Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironment

Abstract Epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors are commonly used to treat non-small cell lung cancers with EGFR mutations, but drug resistance often emerges. Intratumor heterogeneity is a known cause of targeted therapy resistance and is considered a major factor in trea...

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Main Authors: Bassel Alsaed, Linh Lin, Jieun Son, Jiaqi Li, Johannes Smolander, Timothy Lopez, Pinar Ö. Eser, Atsuko Ogino, Chiara Ambrogio, Yoonji Eum, Tran Thai, Haiyun Wang, Eva Sutinen, Hilma Mutanen, Hanna Duàn, Nina Bobik, Kristian Borenius, William W. Feng, Behnam Nabet, Satu Mustjoki, Sanna Laaksonen, Benjamin K. Eschle, Michael J. Poitras, David Barbie, Ilkka Ilonen, Prafulla Gokhale, Pasi A. Jänne, Heidi M. Haikala
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55378-5
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author Bassel Alsaed
Linh Lin
Jieun Son
Jiaqi Li
Johannes Smolander
Timothy Lopez
Pinar Ö. Eser
Atsuko Ogino
Chiara Ambrogio
Yoonji Eum
Tran Thai
Haiyun Wang
Eva Sutinen
Hilma Mutanen
Hanna Duàn
Nina Bobik
Kristian Borenius
William W. Feng
Behnam Nabet
Satu Mustjoki
Sanna Laaksonen
Benjamin K. Eschle
Michael J. Poitras
David Barbie
Ilkka Ilonen
Prafulla Gokhale
Pasi A. Jänne
Heidi M. Haikala
author_facet Bassel Alsaed
Linh Lin
Jieun Son
Jiaqi Li
Johannes Smolander
Timothy Lopez
Pinar Ö. Eser
Atsuko Ogino
Chiara Ambrogio
Yoonji Eum
Tran Thai
Haiyun Wang
Eva Sutinen
Hilma Mutanen
Hanna Duàn
Nina Bobik
Kristian Borenius
William W. Feng
Behnam Nabet
Satu Mustjoki
Sanna Laaksonen
Benjamin K. Eschle
Michael J. Poitras
David Barbie
Ilkka Ilonen
Prafulla Gokhale
Pasi A. Jänne
Heidi M. Haikala
author_sort Bassel Alsaed
collection DOAJ
description Abstract Epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors are commonly used to treat non-small cell lung cancers with EGFR mutations, but drug resistance often emerges. Intratumor heterogeneity is a known cause of targeted therapy resistance and is considered a major factor in treatment failure. This study identifies clones of EGFR-mutant non-small cell lung tumors expressing low levels of both wild-type and mutant EGFR protein. These EGFR-low cells are intrinsically more tolerant to EGFR inhibitors, more invasive, and exhibit an epithelial-to-mesenchymal-like phenotype compared to their EGFR-high counterparts. The EGFR-low cells secrete Transforming growth factor beta (TGFβ) family cytokines, leading to increased recruitment of cancer-associated fibroblasts and immune suppression, thus contributing to the drug-tolerant tumor microenvironment. Notably, pharmacological induction of EGFR using epigenetic inhibitors sensitizes the resistant cells to EGFR inhibition. These findings suggest that intrinsic drug resistance can be prevented or reversed using combination therapies.
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spelling doaj-art-c8a6f8fe8f964bb5979968858901dd632025-08-20T02:53:53ZengNature PortfolioNature Communications2041-17232025-01-0116111710.1038/s41467-024-55378-5Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironmentBassel Alsaed0Linh Lin1Jieun Son2Jiaqi Li3Johannes Smolander4Timothy Lopez5Pinar Ö. Eser6Atsuko Ogino7Chiara Ambrogio8Yoonji Eum9Tran Thai10Haiyun Wang11Eva Sutinen12Hilma Mutanen13Hanna Duàn14Nina Bobik15Kristian Borenius16William W. Feng17Behnam Nabet18Satu Mustjoki19Sanna Laaksonen20Benjamin K. Eschle21Michael J. Poitras22David Barbie23Ilkka Ilonen24Prafulla Gokhale25Pasi A. Jänne26Heidi M. Haikala27Translational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiTranslational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteTranslational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Molecular Biotechnology and Health Sciences, Molecular Biotechnology Center, University of TorinoDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteSchool of Life Sciences and Technology, Tongji UniversityIndividualized Drug Therapy Research Program, Faculty of Medicine, University of HelsinkiTranslational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiTranslational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiTranslational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiDepartment of General Thoracic and Esophageal Surgery, Heart and Lung Center, Helsinki University Hospital & University of HelsinkiDepartment of Medical Oncology, Dana-Farber Cancer InstituteHuman Biology Division, Fred Hutchinson Cancer CenterTranslational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiDepartment of Pathology, Helsinki University Hospital & University of HelsinkiDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteiCAN Digital Precision Cancer Medicine FlagshipDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteTranslational Immunology Research Program (TRIMM), Research Programs Unit, Faculty of Medicine, University of HelsinkiAbstract Epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors are commonly used to treat non-small cell lung cancers with EGFR mutations, but drug resistance often emerges. Intratumor heterogeneity is a known cause of targeted therapy resistance and is considered a major factor in treatment failure. This study identifies clones of EGFR-mutant non-small cell lung tumors expressing low levels of both wild-type and mutant EGFR protein. These EGFR-low cells are intrinsically more tolerant to EGFR inhibitors, more invasive, and exhibit an epithelial-to-mesenchymal-like phenotype compared to their EGFR-high counterparts. The EGFR-low cells secrete Transforming growth factor beta (TGFβ) family cytokines, leading to increased recruitment of cancer-associated fibroblasts and immune suppression, thus contributing to the drug-tolerant tumor microenvironment. Notably, pharmacological induction of EGFR using epigenetic inhibitors sensitizes the resistant cells to EGFR inhibition. These findings suggest that intrinsic drug resistance can be prevented or reversed using combination therapies.https://doi.org/10.1038/s41467-024-55378-5
spellingShingle Bassel Alsaed
Linh Lin
Jieun Son
Jiaqi Li
Johannes Smolander
Timothy Lopez
Pinar Ö. Eser
Atsuko Ogino
Chiara Ambrogio
Yoonji Eum
Tran Thai
Haiyun Wang
Eva Sutinen
Hilma Mutanen
Hanna Duàn
Nina Bobik
Kristian Borenius
William W. Feng
Behnam Nabet
Satu Mustjoki
Sanna Laaksonen
Benjamin K. Eschle
Michael J. Poitras
David Barbie
Ilkka Ilonen
Prafulla Gokhale
Pasi A. Jänne
Heidi M. Haikala
Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironment
Nature Communications
title Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironment
title_full Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironment
title_fullStr Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironment
title_full_unstemmed Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironment
title_short Intratumor heterogeneity of EGFR expression mediates targeted therapy resistance and formation of drug tolerant microenvironment
title_sort intratumor heterogeneity of egfr expression mediates targeted therapy resistance and formation of drug tolerant microenvironment
url https://doi.org/10.1038/s41467-024-55378-5
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