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Succinate induces skeletal muscle fiber remodeling via SUNCR1 signaling pathway.
EMBO Rep 2019; :e47892ER

Abstract

The conversion of skeletal muscle fiber from fast twitch to slow-twitch is important for sustained and tonic contractile events, maintenance of energy homeostasis, and the alleviation of fatigue. Skeletal muscle remodeling is effectively induced by endurance or aerobic exercise, which also generates several tricarboxylic acid (TCA) cycle intermediates, including succinate. However, whether succinate regulates muscle fiber-type transitions remains unclear. Here, we found that dietary succinate supplementation increased endurance exercise ability, myosin heavy chain I expression, aerobic enzyme activity, oxygen consumption, and mitochondrial biogenesis in mouse skeletal muscle. By contrast, succinate decreased lactate dehydrogenase activity, lactate production, and myosin heavy chain IIb expression. Further, by using pharmacological or genetic loss-of-function models generated by phospholipase Cβ antagonists, SUNCR1 global knockout, or SUNCR1 gastrocnemius-specific knockdown, we found that the effects of succinate on skeletal muscle fiber-type remodeling are mediated by SUNCR1 and its downstream calcium/NFAT signaling pathway. In summary, our results demonstrate succinate induces transition of skeletal muscle fiber via SUNCR1 signaling pathway. These findings suggest the potential beneficial use of succinate-based compounds in both athletic and sedentary populations.

Authors+Show Affiliations

Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Division of Endocrinology, Department of Medicine, The University of Illinois at Chicago, Chicago, IL, USA.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Division of Endocrinology, Department of Medicine, The University of Illinois at Chicago, Chicago, IL, USA.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China. National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.Guangdong Province Key Laboratory of Animal Nutritional Regulation, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China. National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong, China.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31318145

Citation

Wang, Tao, et al. "Succinate Induces Skeletal Muscle Fiber Remodeling Via SUNCR1 Signaling Pathway." EMBO Reports, 2019, pp. e47892.
Wang T, Xu YQ, Yuan YX, et al. Succinate induces skeletal muscle fiber remodeling via SUNCR1 signaling pathway. EMBO Rep. 2019.
Wang, T., Xu, Y. Q., Yuan, Y. X., Xu, P. W., Zhang, C., Li, F., ... Jiang, Q. Y. (2019). Succinate induces skeletal muscle fiber remodeling via SUNCR1 signaling pathway. EMBO Reports, pp. e47892. doi:10.15252/embr.201947892.
Wang T, et al. Succinate Induces Skeletal Muscle Fiber Remodeling Via SUNCR1 Signaling Pathway. EMBO Rep. 2019 Jul 18;e47892. PubMed PMID: 31318145.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Succinate induces skeletal muscle fiber remodeling via SUNCR1 signaling pathway. AU - Wang,Tao, AU - Xu,Ya-Qiong, AU - Yuan,Ye-Xian, AU - Xu,Ping-Wen, AU - Zhang,Cha, AU - Li,Fan, AU - Wang,Li-Na, AU - Yin,Cong, AU - Zhang,Lin, AU - Cai,Xing-Cai, AU - Zhu,Can-Jun, AU - Xu,Jing-Ren, AU - Liang,Bing-Qing, AU - Schaul,Sarah, AU - Xie,Pei-Pei, AU - Yue,Dong, AU - Liao,Zheng-Rui, AU - Yu,Lu-Lu, AU - Luo,Lv, AU - Zhou,Gan, AU - Yang,Jin-Ping, AU - He,Zhi-Hui, AU - Du,Man, AU - Zhou,Yu-Ping, AU - Deng,Bai-Chuan, AU - Wang,Song-Bo, AU - Gao,Ping, AU - Zhu,Xiao-Tong, AU - Xi,Qian-Yun, AU - Zhang,Yong-Liang, AU - Shu,Gang, AU - Jiang,Qing-Yan, Y1 - 2019/07/18/ PY - 2019/02/07/received PY - 2019/06/13/revised PY - 2019/06/26/accepted PY - 2019/7/19/entrez KW - SUNCR1 KW - aerobic exercise KW - fiber type KW - skeletal muscle KW - succinate SP - e47892 EP - e47892 JF - EMBO reports JO - EMBO Rep. N2 - The conversion of skeletal muscle fiber from fast twitch to slow-twitch is important for sustained and tonic contractile events, maintenance of energy homeostasis, and the alleviation of fatigue. Skeletal muscle remodeling is effectively induced by endurance or aerobic exercise, which also generates several tricarboxylic acid (TCA) cycle intermediates, including succinate. However, whether succinate regulates muscle fiber-type transitions remains unclear. Here, we found that dietary succinate supplementation increased endurance exercise ability, myosin heavy chain I expression, aerobic enzyme activity, oxygen consumption, and mitochondrial biogenesis in mouse skeletal muscle. By contrast, succinate decreased lactate dehydrogenase activity, lactate production, and myosin heavy chain IIb expression. Further, by using pharmacological or genetic loss-of-function models generated by phospholipase Cβ antagonists, SUNCR1 global knockout, or SUNCR1 gastrocnemius-specific knockdown, we found that the effects of succinate on skeletal muscle fiber-type remodeling are mediated by SUNCR1 and its downstream calcium/NFAT signaling pathway. In summary, our results demonstrate succinate induces transition of skeletal muscle fiber via SUNCR1 signaling pathway. These findings suggest the potential beneficial use of succinate-based compounds in both athletic and sedentary populations. SN - 1469-3178 UR - https://www.unboundmedicine.com/medline/citation/31318145/Succinate_induces_skeletal_muscle_fiber_remodeling_via_SUNCR1_signaling_pathway L2 - https://doi.org/10.15252/embr.201947892 DB - PRIME DP - Unbound Medicine ER -