Rare germline variants in the E-cadherin gene CDH1 are associated with the risk of brain tumors of neuroepithelial and epithelial origin.

Adenoma / genetics Aniline Compounds / therapeutic use Animals Antibody Diversity Antigens, CD / genetics Brain Neoplasms / drug therapy Cadherins / genetics Carcinoma / drug therapy DNA, Neoplasm / genetics Gene Knock-In Techniques Genetic Variation HEK293 Cells Humans Neoplasms, Neuroepithelial / drug therapy Oligodendroglioma / genetics Protein Kinase Inhibitors / therapeutic use Purines / therapeutic use Rats Rats, Sprague-Dawley Whole Genome Sequencing
CDH1 E-cadherin Familial glioma Oligodendroglioma Whole-genome sequencing β-catenin

Journal

Acta neuropathologica
ISSN: 1432-0533
Titre abrégé: Acta Neuropathol
Pays: Germany
ID NLM: 0412041

Informations de publication

Date de publication:
07 2021
Historique:
received: 26 01 2021
accepted: 04 04 2021
revised: 25 03 2021
pubmed: 1 5 2021
medline: 11 1 2022
entrez: 30 4 2021
Statut: ppublish

Résumé

The genetic basis of brain tumor development is poorly understood. Here, leukocyte DNA of 21 patients from 15 families with ≥ 2 glioma cases each was analyzed by whole-genome or targeted sequencing. As a result, we identified two families with rare germline variants, p.(A592T) or p.(A817V), in the E-cadherin gene CDH1 that co-segregate with the tumor phenotype, consisting primarily of oligodendrogliomas, WHO grade II/III, IDH-mutant, 1p/19q-codeleted (ODs). Rare CDH1 variants, previously shown to predispose to gastric and breast cancer, were significantly overrepresented in these glioma families (13.3%) versus controls (1.7%). In 68 individuals from 28 gastric cancer families with pathogenic CDH1 germline variants, brain tumors, including a pituitary adenoma, were observed in three cases (4.4%), a significantly higher prevalence than in the general population (0.2%). Furthermore, rare CDH1 variants were identified in tumor DNA of 6/99 (6%) ODs. CDH1 expression was detected in undifferentiated and differentiating oligodendroglial cells isolated from rat brain. Functional studies using CRISPR/Cas9-mediated knock-in or stably transfected cell models demonstrated that the identified CDH1 germline variants affect cell membrane expression, cell migration and aggregation. E-cadherin ectodomain containing variant p.(A592T) had an increased intramolecular flexibility in a molecular dynamics simulation model. E-cadherin harboring intracellular variant p.(A817V) showed reduced β-catenin binding resulting in increased cytosolic and nuclear β-catenin levels reverted by treatment with the MAPK interacting serine/threonine kinase 1 inhibitor CGP 57380. Our data provide evidence for a role of deactivating CDH1 variants in the risk and tumorigenesis of neuroepithelial and epithelial brain tumors, particularly ODs, possibly via WNT/β-catenin signaling.

Identifiants

DOI: 10.1007/s00401-021-02307-1 PMID: 33929593 PMC: PMC8217027
pubmed: 33929593
doi: 10.1007/s00401-021-02307-1
pii: 10.1007/s00401-021-02307-1
pmc: PMC8217027
doi:

Substances chimiques

Aniline Compounds 0
Antigens, CD 0
CDH1 protein, human 0
CGP 57380 0
Cadherins 0
DNA, Neoplasm 0
Protein Kinase Inhibitors 0
Purines 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

191-210

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Auteurs

Alisa Förster (A)

Department of Human Genetics OE 6300, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany.
ORCID: 0000-0002-7842-8483

Frank Brand (F)

Department of Human Genetics OE 6300, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany.

Rouzbeh Banan (R)

Department of Neuropathology, Institute of Pathology, Hannover Medical School, Hannover, Germany.
Department of Neuropathology, Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany.

Robert Hüneburg (R)

National Center for Hereditary Tumor Syndromes, University Hospital Bonn, Bonn, Germany.
Department of Internal Medicine I, University Hospital Bonn, Bonn, Germany.

Christine A M Weber (CAM)

Department of Human Genetics OE 6300, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany.

Wiebke Ewert (W)

Institute for Biophysical Chemistry, Hannover Medical School, Hannover, Germany.

Jessica Kronenberg (J)

Clinical Neuroimmunology and Neurochemistry, Department of Neurology, Hannover Medical School, Hannover, Germany.
Center for Systems Neuroscience, University of Veterinary Medicine Hannover, Hannover, Germany.
Radiation Biology Department, Institute of Aerospace Medicine, German Aerospace Centre (DLR), Köln, Germany.

