all three skeletal muscles and decreased in the EDL and GAS during LT. Compared with the SA group, glutathione peroxidase 1 (GPx1) and catalase (CAT) protein expression in the SOL and superoxide dismutase 1 (SOD1) and SOD2 expression in the GAS increased significantly during the entire hibernation season. Furthermore, SOD1 in the IBA group and CAT and GPx1 in the ET and LT groups increased significantly in the EDL. The activities of most tested antioxidant enzymes were higher in the IBA group than in the LT group, whereas CAT remained highly active throughout the hibernation season in all three muscles. Nrf2 and p-Nrf2 protein levels were significantly elevated in the SOL and EDL during hibernation, and increased during the PRE, IBA, and ET states in the GAS. Thus, activation of the Nrf2/Keap1 antioxidant pathway resulted in the elimination of excess reactive oxygen species (ROS). Specifically, ROS levels were maintained at physiological levels by the up-regulation of antioxidant enzyme expression in skeletal muscles under oxidative stress during hibernation, thus preventing oxidative injury over the torpor-arousal cycle. Different antioxidant patterns and oxidative stress levels were also observed among the different skeletal muscles of hibernating Daurian ground squirrels.

Dataset Information

A Temporal Examination of Cytoplasmic Ca2 + Levels, Sarcoplasmic Reticulum Ca2 + Levels, and Ca2 + -Handling-Related Proteins in Different Skeletal Muscles of Hibernating Daurian Ground Squirrels.

Publications

A Temporal Examination of Cytoplasmic Ca<sup>2 +</sup> Levels, Sarcoplasmic Reticulum Ca<sup>2 +</sup> Levels, and Ca<sup>2 +</sup> -Handling-Related Proteins in Different Skeletal Muscles of Hibernating Daurian Ground Squirrels.

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