HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis

Introduction: Cardiac fibrosis is the main driver for adverse remodeling and progressive functional decline in nearly all types of heart disease including myocardial infarction (MI). The activation of cardiac fibroblasts (CF) into myofibroblasts is responsible for cardiac fibrosis. Unfortunately, no...

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Main Authors: Qian Mao, Xiaojin Zhang, Jinna Yang, Qiuyue Kong, Hao Cheng, Wansu Yu, Xiaofei Cao, Yuehua Li, Chuanfu Li, Li Liu, Zhengnian Ding
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Journal of Advanced Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S2090123224000250
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author Qian Mao
Xiaojin Zhang
Jinna Yang
Qiuyue Kong
Hao Cheng
Wansu Yu
Xiaofei Cao
Yuehua Li
Chuanfu Li
Li Liu
Zhengnian Ding
author_facet Qian Mao
Xiaojin Zhang
Jinna Yang
Qiuyue Kong
Hao Cheng
Wansu Yu
Xiaofei Cao
Yuehua Li
Chuanfu Li
Li Liu
Zhengnian Ding
author_sort Qian Mao
collection DOAJ
description Introduction: Cardiac fibrosis is the main driver for adverse remodeling and progressive functional decline in nearly all types of heart disease including myocardial infarction (MI). The activation of cardiac fibroblasts (CF) into myofibroblasts is responsible for cardiac fibrosis. Unfortunately, no ideal approach for controlling CF activation currently exists. Objectives: This study investigated the role of Heat shock protein A12A (HSPA12A), an atypical member of the HSP70 family, in CF activation and MI-induced cardiac fibrosis. Methods: Primary CF and Hspa12a knockout mice were used in the experiments. CF activation was indicated by the upregulation of myofibroblast characters including alpha-Smooth muscle actin (αSMA), Collagen, and Fibronectin. Cardiac fibrosis was illustrated by Masson’s trichrome and picrosirius staining. Cardiac function was examined using echocardiography. Glycolytic activity was indicated by levels of extracellular lactate and the related protein expression. Protein stability was examined following cycloheximide and MG132 treatment. Protein-protein interaction was examined by immunoprecipitation-immunoblotting analysis. Results: HSPA12A displayed a high expression level in quiescent CF but showed a decreased expression in activated CF, while ablation of HSPA12A in mice promoted CF activation and cardiac fibrosis following MI. HSPA12A overexpression inhibited the activation of primary CF through inhibiting glycolysis, while HSPA12A knockdown showed the opposite effects. Moreover, HSPA12A upregulated the protein expression of transcription factor p53, by which mediated the HSPA12A-induced inhibition of glycolysis and CF activation. Mechanistically, this action of HSPA12A was achieved by acting as a scaffolding protein to bind p53 and ubiquitin specific protease 10 (USP10), thereby promoting the USP10-mediated p53 protein stability and the p53-medicated glycolysis inhibition. Conclusion: The present study provided clear evidence that HSPA12A is a novel endogenous inhibitor of CF activation and cardiac fibrosis. Targeting HSPA12A in CF could represent a promising strategy for the management of cardiac fibrosis in patients.