Christopher Previti (C)

Genomics and Proteomics Core Facility, High Throughput Sequencing Unit W190, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Omics IT and Data Management Core Facility W610, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Natalie Elyan (N)

Department of Human Genetics OE 6300, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany.

Ulrike Beyer (U)

Department of Human Genetics OE 6300, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany.

Helge Martens (H)

Department of Human Genetics OE 6300, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany.

Bujung Hong (B)

Department of Neurosurgery, Hannover Medical School, Hannover, Germany.

Jan H Bräsen (JH)

Nephropathology, Institute of Pathology, Hannover Medical School, Hannover, Germany.

Andreas Erbersdobler (A)

Institute of Pathology, University of Rostock, Rostock, Germany.

Joachim K Krauss (JK)

Department of Neurosurgery, Hannover Medical School, Hannover, Germany.

Martin Stangel (M)

Clinical Neuroimmunology and Neurochemistry, Department of Neurology, Hannover Medical School, Hannover, Germany.
Center for Systems Neuroscience, University of Veterinary Medicine Hannover, Hannover, Germany.

Amir Samii (A)

Department of Neurosurgery, International Neuroscience Institute, Hannover, Germany.

Stephan Wolf (S)

Genomics and Proteomics Core Facility, High Throughput Sequencing Unit W190, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Matthias Preller (M)

Institute for Biophysical Chemistry, Hannover Medical School, Hannover, Germany.
Department of Natural Sciences, University of Applied Sciences Bonn-Rhein-Sieg, Rheinbach, Germany.

Stefan Aretz (S)

National Center for Hereditary Tumor Syndromes, University Hospital Bonn, Bonn, Germany.
Institute of Human Genetics, Medical Faculty, University of Bonn, Bonn, Germany.

Bettina Wiese (B)

Department of Neurosurgery, Hannover Medical School, Hannover, Germany.
Department of Neurology, Henriettenstift, Diakovere Krankenhaus gGmbH, Hannover, Germany.

Christian Hartmann (C)

Department of Neuropathology, Institute of Pathology, Hannover Medical School, Hannover, Germany.

Ruthild G Weber (RG)

Department of Human Genetics OE 6300, Hannover Medical School, Carl-Neuberg-Str. 1, 30625, Hannover, Germany. Weber.Ruthild@mh-hannover.de.
ORCID: 0000-0001-6610-1080

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Classifications MeSH

Recherchemedicale.com › Tumeurs › Tumeurs par type histologique › Tumeurs épithéliales épidermoïdes et glandulaires › Adénomes › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Composés chimiques organiques › Amines › Dérivés de l'aniline › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Eucaryotes › Animaux › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Phénomènes du système immunitaire › Phénomènes immunogénétiques › Diversité des anticorps › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Facteurs biologiques › Marqueurs biologiques › Antigènes de différenciation › Antigènes CD › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Maladies du système nerveux › Tumeurs du système nerveux › Tumeurs du système nerveux central › Tumeurs du cerveau › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Facteurs biologiques › Antigènes › Antigènes de surface › Molécules d'adhérence cellulaire › Cadhérines › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Tumeurs › Tumeurs par type histologique › Tumeurs épithéliales épidermoïdes et glandulaires › Carcinomes › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ADN › ADN tumoral › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Techniques d'investigation › Techniques génétiques › Ciblage de gène › Techniques de knock-in de gènes › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Phénomènes génétiques › Variation génétique › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Cellules › Cellules épithéliales › Cellules HEK293 › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Tumeurs › Tumeurs par type histologique › Tumeurs du tissu nerveux › Tumeurs neuroectodermiques › Tumeurs neuroépitheliales › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Tumeurs › Tumeurs par type histologique › Tumeurs du tissu nerveux › Tumeurs neuroectodermiques › Tumeurs neuroépitheliales › Gliome › Oligodendrogliome › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Actions chimiques et utilisations › Actions pharmacologiques › Mécanismes moléculaires de l'action pharmacologique › Antienzymes › Inhibiteurs de protéines kinases › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Composés hétérocycliques › Composés hétérocycliques à cycles fusionnés › Composés hétérobicycliques › Purines › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Rats › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Rats › Rat Sprague-Dawley › Rare germline variants in the E-cadherin gene...
Recherchemedicale.com › Techniques d'investigation › Techniques génétiques › Analyse de séquence › Analyse de séquence d'ADN › Séquençage du génome entier › Rare germline variants in the E-cadherin gene...