Recurrent fusions in PLAGL1 define a distinct subset of pediatric-type supratentorial neuroepithelial tumors


Por: Sievers P, Henneken SC, Blume C, Sill M, Schrimpf D, Stichel D, Okonechnikov K, Reuss DE, Benzel J, Maaß KK, Kool M, Sturm D, Zheng T, Ghasemi DR, Kohlhof-Meinecke P, Cruz-Martínez O, Suñol M, Lavarino C, Ruf V, Boldt HB, Pagès M, Pouget C, Schweizer L, Kranendonk MEG, Akhtar N, Bunkowski S, Stadelmann C, Schüller U, Mueller WC, Dohmen H, Acker T, Harter PN, Mawrin C, Beschorner R, Brandner S, Snuderl M, Abdullaev Z, Aldape K, Gilbert MR, Armstrong TS, Ellison DW, Capper D, Ichimura K, Reifenberger G, Grundy RG, Jabado N, Krskova L, Zapotocky M, Vicha A, Varlet P, Wesseling P, Rutkowski S, Korshunov A, Wick W, Pfister SM, Jones DTW, von Deimling A, Pajtler KW and Sahm F

Publicada: 1 nov 2021 Ahead of Print: 1 ago 2021
Resumen:
Ependymomas encompass a heterogeneous group of central nervous system (CNS) neoplasms that occur along the entire neuroaxis. In recent years, extensive (epi-)genomic profiling efforts have identified several molecular groups of ependymoma that are characterized by distinct molecular alterations and/or patterns. Based on unsupervised visualization of a large cohort of genome-wide DNA methylation data, we identified a highly distinct group of pediatric-type tumors (n = 40) forming a cluster separate from all established CNS tumor types, of which a high proportion were histopathologically diagnosed as ependymoma. RNA sequencing revealed recurrent fusions involving the pleomorphic adenoma gene-like 1 (PLAGL1) gene in 19 of 20 of the samples analyzed, with the most common fusion being EWSR1:PLAGL1 (n = 13). Five tumors showed a PLAGL1:FOXO1 fusion and one a PLAGL1:EP300 fusion. High transcript levels of PLAGL1 were noted in these tumors, with concurrent overexpression of the imprinted genes H19 and IGF2, which are regulated by PLAGL1. Histopathological review of cases with sufficient material (n = 16) demonstrated a broad morphological spectrum of tumors with predominant ependymoma-like features. Immunohistochemically, tumors were GFAP positive and OLIG2- and SOX10 negative. In 3/16 of the cases, a dot-like positivity for EMA was detected. All tumors in our series were located in the supratentorial compartment. Median age of the patients at the time of diagnosis was 6.2 years. Median progression-free survival was 35 months (for 11 patients with data available). In summary, our findings suggest the existence of a novel group of supratentorial neuroepithelial tumors that are characterized by recurrent PLAGL1 fusions and enriched for pediatric patients.

Filiaciones:
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

Henneken SC:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany

Blume C:
 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

 Bioinformatics and Omics Data Analytics, German Cancer Research Center (DKFZ), Heidelberg, Germany

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

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

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

Okonechnikov K:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany

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

Benzel J:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany

Maaß KK:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany

 Department of Pediatric Oncology, Hematology, Immunology and Pulmonology, University Hospital Heidelberg, Heidelberg, Germany

Kool 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

 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

Sturm D:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Department of Pediatric Oncology, Hematology, Immunology and Pulmonology, University Hospital Heidelberg, Heidelberg, Germany

 Pediatric Glioma Research Group, German Cancer Research Center (DKFZ), Heidelberg, Germany

Zheng T:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany

 Faculty of Biosciences, Heidelberg University, 69117, Heidelberg, Germany

Ghasemi DR:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany

Kohlhof-Meinecke P:
 Department of Pathology, Klinikum Stuttgart, Stuttgart, Germany

Cruz-Martínez O:
 Department of Pediatric Oncology, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona, Spain

Suñol M:
 Department of Pathology, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona, Spain

Lavarino C:
 Laboratory of Molecular Oncology, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona, Spain

Ruf V:
 Institute of Neuropathology, Ludwig-Maximilian University, Munich, Germany

Boldt HB:
 Department of Pathology, Odense University Hospital, Odense, Denmark

 Department of Clinical Research, University of Southern Denmark, Odense, Denmark

Pagès M:
 Department of Neuropathology, GHU Paris Psychiatry and Neurosciences, Sainte-Anne Hospital, Paris, France

 Laboratory of Translational Research in Pediatric Oncology, SIREDO, INSERM U830, Institut Curie, Paris Sciences Lettres University, Paris, France

