Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathways

Abstract Background Cardiac hypertrophy is a precursor to heart failure and represents a significant global cause of mortality, thereby necessitating timely and effective therapeutic interventions. Zinc finger protein 36 (Zfp36) is recognised as a critical regulator of ferroptosis; however, its role...

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Main Authors: Mingyu Zhang, Xiaoxiang Guan, Zheng Dong, Chenxu Yang, Chao Xiong, Wenzheng Cheng, Aijing Shang, Yaru Liu, Xiaofei Guo, Bowen Zhang, Bo Zhang, Saidi Jin, Wenyi Qi, Berezhnova Tatjana Alexandrovna, Yuan Jiang, Zhimin Du, Chaoqian Xu
Format: Article
Language:English
Published: Wiley 2025-03-01
Series:Clinical and Translational Medicine
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Online Access:https://doi.org/10.1002/ctm2.70247
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author Mingyu Zhang
Xiaoxiang Guan
Zheng Dong
Chenxu Yang
Chao Xiong
Wenzheng Cheng
Aijing Shang
Yaru Liu
Xiaofei Guo
Bowen Zhang
Bo Zhang
Saidi Jin
Wenyi Qi
Berezhnova Tatjana Alexandrovna
Yuan Jiang
Zhimin Du
Chaoqian Xu
author_facet Mingyu Zhang
Xiaoxiang Guan
Zheng Dong
Chenxu Yang
Chao Xiong
Wenzheng Cheng
Aijing Shang
Yaru Liu
Xiaofei Guo
Bowen Zhang
Bo Zhang
Saidi Jin
Wenyi Qi
Berezhnova Tatjana Alexandrovna
Yuan Jiang
Zhimin Du
Chaoqian Xu
author_sort Mingyu Zhang
collection DOAJ
description Abstract Background Cardiac hypertrophy is a precursor to heart failure and represents a significant global cause of mortality, thereby necessitating timely and effective therapeutic interventions. Zinc finger protein 36 (Zfp36) is recognised as a critical regulator of ferroptosis; however, its role and underlying mechanisms in cardiac hypertrophy remain largely unexplored. This study aims to investigate the regulatory function of Zfp36 in ferroptosis within the context of cardiac hypertrophy. Methods and results Single‐cell sequencing analysis demonstrated a reduction in Zfp36 expression associated with cardiac hypertrophy. Zfp36 was observed to mitigate ferroptosis and reduce hypertrophic phenotypes in cardiomyocytes subjected to Angiotensin II (Ang II) and in myocardial tissues induced by transverse aortic constriction. The ferroptosis inhibitor Ferrostatin‐1 was shown to alleviate hypertrophy when co‐incubated with si‐Zfp36 and Ang II. Mechanistically, Zfp36 binds to the 3′ untranslated region (3′UTR) of Ythdc2 mRNA, facilitating its degradation. Ythdc2 subsequently binds to SLC7A11 mRNA, enhancing its decay, which leads to a reduction in glutathione (GSH) levels, thereby exacerbating ferroptosis and cardiac hypertrophy. Furthermore, overexpression of Ythdc2 reversed the protective effects conferred by Zfp36, while silencing of Ythdc2 counteracted the effects of Zfp36 knockdown. Conclusions This study elucidates the role of Zfp36 in cardiac hypertrophy, specifically detailing its modulatory mechanism via the Ythdc2/SLC7A11/GSH ferroptosis pathway. These insights lay the groundwork for innovative approaches to understanding the pathological mechanisms underlying cardiac hypertrophy and enhancing clinical interventions. Key points Zfp36 was initially demonstrated to attenuate cardiac hypertrophy through the inhibition of ferroptosis in cardiomyocytes, providing a new target for therapeutic strategies targeting ferroptosis. Zfp36 facilitated the degradation of Ythdc2 mRNA by binding to it, subsequently inhibiting Ythdc2‐mediated degradation of SLC7A11 mRNA, and maintaining GSH levels. This elucidates a previously unrecognized regulatory pathway in the context of cardiac hypertrophy.
