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Controllable oxidative stress and tissue specificity in major tissues during the torpor-arousal cycle in hibernating Daurian ground squirrels.

ABSTRACT: 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.

SUBMITTER: Wei Y

PROVIDER: S-EPMC6223210 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Controllable oxidative stress and tissue specificity in major tissues during the torpor-arousal cycle in hibernating Daurian ground squirrels.

Wei Yanhong Y Zhang Jie J Xu Shenhui S Peng Xin X Yan Xia X Li Xiaoyu X Wang Huiping H Chang Hui H Gao Yunfang Y

Open biology 20181010 10

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 (<i>Spermophilus dauricus</i>). Our data showed that the levels of hydrogen peroxide significantly increased in the heart and brain during late torpor (LT) compared with ...[more]

PMID: 30305429

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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.

Project description:MicroRNAs (miRNAs) are small non-coding RNAs that are important in regulating metabolic stress. In this study, we determined the expression and structural characteristics of 20 miRNAs in brown (BAT) and white adipose tissue (WAT) during torpor in thirteen-lined ground squirrels. Using a modified stem-loop technique, we found that during torpor, expression of six miRNAs including let-7a, let-7b, miR-107, miR-150, miR-222 and miR-31 was significantly downregulated in WAT (P<0.05), which was 16%-54% of euthermic non-torpid control squirrels, whereas expression of three miRNAs including miR-143, miR-200a and miR-519d was found to be upregulated by 1.32-2.34-fold. Similarly, expression of more miRNAs was downregulated in BAT during torpor. We detected reduced expression of 6 miRNAs including miR-103a, miR-107, miR-125b, miR-21, miR-221 and miR-31 (48%-70% of control), while only expression of miR-138 was significantly upregulated (2.91±0.8-fold of the control, P<0.05). Interestingly, miRNAs found to be downregulated in WAT during torpor were similar to those dysregulated in obese humans for increased adipogenesis, whereas miRNAs with altered expression in BAT during torpor were linked to mitochondrial ?-oxidation. miRPath target prediction analysis showed that miRNAs downregulated in both WAT and BAT were associated with the regulation of mitogen-activated protein kinase (MAPK) signaling, while the miRNAs upregulated in WAT were linked to transforming growth factor ? (TGF?) signaling. Compared to mouse sequences, no unique nucleotide substitutions within the stem-loop region were discovered for the associated pre-miRNAs for the miRNAs used in this study, suggesting no structure-influenced changes in pre-miRNA processing efficiency in the squirrel. As well, the expression of miRNA processing enzyme Dicer remained unchanged in both tissues during torpor. Overall, our findings suggest that changes of miRNA expression in adipose tissues may be linked to distinct biological roles in WAT and BAT during hibernation and may involve the regulation of signaling cascades.

Dataset Information

Controllable oxidative stress and tissue specificity in major tissues during the torpor-arousal cycle in hibernating Daurian ground squirrels.

Publications

Controllable oxidative stress and tissue specificity in major tissues during the torpor-arousal cycle in hibernating Daurian ground squirrels.

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