LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosis

Regulated necrosis (necroptosis) and apoptosis are important biological features of ischemia-reperfusion (I/R) injury. However, the molecular mechanisms underlying myocardial necroptosis remain elusive. Leucine rich repeat containing G protein-coupled receptor 6 (LGR6) has been reported to play impo...

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Main Authors: Mengmeng Zhao, Zihui Zheng, Jianfang Liu, Yao Xu, Jishou Zhang, Shanshan Peng, Juan-Juan Qin, Jun Wan, Menglong Wang
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Redox Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2213231724003781
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author Mengmeng Zhao
Zihui Zheng
Jianfang Liu
Yao Xu
Jishou Zhang
Shanshan Peng
Juan-Juan Qin
Jun Wan
Menglong Wang
author_facet Mengmeng Zhao
Zihui Zheng
Jianfang Liu
Yao Xu
Jishou Zhang
Shanshan Peng
Juan-Juan Qin
Jun Wan
Menglong Wang
author_sort Mengmeng Zhao
collection DOAJ
description Regulated necrosis (necroptosis) and apoptosis are important biological features of ischemia-reperfusion (I/R) injury. However, the molecular mechanisms underlying myocardial necroptosis remain elusive. Leucine rich repeat containing G protein-coupled receptor 6 (LGR6) has been reported to play important roles in various cardiovascular disease. In this study, we aimed to determine whether LGR6 suppresses I/R-induced myocardial necroptosis and the underlying molecular mechanisms. We generated LGR6 knockout mice and used ligation of left anterior descending coronary artery to produce an in vivo I/R model. The effects of LGR6 and its downstream molecules were subsequently identified using RNA sequencing and CHIP assays. We observed significantly downregulated LGR6 expression in hearts post myocardial I/R and cardiomyocytes post hypoxia and reoxygenation (HR). LGR6 deficiency promoted and LGR6 overexpression inhibited necroptosis and acute myocardial injury after I/R. Mechanistically, in vivo and in vitro experiments suggest that LGR6 regulates the expression of STAT2 and ZBP1 by activating the Wnt signaling pathway, thereby inhibiting cardiomyocyte necroptosis after HR. Inhibiting STAT2 and ZBP1 effectively alleviated the aggravating effect of LGR6 deficiency on myocardial necroptosis after I/R. Furthermore, activating LGR6 with RSPO3 also effectively protected mice from acute myocardial I/R injury. Our findings reveal that RSPO3-LGR6 axis downregulates the expression of STAT2 and ZBP1 through the Wnt signaling pathway, thereby inhibiting I/R-induced myocardial injury and necroptosis. Targeting the RSPO3-LGR6 axis may be a potential therapeutic strategy to treat myocardial I/R injury.
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spelling doaj-art-9b9081dbe8e4480683d45a8aac8038d52024-12-08T06:09:56ZengElsevierRedox Biology2213-23172024-12-0178103400LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosisMengmeng Zhao0Zihui Zheng1Jianfang Liu2Yao Xu3Jishou Zhang4Shanshan Peng5Juan-Juan Qin6Jun Wan7Menglong Wang8Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, ChinaDepartment of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, ChinaDepartment of Geriatrics, Zhongnan Hospital of Wuhan University, Wuhan, China; Center for Healthy Aging, Wuhan University School of Nursing, Wuhan, China; Corresponding author. Department of Geriatrics, Zhongnan Hospital of Wuhan University, 169 Donghu Road, Wuhan, 430060, China.Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Corresponding author. Department of Cardiology, Renmin Hospital of Wuhan University, 238 Jiefang Road, Wuhan, 430060, China.Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan, China; Cardiovascular Research Institute, Wuhan University, Wuhan, China; Hubei Key Laboratory of Cardiology, Wuhan, China; Corresponding author. Department of Cardiology, Renmin Hospital of Wuhan University, 238 Jiefang Road, Wuhan, 430060, China.Regulated necrosis (necroptosis) and apoptosis are important biological features of ischemia-reperfusion (I/R) injury. However, the molecular mechanisms underlying myocardial necroptosis remain elusive. Leucine rich repeat containing G protein-coupled receptor 6 (LGR6) has been reported to play important roles in various cardiovascular disease. In this study, we aimed to determine whether LGR6 suppresses I/R-induced myocardial necroptosis and the underlying molecular mechanisms. We generated LGR6 knockout mice and used ligation of left anterior descending coronary artery to produce an in vivo I/R model. The effects of LGR6 and its downstream molecules were subsequently identified using RNA sequencing and CHIP assays. We observed significantly downregulated LGR6 expression in hearts post myocardial I/R and cardiomyocytes post hypoxia and reoxygenation (HR). LGR6 deficiency promoted and LGR6 overexpression inhibited necroptosis and acute myocardial injury after I/R. Mechanistically, in vivo and in vitro experiments suggest that LGR6 regulates the expression of STAT2 and ZBP1 by activating the Wnt signaling pathway, thereby inhibiting cardiomyocyte necroptosis after HR. Inhibiting STAT2 and ZBP1 effectively alleviated the aggravating effect of LGR6 deficiency on myocardial necroptosis after I/R. Furthermore, activating LGR6 with RSPO3 also effectively protected mice from acute myocardial I/R injury. Our findings reveal that RSPO3-LGR6 axis downregulates the expression of STAT2 and ZBP1 through the Wnt signaling pathway, thereby inhibiting I/R-induced myocardial injury and necroptosis. Targeting the RSPO3-LGR6 axis may be a potential therapeutic strategy to treat myocardial I/R injury.http://www.sciencedirect.com/science/article/pii/S2213231724003781LGR6NecroptosisZBP1STAT2Myocardial ischemia-reperfusion injury
spellingShingle Mengmeng Zhao
Zihui Zheng
Jianfang Liu
Yao Xu
Jishou Zhang
Shanshan Peng
Juan-Juan Qin
Jun Wan
Menglong Wang
LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosis
Redox Biology
LGR6
Necroptosis
ZBP1
STAT2
Myocardial ischemia-reperfusion injury
title LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosis
title_full LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosis
title_fullStr LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosis
title_full_unstemmed LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosis
title_short LGR6 protects against myocardial ischemia-reperfusion injury via suppressing necroptosis
title_sort lgr6 protects against myocardial ischemia reperfusion injury via suppressing necroptosis
topic LGR6
Necroptosis
ZBP1
STAT2
Myocardial ischemia-reperfusion injury
url http://www.sciencedirect.com/science/article/pii/S2213231724003781
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