MAPK-pathway inhibition mediates inflammatory reprogramming and sensitizes tumors to targeted activation of innate immunity sensor RIG-I.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
17 09 2021
Historique:
received: 25 11 2020
accepted: 23 08 2021
entrez: 18 9 2021
pubmed: 19 9 2021
medline: 13 10 2021
Statut: epublish

Résumé

Kinase inhibitors suppress the growth of oncogene driven cancer but also enforce the selection of treatment resistant cells that are thought to promote tumor relapse in patients. Here, we report transcriptomic and functional genomics analyses of cells and tumors within their microenvironment across different genotypes that persist during kinase inhibitor treatment. We uncover a conserved, MAPK/IRF1-mediated inflammatory response in tumors that undergo stemness- and senescence-associated reprogramming. In these tumor cells, activation of the innate immunity sensor RIG-I via its agonist IVT4, triggers an interferon and a pro-apoptotic response that synergize with concomitant kinase inhibition. In humanized lung cancer xenografts and a syngeneic Egfr-driven lung cancer model these effects translate into reduction of exhausted CD8

Identifiants

pubmed: 34535668
doi: 10.1038/s41467-021-25728-8
pii: 10.1038/s41467-021-25728-8
pmc: PMC8448826
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Cytokines 0
IRF1 protein, human 0
Interferon Regulatory Factor-1 0
MAVS protein, human 0
Protein Kinase Inhibitors 0
Receptors, Immunologic 0
ErbB Receptors EC 2.7.10.1
RIGI protein, human EC 3.6.1.-
DEAD Box Protein 58 EC 3.6.4.13

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5505

Subventions

Organisme : NCI NIH HHS
ID : P30 CA045508
Pays : United States

Informations de copyright

© 2021. The Author(s).

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Auteurs

Johannes Brägelmann (J)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. johannes.braegelmann@uni-koeln.de.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. johannes.braegelmann@uni-koeln.de.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. johannes.braegelmann@uni-koeln.de.
Mildred Scheel School of Oncology Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. johannes.braegelmann@uni-koeln.de.

Carina Lorenz (C)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Sven Borchmann (S)

Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department I of Internal Medicine, Center for Integrated Oncology Aachen Bonn Cologne Duesseldorf, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Else-Kröner-Forschungskolleg Clonal Evolution in Cancer, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Kazuya Nishii (K)

Department of Hematology, Oncology and Respiratory Medicine, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan.

Julia Wegner (J)

Institute of Clinical Chemistry and Clinical Pharmacology, University Hospital Bonn, Bonn, Germany.

Lydia Meder (L)

Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Mildred Scheel School of Oncology Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department I of Internal Medicine, Center for Integrated Oncology Aachen Bonn Cologne Duesseldorf, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Jenny Ostendorp (J)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

David F Ast (DF)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Mildred Scheel School of Oncology Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Alena Heimsoeth (A)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Takamasa Nakasuka (T)

Department of Hematology, Oncology and Respiratory Medicine, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan.

Atsuko Hirabae (A)

Department of Hematology, Oncology and Respiratory Medicine, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan.

Sachi Okawa (S)

Department of Hematology, Oncology and Respiratory Medicine, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan.

Marcel A Dammert (MA)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Dennis Plenker (D)

Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 11724, USA.
Lustgarten Foundation Pancreatic Cancer Research Laboratory, Cold Spring Harbor, NY, 11724, USA.

Sebastian Klein (S)

Else-Kröner-Forschungskolleg Clonal Evolution in Cancer, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Philipp Lohneis (P)

Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Jianing Gu (J)

Institute for Developmental Cancer Therapeutics, West German Cancer Center, University Hospital Essen, Essen, Germany.
Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany.

Laura K Godfrey (LK)

Institute for Developmental Cancer Therapeutics, West German Cancer Center, University Hospital Essen, Essen, Germany.
Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany.

Jan Forster (J)

Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany.
Genome Informatics, Institute of Human Genetics, University Duisburg-Essen, Essen, Germany.

Marija Trajkovic-Arsic (M)

Institute for Developmental Cancer Therapeutics, West German Cancer Center, University Hospital Essen, Essen, Germany.
Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany.

Thomas Zillinger (T)

Institute of Clinical Chemistry and Clinical Pharmacology, University Hospital Bonn, Bonn, Germany.

Mareike Haarmann (M)

Mildred Scheel School of Oncology Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Alexander Quaas (A)

Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Stefanie Lennartz (S)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Marcel Schmiel (M)

Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Joshua D'Rozario (J)

Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Emily S Thomas (ES)

Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Imperial College London, London, UK.

Henry Li (H)

Crown Bioscience, San Diego, CA, USA.

Clemens A Schmitt (CA)

Department of Hematology, Oncology and Tumor Immunology, Charité - University Medical Center, Virchow Campus, and Molekulares Krebsforschungszentrum, Berlin, Germany.
Max-Delbrück-Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.
Department of Hematology and Oncology, Kepler University Hospital, Johannes Kepler University, Linz, Austria.

Julie George (J)

Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department of Head and Neck Surgery, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Roman K Thomas (RK)

Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
German Cancer Research Center, German Cancer Consortium (DKTK), Heidelberg, Germany.

Silvia von Karstedt (S)

Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Gunther Hartmann (G)

Institute of Clinical Chemistry and Clinical Pharmacology, University Hospital Bonn, Bonn, Germany.

Reinhard Büttner (R)

Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Roland T Ullrich (RT)

Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Department I of Internal Medicine, Center for Integrated Oncology Aachen Bonn Cologne Duesseldorf, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Jens T Siveke (JT)

Institute for Developmental Cancer Therapeutics, West German Cancer Center, University Hospital Essen, Essen, Germany.
Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany.

Kadoaki Ohashi (K)

Department of Hematology, Oncology and Respiratory Medicine, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan.
Department of Respiratory Medicine, Okayama University Hospital, Japan, 2-5-1 Shikata-cho, Kitaku, Okayama, 700-8558, Japan.

Martin Schlee (M)

Institute of Clinical Chemistry and Clinical Pharmacology, University Hospital Bonn, Bonn, Germany.

Martin L Sos (ML)

Molecular Pathology, Institute of Pathology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. martin.sos@uni-koeln.de.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. martin.sos@uni-koeln.de.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. martin.sos@uni-koeln.de.

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