SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPL

Summary: Protein SUMOylation is crucial in both physiological and pathological contexts, but its role in acute liver injury (ALI) is poorly understood. We found that SENP3, a SUMO2/3 protease, rapidly accumulates in hepatocytes around the pericentral vein zone within 2 h of carbon tetrachloride (CCl...

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Main Authors: Xinyuan Xiong, Yang Zhi, Nan Yang, Wenzhen Zhao, Shu Wang, Huiqin Zhu, Jieting Tang, Jing Yi, Xuxu Sun, Jie Yang
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225013288
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author Xinyuan Xiong
Yang Zhi
Nan Yang
Wenzhen Zhao
Shu Wang
Huiqin Zhu
Jieting Tang
Jing Yi
Xuxu Sun
Jie Yang
author_facet Xinyuan Xiong
Yang Zhi
Nan Yang
Wenzhen Zhao
Shu Wang
Huiqin Zhu
Jieting Tang
Jing Yi
Xuxu Sun
Jie Yang
author_sort Xinyuan Xiong
collection DOAJ
description Summary: Protein SUMOylation is crucial in both physiological and pathological contexts, but its role in acute liver injury (ALI) is poorly understood. We found that SENP3, a SUMO2/3 protease, rapidly accumulates in hepatocytes around the pericentral vein zone within 2 h of carbon tetrachloride (CCl4)-induced liver injury in mice. Knockout of SENP3 in hepatocytes worsens liver damage and promotes pyroptosis. Mechanistically, SENP3 interacts with the RNA-binding protein HNRNPL, facilitating its deSUMOylation and proteasomal degradation. This reduction of HNRNPL decreases nuclear paraspeckle assembly transcript 1 (Neat1) levels, impairing its ability to activate caspase-1 and induce pyroptosis. Moreover, in patients with drug-induced ALI, the levels of both SENP3 and HNRNPL are strongly correlated with pyroptosis. In conclusion, the SENP3-HNRNPL-Neat1 axis functions as a rapid stress sensor to mitigate excessive pyroptosis during ALI, making SENP3 and HNRNPL promising therapeutic targets.
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spelling doaj-art-78a2e4b720d345818fc0e0eefb6739072025-08-20T02:47:28ZengElsevieriScience2589-00422025-08-0128811306710.1016/j.isci.2025.113067SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPLXinyuan Xiong0Yang Zhi1Nan Yang2Wenzhen Zhao3Shu Wang4Huiqin Zhu5Jieting Tang6Jing Yi7Xuxu Sun8Jie Yang9Department of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDivision of Gastroenterology and Hepatology, Renji Hospital, Shanghai Jiao Tong University School of Medicine, NHC Key Laboratory of Digestive Diseases, Shanghai Research Center of Fatty Liver Disease, Shanghai, ChinaDepartment of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Department of Histology and Embryology, School of Basic Medical Science, Dali University, Dali, ChinaDepartment of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDivision of Gastroenterology and Hepatology, Renji Hospital, Shanghai Jiao Tong University School of Medicine, NHC Key Laboratory of Digestive Diseases, Shanghai Research Center of Fatty Liver Disease, Shanghai, ChinaDepartment of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Corresponding authorDepartment of Biochemistry and Molecular Cell Biology, State Key Laboratory of Oncogenes and Related Genes, Shanghai Key Laboratory for Tumor Microenvironment and Inflammation, Key Laboratory of Cell Differentiation and Apoptosis of Chinese Ministry of Education, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Corresponding authorSummary: Protein SUMOylation is crucial in both physiological and pathological contexts, but its role in acute liver injury (ALI) is poorly understood. We found that SENP3, a SUMO2/3 protease, rapidly accumulates in hepatocytes around the pericentral vein zone within 2 h of carbon tetrachloride (CCl4)-induced liver injury in mice. Knockout of SENP3 in hepatocytes worsens liver damage and promotes pyroptosis. Mechanistically, SENP3 interacts with the RNA-binding protein HNRNPL, facilitating its deSUMOylation and proteasomal degradation. This reduction of HNRNPL decreases nuclear paraspeckle assembly transcript 1 (Neat1) levels, impairing its ability to activate caspase-1 and induce pyroptosis. Moreover, in patients with drug-induced ALI, the levels of both SENP3 and HNRNPL are strongly correlated with pyroptosis. In conclusion, the SENP3-HNRNPL-Neat1 axis functions as a rapid stress sensor to mitigate excessive pyroptosis during ALI, making SENP3 and HNRNPL promising therapeutic targets.http://www.sciencedirect.com/science/article/pii/S2589004225013288Molecular mechanism of gene regulationMolecular networkIntegrative aspects of cell biology
spellingShingle Xinyuan Xiong
Yang Zhi
Nan Yang
Wenzhen Zhao
Shu Wang
Huiqin Zhu
Jieting Tang
Jing Yi
Xuxu Sun
Jie Yang
SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPL
iScience
Molecular mechanism of gene regulation
Molecular network
Integrative aspects of cell biology
title SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPL
title_full SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPL
title_fullStr SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPL
title_full_unstemmed SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPL
title_short SENP3 protects hepatocyte from pyroptosis during acute liver injury through deSUMOylation of HNRNPL
title_sort senp3 protects hepatocyte from pyroptosis during acute liver injury through desumoylation of hnrnpl
topic Molecular mechanism of gene regulation
Molecular network
Integrative aspects of cell biology
url http://www.sciencedirect.com/science/article/pii/S2589004225013288
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