The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in context

Summary: Background: Excitatory amino acid transporter 2 (EAAT2) is the predominant glutamate transporter and a key mediator of excitatory neurotransmission in the human brain. Here we present a cohort of 18 individuals harbouring 13 different SLC1A2 variants, who all present with neurodevelopmenta...

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Main Authors: Peter Kovermann, Allan Bayat, Christina D. Fenger, Lisette Leeuwen, Artem Borovikov, Artem Sharkov, Virginie Levrat, Gaetan Lesca, Laurence Perrin, Jonathan Levy, Christoph Fahlke, Rikke S. Møller, Anders A. Jensen
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Language:English
Published: Elsevier 2025-04-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352396425000921
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author Peter Kovermann
Allan Bayat
Christina D. Fenger
Lisette Leeuwen
Artem Borovikov
Artem Sharkov
Virginie Levrat
Gaetan Lesca
Laurence Perrin
Jonathan Levy
Christoph Fahlke
Rikke S. Møller
Anders A. Jensen
author_facet Peter Kovermann
Allan Bayat
Christina D. Fenger
Lisette Leeuwen
Artem Borovikov
Artem Sharkov
Virginie Levrat
Gaetan Lesca
Laurence Perrin
Jonathan Levy
Christoph Fahlke
Rikke S. Møller
Anders A. Jensen
author_sort Peter Kovermann
collection DOAJ
description Summary: Background: Excitatory amino acid transporter 2 (EAAT2) is the predominant glutamate transporter and a key mediator of excitatory neurotransmission in the human brain. Here we present a cohort of 18 individuals harbouring 13 different SLC1A2 variants, who all present with neurodevelopmental impairment with variable symptoms and disease severities, and we delineate the impact of these variants on EAAT2 function. Methods: The consequences of nine novel missense SLC1A2 variants for expression, transport and anion channel properties of EAAT2 expressed in mammalian cells were characterized by confocal microscopy, enzyme-linked immunosorbent and [3H]-D-aspartate uptake assays, and electrophysiological recordings. Findings: Ten of the 13 SLC1A2 variants mediated significant changes to EAAT2 expression and/or function. These molecular phenotypes were classified into three categories: overall loss-of-function (F249Sfs∗17, A432D, A439V, c.1421+1G>C), mild gain-of-anion-channel function (I276S, G360A), and mixed loss-of-transport/gain-of-anion-channel function (G82R, L85R, L85P, P289R). In contrast, L37P, H542R and I546T did not mediate significant changes to EAAT2 expression or function. Although specific clinical outcomes in individuals carrying variants within each category varied somewhat, the three categories overall translated into distinct clinical phenotypes in terms of phenotypic traits and severity. Interpretation: The observed associations between functional effects and clinical phenotypes produced by these variants offer valuable insights for future predictions of progression and severity of SLC1A2-associated neurodevelopmental disorders. Furthermore, these associations between variant-induced changes in EAAT2 function and phenotypic traits could assist in tailoring personalized treatments of these disorders. Funding: This work was funded by the German Ministry of Education and Research and by the Lundbeck Foundation.
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spelling doaj-art-4378dcfac2b74eb08a34110db88ea17a2025-08-20T01:55:11ZengElsevierEBioMedicine2352-39642025-04-0111410564810.1016/j.ebiom.2025.105648The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in contextPeter Kovermann0Allan Bayat1Christina D. Fenger2Lisette Leeuwen3Artem Borovikov4Artem Sharkov5Virginie Levrat6Gaetan Lesca7Laurence Perrin8Jonathan Levy9Christoph Fahlke10Rikke S. Møller11Anders A. Jensen12Forschungszentrum Jülich GmbH, Institute of Biological Information Processing 1 (IBI-1), Molekular- und Zellphysiologie, Jülich D-52428, GermanyDepartment of Regional Health Research, University of Southern Denmark, Odense M DK-5230, Denmark; Department of Pediatrics, Danish Epilepsy Centre Filadelfia (member of ERN EpiCARE), Dianalund DK-4293, Denmark; Department of Epilepsy Genetics and Personalized Medicine, Danish Epilepsy Centre Filadelfia (member of ERN EpiCARE), Dianalund DK-4293, DenmarkDepartment of Epilepsy Genetics and Personalized Medicine, Danish Epilepsy Centre Filadelfia (member of ERN EpiCARE), Dianalund DK-4293, Denmark; Amplexa Genetics, Odense C DK-5000, DenmarkDepartment of Genetics, University Medical Center Groningen, Groningen, the NetherlandsResearch Centre for Medical Genetics, Moscow, RussiaVeltischev Research and Clinical Institute for Pediatrics