The genetic landscape of choroid plexus tumors in children and adults.


Journal

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

Informations de publication

Date de publication:
12 04 2021
Historique:
pubmed: 30 11 2020
medline: 21 5 2021
entrez: 29 11 2020
Statut: ppublish

Résumé

Choroid plexus tumors (CPTs) are intraventricular brain tumors predominantly arising in children but also affecting adults. In most cases, driver mutations have not been identified, although there are reports of frequent chromosome-wide copy-number alterations and TP53 mutations, especially in choroid plexus carcinomas (CPCs). DNA methylation profiling and RNA-sequencing was performed in a series of 47 CPTs. Samples comprised 35 choroid plexus papillomas (CPPs), 6 atypical choroid plexus papillomas (aCPPs) and 6 CPCs plus three recurrences thereof. Targeted TP53 and TERT promotor sequencing was performed in all samples. Whole exome sequencing (WES) and linked-read whole genome sequencing (WGS) was performed in 25 and 4 samples, respectively. Tumors comprised the molecular subgroups "pediatric A" (N=11), "pediatric B" (N=12) and "adult" (N=27). Copy-number alterations mainly represented whole-chromosomal alterations with subgroup-specific enrichments (gains of Chr1, 2 and 21q in "pediatric B" and gains of Chr5 and 9 and loss of Chr21q in "adult"). RNA sequencing yielded a novel CCDC47-PRKCA fusion transcript in one adult choroid plexus papilloma patient with aggressive clinical course; an underlying Chr17 inversion was demonstrated by linked-read WGS. WES and targeted sequencing showed TP53 mutations in 7/47 CPTs (15%), five of which were children. On the contrary, TERT promoter mutations were encountered in 7/28 adult patients (25%) and associated with shorter progression-free survival (log-rank test, p=0.015). Pediatric CPTs lack recurrent driver alterations except for TP53, whereas CPTs in adults show TERT promoter mutations or a novel CCDC47-PRKCA gene fusion, being associated with a more unfavorable clinical course.

Sections du résumé

BACKGROUND
Choroid plexus tumors (CPTs) are intraventricular brain tumors predominantly arising in children but also affecting adults. In most cases, driver mutations have not been identified, although there are reports of frequent chromosome-wide copy-number alterations and TP53 mutations, especially in choroid plexus carcinomas (CPCs).
METHODS
DNA methylation profiling and RNA-sequencing was performed in a series of 47 CPTs. Samples comprised 35 choroid plexus papillomas (CPPs), 6 atypical choroid plexus papillomas (aCPPs) and 6 CPCs plus three recurrences thereof. Targeted TP53 and TERT promotor sequencing was performed in all samples. Whole exome sequencing (WES) and linked-read whole genome sequencing (WGS) was performed in 25 and 4 samples, respectively.
RESULTS
Tumors comprised the molecular subgroups "pediatric A" (N=11), "pediatric B" (N=12) and "adult" (N=27). Copy-number alterations mainly represented whole-chromosomal alterations with subgroup-specific enrichments (gains of Chr1, 2 and 21q in "pediatric B" and gains of Chr5 and 9 and loss of Chr21q in "adult"). RNA sequencing yielded a novel CCDC47-PRKCA fusion transcript in one adult choroid plexus papilloma patient with aggressive clinical course; an underlying Chr17 inversion was demonstrated by linked-read WGS. WES and targeted sequencing showed TP53 mutations in 7/47 CPTs (15%), five of which were children. On the contrary, TERT promoter mutations were encountered in 7/28 adult patients (25%) and associated with shorter progression-free survival (log-rank test, p=0.015).
CONCLUSION
Pediatric CPTs lack recurrent driver alterations except for TP53, whereas CPTs in adults show TERT promoter mutations or a novel CCDC47-PRKCA gene fusion, being associated with a more unfavorable clinical course.

