A subset of pediatric-type thalamic gliomas share a distinct DNA methylation profile, H3K27me3 loss and frequent alteration of EGFR.


Journal

Neuro-oncology
ISSN: 1523-5866
Titre abrégé: Neuro Oncol
Pays: England
ID NLM: 100887420

Informations de publication

Date de publication:
30 01 2021
Historique:
pubmed: 2 11 2020
medline: 28 4 2021
entrez: 1 11 2020
Statut: ppublish

Résumé

Malignant astrocytic gliomas in children show a remarkable biological and clinical diversity. Small in-frame insertions or missense mutations in the epidermal growth factor receptor gene (EGFR) have recently been identified in a distinct subset of pediatric-type bithalamic gliomas with a unique DNA methylation pattern. Here, we investigated an epigenetically homogeneous cohort of malignant gliomas (n = 58) distinct from other subtypes and enriched for pediatric cases and thalamic location, in comparison with this recently identified subtype of pediatric bithalamic gliomas. EGFR gene amplification was detected in 16/58 (27%) tumors, and missense mutations or small in-frame insertions in EGFR were found in 20/30 tumors with available sequencing data (67%; 5 of them co-occurring with EGFR amplification). Additionally, 8 of the 30 tumors (27%) harbored an H3.1 or H3.3 K27M mutation (6 of them with a concomitant EGFR alteration). All tumors tested showed loss of H3K27me3 staining, with evidence of overexpression of the EZH inhibitory protein (EZHIP) in the H3 wildtype cases. Although some tumors indeed showed a bithalamic growth pattern, a significant proportion of tumors occurred in the unilateral thalamus or in other (predominantly midline) locations. Our findings present a distinct molecular class of pediatric-type malignant gliomas largely overlapping with the recently reported bithalamic gliomas characterized by EGFR alteration, but additionally showing a broader spectrum of EGFR alterations and tumor localization. Global H3K27me3 loss in this group appears to be mediated by either H3 K27 mutation or EZHIP overexpression. EGFR inhibition may represent a potential therapeutic strategy in these highly aggressive gliomas.

Sections du résumé

BACKGROUND
Malignant astrocytic gliomas in children show a remarkable biological and clinical diversity. Small in-frame insertions or missense mutations in the epidermal growth factor receptor gene (EGFR) have recently been identified in a distinct subset of pediatric-type bithalamic gliomas with a unique DNA methylation pattern.
METHODS
Here, we investigated an epigenetically homogeneous cohort of malignant gliomas (n = 58) distinct from other subtypes and enriched for pediatric cases and thalamic location, in comparison with this recently identified subtype of pediatric bithalamic gliomas.
RESULTS
EGFR gene amplification was detected in 16/58 (27%) tumors, and missense mutations or small in-frame insertions in EGFR were found in 20/30 tumors with available sequencing data (67%; 5 of them co-occurring with EGFR amplification). Additionally, 8 of the 30 tumors (27%) harbored an H3.1 or H3.3 K27M mutation (6 of them with a concomitant EGFR alteration). All tumors tested showed loss of H3K27me3 staining, with evidence of overexpression of the EZH inhibitory protein (EZHIP) in the H3 wildtype cases. Although some tumors indeed showed a bithalamic growth pattern, a significant proportion of tumors occurred in the unilateral thalamus or in other (predominantly midline) locations.
CONCLUSIONS
Our findings present a distinct molecular class of pediatric-type malignant gliomas largely overlapping with the recently reported bithalamic gliomas characterized by EGFR alteration, but additionally showing a broader spectrum of EGFR alterations and tumor localization. Global H3K27me3 loss in this group appears to be mediated by either H3 K27 mutation or EZHIP overexpression. EGFR inhibition may represent a potential therapeutic strategy in these highly aggressive gliomas.

Identifiants

pubmed: 33130881
pii: 5948536
doi: 10.1093/neuonc/noaa251
pmc: PMC7850075
doi:

Substances chimiques

Histones 0
EGFR protein, human EC 2.7.10.1
ErbB Receptors EC 2.7.10.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

34-43

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Neuro-Oncology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Auteurs

Philipp Sievers (P)

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.
Clinical Cooperation Unit Neuropathology, German Consortium for Translational Cancer Research (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Martin Sill (M)

Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.
Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Daniel Schrimpf (D)

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.
Clinical Cooperation Unit Neuropathology, German Consortium for Translational Cancer Research (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Damian Stichel (D)

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.
Clinical Cooperation Unit Neuropathology, German Consortium for Translational Cancer Research (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

David E Reuss (DE)

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.
Clinical Cooperation Unit Neuropathology, German Consortium for Translational Cancer Research (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Dominik Sturm (D)

Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.
Pediatric Glioma Research Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Department of Pediatric Oncology, Hematology, Immunology, and Pulmonology, University Hospital Heidelberg, Heidelberg, Germany.

