NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in mice

We previously found that loss of the X-linked gene NEXMIF results in ASD and intellectual disability (ID). Duplication of chromosomal segments containing NEXMIF has been associated with ASD/ID in humans, but the direct link to the NEXMIF gene, as well as the behavioral and cellular consequences of N...

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Main Authors: KathrynAnn Odamah, Mauricio Toyoki Nishizawa Criales, Heng-Ye Man
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-06-01
Series:Frontiers in Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2025.1556570/full
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author KathrynAnn Odamah
Mauricio Toyoki Nishizawa Criales
Heng-Ye Man
Heng-Ye Man
Heng-Ye Man
author_facet KathrynAnn Odamah
Mauricio Toyoki Nishizawa Criales
Heng-Ye Man
Heng-Ye Man
Heng-Ye Man
author_sort KathrynAnn Odamah
collection DOAJ
description We previously found that loss of the X-linked gene NEXMIF results in ASD and intellectual disability (ID). Duplication of chromosomal segments containing NEXMIF has been associated with ASD/ID in humans, but the direct link to the NEXMIF gene, as well as the behavioral and cellular consequences of NEXMIF overexpression, have not yet been explored. Here, we developed a lentivirus containing the human NEXMIF gene which was bilaterally injected into the ventricles of newborn mice. At adolescent ages, the mice were subjected to various behavioral assays to assess the presence of ASD-like behaviors and comorbidities, followed by the collection of brain tissue to examine changes in neuron morphology, protein expression, and the transcriptome. We report that NEXMIF overexpression in mice led to impaired communication, short-term memory deficits, reduced social behavior, hyperactivity, repetitive/restrictive behaviors, anxiety-like behavior, and altered nociception at adolescent ages, accompanied by attenuated dendritic spine density. RNA sequencing revealed that elevated NEXMIF dosage leads to strong dysregulation in the expression of genes involved in synaptic transmission, neuron differentiation, and post-synaptic membrane potential. Moreover, cultured neurons overexpressing NEXMIF displayed increased dendritic arborization. These findings indicate that NEXMIF overexpression results in transcriptional and cellular deficits that contribute to the development of ASD-like behaviors.
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spelling doaj-art-b21cf2b576e14084bc8168534816b6852025-08-20T02:07:38ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2025-06-011910.3389/fnins.2025.15565701556570NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in miceKathrynAnn Odamah0Mauricio Toyoki Nishizawa Criales1Heng-Ye Man2Heng-Ye Man3Heng-Ye Man4Department of Biology, Boston University, Boston, MA, United StatesDepartment of Biology, Boston University, Boston, MA, United StatesDepartment of Biology, Boston University, Boston, MA, United StatesDepartment of Pharmacology, Physiology & Biophysics, Boston University School of Medicine, Boston, MA, United StatesCenter for Systems Neuroscience, Boston University, Boston, MA, United StatesWe previously found that loss of the X-linked gene NEXMIF results in ASD and intellectual disability (ID). Duplication of chromosomal segments containing NEXMIF has been associated with ASD/ID in humans, but the direct link to the NEXMIF gene, as well as the behavioral and cellular consequences of NEXMIF overexpression, have not yet been explored. Here, we developed a lentivirus containing the human NEXMIF gene which was bilaterally injected into the ventricles of newborn mice. At adolescent ages, the mice were subjected to various behavioral assays to assess the presence of ASD-like behaviors and comorbidities, followed by the collection of brain tissue to examine changes in neuron morphology, protein expression, and the transcriptome. We report that NEXMIF overexpression in mice led to impaired communication, short-term memory deficits, reduced social behavior, hyperactivity, repetitive/restrictive behaviors, anxiety-like behavior, and altered nociception at adolescent ages, accompanied by attenuated dendritic spine density. RNA sequencing revealed that elevated NEXMIF dosage leads to strong dysregulation in the expression of genes involved in synaptic transmission, neuron differentiation, and post-synaptic membrane potential. Moreover, cultured neurons overexpressing NEXMIF displayed increased dendritic arborization. These findings indicate that NEXMIF overexpression results in transcriptional and cellular deficits that contribute to the development of ASD-like behaviors.https://www.frontiersin.org/articles/10.3389/fnins.2025.1556570/fullAutism Spectrum disorderX-linked intellectual disability (XLID)overexpressionmouse behaviorNEXMIF geneNEXMIF duplication
spellingShingle KathrynAnn Odamah
Mauricio Toyoki Nishizawa Criales
Heng-Ye Man
Heng-Ye Man
Heng-Ye Man
NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in mice
Frontiers in Neuroscience
Autism Spectrum disorder
X-linked intellectual disability (XLID)
overexpression
mouse behavior
NEXMIF gene
NEXMIF duplication
title NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in mice
title_full NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in mice
title_fullStr NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in mice
title_full_unstemmed NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in mice
title_short NEXMIF overexpression is associated with autism-like behaviors and alterations in dendritic arborization and spine formation in mice
title_sort nexmif overexpression is associated with autism like behaviors and alterations in dendritic arborization and spine formation in mice
topic Autism Spectrum disorder
X-linked intellectual disability (XLID)
overexpression
mouse behavior
NEXMIF gene
NEXMIF duplication
url https://www.frontiersin.org/articles/10.3389/fnins.2025.1556570/full
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