and Pediatric Surgery of the Pirogov Russian National Research Medical University, Moscow, Russia; Genomed Ltd., Moscow, RussiaService de Pédiatrie, Centre Hospitalier Annecy Genevois, Pringy, FranceDepartment of Medical Genetics, University Hospital of Lyon and Claude Bernard Lyon University, Lyon, France; Pathophysiology and Genetics of Neuron and Muscle (PNMG), UCBL, CNRS UMR5261 - INSERM U1315, Lyon, FranceDepartment of Genetics, APHP Nord, Robert Debré University Hospital, Paris 75019, FranceDepartment of Genetics, APHP Nord, Robert Debré University Hospital, Paris 75019, France; Multi-site Medical Biology Laboratory SeqOIA-FMG2025, Paris 75014, FranceForschungszentrum Jülich GmbH, Institute of Biological Information Processing 1 (IBI-1), Molekular- und Zellphysiologie, Jülich D-52428, GermanyDepartment of Regional Health Research, University of Southern Denmark, Odense M DK-5230, Denmark; Department of Epilepsy Genetics and Personalized Medicine, Danish Epilepsy Centre Filadelfia (member of ERN EpiCARE), Dianalund DK-4293, DenmarkDepartment of Drug Design and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen Ø DK-2100, Denmark; Corresponding author. Department of Drug Design and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Universitetsparken 2, Copenhagen Ø DK-2100, Denmark.Summary: Background: Excitatory amino acid transporter 2 (EAAT2) is the predominant glutamate transporter and a key mediator of excitatory neurotransmission in the human brain. Here we present a cohort of 18 individuals harbouring 13 different SLC1A2 variants, who all present with neurodevelopmental impairment with variable symptoms and disease severities, and we delineate the impact of these variants on EAAT2 function. Methods: The consequences of nine novel missense SLC1A2 variants for expression, transport and anion channel properties of EAAT2 expressed in mammalian cells were characterized by confocal microscopy, enzyme-linked immunosorbent and [3H]-D-aspartate uptake assays, and electrophysiological recordings. Findings: Ten of the 13 SLC1A2 variants mediated significant changes to EAAT2 expression and/or function. These molecular phenotypes were classified into three categories: overall loss-of-function (F249Sfs∗17, A432D, A439V, c.1421+1G>C), mild gain-of-anion-channel function (I276S, G360A), and mixed loss-of-transport/gain-of-anion-channel function (G82R, L85R, L85P, P289R). In contrast, L37P, H542R and I546T did not mediate significant changes to EAAT2 expression or function. Although specific clinical outcomes in individuals carrying variants within each category varied somewhat, the three categories overall translated into distinct clinical phenotypes in terms of phenotypic traits and severity. Interpretation: The observed associations between functional effects and clinical phenotypes produced by these variants offer valuable insights for future predictions of progression and severity of SLC1A2-associated neurodevelopmental disorders. Furthermore, these associations between variant-induced changes in EAAT2 function and phenotypic traits could assist in tailoring personalized treatments of these disorders. Funding: This work was funded by the German Ministry of Education and Research and by the Lundbeck Foundation.http://www.sciencedirect.com/science/article/pii/S2352396425000921EpilepsySLC1A2Excitatory amino acid transporter 2 (EAAT2)Genetic variantsTransporter uptakePatch clamp
spellingShingle Peter Kovermann
Allan Bayat
Christina D. Fenger
Lisette Leeuwen
Artem Borovikov
Artem Sharkov
Virginie Levrat
Gaetan Lesca
Laurence Perrin
Jonathan Levy
Christoph Fahlke
Rikke S. Møller
Anders A. Jensen
The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in context
EBioMedicine
Epilepsy
SLC1A2
Excitatory amino acid transporter 2 (EAAT2)
Genetic variants
Transporter uptake
Patch clamp
title The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in context
title_full The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in context
title_fullStr The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in context
title_full_unstemmed The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in context
title_short The severity of SLC1A2-associated neurodevelopmental disorders correlates with transporter dysfunctionResearch in context
title_sort severity of slc1a2 associated neurodevelopmental disorders correlates with transporter dysfunctionresearch in context
topic Epilepsy
SLC1A2
Excitatory amino acid transporter 2 (EAAT2)
Genetic variants
Transporter uptake
Patch clamp
url http://www.sciencedirect.com/science/article/pii/S2352396425000921
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