Identifiants

pubmed: 33249490
pii: 6010433
doi: 10.1093/neuonc/noaa267
pmc: PMC8041331
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

650-660

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.

Références

Int J Cancer. 2014 Jun 15;134(12):2993-4
pubmed: 24285288
Acta Neuropathol. 2013 Dec;126(6):907-15
pubmed: 24154961
J Neuropathol Exp Neurol. 2006 Nov;65(11):1069-73
pubmed: 17086103
Bioinformatics. 2018 Jan 15;34(2):353-360
pubmed: 29112732
Nature. 2020 Feb;578(7793):82-93
pubmed: 32025007
J Clin Oncol. 2010 Apr 20;28(12):1995-2001
pubmed: 20308654
Bioinformatics. 2018 Dec 15;34(24):4205-4212
pubmed: 29945233
Cancer Genet Cytogenet. 1996 Sep;90(2):130-1
pubmed: 8830721
Science. 2013 Feb 22;339(6122):957-9
pubmed: 23348506
Neuro Oncol. 2014 Oct;16 Suppl 4:iv1-63
pubmed: 25304271
Neuro Oncol. 2016 Jun;18(6):790-6
pubmed: 26826203
J Neuropathol Exp Neurol. 2015 Feb;74(2):110-20
pubmed: 25575132
Nature. 2014 Feb 27;506(7489):445-50
pubmed: 24553142
J Neurooncol. 2009 Dec;95(3):383-392
pubmed: 19543851
Acta Neuropathol. 2002 Jan;103(1):1-10
pubmed: 11837741
Nature. 2017 Jul 19;547(7663):311-317
pubmed: 28726821
Clin Cancer Res. 2015 Jan 1;21(1):184-92
pubmed: 25336695
J Clin Neurosci. 2013 Jun;20(6):808-12
pubmed: 23623658
Cancer Cell. 2015 May 11;27(5):728-43
pubmed: 25965575
Brain Pathol. 2013 Mar;23(2):121-8
pubmed: 22725730
Nature. 2018 Mar 22;555(7697):469-474
pubmed: 29539639
JAMA Dermatol. 2016 Mar;152(3):318-22
pubmed: 26676968
Nat Commun. 2018 Jun 18;9(1):2371
pubmed: 29915258
Cancer Cell. 2015 May 11;27(5):712-27
pubmed: 25965574
Nature. 2014 Feb 27;506(7489):451-5
pubmed: 24553141
J Mol Diagn. 2017 Jan;19(1):4-23
pubmed: 27993330
Bioinformatics. 2013 Oct 15;29(20):2539-46
pubmed: 23956304
Cancer Genet Cytogenet. 1993 Nov;71(1):40-9
pubmed: 8275451
Epigenetics. 2014 Oct;9(10):1431-8
pubmed: 25437057
Nature. 2018 Jul;559(7714):E10
pubmed: 29875405
Microsc Res Tech. 2001 Jan 1;52(1):104-11
pubmed: 11135453
Nat Commun. 2013;4:2185
pubmed: 23887589
Nature. 2020 Feb;578(7793):102-111
pubmed: 32025015
Pharmacol Res. 2007 Jun;55(6):477-86
pubmed: 17548205
Acta Neuropathol. 2015 Jun;129(6):925-7
pubmed: 25935663
Nat Genet. 1994 Jul;7(3):433-9
pubmed: 7920665
J Neurooncol. 2017 Oct;135(1):151-160
pubmed: 28677107
Nucleic Acids Res. 2016 Mar 18;44(5):e47
pubmed: 26582927
Oncol Lett. 2019 Nov;18(5):5063-5076
pubmed: 31612017
Genes Chromosomes Cancer. 1994 Dec;11(4):267-70
pubmed: 7533531
Bioinformatics. 2012 Dec 15;28(24):3232-9
pubmed: 23093608
Cancer Genet Cytogenet. 1996 Mar;87(1):7-10
pubmed: 8646745

Auteurs

Christian Thomas (C)

Institute of Neuropathology, University Hospital Münster, Münster, Germany.

