The GRIA3 c.2477G > A Variant Causes an Exaggerated Startle Reflex, Chorea, and Multifocal Myoclonus.


Journal

Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688

Informations de publication

Date de publication:
07 2020
Historique:
received: 27 09 2019
revised: 24 02 2020
accepted: 03 03 2020
pubmed: 6 5 2020
medline: 28 4 2021
entrez: 6 5 2020
Statut: ppublish

Résumé

Hemizygous mutations in GRIA3 encoding the GluA3 subunit of the amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor are known to be associated with neurodevelopmental disorders, including intellectual disability, hypotonia, an autism spectrum disorder, sleep disturbances, and epilepsy in males. To describe a new and consistent phenotype in 4 affected male patients associated with an undescribed deleterious variant in GRIA3. We evaluated a large French family in which segregate a singular phenotype according to an apparent X-linked mode of inheritance. Molecular analyses using next generation sequencing and in vitro functional studies using 2-electrode voltage clamp recordings on Xenopus laevis oocytes and a β-lactamase reporter assay in transfected human embryonic kidney (HEK293) cells were performed. In addition to mild intellectual disability and dysarthria, affected patients presented a tightly consistent early-onset movement disorder combining an exaggerated startle reflex with generalized chorea and multifocal myoclonus. The unreported GRIA3 missense variant c.2477G > A; p.(Gly826Asp) affecting the fourth transmembrane domain of the protein was identified in index patients and their unaffected mothers. Functional studies revealed that variant receptors show decreased current response evoked by agonist (ie, kainic acid and glutamate) and reduced expression on the cell surface in favor of pathogenicity by a loss-of-function mechanism. Taken together, our results suggest that apart from known GRIA3-related disorders, an undescribed mutation-specific singular movement disorder does exist. We thus advocate considering GRIA3 mutations in the differential diagnosis of hyperekplexia and generalized chorea with myoclonus. © 2020 International Parkinson and Movement Disorder Society.

Sections du résumé

BACKGROUND
Hemizygous mutations in GRIA3 encoding the GluA3 subunit of the amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor are known to be associated with neurodevelopmental disorders, including intellectual disability, hypotonia, an autism spectrum disorder, sleep disturbances, and epilepsy in males.
OBJECTIVE
To describe a new and consistent phenotype in 4 affected male patients associated with an undescribed deleterious variant in GRIA3.
METHODS
We evaluated a large French family in which segregate a singular phenotype according to an apparent X-linked mode of inheritance. Molecular analyses using next generation sequencing and in vitro functional studies using 2-electrode voltage clamp recordings on Xenopus laevis oocytes and a β-lactamase reporter assay in transfected human embryonic kidney (HEK293) cells were performed.
RESULTS
In addition to mild intellectual disability and dysarthria, affected patients presented a tightly consistent early-onset movement disorder combining an exaggerated startle reflex with generalized chorea and multifocal myoclonus. The unreported GRIA3 missense variant c.2477G > A; p.(Gly826Asp) affecting the fourth transmembrane domain of the protein was identified in index patients and their unaffected mothers. Functional studies revealed that variant receptors show decreased current response evoked by agonist (ie, kainic acid and glutamate) and reduced expression on the cell surface in favor of pathogenicity by a loss-of-function mechanism.
CONCLUSIONS
Taken together, our results suggest that apart from known GRIA3-related disorders, an undescribed mutation-specific singular movement disorder does exist. We thus advocate considering GRIA3 mutations in the differential diagnosis of hyperekplexia and generalized chorea with myoclonus. © 2020 International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 32369665
doi: 10.1002/mds.28058
pmc: PMC9190290
mid: NIHMS1811513
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1224-1232

Subventions

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 : R01 NS065371
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

© 2020 International Parkinson and Movement Disorder Society.

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Auteurs

Juliette Piard (J)

Centre de Génétique Humaine, Université de Franche-Comté, CHU, Besançon, France.
Unité de recherche en neurosciences intégratives et cognitives EA481, Université de Franche-Comté, Besançon, France.

Matthieu Béreau (M)

Unité de recherche en neurosciences intégratives et cognitives EA481, Université de Franche-Comté, Besançon, France.
Service de Neurologie, CHU, Besançon, France.

Wenshu XiangWei (W)

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

Thomas Wirth (T)

Département de Neurologie, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

Daniel Amsallem (D)

Service de Neuropédiatrie, CHU, Besançon, France.

Lauren Buisson (L)

Service de Neuropédiatrie, CHU, Besançon, France.

Philippe Richard (P)

Service de Neurologie, CHU, Besançon, France.

Nana Liu (N)

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

Yuchen Xu (Y)

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

Scott J Myers (SJ)

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

Stephen F Traynelis (SF)

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

Jameleddine Chelly (J)

Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France.

Mathieu Anheim (M)

Département de Neurologie, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.
Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France.
Fédération de Médecine Translationnelle de Strasbourg, Université de Strasbourg, Strasbourg, France.

Martine Raynaud (M)

CHRU de Tours, Service de Génétique, Tours, France.
UMR1253, iBrain, Université de Tours, Inserm, Tours, France.

Lionel Van Maldergem (LV)

Centre de Génétique Humaine, Université de Franche-Comté, CHU, Besançon, France.
Unité de recherche en neurosciences intégratives et cognitives EA481, Université de Franche-Comté, Besançon, France.
Clinical Investigation Center 1431, National Institute of Health and Medical Research, Besançon, France.

Hongjie Yuan (H)

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

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