TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinoma

Abstract Hepatocellular carcinoma (HCC) is a leading cause of global cancer-associated mortality. Although various therapies have substantially ameliorated clinical outcome, patients invariably suffer from cancer relapse, highlighting the need for more optimized therapeutic strategies. Here, we repo...

Full description

Saved in:
Bibliographic Details
Main Authors: Jing He, Mingen Lin, Fei Teng, Xue Sun, Ziyin Tian, Jiaxi Li, Yan Ma, Yue Dai, Yi Gao, Hongchen Li, Tongguan Tian, Kai Xu, Xinxing Li, Lei Lv, Yanping Xu
Format: Article
Language:English
Published: Nature Publishing Group 2025-06-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07745-3
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850224346206830592
author Jing He
Mingen Lin
Fei Teng
Xue Sun
Ziyin Tian
Jiaxi Li
Yan Ma
Yue Dai
Yi Gao
Hongchen Li
Tongguan Tian
Kai Xu
Xinxing Li
Lei Lv
Yanping Xu
author_facet Jing He
Mingen Lin
Fei Teng
Xue Sun
Ziyin Tian
Jiaxi Li
Yan Ma
Yue Dai
Yi Gao
Hongchen Li
Tongguan Tian
Kai Xu
Xinxing Li
Lei Lv
Yanping Xu
author_sort Jing He
collection DOAJ
description Abstract Hepatocellular carcinoma (HCC) is a leading cause of global cancer-associated mortality. Although various therapies have substantially ameliorated clinical outcome, patients invariably suffer from cancer relapse, highlighting the need for more optimized therapeutic strategies. Here, we report that deficiency of DNA methylcytosine dioxygenase TET2 sensitizes HCC cells to sorafenib and verteporfin treatments. Mechanistically, knockout of TET2 enhances the dephosphorylation of YAP Ser127, thus promoting its activity. RNA-seq analysis reveals that MC1R, a GPCR, is strikingly decreased upon TET2 deficiency. Furthermore, TET2 catalyzes demethylation of MC1R promoter to stimulate its transcription. MC1R subsequently boosts cAMP-PKA signaling to phosphorylate YAP Ser127 in both ligand dependent and independent manners. Importantly, deletion of MC1R accelerates tumor growth of HCC, which is reversed by the treatment of YAP-TEAD complex inhibitor verteporfin. Synergistic combination of MC1R expression driver vitamin C and its ligand α-MSH dramatically represses HCC growth. Notably, TET2-MC1R-YAP axis is evidenced in HCC specimens and plays a vital role in prognosis of HCC. Collectively, these findings not only elucidate a previously unidentified epigenetic regulatory mechanism of MC1R transcription and underscore the functional significance of MC1R signaling in tumorigenesis of HCC, but also provide potential targets and clinical strategies for HCC therapy.
format Article
id doaj-art-dc5613464ec0426bbaa9504f7262b511
institution OA Journals
issn 2041-4889
language English
publishDate 2025-06-01
publisher Nature Publishing Group
record_format Article
series Cell Death and Disease
spelling doaj-art-dc5613464ec0426bbaa9504f7262b5112025-08-20T02:05:39ZengNature Publishing GroupCell Death and Disease2041-48892025-06-0116111210.1038/s41419-025-07745-3TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinomaJing He0Mingen Lin1Fei Teng2Xue Sun3Ziyin Tian4Jiaxi Li5Yan Ma6Yue Dai7Yi Gao8Hongchen Li9Tongguan Tian10Kai Xu11Xinxing Li12Lei Lv13Yanping Xu14Tongji Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityDepartment of Liver Surgery and Organ Transplantation, Changzheng Hospital, Naval Medical UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityTongji Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji UniversityTongji Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji UniversityTongji Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji UniversityDepartment of Gastrointestinal Surgery, Tongji Hospital Medical College of Tongji UniversityMOE Key Laboratory of Metabolism and Molecular Medicine, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan UniversityTongji Hospital, Shanghai Key Laboratory of Signaling and Disease Research, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji UniversityAbstract Hepatocellular carcinoma (HCC) is a leading cause of global cancer-associated mortality. Although various therapies have substantially ameliorated clinical outcome, patients invariably suffer from cancer relapse, highlighting the need for more optimized therapeutic strategies. Here, we report that deficiency of DNA methylcytosine dioxygenase TET2 sensitizes HCC cells to sorafenib and verteporfin treatments. Mechanistically, knockout of TET2 enhances the dephosphorylation of YAP Ser127, thus promoting its activity. RNA-seq analysis reveals that MC1R, a GPCR, is strikingly decreased upon TET2 deficiency. Furthermore, TET2 catalyzes demethylation of MC1R promoter to stimulate its transcription. MC1R subsequently boosts cAMP-PKA signaling to phosphorylate YAP Ser127 in both ligand dependent and independent manners. Importantly, deletion of MC1R accelerates tumor growth of HCC, which is reversed by the treatment of YAP-TEAD complex inhibitor verteporfin. Synergistic combination of MC1R expression driver vitamin C and its ligand α-MSH dramatically represses HCC growth. Notably, TET2-MC1R-YAP axis is evidenced in HCC specimens and plays a vital role in prognosis of HCC. Collectively, these findings not only elucidate a previously unidentified epigenetic regulatory mechanism of MC1R transcription and underscore the functional significance of MC1R signaling in tumorigenesis of HCC, but also provide potential targets and clinical strategies for HCC therapy.https://doi.org/10.1038/s41419-025-07745-3
spellingShingle Jing He
Mingen Lin
Fei Teng
Xue Sun
Ziyin Tian
Jiaxi Li
Yan Ma
Yue Dai
Yi Gao
Hongchen Li
Tongguan Tian
Kai Xu
Xinxing Li
Lei Lv
Yanping Xu
TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinoma
Cell Death and Disease
title TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinoma
title_full TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinoma
title_fullStr TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinoma
title_full_unstemmed TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinoma
title_short TET2 orchestrates YAP signaling to potentiate targetable vulnerability in hepatocellular carcinoma
title_sort tet2 orchestrates yap signaling to potentiate targetable vulnerability in hepatocellular carcinoma
url https://doi.org/10.1038/s41419-025-07745-3
work_keys_str_mv AT jinghe tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT mingenlin tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT feiteng tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT xuesun tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT ziyintian tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT jiaxili tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT yanma tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT yuedai tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT yigao tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT hongchenli tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT tongguantian tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT kaixu tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT xinxingli tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT leilv tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma
AT yanpingxu tet2orchestratesyapsignalingtopotentiatetargetablevulnerabilityinhepatocellularcarcinoma