Treatment-Induced Tumor Dormancy through YAP-Mediated Transcriptional Reprogramming of the Apoptotic Pathway
Eradicating tumor dormancy that develops following epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor (TKI) treatment of EGFR-mutant non-small cell lung cancer, is an attractive therapeutic strategy but the mechanisms governing this process are poorly understood. Blockade of ERK1/2 re...
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| Published in | Cancer cell Vol. 37; no. 1; pp. 104 - 122.e12 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
13.01.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Eradicating tumor dormancy that develops following epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor (TKI) treatment of EGFR-mutant non-small cell lung cancer, is an attractive therapeutic strategy but the mechanisms governing this process are poorly understood. Blockade of ERK1/2 reactivation following EGFR TKI treatment by combined EGFR/MEK inhibition uncovers cells that survive by entering a senescence-like dormant state characterized by high YAP/TEAD activity. YAP/TEAD engage the epithelial-to-mesenchymal transition transcription factor SLUG to directly repress pro-apoptotic BMF, limiting drug-induced apoptosis. Pharmacological co-inhibition of YAP and TEAD, or genetic deletion of YAP1, all deplete dormant cells by enhancing EGFR/MEK inhibition-induced apoptosis. Enhancing the initial efficacy of targeted therapies could ultimately lead to prolonged treatment responses in cancer patients.
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•Loss of EGFR signaling leads to senescence-like dormancy in EGFR-mutant lung cancer•YAP promotes survival and dormancy in the absence of EGFR downstream signaling•YAP/TEAD/SLUG suppress apoptosis through transcriptional repression of BMF•A TEAD inhibitor enhances EGFR inhibitor-mediated apoptosis and prevents dormancy
Kurppa et al. show that YAP activation mediates resistance to combined EGFR/MEK inhibition by inducing dormancy in non-small-cell lung cancer cells. Targeting the YAP pathway, in part by using a newly developed covalent TEAD inhibitor, promotes apoptosis of the dormant therapy-resistant cancer cells. |
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| AbstractList | Eradicating tumor dormancy that develops following epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor (TKI) treatment of EGFR-mutant non-small cell lung cancer, is an attractive therapeutic strategy but the mechanisms governing this process are poorly understood. Blockade of ERK1/2 reactivation following EGFR TKI treatment by combined EGFR/MEK inhibition uncovers cells that survive by entering a senescence-like dormant state characterized by high YAP/TEAD activity. YAP/TEAD engage the epithelial-to-mesenchymal transition transcription factor SLUG to directly repress pro-apoptotic BMF, limiting drug-induced apoptosis. Pharmacological co-inhibition of YAP and TEAD, or genetic deletion of YAP1, all deplete dormant cells by enhancing EGFR/MEK inhibition-induced apoptosis. Enhancing the initial efficacy of targeted therapies could ultimately lead to prolonged treatment responses in cancer patients. Eradicating tumor dormancy that develops following epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor (TKI) treatment of EGFR -mutant non-small cell lung cancer (NSCLC), is an attractive therapeutic strategy but the mechanisms governing this process are poorly understood. Blockade of ERK1/2 reactivation following EGFR TKI treatment by combined EGFR/MEK inhibition uncovers cells that survive by entering a senescence-like dormant state characterized by high YAP/TEAD activity. YAP/TEAD engage the epithelial-to-mesenchymal transition (EMT) transcription factor SLUG to directly repress pro-apoptotic BMF , limiting drug-induced apoptosis. Pharmacological co-inhibition of YAP and TEAD, or genetic deletion of YAP1 , all deplete dormant cells by enhancing EGFR/MEK inhibition-induced apoptosis. Enhancing the initial efficacy of targeted therapies could ultimately lead to prolonged treatment responses in cancer patients. Kurppa et al. show that YAP activation mediates resistance to combined EGFR/MEK inhibition by inducing dormancy in non-small cell lung cancer cells. Targeting the YAP pathway, in