Somatic rearrangements causing oncogenic ectodomain deletions of FGFR1 in squamous cell lung cancer.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
01 11 2023
Historique:
received: 07 03 2023
accepted: 17 08 2023
medline: 2 11 2023
pubmed: 22 8 2023
entrez: 22 8 2023
Statut: epublish

Résumé

The discovery of frequent 8p11-p12 amplifications in squamous cell lung cancer (SQLC) has fueled hopes that FGFR1, located inside this amplicon, might be a therapeutic target. In a clinical trial, only 11% of patients with 8p11 amplification (detected by FISH) responded to FGFR kinase inhibitor treatment. To understand the mechanism of FGFR1 dependency, we performed deep genomic characterization of 52 SQLCs with 8p11-p12 amplification, including 10 tumors obtained from patients who had been treated with FGFR inhibitors. We discovered somatically altered variants of FGFR1 with deletion of exons 1-8 that resulted from intragenic tail-to-tail rearrangements. These ectodomain-deficient FGFR1 variants (ΔEC-FGFR1) were expressed in the affected tumors and were tumorigenic in both in vitro and in vivo models of lung cancer. Mechanistically, breakage-fusion-bridges were the source of 8p11-p12 amplification, resulting from frequent head-to-head and tail-to-tail rearrangements. Generally, tail-to-tail rearrangements within or in close proximity upstream of FGFR1 were associated with FGFR1 dependency. Thus, the genomic events shaping the architecture of the 8p11-p12 amplicon provide a mechanistic explanation for the emergence of FGFR1-driven SQLC. Specifically, we believe that FGFR1 ectodomain-deficient and FGFR1-centered amplifications caused by tail-to-tail rearrangements are a novel somatic genomic event that might be predictive of therapeutically relevant FGFR1 dependency.

Identifiants

pubmed: 37606995
pii: 170217
doi: 10.1172/JCI170217
pmc: PMC10617767
doi:
pii:

Substances chimiques

Receptor, Fibroblast Growth Factor, Type 1 EC 2.7.10.1
Protein Kinase Inhibitors 0
FGFR1 protein, human EC 2.7.10.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : P50 CA070907
Pays : United States
Organisme : Medical Research Council
ID : MR/S00811X/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 214342/Z/18/Z
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn
Type : CommentIn

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Auteurs

Florian Malchers (F)

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

Lucia Nogova (L)

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

Martijn Ha van Attekum (MH)

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

Lukas Maas (L)

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

Johannes Brägelmann (J)

University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Translational Genomics, Cologne, Germany Germany.
Mildred Scheel School of Oncology, Cologne, University Hospital Cologne, Medical Faculty, Cologne, Germany.
University of Cologne, Faculty of Medicine and University Hospital Cologne, Institute of Pathology, Cologne, Germany.

Christoph Bartenhagen (C)

Department of Experimental Pediatric Oncology, University Children's Hospital of Cologne, University Hospital Cologne, Medical Faculty, Cologne, Germany.

Luc Girard (L)

University of Texas Southwestern Medical Center, Dallas, Texas, USA.

Graziella Bosco (G)

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

Ilona Dahmen (I)

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

Sebastian Michels (S)

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

Clare E Weeden (CE)

Personalized Oncology Division, Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne, Parkville, Australia.

Andreas H Scheel (AH)

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

Lydia Meder (L)

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

Kristina Golfmann (K)

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

Philipp Schuldt (P)

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

Janna Siemanowski (J)

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

Jan Rehker (J)

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

Sabine Merkelbach-Bruse (S)

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

Roopika Menon (R)

DISCO Pharmaceuticals GmbH, Cologne, Germany.

Oliver Gautschi (O)

University of Berne and Cantonal Hospital of Lucerne, Cantonal Hospital of Lucerne, Lucerne, Switzerland.

Johannes M Heuckmann (JM)

DISCO Pharmaceuticals GmbH, Cologne, Germany.

Elisabeth Brambilla (E)

Département d'Anatomie et Cytologie Pathologiques, Grenoble, France.

Marie-Liesse Asselin-Labat (ML)

Personalized Oncology Division, Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne, Parkville, Australia.

Thorsten Persigehl (T)

Institute for Diagnostic and Interventional Radiology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

John D Minna (JD)

University of Texas Southwestern Medical Center, Dallas, Texas, USA.

Henning Walczak (H)

Institute of Biochemistry I, Medical Faculty, University of Cologne, Cologne, Germany.
CECAD Cluster of Excellence, University of Cologne, Cologne, Germany.
Centre for Cell Death, Cancer, and Inflammation (CCCI), UCL Cancer Institute, University College London, London, United Kingdom.

Roland T Ullrich (RT)

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

Matthias Fischer (M)

Department of Experimental Pediatric Oncology, University Children's Hospital of Cologne, University Hospital Cologne, Medical Faculty, Cologne, Germany.
Center for Molecular Medicine Cologne (CMMC), Cologne, Germany.

Hans Christian Reinhardt (HC)

Department of Hematology and Stem Cell Transplantation, University Hospital Essen, University Duisburg-Essen, Essen, Germany.

Jürgen Wolf (J)

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

Reinhard Büttner (R)

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

Martin Peifer (M)

University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Translational Genomics, Cologne, Germany Germany.
Center for Molecular Medicine Cologne (CMMC), Cologne, Germany.

Julie George (J)

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

Roman K Thomas (RK)

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

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