PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular Carcinoma

Abstract Advanced hepatocellular carcinoma (HCC) is characterized by poor prognosis, primarily due to limited therapeutic options and resistance to treatment. Although the combination of tyrosine kinase inhibitors (TKIs) and immune checkpoint inhibitors (ICIs) has shown promising potential, the unde...

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Main Authors: Jitong Zhou, Meng Gao, Shikun Zhang, Wing‐Wa Guo, Wenzhi He, Minghe Zhang, Xi Chen, Cairang Dongzhi, Xiaomian Li, Yufeng Yuan, Weijie Ma
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202501730
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author Jitong Zhou
Meng Gao
Shikun Zhang
Wing‐Wa Guo
Wenzhi He
Minghe Zhang
Xi Chen
Cairang Dongzhi
Xiaomian Li
Yufeng Yuan
Weijie Ma
author_facet Jitong Zhou
Meng Gao
Shikun Zhang
Wing‐Wa Guo
Wenzhi He
Minghe Zhang
Xi Chen
Cairang Dongzhi
Xiaomian Li
Yufeng Yuan
Weijie Ma
author_sort Jitong Zhou
collection DOAJ
description Abstract Advanced hepatocellular carcinoma (HCC) is characterized by poor prognosis, primarily due to limited therapeutic options and resistance to treatment. Although the combination of tyrosine kinase inhibitors (TKIs) and immune checkpoint inhibitors (ICIs) has shown promising potential, the underlying mechanisms remain inadequately understood. Here, serine/threonine‐specific protein phosphatase (PP1A) is upregulated in Lenvatinib‐resistant HCC cells and correlates with poor prognosis. Functional experiments revealed that PP1A promotes HCC progression both in vitro and in vivo. Transcriptomic analysis and ferroptosis metabolite profiling (e.g., ROS, Fe2⁺, lipid‐ROS, and GSH) demonstrated that PP1A inhibits Lenvatinib‐induced ferroptosis by dephosphorylating Keap1 at site 104. This disruption of the Keap1‐Nrf2 interaction enhances the transcription of ferroptosis‐related markers and immune checkpoint PD‐L1. Notably, single‐cell sequencing and co‐culture experiments revealed that PP1A knockdown alleviates T cell exhaustion and immune evasion, thereby improving antitumor immunity. In vivo experiments further demonstrated that PP1A knockdown significantly enhances the efficacy of Lenvatinib‐ICIs combination therapy. Overall, our findings highlight PP1A as a critical regulator of ferroptosis and antitumor immunity, suggesting its potential as a predictive biomarker and therapeutic target for improving outcomes in advanced HCC.
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spelling doaj-art-b66faaabbca84663bedf5e6ca7e74d9d2025-08-20T02:40:00ZengWileyAdvanced Science2198-38442025-07-011227n/an/a10.1002/advs.202501730PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular CarcinomaJitong Zhou0Meng Gao1Shikun Zhang2Wing‐Wa Guo3Wenzhi He4Minghe Zhang5Xi Chen6Cairang Dongzhi7Xiaomian Li8Yufeng Yuan9Weijie Ma10Department of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaDepartment of Hepatobiliary and Pancreatic SurgeryZhongnan Hospital of Wuhan UniversityWuhan 430071 P. R. ChinaAbstract Advanced hepatocellular carcinoma (HCC) is characterized by poor prognosis, primarily due to limited therapeutic options and resistance to treatment. Although the combination of tyrosine kinase inhibitors (TKIs) and immune checkpoint inhibitors (ICIs) has shown promising potential, the underlying mechanisms remain inadequately understood. Here, serine/threonine‐specific protein phosphatase (PP1A) is upregulated in Lenvatinib‐resistant HCC cells and correlates with poor prognosis. Functional experiments revealed that PP1A promotes HCC progression both in vitro and in vivo. Transcriptomic analysis and ferroptosis metabolite profiling (e.g., ROS, Fe2⁺, lipid‐ROS, and GSH) demonstrated that PP1A inhibits Lenvatinib‐induced ferroptosis by dephosphorylating Keap1 at site 104. This disruption of the Keap1‐Nrf2 interaction enhances the transcription of ferroptosis‐related markers and immune checkpoint PD‐L1. Notably, single‐cell sequencing and co‐culture experiments revealed that PP1A knockdown alleviates T cell exhaustion and immune evasion, thereby improving antitumor immunity. In vivo experiments further demonstrated that PP1A knockdown significantly enhances the efficacy of Lenvatinib‐ICIs combination therapy. Overall, our findings highlight PP1A as a critical regulator of ferroptosis and antitumor immunity, suggesting its potential as a predictive biomarker and therapeutic target for improving outcomes in advanced HCC.https://doi.org/10.1002/advs.202501730combination therapyferroptosisimmune checkpoint inhibitorslenvatinibPD‐L1PP1A
spellingShingle Jitong Zhou
Meng Gao
Shikun Zhang
Wing‐Wa Guo
Wenzhi He
Minghe Zhang
Xi Chen
Cairang Dongzhi
Xiaomian Li
Yufeng Yuan
Weijie Ma
PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular Carcinoma
Advanced Science
combination therapy
ferroptosis
immune checkpoint inhibitors
lenvatinib
PD‐L1
PP1A
title PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular Carcinoma
title_full PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular Carcinoma
title_fullStr PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular Carcinoma
title_full_unstemmed PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular Carcinoma
title_short PP1A Modulates the Efficacy of Lenvatinib Plus ICIs Therapy by Inhibiting Ferroptosis in Hepatocellular Carcinoma
title_sort pp1a modulates the efficacy of lenvatinib plus icis therapy by inhibiting ferroptosis in hepatocellular carcinoma
topic combination therapy
ferroptosis
immune checkpoint inhibitors
lenvatinib
PD‐L1
PP1A
url https://doi.org/10.1002/advs.202501730
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