part by using a newly developed covalent TEAD inhibitor, promotes apoptosis of the dormant therapy-resistant cancer cells. Eradicating tumor dormancy that develops following epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor (TKI) treatment of EGFR-mutant non-small cell lung cancer, is an attractive therapeutic strategy but the mechanisms governing this process are poorly understood. Blockade of ERK1/2 reactivation following EGFR TKI treatment by combined EGFR/MEK inhibition uncovers cells that survive by entering a senescence-like dormant state characterized by high YAP/TEAD activity. YAP/TEAD engage the epithelial-to-mesenchymal transition transcription factor SLUG to directly repress pro-apoptotic BMF, limiting drug-induced apoptosis. Pharmacological co-inhibition of YAP and TEAD, or genetic deletion of YAP1, all deplete dormant cells by enhancing EGFR/MEK inhibition-induced apoptosis. Enhancing the initial efficacy of targeted therapies could ultimately lead to prolonged treatment responses in cancer patients. [Display omitted] •Loss of EGFR signaling leads to senescence-like dormancy in EGFR-mutant lung cancer•YAP promotes survival and dormancy in the absence of EGFR downstream signaling•YAP/TEAD/SLUG suppress apoptosis through transcriptional repression of BMF•A TEAD inhibitor enhances EGFR inhibitor-mediated apoptosis and prevents dormancy Kurppa et al. show that YAP activation mediates resistance to combined EGFR/MEK inhibition by inducing dormancy in non-small-cell lung cancer cells. Targeting the YAP pathway, in part by using a newly developed covalent TEAD inhibitor, promotes apoptosis of the dormant therapy-resistant cancer cells. |
| Author | Jänne, Pasi A. Wang, Haiyun Bertram, Arrien A. Kirschmeier, Paul T. Gray, Nathanael S. Ebert, Benjamin L. Li, Shuai Lim, Klothilda Shin, Bo Hee Gokhale, Prafulla C. Paweletz, Cloud P. Haikala, Heidi M. Xu, Man Boettcher, Steffen Awad, Mark M. Knelson, Erik H. Shalhout, Sophia Choi, Jihyun Tillgren, Michelle L. Kurppa, Kari J. Cejas, Paloma Wilkens, Margaret K. Zhang, Tinghu Thai, Tran Long, Henry W. Wong, Kwok-Kin Fan, Mengyang Gao, Yang Marto, Jarrod A. Haq, Rizwan Bahcall, Magda Beroukhim, Rameen Portell, Andrew Ficarro, Scott B. Xie, Yingtian Bandopadhayay, Pratiti Liu, Yao Lizotte, Patrick H. To, Ciric Camargo, Fernando D. Vajdi, Amir Barbie, David A. Chen, Ting Mushajiang, Mierzhati |
| AuthorAffiliation | 10 School of Life Science and Technology, Tongji University, 200092 Shanghai, China 14 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA 16 Howard Hughes Medical Institute, Dana-Farber Cancer Institute, Boston, MA, 02215, USA 15 Experimental Therapeutics Core, Dana-Farber Cancer Institute, Boston, MA 02210, USA 19 Department of Molecular and Cellular Oncology, Dana Farber Cancer Institute, Boston, MA 02215, USA 3 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02215, USA 8 Department of Oncologic Pathology, Dana Farber Cancer Institute; Department of Pathology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02215, USA 7 Blais Proteomics Center, Dana Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA 20 Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA 6 Belfer Center for Applied Cancer Science, Dana-Farber Cancer Institute, Boston, MA 02215 USA 13 Stem Cell P |
| AuthorAffiliation_xml | – name: 14 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – name: 19 Department of Molecular and Cellular Oncology, Dana Farber Cancer Institute, Boston, MA 02215, USA – name: 6 Belfer Center for Applied Cancer Science, Dana-Farber Cancer Institute, Boston, MA 02215 USA – name: 15 Experimental Therapeutics Core, Dana-Farber Cancer Institute, Boston, MA 02210, USA – name: 10 School of Life Science and Technology, Tongji University, 200092 Shanghai, China – name: 3 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02215, USA – name: 5 Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, MA 02215, USA – name: 11 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – name: 7 Blais Proteomics Center, Dana Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – name: 9 Division of Hematology & Medical Oncology, Laura and Isaac Perlmutter Cancer Center, New York University Langone Medical Center, New York, NY, USA – name: 1 Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215 