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spelling doaj-art-e89a68c222704d30820747b1acbdd20f2024-12-18T08:48:06ZengElsevierJournal of Advanced Research2090-12322025-01-0167217229HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosisQian Mao0Xiaojin Zhang1Jinna Yang2Qiuyue Kong3Hao Cheng4Wansu Yu5Xiaofei Cao6Yuehua Li7Chuanfu Li8Li Liu9Zhengnian Ding10Department of Anesthesiology, First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, ChinaDepartment of Geriatrics, Jiangsu Provincial Key Laboratory of Geriatrics, The First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, ChinaDepartment of Geriatrics, Jiangsu Provincial Key Laboratory of Geriatrics, The First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, ChinaDepartment of Anesthesiology, First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, ChinaDepartment of Anesthesiology, The First Affiliated Hospital with Wannan Medical College, Wuhu, ChinaDepartment of Geriatrics, Jiangsu Provincial Key Laboratory of Geriatrics, The First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, ChinaDepartment of Anesthesiology, First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, ChinaKey Laboratory of Targeted Intervention of Cardiovascular Disease, Collaborative Innovation Center for Cardiovascular Disease Translational Medicine, Nanjing Medical University, ChinaDepartments of Surgery, East Tennessee State University, Johnson City, TN 37614, USADepartment of Geriatrics, Jiangsu Provincial Key Laboratory of Geriatrics, The First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, China; Key Laboratory of Targeted Intervention of Cardiovascular Disease, Collaborative Innovation Center for Cardiovascular Disease Translational Medicine, Nanjing Medical University, ChinaDepartment of Anesthesiology, First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, China; Corresponding author at: Department of Anesthesiology, First Affiliated Hospital with Nanjing Medical University, Guangzhou Rd 300, Nanjing 210029, China.Introduction: Cardiac fibrosis is the main driver for adverse remodeling and progressive functional decline in nearly all types of heart disease including myocardial infarction (MI). The activation of cardiac fibroblasts (CF) into myofibroblasts is responsible for cardiac fibrosis. Unfortunately, no ideal approach for controlling CF activation currently exists. Objectives: This study investigated the role of Heat shock protein A12A (HSPA12A), an atypical member of the HSP70 family, in CF activation and MI-induced cardiac fibrosis. Methods: Primary CF and Hspa12a knockout mice were used in the experiments. CF activation was indicated by the upregulation of myofibroblast characters including alpha-Smooth muscle actin (αSMA), Collagen, and Fibronectin. Cardiac fibrosis was illustrated by Masson’s trichrome and picrosirius staining. Cardiac function was examined using echocardiography. Glycolytic activity was indicated by levels of extracellular lactate and the related protein expression. Protein stability was examined following cycloheximide and MG132 treatment. Protein-protein interaction was examined by immunoprecipitation-immunoblotting analysis. Results: HSPA12A displayed a high expression level in quiescent CF but showed a decreased expression in activated CF, while ablation of HSPA12A in mice promoted CF activation and cardiac fibrosis following MI. HSPA12A overexpression inhibited the activation of primary CF through inhibiting glycolysis, while HSPA12A knockdown showed the opposite effects. Moreover, HSPA12A upregulated the protein expression of transcription factor p53, by which mediated the HSPA12A-induced inhibition of glycolysis and CF activation. Mechanistically, this action of HSPA12A was achieved by acting as a scaffolding protein to bind p53 and ubiquitin specific protease 10 (USP10), thereby promoting the USP10-mediated p53 protein stability and the p53-medicated glycolysis inhibition. Conclusion: The present study provided clear evidence that HSPA12A is a novel endogenous inhibitor of CF activation and cardiac fibrosis. Targeting HSPA12A in CF could represent a promising strategy for the management of cardiac fibrosis in patients.http://www.sciencedirect.com/science/article/pii/S2090123224000250Cardiac fibroblast activationCardiac fibrosisHSPA12AGlycolysisP53USP10
spellingShingle Qian Mao
Xiaojin Zhang
Jinna Yang
Qiuyue Kong
Hao Cheng
Wansu Yu
Xiaofei Cao
Yuehua Li
Chuanfu Li
Li Liu
Zhengnian Ding
HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis
Journal of Advanced Research
Cardiac fibroblast activation
Cardiac fibrosis
HSPA12A
Glycolysis
P53
USP10
title HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis
title_full HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis
title_fullStr HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis
title_full_unstemmed HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis
title_short HSPA12A acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis
title_sort hspa12a acts as a scaffolding protein to inhibit cardiac fibroblast activation and cardiac fibrosis
topic Cardiac fibroblast activation
Cardiac fibrosis
HSPA12A
Glycolysis
P53
USP10
url http://www.sciencedirect.com/science/article/pii/S2090123224000250
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