Jürgen Hench (J)

Institute for Medical Genetics and Pathology, University Hospital Basel, Basel, Switzerland.

Stephan Frank (S)

Institute for Medical Genetics and Pathology, University Hospital Basel, Basel, Switzerland.

Lenka Krskova (L)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.
Department of Pathology and Molecular Medicine, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.

Ales Vicha (A)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.
Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.

Michal Zapotocky (M)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.
Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.

Brigitte Bison (B)

Institute of Diagnostic and Interventional Neuroradiology, University Hospital Würzburg, Würzburg, Germany.

David Castel (D)

Molecular Predictors and New Targets in Oncology, INSERM, Gustave Roussy, Université Paris-Saclay, Villejuif, France.
Département de Cancérologie de l'Enfant et de l'Adolescent, Gustave Roussy, Université Paris-Saclay, Villejuif, France.

Jacques Grill (J)

Molecular Predictors and New Targets in Oncology, INSERM, Gustave Roussy, Université Paris-Saclay, Villejuif, France.
Département de Cancérologie de l'Enfant et de l'Adolescent, Gustave Roussy, Université Paris-Saclay, Villejuif, France.

Marie-Anne Debily (MA)

Molecular Predictors and New Targets in Oncology, INSERM, Gustave Roussy, Université Paris-Saclay, Villejuif, France.
Département de Biologie, Univ. Evry, Université Paris-Saclay, Evry, France.

Patrick N Harter (PN)

Institute of Neurology (Edinger Institute), Goethe University, Frankfurt am Main, Germany.
German Cancer Consortium (DKTK), Partner Site Frankfurt/Mainz, Frankfurt am Main, Germany.
German Cancer Research Center (DKFZ), Heidelberg, Germany.
Frankfurt Cancer Institute (FCI), Frankfurt am Main, Germany.

Matija Snuderl (M)

Department of Pathology, NYU Langone Medical Center, New York, New York, USA.

Christof M Kramm (CM)

Division of Pediatric Hematology and Oncology, University Medical Center Göttingen, Göttingen, Germany.

Guido Reifenberger (G)

Institute of Neuropathology, Heinrich Heine University, Düsseldorf, Germany.
German Cancer Consortium (DKTK), Partner Site Essen/Düsseldorf, Germany.

Andrey Korshunov (A)

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.
Clinical Cooperation Unit Neuropathology, German Consortium for Translational Cancer Research (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.

Nada Jabado (N)

Department of Human Genetics, McGill University, Montreal, QC H3A 1B1, Canada.
Department of Pediatrics, McGill University, Montreal, QC H4A 3J1, Canada.
The Research Institute of the McGill University Health Center, Montreal, QC H4A 3J1, Canada (N.J.).

Pieter Wesseling (P)

Department of Pathology, Amsterdam University Medical Centers, Location VUmc and Brain Tumor Center Amsterdam, Amsterdam, the Netherlands (P.W.).
Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands (P.W.).

Wolfgang Wick (W)

Clinical Cooperation Unit Neurooncology, German Consortium for Translational Cancer Research (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
Department of Neurology and Neurooncology Program, National Center for Tumor Diseases, Heidelberg University Hospital, Heidelberg, Germany.

David A Solomon (DA)

Department of Pathology, University of California San Francisco (UCSF), San Francisco, California, USA (D.A.S., A.P.).
Clinical Cancer Genomics Laboratory, University of California San Francisco, San Francisco, California, USA (D.A.S.).

Arie Perry (A)

Department of Pathology, University of California San Francisco (UCSF), San Francisco, California, USA (D.A.S., A.P.).
Department of Neurological Surgery, University of California San Francisco, San Francisco, California, USA (A.P.).

Thomas S Jacques (TS)

Developmental Biology and Cancer Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London, UK.
Department of Histopathology, Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK.

Chris Jones (C)

Division of Molecular Pathology, Institute of Cancer Research, London, UK.

Olaf Witt (O)

Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.
Department of Pediatric Oncology, Hematology, Immunology, and Pulmonology, University Hospital Heidelberg, Heidelberg, Germany.
Clinical Cooperation Unit Pediatric Oncology, German Cancer Research Center (DKFZ) and German Consortium for Translational Cancer Research (DKTK), Heidelberg, Germany (O.W.).

Stefan M Pfister (SM)

Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.
Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Andreas von Deimling (A)

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.
Clinical Cooperation Unit Neuropathology, German Consortium for Translational Cancer Research (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

David T W Jones (DTW)

Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.
Pediatric Glioma Research Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Felix Sahm (F)

Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.

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