USA – name: 13 Stem Cell Program, Boston Children’s Hospital, Boston, MA 02215, USA; Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA – name: 8 Department of Oncologic Pathology, Dana Farber Cancer Institute; Department of Pathology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02215, USA – name: 17 Department of Medicine, Harvard Medical School, Boston, MA 02115, USA – name: 21 These authors contributed equally – name: 2 Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – name: 16 Howard Hughes Medical Institute, Dana-Farber Cancer Institute, Boston, MA, 02215, USA – name: 18 Dana-Farber/Boston Children’s Cancer and Blood Disorders Center, Boston, MA 02115, USA – name: 12 Department of Pediatrics, Harvard Medical School, Boston, MA 02215, USA – name: 20 Lowe Center for Thoracic Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – name: 4 Department of Informatics and Analytics, Dana-Farber Cancer Institute, Boston, MA 02215, USA |
| Author_xml | – sequence: 1 givenname: Kari J. surname: Kurppa fullname: Kurppa, Kari J. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 2 givenname: Yao surname: Liu fullname: Liu, Yao organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 3 givenname: Ciric surname: To fullname: To, Ciric organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 4 givenname: Tinghu surname: Zhang fullname: Zhang, Tinghu organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 5 givenname: Mengyang surname: Fan fullname: Fan, Mengyang organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 6 givenname: Amir surname: Vajdi fullname: Vajdi, Amir organization: Department of Informatics and Analytics, Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 7 givenname: Erik H. surname: Knelson fullname: Knelson, Erik H. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 8 givenname: Yingtian surname: Xie fullname: Xie, Yingtian organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 9 givenname: Klothilda surname: Lim fullname: Lim, Klothilda organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 10 givenname: Paloma surname: Cejas fullname: Cejas, Paloma organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 11 givenname: Andrew surname: Portell fullname: 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USA – sequence: 16 givenname: Heidi M. surname: Haikala fullname: Haikala, Heidi M. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 17 givenname: Haiyun surname: Wang fullname: Wang, Haiyun organization: School of Life Science and Technology, Tongji University, 200092 Shanghai, China – sequence: 18 givenname: Magda surname: Bahcall fullname: Bahcall, Magda organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 19 givenname: Yang surname: Gao fullname: Gao, Yang organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 20 givenname: Sophia surname: Shalhout fullname: Shalhout, Sophia organization: Stem Cell Program, Boston Children's Hospital, Boston, MA 02215, USA – sequence: 21 givenname: Steffen surname: Boettcher fullname: Boettcher, Steffen organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 22 givenname: Bo Hee surname: Shin fullname: Shin, Bo Hee organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 23 givenname: Tran surname: Thai fullname: Thai, Tran organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 24 givenname: Margaret K. surname: Wilkens fullname: Wilkens, Margaret K. organization: Experimental Therapeutics Core, Dana-Farber Cancer Institute, Boston, MA 02210, USA – sequence: 25 givenname: Michelle L. surname: Tillgren fullname: Tillgren, Michelle L. organization: Experimental Therapeutics Core, Dana-Farber Cancer Institute, Boston, MA 02210, USA – sequence: 26 givenname: Mierzhati surname: Mushajiang fullname: Mushajiang, Mierzhati organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 27 givenname: Man surname: Xu fullname: Xu, Man organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 28 givenname: Jihyun surname: Choi fullname: Choi, Jihyun organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 29 givenname: Arrien A. surname: Bertram fullname: Bertram, Arrien A. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 30 givenname: Benjamin L. surname: Ebert fullname: Ebert, Benjamin L. