Heterogeneous clinical and functional features of GRIN2D-related developmental and epileptic encephalopathy.


Journal

Brain : a journal of neurology
ISSN: 1460-2156
Titre abrégé: Brain
Pays: England
ID NLM: 0372537

Informations de publication

Date de publication:
01 10 2019
Historique:
received: 14 01 2019
revised: 30 04 2019
accepted: 31 05 2019
pubmed: 11 9 2019
medline: 17 6 2020
entrez: 11 9 2019
Statut: ppublish

Résumé

N-methyl d-aspartate receptors are ligand-gated ionotropic receptors mediating a slow, calcium-permeable component of excitatory synaptic transmission in the CNS. Variants in genes encoding NMDAR subunits have been associated with a spectrum of neurodevelopmental disorders. Here we report six novel GRIN2D variants and one previously-described disease-associated GRIN2D variant in two patients with developmental and epileptic encephalopathy. GRIN2D encodes for the GluN2D subunit protein; the GluN2D amino acids affected by the variants in this report are located in the pre-M1 helix, transmembrane domain M3, and the intracellular carboxyl terminal domain. Functional analysis in vitro reveals that all six variants decreased receptor surface expression, which may underline some shared clinical symptoms. In addition the GluN2D(Leu670Phe), (Ala675Thr) and (Ala678Asp) substitutions confer significantly enhanced agonist potency, and/or increased channel open probability, while the GluN2D(Ser573Phe), (Ser1271Phe) and (Arg1313Trp) substitutions result in a mild increase of agonist potency, reduced sensitivity to endogenous protons, and decreased channel open probability. The GluN2D(Ser573Phe), (Ala675Thr), and (Ala678Asp) substitutions significantly decrease current amplitude, consistent with reduced surface expression. The GluN2D(Leu670Phe) variant slows current response deactivation time course and increased charge transfer. GluN2D(Ala678Asp) transfection significantly decreased cell viability of rat cultured cortical neurons. In addition, we evaluated a set of FDA-approved NMDAR channel blockers to rescue functional changes of mutant receptors. This work suggests the complexity of the pathological mechanisms of GRIN2D-mediated developmental and epileptic encephalopathy, as well as the potential benefit of precision medicine.

Identifiants

pubmed: 31504254
pii: 5557839
doi: 10.1093/brain/awz232
pmc: PMC6763743
doi:

Substances chimiques

GRIN2D protein, human 0
NR2D NMDA receptor 0
Receptors, N-Methyl-D-Aspartate 0
Glutamic Acid 3KX376GY7L

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3009-3027

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS065371
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS043277
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS036654
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD082373
Pays : United States
Organisme : NINDS NIH HHS
ID : R24 NS092989
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS111619
Pays : United States

Informations de copyright

© The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oup.com.

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Auteurs

Wenshu XiangWei (W)

Department of Pediatrics and Pediatric Epilepsy Center, Peking University First Hospital, Beijing, China.
Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.

Varun Kannan (V)

Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.

Yuchen Xu (Y)

Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.
Department of Neurology, Xiangya Hospital, Central South University, Changsha, Hunan, China.

Gabrielle J Kosobucki (GJ)

Department of Neurobiology, University of Pittsburgh School of Medicine and Pittsburgh Institute for Neurodegenerative Diseases, Pittsburgh PA, USA.

Anthony J Schulien (AJ)

Department of Neurobiology, University of Pittsburgh School of Medicine and Pittsburgh Institute for Neurodegenerative Diseases, Pittsburgh PA, USA.

Hirofumi Kusumoto (H)

Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.

Christelle Moufawad El Achkar (C)

Division of Epilepsy, Department of Neurology, Boston Children's Hospital, Boston, MA, USA.
Department of Neurology, Harvard Medical School, Boston, MA, USA.

Subhrajit Bhattacharya (S)

Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.

Gaetan Lesca (G)

Service de Genetique, Centre de Reference Anomalies du Developpement, Hospices Civils de Lyon, Bron, France; INSERM U1028, CNRS UMR5292, Paris, France.
Centre de Recherche en Neurosciences de Lyon, GENDEV Team, Universite Claude Bernard Lyon 1, Bron, France; Claude Bernard Lyon I University, Lyon, France.

Sylvie Nguyen (S)

Department of Pediatric Neurology, University Hospital of Lille, and Lille Reference Centre for Rare Epileptic Disorders, Lille, France.

Katherine L Helbig (KL)

Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA, USA.

Jean-Marie Cuisset (JM)

Department of Pediatric Neurology, University Hospital of Lille, and Lille Reference Centre for Rare Epileptic Disorders, Lille, France.

Christina Dühring Fenger (CD)

Danish Epilepsy Centre Filadelfia, Dianalund, Denmark.

Dragan Marjanovic (D)

Danish Epilepsy Centre Filadelfia, Dianalund, Denmark.

Elisabeth Schuler (E)

Division of Child Neurology and Inherited Metabolic Diseases, Centre for Paediatrics and Adolescent Medicine, University Hospital Heidelberg, Heidelberg, Germany.

Ye Wu (Y)

Department of Pediatrics and Pediatric Epilepsy Center, Peking University First Hospital, Beijing, China.

Xinhua Bao (X)

Department of Pediatrics and Pediatric Epilepsy Center, Peking University First Hospital, Beijing, China.

Yuehua Zhang (Y)

Department of Pediatrics and Pediatric Epilepsy Center, Peking University First Hospital, Beijing, China.

Nina Dirkx (N)

Neurogenetics Group, University of Antwerp, Belgium.
Laboratory of Neurogenetics, Institute Born-Bunge, University of Antwerp, Antwerp, Belgium.

An-Sofie Schoonjans (AS)

Department of Child Neurology, Antwerp University Hospital, Antwerp, Belgium.

Steffen Syrbe (S)

Division of Child Neurology and Inherited Metabolic Diseases, Centre for Paediatrics and Adolescent Medicine, University Hospital Heidelberg, Heidelberg, Germany.

Scott J Myers (SJ)

Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.
Center for Functional Evaluation of Rare Variants (CFERV), Emory University School of Medicine, Atlanta, GA, USA.

Annapurna Poduri (A)

Division of Epilepsy, Department of Neurology, Boston Children's Hospital, Boston, MA, USA.
Department of Neurology, Harvard Medical School, Boston, MA, USA.

Elias Aizenman (E)

Department of Neurobiology, University of Pittsburgh School of Medicine and Pittsburgh Institute for Neurodegenerative Diseases, Pittsburgh PA, USA.

Stephen F Traynelis (SF)

Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.
Center for Functional Evaluation of Rare Variants (CFERV), Emory University School of Medicine, Atlanta, GA, USA.

Johannes R Lemke (JR)

Institute of Human Genetics, University of Leipzig Hospitals and Clinics, Leipzig, Germany.

Hongjie Yuan (H)

Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA, USA.
Center for Functional Evaluation of Rare Variants (CFERV), Emory University School of Medicine, Atlanta, GA, USA.

Yuwu Jiang (Y)

Department of Pediatrics and Pediatric Epilepsy Center, Peking University First Hospital, Beijing, China.

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