Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytes

Abstract Anthracycline antitumor drug doxorubicin (DOX) induces severe cardiotoxicity. Deubiquitinating enzymes (DUBs) are crucial for protein stability and function and play a significant role in cardiac pathophysiology. By comparing RNA sequencing datasets and conducting functional screening, we d...

Full description

Saved in:
Bibliographic Details
Main Authors: Xiaowen Shi, Jianjiang Xu, Xin Zhong, Yuanyuan Qian, Liming Lin, Zimin Fang, Bozhi Ye, Yiting Lyu, Ran Zhang, Zhanxiong Zheng, Jibo Han
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Cell Communication and Signaling
Subjects:
Online Access:https://doi.org/10.1186/s12964-024-01955-6
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850253852260958208
author Xiaowen Shi
Jianjiang Xu
Xin Zhong
Yuanyuan Qian
Liming Lin
Zimin Fang
Bozhi Ye
Yiting Lyu
Ran Zhang
Zhanxiong Zheng
Jibo Han
author_facet Xiaowen Shi
Jianjiang Xu
Xin Zhong
Yuanyuan Qian
Liming Lin
Zimin Fang
Bozhi Ye
Yiting Lyu
Ran Zhang
Zhanxiong Zheng
Jibo Han
author_sort Xiaowen Shi
collection DOAJ
description Abstract Anthracycline antitumor drug doxorubicin (DOX) induces severe cardiotoxicity. Deubiquitinating enzymes (DUBs) are crucial for protein stability and function and play a significant role in cardiac pathophysiology. By comparing RNA sequencing datasets and conducting functional screening, we determined that Myb-like, SWIRM, and MPN domains 1 (MYSM1) is a key regulator of DOX-induced cardiotoxicity. In this study, we aimed to explore the function and regulatory mechanisms of MYSM1 in DOX-induced cardiotoxicity. Genetic knockdown of MYSM1 significantly mitigated DOX-induced cardiomyopathy. Correspondingly, cardiomyocyte-specific knockdown of MYSM1 by AAV9 protected the heart from DOX-induced cardiotoxicity. Gain- and loss-of-function analysis verified that MYSM1 mediated DOX-induced cardiomyocyte injury in vitro. Through a Co-IP combined with LC-MS/MS analysis, we discovered that MYSM1 directly interacted with tripartite motif-containing protein 21 (TRIM21). Mechanistic investigations revealed that MYSM1 regulates the deubiquitination and the stability of TRIM21 via its MPN domain. Furthermore, MYSM1 exacerbated DOX-induced cardiotoxicity by enhancing ferroptosis. This study identified MYSM1 as a potential therapeutic target for DOX-induced cardiotoxicity and illustrated a MYSM1-TRIM21-ferroptosis axis in regulating DOX-induced cardiotoxicity.
format Article
id doaj-art-b10407e7045d4f0085441caeb0acc6f5
institution OA Journals
issn 1478-811X
language English
publishDate 2024-12-01
publisher BMC
record_format Article
series Cell Communication and Signaling
spelling doaj-art-b10407e7045d4f0085441caeb0acc6f52025-08-20T01:57:16ZengBMCCell Communication and Signaling1478-811X2024-12-0122111610.1186/s12964-024-01955-6Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytesXiaowen Shi0Jianjiang Xu1Xin Zhong2Yuanyuan Qian3Liming Lin4Zimin Fang5Bozhi Ye6Yiting Lyu7Ran Zhang8Zhanxiong Zheng9Jibo Han10Department of Cardiology, The Second Affiliated Hospital of Jiaxing UniversityDepartment of Cardiology, The Second Affiliated Hospital of Jiaxing UniversityDepartment of Cardiology, The Second Affiliated Hospital of Jiaxing UniversityKey Laboratory of Blood-stasis-toxin Syndrome of Zhejiang Province, Zhejiang Chinese Medical UniversityDepartment of Cardiology, the First Affiliated Hospital, Wenzhou Medical UniversityDepartment of Ultrasound, Puer People’s HospitalDepartment of Cardiology, the First Affiliated Hospital, Wenzhou Medical UniversityDepartment of Cardiology, The Second Affiliated Hospital of Jiaxing UniversityDepartment of Cardiology, The Second Affiliated Hospital of Jiaxing UniversityDepartment of Cardiology, The Second Affiliated Hospital of Jiaxing UniversityDepartment of Cardiology, The Second Affiliated Hospital of Jiaxing UniversityAbstract Anthracycline antitumor drug doxorubicin (DOX) induces severe cardiotoxicity. Deubiquitinating enzymes (DUBs) are crucial for protein stability and function and play a significant role in cardiac pathophysiology. By comparing RNA sequencing datasets and conducting functional screening, we determined that Myb-like, SWIRM, and MPN domains 1 (MYSM1) is a key regulator of DOX-induced cardiotoxicity. In this study, we aimed to explore the function and regulatory mechanisms of MYSM1 in DOX-induced cardiotoxicity. Genetic knockdown of MYSM1 significantly mitigated DOX-induced cardiomyopathy. Correspondingly, cardiomyocyte-specific knockdown of MYSM1 by AAV9 protected the heart from DOX-induced cardiotoxicity. Gain- and loss-of-function analysis verified that MYSM1 mediated DOX-induced cardiomyocyte injury in vitro. Through a Co-IP combined with LC-MS/MS analysis, we discovered that MYSM1 directly interacted with tripartite motif-containing protein 21 (TRIM21). Mechanistic investigations revealed that MYSM1 regulates the deubiquitination and the stability of TRIM21 via its MPN domain. Furthermore, MYSM1 exacerbated DOX-induced cardiotoxicity by enhancing ferroptosis. This study identified MYSM1 as a potential therapeutic target for DOX-induced cardiotoxicity and illustrated a MYSM1-TRIM21-ferroptosis axis in regulating DOX-induced cardiotoxicity.https://doi.org/10.1186/s12964-024-01955-6DoxorubicinCardiotoxicityDeubiquitinating enzymesMYSM1TRIM21Ferroptosis
spellingShingle Xiaowen Shi
Jianjiang Xu
Xin Zhong
Yuanyuan Qian
Liming Lin
Zimin Fang
Bozhi Ye
Yiting Lyu
Ran Zhang
Zhanxiong Zheng
Jibo Han
Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytes
Cell Communication and Signaling
Doxorubicin
Cardiotoxicity
Deubiquitinating enzymes
MYSM1
TRIM21
Ferroptosis
title Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytes
title_full Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytes
title_fullStr Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytes
title_full_unstemmed Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytes
title_short Deubiquitinase MYSM1 promotes doxorubicin-induced cardiotoxicity by mediating TRIM21-ferroptosis axis in cardiomyocytes
title_sort deubiquitinase mysm1 promotes doxorubicin induced cardiotoxicity by mediating trim21 ferroptosis axis in cardiomyocytes
topic Doxorubicin
Cardiotoxicity
Deubiquitinating enzymes
MYSM1
TRIM21
Ferroptosis
url https://doi.org/10.1186/s12964-024-01955-6
work_keys_str_mv AT xiaowenshi deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT jianjiangxu deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT xinzhong deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT yuanyuanqian deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT liminglin deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT ziminfang deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT bozhiye deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT yitinglyu deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT ranzhang deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT zhanxiongzheng deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes
AT jibohan deubiquitinasemysm1promotesdoxorubicininducedcardiotoxicitybymediatingtrim21ferroptosisaxisincardiomyocytes