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spelling doaj-art-9d838d3c0b0f45fda796a5dc3e26931f2025-08-20T03:47:36ZengWileyClinical and Translational Medicine2001-13262025-03-01153n/an/a10.1002/ctm2.70247Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathwaysMingyu Zhang0Xiaoxiang Guan1Zheng Dong2Chenxu Yang3Chao Xiong4Wenzheng Cheng5Aijing Shang6Yaru Liu7Xiaofei Guo8Bowen Zhang9Bo Zhang10Saidi Jin11Wenyi Qi12Berezhnova Tatjana Alexandrovna13Yuan Jiang14Zhimin Du15Chaoqian Xu16State Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaDepartment of Clinical Pharmacy the First Affiliated Hospital of Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaDepartment of Pharmacology, Voronezh State Medical University Named After N.N. Burdenko VoronezhState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaState Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD) Department of Pharmacology (State Key Labratoray ‐Province Key Laboratories of Biomedicine‐Pharmaceutics of China Key Laboratory of Cardiovascular Research, Ministry of Education) College of Pharmacy Harbin Medical University Harbin ChinaAbstract Background Cardiac hypertrophy is a precursor to heart failure and represents a significant global cause of mortality, thereby necessitating timely and effective therapeutic interventions. Zinc finger protein 36 (Zfp36) is recognised as a critical regulator of ferroptosis; however, its role and underlying mechanisms in cardiac hypertrophy remain largely unexplored. This study aims to investigate the regulatory function of Zfp36 in ferroptosis within the context of cardiac hypertrophy. Methods and results Single‐cell sequencing analysis demonstrated a reduction in Zfp36 expression associated with cardiac hypertrophy. Zfp36 was observed to mitigate ferroptosis and reduce hypertrophic phenotypes in cardiomyocytes subjected to Angiotensin II (Ang II) and in myocardial tissues induced by transverse aortic constriction. The ferroptosis inhibitor Ferrostatin‐1 was shown to alleviate hypertrophy when co‐incubated with si‐Zfp36 and Ang II. Mechanistically, Zfp36 binds to the 3′ untranslated region (3′UTR) of Ythdc2 mRNA, facilitating its degradation. Ythdc2 subsequently binds to SLC7A11 mRNA, enhancing its decay, which leads to a reduction in glutathione (GSH) levels, thereby exacerbating ferroptosis and cardiac hypertrophy. Furthermore, overexpression of Ythdc2 reversed the protective effects conferred by Zfp36, while silencing of Ythdc2 counteracted the effects of Zfp36 knockdown. Conclusions This study elucidates the role of Zfp36 in cardiac hypertrophy, specifically detailing its modulatory mechanism via the Ythdc2/SLC7A11/GSH ferroptosis pathway. These insights lay the groundwork for innovative approaches to understanding the pathological mechanisms underlying cardiac hypertrophy and enhancing clinical interventions. Key points Zfp36 was initially demonstrated to attenuate cardiac hypertrophy through the inhibition of ferroptosis in cardiomyocytes, providing a new target for therapeutic strategies targeting ferroptosis. Zfp36 facilitated the degradation of Ythdc2 mRNA by binding to it, subsequently inhibiting Ythdc2‐mediated degradation of SLC7A11 mRNA, and maintaining GSH levels. This elucidates a previously unrecognized regulatory pathway in the context of cardiac hypertrophy.https://doi.org/10.1002/ctm2.70247cardiac hypertrophyferroptosisRNA bindingYthdc2Zfp36
spellingShingle Mingyu Zhang
Xiaoxiang Guan
Zheng Dong
Chenxu Yang
Chao Xiong
Wenzheng Cheng
Aijing Shang
Yaru Liu
Xiaofei Guo
Bowen Zhang
Bo Zhang
Saidi Jin
Wenyi Qi
Berezhnova Tatjana Alexandrovna
Yuan Jiang
Zhimin Du
Chaoqian Xu
Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathways
Clinical and Translational Medicine
cardiac hypertrophy
ferroptosis
RNA binding
Ythdc2
Zfp36
title Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathways
title_full Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathways
title_fullStr Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathways
title_full_unstemmed Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathways
title_short Targeting Zfp36 to combat cardiac hypertrophy: Insights into ferroptosis pathways
title_sort targeting zfp36 to combat cardiac hypertrophy insights into ferroptosis pathways
topic cardiac hypertrophy
ferroptosis
RNA binding
Ythdc2
Zfp36
url https://doi.org/10.1002/ctm2.70247
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