Pouget C:
 Department of Pathology, CHRU, Nancy, France

Schweizer L:
 Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Neuropathology, Berlin, Germany

 German Cancer Consortium (DKTK), partner site Berlin, German Cancer Research Center (DKFZ), Heidelberg, Germany

Kranendonk MEG:
 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

 Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands

Akhtar N:
 Manchester Royal Infirmary, Manchester University NHS Foundation Trust, Manchester, UK

 Shaukat Khanum Memorial Cancer Hospital and Research Centre, Lahore, Pakistan

Bunkowski S:
 Institute for Neuropathology, University Medical Centre Göttingen, Göttingen, Germany

Stadelmann C:
 Institute for Neuropathology, University Medical Centre Göttingen, Göttingen, Germany

Schüller U:
 Institute of Neuropathology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

 Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

 Research Institute Children's Cancer Center Hamburg, Hamburg, Germany

Mueller WC:
 Paul-Flechsig Institute of Neuropathology, University Hospital and Faculty of Medicine, Leipzig, Germany

Dohmen H:
 Institute of Neuropathology, University of Giessen, Giessen, Germany

Acker T:
 Institute of Neuropathology, University of Giessen, Giessen, Germany

Harter PN:
 Frankfurt Cancer Institute (FCI), University Hospital, Goethe University Frankfurt am Main, Frankfurt am Main, Germany

 Institute of Neurology (Edinger-Institute), University Hospital, Goethe University Frankfurt am Main, Frankfurt am Main, Germany

 German Cancer Consortium (DKTK), Partner site Frankfurt/Mainz, Frankfurt am Main, Germany

 German Cancer Research Center (DKFZ), Heidelberg, Germany

Mawrin C:
 Department of Neuropathology, Otto-Von-Guericke University, Magdeburg, Germany

Beschorner R:
 Department of Neuropathology, University of Tübingen, Tübingen, Germany

Brandner S:
 Division of Neuropathology, National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Foundation Trust, Queen Square, London, UK

 Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, Queen Square, London, UK

Snuderl M:
 Department of Pathology, NYU Langone Medical Center, New York, NY, USA

Abdullaev Z:
 Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA

Aldape K:
 Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA

Gilbert MR:
 Neuro-Oncology Branch, National Cancer Institute, Bethesda, MD, USA

Armstrong TS:
 Neuro-Oncology Branch, National Cancer Institute, Bethesda, MD, USA

Ellison DW:
 Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN, USA

Capper D:
 Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Neuropathology, Berlin, Germany

 German Cancer Consortium (DKTK), partner site Berlin, German Cancer Research Center (DKFZ), Heidelberg, Germany

Ichimura K:
 Division of Brain Tumor Translational Research, National Cancer Center Research Institute, Chuo-ku, Tokyo, Japan

Reifenberger G:
 Institute of Neuropathology, Heinrich Heine University, Düsseldorf, Germany

 German Cancer Consortium (DKTK), Partner Site Essen/Düsseldorf, Essen/Düsseldorf, Germany

Grundy RG:
 Children's Brain Tumour Research Centre, University of Nottingham, Nottingham, UK

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

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

Zapotocky M:
 Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic

 Department of Pediatric Haematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic

Vicha A:
 Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic

 Department of Pediatric Haematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic

Varlet P:
 Department of Neuropathology, GHU Paris Psychiatry and Neurosciences, Sainte-Anne Hospital, Paris, France

Wesseling P:
 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

 Department of Pathology, Amsterdam University Medical Centers, Location VUmc and Brain Tumor Center Amsterdam, Amsterdam, The Netherlands

Rutkowski S:
 Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

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

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

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

 Department of Pediatric Oncology, Hematology, Immunology and Pulmonology, University Hospital Heidelberg, Heidelberg, Germany

Jones DTW:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany

 Pediatric Glioma Research Group, German Cancer Research Center (DKFZ), Heidelberg, Germany

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

Pajtler KW:
 Hopp Children's Cancer Center Heidelberg (KiTZ), Heidelberg, Germany.

 Division of Pediatric Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

 Department of Pediatric Oncology, Hematology, Immunology and Pulmonology, University Hospital Heidelberg, Heidelberg, Germany.

Sahm F:
 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.
ISSN: 00016322





ACTA NEUROPATHOLOGICA
Editorial
SPRINGER, ONE NEW YORK PLAZA, SUITE 4600 , NEW YORK, NY 10004, UNITED STATES, Alemania
Tipo de documento: Article
Volumen: 142 Número: 5
Páginas: 827-839
WOS Id: 000681517000001
ID de PubMed: 34355256
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