An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung Tumorigenesis

Abstract Despite epidermal growth factor receptor (EGFR) is a pivotal oncogene for several cancers, including lung adenocarcinoma (LUAD), how it senses extracellular matrix (ECM) rigidity remain elusive in the context of the increasing role of tissue rigidity on various hallmarks of cancer developme...

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Main Authors: Reza Bayat Mokhtari, Divyaleka Sampath, Paige Eversole, Melissa Ong Yu Lin, Dmitriy A. Bosykh, Gandhi T.K. Boopathy, Aravind Sivakumar, Cheng‐Chun Wang, Ramesh Kumar, Joe Yeong Poh Sheng, Ellen Karasik, Barbara A. Foster, Han Yu, Xiang Ling, Wenjie Wu, Fengzhi Li, Zoë Weaver Ohler, Christine F. Brainson, David W. Goodrich, Wanjin Hong, Sayan Chakraborty
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202413443
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author Reza Bayat Mokhtari
Divyaleka Sampath
Paige Eversole
Melissa Ong Yu Lin
Dmitriy A. Bosykh
Gandhi T.K. Boopathy
Aravind Sivakumar
Cheng‐Chun Wang
Ramesh Kumar
Joe Yeong Poh Sheng
Ellen Karasik
Barbara A. Foster
Han Yu
Xiang Ling
Wenjie Wu
Fengzhi Li
Zoë Weaver Ohler
Christine F. Brainson
David W. Goodrich
Wanjin Hong
Sayan Chakraborty
author_facet Reza Bayat Mokhtari
Divyaleka Sampath
Paige Eversole
Melissa Ong Yu Lin
Dmitriy A. Bosykh
Gandhi T.K. Boopathy
Aravind Sivakumar
Cheng‐Chun Wang
Ramesh Kumar
Joe Yeong Poh Sheng
Ellen Karasik
Barbara A. Foster
Han Yu
Xiang Ling
Wenjie Wu
Fengzhi Li
Zoë Weaver Ohler
Christine F. Brainson
David W. Goodrich
Wanjin Hong
Sayan Chakraborty
author_sort Reza Bayat Mokhtari
collection DOAJ
description Abstract Despite epidermal growth factor receptor (EGFR) is a pivotal oncogene for several cancers, including lung adenocarcinoma (LUAD), how it senses extracellular matrix (ECM) rigidity remain elusive in the context of the increasing role of tissue rigidity on various hallmarks of cancer development. Here it is shown that EGFR dictates tumorigenic agrin expression in lung cancer cell lines, genetically engineered EGFR‐driven mouse models, and human specimens. Agrin expression confers substrate stiffness‐dependent oncogenic attributes to EGFR‐reliant cancer cells. Mechanistically, agrin mechanoactivates EGFR through epidermal growth factor (EGF)‐dependent and independent modes, thereby sensitizing its activity toward localized cancer cell‐ECM adherence and bulk rigidity by fostering interactions with integrin β1. Notably, a feed‐forward loop linking agrin–EGFR rigidity response to YAP–TEAD mechanosensing is essential for tumorigenesis. Together, the combined inhibition of EGFR–YAP/TEAD may offer a strategy to reduce lung tumorigenesis by disrupting agrin‐EGFR mechanotransduction, uncovering a therapeutic vulnerability for EGFR‐addicted lung cancers.
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spelling doaj-art-aff06d37e4704fef8b23bbe745446fac2025-08-20T03:20:10ZengWileyAdvanced Science2198-38442025-05-011220n/an/a10.1002/advs.202413443An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung TumorigenesisReza Bayat Mokhtari0Divyaleka Sampath1Paige Eversole2Melissa Ong Yu Lin3Dmitriy A. Bosykh4Gandhi T.K. Boopathy5Aravind Sivakumar6Cheng‐Chun Wang7Ramesh Kumar8Joe Yeong Poh Sheng9Ellen Karasik10Barbara A. Foster11Han Yu12Xiang Ling13Wenjie Wu14Fengzhi Li15Zoë Weaver Ohler16Christine F. Brainson17David W. Goodrich18Wanjin Hong19Sayan Chakraborty20Department of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USAInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeDepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USAInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeDepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USAInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeDepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USADepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USADepartment of Biostatistics Roswell Park Comprehensive Cancer Center Buffalo NY 14263 USADepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USADepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USADepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USACenter for Advanced Preclinical Research Frederick National Laboratory for Cancer Research National Cancer Institute NIH Bethesda MD 20892‐1088 USADepartment of Toxicology and Cancer Biology Markey Cancer Center University of Kentucky Lexington KY 40536 USADepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USAInstitute of Molecular and Cell Biology 61 Biopolis Drive Proteos Singapore 138673 SingaporeDepartment of Pharmacology and Therapeutics Roswell Park Comprehensive Cancer Center 265 Elm and Carlton Streets Buffalo NY 14263 USAAbstract Despite epidermal growth factor receptor (EGFR) is a pivotal oncogene for several cancers, including lung adenocarcinoma (LUAD), how it senses extracellular matrix (ECM) rigidity remain elusive in the context of the increasing role of tissue rigidity on various hallmarks of cancer development. Here it is shown that EGFR dictates tumorigenic agrin expression in lung cancer cell lines, genetically engineered EGFR‐driven mouse models, and human specimens. Agrin expression confers substrate stiffness‐dependent oncogenic attributes to EGFR‐reliant cancer cells. Mechanistically, agrin mechanoactivates EGFR through epidermal growth factor (EGF)‐dependent and independent modes, thereby sensitizing its activity toward localized cancer cell‐ECM adherence and bulk rigidity by fostering interactions with integrin β1. Notably, a feed‐forward loop linking agrin–EGFR rigidity response to YAP–TEAD mechanosensing is essential for tumorigenesis. Together, the combined inhibition of EGFR–YAP/TEAD may offer a strategy to reduce lung tumorigenesis by disrupting agrin‐EGFR mechanotransduction, uncovering a therapeutic vulnerability for EGFR‐addicted lung cancers.https://doi.org/10.1002/advs.202413443agrinEGFR, extracellular matrixhippo pathwaylung cancerYAP/TAZ
spellingShingle Reza Bayat Mokhtari
Divyaleka Sampath
Paige Eversole
Melissa Ong Yu Lin
Dmitriy A. Bosykh
Gandhi T.K. Boopathy
Aravind Sivakumar
Cheng‐Chun Wang
Ramesh Kumar
Joe Yeong Poh Sheng
Ellen Karasik
Barbara A. Foster
Han Yu
Xiang Ling
Wenjie Wu
Fengzhi Li
Zoë Weaver Ohler
Christine F. Brainson
David W. Goodrich
Wanjin Hong
Sayan Chakraborty
An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung Tumorigenesis
Advanced Science
agrin
EGFR, extracellular matrix
hippo pathway
lung cancer
YAP/TAZ
title An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung Tumorigenesis
title_full An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung Tumorigenesis
title_fullStr An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung Tumorigenesis
title_full_unstemmed An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung Tumorigenesis
title_short An Agrin–YAP/TAZ Rigidity Sensing Module Drives EGFR‐Addicted Lung Tumorigenesis
title_sort agrin yap taz rigidity sensing module drives egfr addicted lung tumorigenesis
topic agrin
EGFR, extracellular matrix
hippo pathway
lung cancer
YAP/TAZ
url https://doi.org/10.1002/advs.202413443
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