Deciphering the role of the MALT1–RC3H1 axis in regulating GPX4 protein stability

J Jun Wang L Long Liao (State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) B Beiping Miao (State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) B Bo Yang B Botai Li (Shanghai Immune Therapy Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) X Xuhui Ma (State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) A Annika Fitz S Shanshan Wu (College of Chemistry and Chemical Engineering, Frontiers Science Center for Rare Isotopes) J Jia He Q Qianqian Zhang S Shuyi Ji (Institute for Regenerative Medicine, Medical Innovation Center and State Key Laboratory of Cardiology, Shanghai East Hospital, School of Medicine, Tongji University) G Guangzhi Jin (Department of Interventional Radiology, Tongren Hospital, Shanghai Jiao Tong University School of Medicine) J Jianming Zhang (Institute of Quantum and Sustainable Technology (IQST), School of Chemistry and Chemical Engineering) Y Ying Cao (State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) H Hui Wang W Wenxin Qin (State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) C Chong Sun (Division Immune Regulation in Cancer, German Cancer Research Center) R René Bernards (State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine) C Cun Wang (State Key Laboratory for Crop Stress Resistance and High-Efficiency Production, Institute of Future Agriculture, Northwest A&F University)

Abstract

Ferroptosis, a unique form of iron-dependent cell death triggered by lipid peroxidation accumulation, holds great promise for cancer therapy. Despite the crucial role of GPX4 in regulating ferroptosis, our understanding of GPX4 protein regulation remains limited. Through FACS-based genome-wide CRISPR screening, we identified MALT1 as a regulator of GPX4 protein. Inhibition of MALT1 expression enhances GPX4 ubiquitination-mediated degradation by up-regulating the E3 ubiquitin ligase RC3H1. Using both rescue assays and functional genetic screening, we demonstrate that pharmacologically targeting MALT1 triggers ferroptosis in liver cancer cells. Moreover, we show that targeting MALT1 synergizes with sorafenib or regorafenib to induce ferroptosis across multiple cancer types. These findings elucidate the modulatory effects of the MALT1–RC3H1 axis on GPX4 stability, revealing a molecular mechanism that could be exploited to induce ferroptosis for cancer therapy.

Article Details

Volume / Issue Vol. 122, Issue 1
Published January 07, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (19)

J

Jun Wang

L

Long Liao

State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

B

Beiping Miao

State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

B

Bo Yang

B

Botai Li

Shanghai Immune Therapy Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

X

Xuhui Ma

State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

A

Annika Fitz

S

Shanshan Wu

College of Chemistry and Chemical Engineering, Frontiers Science Center for Rare Isotopes

J

Jia He

Q

Qianqian Zhang

S

Shuyi Ji

Institute for Regenerative Medicine, Medical Innovation Center and State Key Laboratory of Cardiology, Shanghai East Hospital, School of Medicine, Tongji University

G

Guangzhi Jin

Department of Interventional Radiology, Tongren Hospital, Shanghai Jiao Tong University School of Medicine

J

Jianming Zhang

Institute of Quantum and Sustainable Technology (IQST), School of Chemistry and Chemical Engineering

Y

Ying Cao

State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

H

Hui Wang

W

Wenxin Qin

State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

C

Chong Sun

Division Immune Regulation in Cancer, German Cancer Research Center

R

René Bernards

State Key Laboratory of Systems Medicine for Cancer, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine

C

Cun Wang

State Key Laboratory for Crop Stress Resistance and High-Efficiency Production, Institute of Future Agriculture, Northwest A&F University