Patrick Soschinski (P)

Institute of Neuropathology, University Hospital Münster, Münster, Germany.

Melissa Zwaig (M)

McGill University Genome Centre, Department of Human Genetics, McGill University, Montreal, Canada.

Spyridon Oikonomopoulos (S)

McGill University Genome Centre, Department of Human Genetics, McGill University, Montreal, Canada.

Konstantin Okonechnikov (K)

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

Kristian W Pajtler (KW)

Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany.
Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ), and German Cancer Consortium (DKTK), Heidelberg, Germany.
Department of Pediatric Oncology, Hematology and Immunology, University Hospital, Heidelberg, Germany.

Martin Sill (M)

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

Leonille Schweizer (L)

Department of Neuropathology, Charité - Universitätsmedizin Berlin, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany, Partner Site Charité Berlin, Berlin, Germany.
Berlin Institute of Health (BIH), Berlin, Germany.

Arend Koch (A)

Department of Neuropathology, Charité - Universitätsmedizin Berlin, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany, Partner Site Charité Berlin, Berlin, Germany.
Berlin Institute of Health (BIH), Berlin, Germany.

Julia Neumann (J)

Department of Neuropathology, University Hospital Hamburg-Eppendorf, Hamburg, Germany.

Ulrich Schüller (U)

Department of Neuropathology, University Hospital 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.

Felix 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.

Laurèl Rauschenbach (L)

Department of Neurosurgery and Spine Surgery, University Hospital Essen, University Duisburg-Essen, Essen, Germany.
DKFZ Division Translational Neurooncology, DKTK partner site, University Hospital Essen, University Duisburg-Essen, Essen, Germany.

Kathy Keyvani (K)

Institute of Neuropathology, University of Duisburg-Essen, Essen, Germany.

Martin Proescholdt (M)

Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ), and German Cancer Consortium (DKTK), Heidelberg, Germany.
Department of Neurosurgery, Regensburg University Hospital, Regensburg, Germany.

Markus J Riemenschneider (MJ)

Department of Neuropathology, Regensburg University Hospital, Regensburg, Germany.

Jochen Segewiß (J)

Institute of Human Genetics, University Hospital Münster, Münster, Germany.

Christian Ruckert (C)

Institute of Human Genetics, University Hospital Münster, Münster, Germany.

Oliver Grauer (O)

Department of Neurology with Institute of Translational Neurology, University Hospital Münster, Münster, Germany.

Camelia-Maria Monoranu (CM)

Department of Neuropathology, Institute of Pathology, University of Würzburg, Germany.

Katrin Lamszus (K)

Department of Neurosurgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Annarita Patrizi (A)

Schaller Research Group Leader at the German Cancer Research Center (DKFZ), Heidelberg, Germany.

Uwe Kordes (U)

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

Reiner Siebert (R)

Institute of Human Genetics, Ulm University and Ulm University Medical Center, Ulm, Germany.

Marcel Kool (M)

Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany.
Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ), and German Cancer Consortium (DKTK), Heidelberg, Germany.
Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Jiannis Ragoussis (J)

McGill University Genome Centre, Department of Human Genetics, McGill University, Montreal, Canada.

William D Foulkes (WD)

Department of Human Genetics, McGill University, Montreal, QC, Canada.

Werner Paulus (W)

Institute of Neuropathology, University Hospital Münster, Münster, Germany.

Barbara Rivera (B)

Program in Molecular Mechanisms and Experimental Therapy in Oncology (Oncobell), IDIBELL, Hospitalet de Llobregat, Barcelona, Spain.
Gerald Bronfman Department of Oncology, McGill University, Montreal, QC, Canada.

Martin Hasselblatt (M)

Institute of Neuropathology, University Hospital Münster, Münster, Germany.

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