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 31 givenname: Rameen surname: Beroukhim fullname: Beroukhim, Rameen organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 32 givenname: Pratiti surname: Bandopadhayay fullname: Bandopadhayay, Pratiti organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 33 givenname: Mark M. surname: Awad fullname: Awad, Mark M. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 34 givenname: Prafulla C. surname: Gokhale fullname: Gokhale, Prafulla C. organization: Belfer Center for Applied Cancer Science, Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 35 givenname: Paul T. surname: Kirschmeier fullname: Kirschmeier, Paul T. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 36 givenname: Jarrod A. surname: Marto fullname: Marto, Jarrod A. organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 37 givenname: Fernando D. surname: Camargo fullname: Camargo, Fernando D. organization: Stem Cell Program, Boston Children's Hospital, Boston, MA 02215, USA – sequence: 38 givenname: Rizwan surname: Haq fullname: Haq, Rizwan organization: Department of Medicine, Harvard Medical School, Boston, MA 02115, USA – sequence: 39 givenname: Cloud P. surname: Paweletz fullname: Paweletz, Cloud P. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 40 givenname: Kwok-Kin surname: Wong fullname: Wong, Kwok-Kin organization: Division of Hematology & Medical Oncology, Laura and Isaac Perlmutter Cancer Center, New York University Langone Medical Center, New York, NY, USA – sequence: 41 givenname: David A. surname: Barbie fullname: Barbie, David A. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 42 givenname: Henry W. surname: Long fullname: Long, Henry W. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA – sequence: 43 givenname: Nathanael S. surname: Gray fullname: Gray, Nathanael S. organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 44 givenname: Pasi A. surname: Jänne fullname: Jänne, Pasi A. email: pasi_janne@dfci.harvard.edu organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31935369$$D View this record in MEDLINE/PubMed |
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| Copyright | 2019 Elsevier Inc. Copyright © 2019 Elsevier Inc. All rights reserved. |
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| Issue | 1 |
| Keywords | lung cancer senescence epidermal growth factor receptor dormancy YAP drug resistance drug tolerance |
| Language | English |
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| Notes | Lead contact: Pasi A. Jänne Author contributions: Conceptualization: KJK, PAJ, TZ, NSG, RH; Investigation: KJK, YL, CT, MF, EHK, KL, AP, PHL, SBF, SL, TC, HH, MB, YG, SS, BHS, TT MKW, MLT, MM. Resources: MX, JC, PTK, DAB FDC, PB, RB, AAB, KKW, MMA; Methodology: SB, BLE, PC, HWL, CPP; Formal Analyses: YX, HW, AV; Writing: KJK and PAJ; Funding acquisition: PAJ, NSG; Supervision, PAJ, NSG, TZ, PCG, JAM. |
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| PublicationTitle | Cancer cell |
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| PublicationYear | 2020 |
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| Snippet | Eradicating tumor dormancy that develops following epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor (TKI) treatment of EGFR-mutant non-small... Eradicating tumor dormancy that develops following epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor (TKI) treatment of EGFR -mutant non-small... |
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| SubjectTerms | Adaptor Proteins, Signal Transducing - metabolism Animals Apoptosis Cell Cycle Proteins - metabolism Cell Line, Tumor Cell Proliferation Cell Survival Cellular Senescence dormancy drug resistance Drug Resistance, Neoplasm drug tolerance epidermal growth factor receptor ErbB Receptors - metabolism Female Gene Deletion Gene Expression Regulation, Neoplastic Humans lung cancer Lung Neoplasms - metabolism Lung Neoplasms - pathology Male MAP Kinase Kinase 1 - metabolism Mice Mice, Knockout Mutation senescence Signal Transduction Transcription Factors - metabolism Transcription, Genetic YAP YAP-Signaling Proteins |
| Title | Treatment-Induced Tumor Dormancy through YAP-Mediated Transcriptional Reprogramming of the Apoptotic Pathway |
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