Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR Inhibitor

Abstract Fibroblast growth factor receptor (FGFR) inhibitors are emerged as an important class of targeted therapies in oncology, targeting key pathways associated with tumor growth, angiogenesis, and resistance to conventional treatments. FIIN‐2, the first irreversible covalent pan‐FGFR inhibitor,...

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Main Authors: Ying Fu, Dandan Zhu, Xiaojuan Chen, Lingzhi Qu, Ming Guo, Shuhong Zhang, Guangyu Xu, Zhuchu Chen, Maoyu Li, Yongheng Chen
Format: Article
Language:English
Published: Wiley 2025-04-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202412578
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author Ying Fu
Dandan Zhu
Xiaojuan Chen
Lingzhi Qu
Ming Guo
Shuhong Zhang
Guangyu Xu
Zhuchu Chen
Maoyu Li
Yongheng Chen
author_facet Ying Fu
Dandan Zhu
Xiaojuan Chen
Lingzhi Qu
Ming Guo
Shuhong Zhang
Guangyu Xu
Zhuchu Chen
Maoyu Li
Yongheng Chen
author_sort Ying Fu
collection DOAJ
description Abstract Fibroblast growth factor receptor (FGFR) inhibitors are emerged as an important class of targeted therapies in oncology, targeting key pathways associated with tumor growth, angiogenesis, and resistance to conventional treatments. FIIN‐2, the first irreversible covalent pan‐FGFR inhibitor, has shown promise in overcoming resistance due to gatekeeper mutations; however, its selectivity and molecular mechanisms in tumors remain poorly understood. In this study, an FIIN‐2 chemical probe is designed and synthesized to identify both established and novel targets in hepatocellular carcinoma (HCC) via chemoproteomic profiling. An integrative multi‐omics approach, including chemoproteomic, phosphoproteomic, transcriptomic, and proteomic analyses, is utilized to elucidate the full spectrum of target proteins, signaling pathways, and downstream effectors regulated by FIIN‐2 in HCC. Notably, adenosine monophosphate‐activated protein kinase α1 (AMPKα1) is identified as a novel target of FIIN‐2, with Cys185 identified as its covalent binding site. These findings reveal that FIIN‐2 can induce autophagy by directly binding to and activating AMPKα1, influencing its anti‐tumor activity in HCC cells. Overall, this study greatly advances the understanding of FIIN‐2′s on‐ and off‐target effects, offering a comprehensive view of its molecular mechanisms in cancer cells. The integrative multi‐omics approach provides a valuable framework for the development and optimization of covalent kinase inhibitors.
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spelling doaj-art-21c3c31e47f44697a3db7ac23bf6bcf42025-08-20T03:06:24ZengWileyAdvanced Science2198-38442025-04-011214n/an/a10.1002/advs.202412578Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR InhibitorYing Fu0Dandan Zhu1Xiaojuan Chen2Lingzhi Qu3Ming Guo4Shuhong Zhang5Guangyu Xu6Zhuchu Chen7Maoyu Li8Yongheng Chen9Department of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaKey Laboratory of Chemical Biology and Traditional Chinese Medicine Ministry of Educational of China Key Laboratory of the Assembly and Application of Organic Functional Molecules of Hunan Province College of Chemistry and Chemical Engineering Hunan Normal University Changsha Hunan 410081 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaDepartment of Oncology NHC Key Laboratory of Cancer Proteomics and State Local Joint Engineering Laboratory for Anticancer Drugs National Clinical Research Center for Geriatric Disorders Xiangya Hospital Central South University Changsha Hunan 410008 ChinaAbstract Fibroblast growth factor receptor (FGFR) inhibitors are emerged as an important class of targeted therapies in oncology, targeting key pathways associated with tumor growth, angiogenesis, and resistance to conventional treatments. FIIN‐2, the first irreversible covalent pan‐FGFR inhibitor, has shown promise in overcoming resistance due to gatekeeper mutations; however, its selectivity and molecular mechanisms in tumors remain poorly understood. In this study, an FIIN‐2 chemical probe is designed and synthesized to identify both established and novel targets in hepatocellular carcinoma (HCC) via chemoproteomic profiling. An integrative multi‐omics approach, including chemoproteomic, phosphoproteomic, transcriptomic, and proteomic analyses, is utilized to elucidate the full spectrum of target proteins, signaling pathways, and downstream effectors regulated by FIIN‐2 in HCC. Notably, adenosine monophosphate‐activated protein kinase α1 (AMPKα1) is identified as a novel target of FIIN‐2, with Cys185 identified as its covalent binding site. These findings reveal that FIIN‐2 can induce autophagy by directly binding to and activating AMPKα1, influencing its anti‐tumor activity in HCC cells. Overall, this study greatly advances the understanding of FIIN‐2′s on‐ and off‐target effects, offering a comprehensive view of its molecular mechanisms in cancer cells. The integrative multi‐omics approach provides a valuable framework for the development and optimization of covalent kinase inhibitors.https://doi.org/10.1002/advs.202412578AMPKα1chemoproteomicsFGFR inhibitorHCCmulti‐omics
spellingShingle Ying Fu
Dandan Zhu
Xiaojuan Chen
Lingzhi Qu
Ming Guo
Shuhong Zhang
Guangyu Xu
Zhuchu Chen
Maoyu Li
Yongheng Chen
Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR Inhibitor
Advanced Science
AMPKα1
chemoproteomics
FGFR inhibitor
HCC
multi‐omics
title Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR Inhibitor
title_full Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR Inhibitor
title_fullStr Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR Inhibitor
title_full_unstemmed Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR Inhibitor
title_short Integrative Multi‐Omics Approaches Reveal Selectivity Profiles and Molecular Mechanisms of FIIN‐2, a Covalent FGFR Inhibitor
title_sort integrative multi omics approaches reveal selectivity profiles and molecular mechanisms of fiin 2 a covalent fgfr inhibitor
topic AMPKα1
chemoproteomics
FGFR inhibitor
HCC
multi‐omics
url https://doi.org/10.1002/advs.202412578
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