Single-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism

Abstract Autism spectrum disorder (ASD) comprises alterations in brain anatomy and physiology that ultimately affect information processing and behavior. In most cases, autism is considered idiopathic, involving alterations in numerous genes whose functions are not extensively documented. We evaluat...

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Main Authors: Isabel Barón-Mendoza, Luis A. Márquez, Aliesha González-Arenas, Jessica Guzmán-Condado, Vladimir A. Martínez-Rojas, Johaly Anguiano-Buenfil, Montserrat Mejía-Hernández, Jorge Luis Almazán, Leonor Pérez-Martínez, Gustavo Pedraza-Alva, Emilio J. Galván, Angélica Zepeda
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Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-84521-x
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author Isabel Barón-Mendoza
Luis A. Márquez
Aliesha González-Arenas
Jessica Guzmán-Condado
Vladimir A. Martínez-Rojas
Johaly Anguiano-Buenfil
Montserrat Mejía-Hernández
Jorge Luis Almazán
Leonor Pérez-Martínez
Gustavo Pedraza-Alva
Emilio J. Galván
Angélica Zepeda
author_facet Isabel Barón-Mendoza
Luis A. Márquez
Aliesha González-Arenas
Jessica Guzmán-Condado
Vladimir A. Martínez-Rojas
Johaly Anguiano-Buenfil
Montserrat Mejía-Hernández
Jorge Luis Almazán
Leonor Pérez-Martínez
Gustavo Pedraza-Alva
Emilio J. Galván
Angélica Zepeda
author_sort Isabel Barón-Mendoza
collection DOAJ
description Abstract Autism spectrum disorder (ASD) comprises alterations in brain anatomy and physiology that ultimately affect information processing and behavior. In most cases, autism is considered idiopathic, involving alterations in numerous genes whose functions are not extensively documented. We evaluated the C58/J mouse strain as an idiopathic model of ASD, emphasizing synaptic transmission as the basis of information processing. Through in silico analysis, we found that the C58/J strain carries single nucleotide polymorphisms (SNPs) compared to the C57BL/6J control strain related to synaptic structure and LTP induction. These SNPs have human orthologs previously associated with ASD. We then assessed chemical potentiation (cLTP) in synaptosomes, the electrophysiological properties of hippocampal CA3 cells, and the induction of LTP in ex-vivo slices. An increased proportion of synaptosomes expressing the GluA1 subunit of AMPA receptor and Nrx1β in the membrane was found in the C57BL/6J control strain, but not in C58/J mice, after cLTP induction. Additionally, several electrophysiological properties of CA3 pyramidal cells and hippocampal communication were altered. Behaviorally, C58/J mice exhibited hyperactivity and subtle memory changes. Our results demonstrate that an idiopathic model of ASD exhibits alterations in hippocampal physiology from the cellular to the circuitry and behavioral levels.
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spelling doaj-art-69d9af1e67014abfacf69da219d21d122025-08-20T03:10:32ZengNature PortfolioScientific Reports2045-23222025-01-0115112110.1038/s41598-024-84521-xSingle-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autismIsabel Barón-Mendoza0Luis A. Márquez1Aliesha González-Arenas2Jessica Guzmán-Condado3Vladimir A. Martínez-Rojas4Johaly Anguiano-Buenfil5Montserrat Mejía-Hernández6Jorge Luis Almazán7Leonor Pérez-Martínez8Gustavo Pedraza-Alva9Emilio J. Galván10Angélica Zepeda11Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de MéxicoDepartamento de Farmacobiología, CINVESTAV Unidad Sur CdMxDepartamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de MéxicoDepartamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de MéxicoDepartamento de Farmacobiología, CINVESTAV Unidad Sur CdMxDepartamento de Farmacobiología, CINVESTAV Unidad Sur CdMxDepartamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de MéxicoLaboratorio de Neuroinmunobiología, Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnología UNAMLaboratorio de Neuroinmunobiología, Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnología UNAMLaboratorio de Neuroinmunobiología, Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnología UNAMDepartamento de Farmacobiología, CINVESTAV Unidad Sur CdMxDepartamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de MéxicoAbstract Autism spectrum disorder (ASD) comprises alterations in brain anatomy and physiology that ultimately affect information processing and behavior. In most cases, autism is considered idiopathic, involving alterations in numerous genes whose functions are not extensively documented. We evaluated the C58/J mouse strain as an idiopathic model of ASD, emphasizing synaptic transmission as the basis of information processing. Through in silico analysis, we found that the C58/J strain carries single nucleotide polymorphisms (SNPs) compared to the C57BL/6J control strain related to synaptic structure and LTP induction. These SNPs have human orthologs previously associated with ASD. We then assessed chemical potentiation (cLTP) in synaptosomes, the electrophysiological properties of hippocampal CA3 cells, and the induction of LTP in ex-vivo slices. An increased proportion of synaptosomes expressing the GluA1 subunit of AMPA receptor and Nrx1β in the membrane was found in the C57BL/6J control strain, but not in C58/J mice, after cLTP induction. Additionally, several electrophysiological properties of CA3 pyramidal cells and hippocampal communication were altered. Behaviorally, C58/J mice exhibited hyperactivity and subtle memory changes. Our results demonstrate that an idiopathic model of ASD exhibits alterations in hippocampal physiology from the cellular to the circuitry and behavioral levels.https://doi.org/10.1038/s41598-024-84521-xNeurodevelopmental disordersHippocampusNeurophysiologyLong term potentiationContextual fear memorySpatial memory
spellingShingle Isabel Barón-Mendoza
Luis A. Márquez
Aliesha González-Arenas
Jessica Guzmán-Condado
Vladimir A. Martínez-Rojas
Johaly Anguiano-Buenfil
Montserrat Mejía-Hernández
Jorge Luis Almazán
Leonor Pérez-Martínez
Gustavo Pedraza-Alva
Emilio J. Galván
Angélica Zepeda
Single-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism
Scientific Reports
Neurodevelopmental disorders
Hippocampus
Neurophysiology
Long term potentiation
Contextual fear memory
Spatial memory
title Single-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism
title_full Single-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism
title_fullStr Single-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism
title_full_unstemmed Single-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism
title_short Single-nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism
title_sort single nucleotide polymorphism analysis accurately predicts multiple impairments in hippocampal activity and memory performance in a murine model of idiopathic autism
topic Neurodevelopmental disorders
Hippocampus
Neurophysiology
Long term potentiation
Contextual fear memory
Spatial memory
url https://doi.org/10.1038/s41598-024-84521-x
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