Language

English

Publication Date

4-1-2025

Journal

Molecular Psychiatry

DOI

10.1038/s41380-024-02761-9

PMID

39349966

PMCID

PMC11919750

PubMedCentral® Posted Date

9-30-2024

PubMedCentral® Full Text Version

Post-print

Abstract

MEF2C is a critical transcription factor in neurodevelopment, whose loss-of-function mutation in humans results in MEF2C haploinsufficiency syndrome (MHS), a severe form of autism spectrum disorder (ASD)/intellectual disability (ID). Despite prior animal studies of MEF2C heterozygosity to mimic MHS, MHS-specific mutations have not been investigated previously, particularly in a human context as hiPSCs afford. Here, for the first time, we use patient hiPSC-derived cerebrocortical neurons and cerebral organoids to characterize MHS deficits. Unexpectedly, we found that decreased neurogenesis was accompanied by activation of a micro-(mi)RNA-mediated gliogenesis pathway. We also demonstrate network-level hyperexcitability in MHS neurons, as evidenced by excessive synaptic and extrasynaptic activity contributing to excitatory/inhibitory (E/I) imbalance. Notably, the predominantly extrasynaptic (e)NMDA receptor antagonist, NitroSynapsin, corrects this aberrant electrical activity associated with abnormal phenotypes. During neurodevelopment, MEF2C regulates many ASD-associated gene networks, suggesting that treatment of MHS deficits may possibly help other forms of ASD as well.

Keywords

Humans, Organoids, Induced Pluripotent Stem Cells, MEF2 Transcription Factors, Neurons, Neurogenesis, MicroRNAs, Autism Spectrum Disorder, Autistic Disorder, Mutation, Haploinsufficiency, Neuroscience, Autism spectrum disorders

Published Open-Access

yes

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