Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairments

Autism spectrum disorder (ASD) is a group of neurodevelopmental disorders characterized by social interaction deficits, restricted interests and repetitive behaviors. The co-occurrence of motor impairments exacerbates the severity and societal impact of ASD, but the underlying mechanism remains to b...

Full description

Saved in:
Bibliographic Details
Main Authors: Jinxin Wang, Yimeng Li, Dai Zhang, Wenzhi Sun, Jun Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Psychiatry
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1396716/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850185452723634176
author Jinxin Wang
Yimeng Li
Dai Zhang
Wenzhi Sun
Jun Li
author_facet Jinxin Wang
Yimeng Li
Dai Zhang
Wenzhi Sun
Jun Li
author_sort Jinxin Wang
collection DOAJ
description Autism spectrum disorder (ASD) is a group of neurodevelopmental disorders characterized by social interaction deficits, restricted interests and repetitive behaviors. The co-occurrence of motor impairments exacerbates the severity and societal impact of ASD, but the underlying mechanism remains to be elucidated. Research on the comorbidities of ASD including motor impairments could benefit in the life quality improvement in patients with ASD. Here we aimed at investigating the motor behaviors in mice with Trio deletion in Purkinje cells (PCs), and further exploring the cellular and molecular mechanisms. The protein level of Calbindin as PCs’ marker was determined. Behaviors including spontaneous locomotion activity, rotarod, beam balance and gait were tested in mice with the ages of 12-week and 20-week. Magnetic resonance imaging (MRI) scanning with T2 and DTI sequencing was performed in 12-week old mice. Although Triofl/fl; Pcp2-Cre mice showed significant impairments of spontaneous locomotion activity in both 12-week and 20-week ages, only the 20-week but not 12-week Triofl/fl; Pcp2-Cre mice showed extra mild abnormal motor, fine motor coordination, and gait. The decreased expression of Calbindin existed in both 12-week and 20-week old mice compared with control. Differentially expressed genes analysis from RNA-Seq and Gene Co-expression Network Analysis (GCNA) showed that Syne1 and its co-expressed genes were upregulated in Triofl/fl; Pcp2-Cre mice compared to controls. In addition, abnormal ADC values suggested the long-term chronic damage in the cerebellum. Together, our findings indicate that the motor dysfunction in ASD are affected by Trio deletion in PCs with delayed in onset, accompanied with alterations in MRI, histological, and epigenetic level.
format Article
id doaj-art-a41b2a2372ed412d83da353a54965ec1
institution OA Journals
issn 1664-0640
language English
publishDate 2025-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Psychiatry
spelling doaj-art-a41b2a2372ed412d83da353a54965ec12025-08-20T02:16:44ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402025-04-011510.3389/fpsyt.2024.13967161396716Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairmentsJinxin Wang0Yimeng Li1Dai Zhang2Wenzhi Sun3Jun Li4State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, ChinaChinese Institute for Brain Research, Beijing, ChinaNHC Key Laboratory of Mental Health, National Clinical Research Center for Mental Disorders, Peking University Sixth Hospital, Peking University Institute of Mental Health, Peking University, Beijing, ChinaChinese Institute for Brain Research, Beijing, ChinaNHC Key Laboratory of Mental Health, National Clinical Research Center for Mental Disorders, Peking University Sixth Hospital, Peking University Institute of Mental Health, Peking University, Beijing, ChinaAutism spectrum disorder (ASD) is a group of neurodevelopmental disorders characterized by social interaction deficits, restricted interests and repetitive behaviors. The co-occurrence of motor impairments exacerbates the severity and societal impact of ASD, but the underlying mechanism remains to be elucidated. Research on the comorbidities of ASD including motor impairments could benefit in the life quality improvement in patients with ASD. Here we aimed at investigating the motor behaviors in mice with Trio deletion in Purkinje cells (PCs), and further exploring the cellular and molecular mechanisms. The protein level of Calbindin as PCs’ marker was determined. Behaviors including spontaneous locomotion activity, rotarod, beam balance and gait were tested in mice with the ages of 12-week and 20-week. Magnetic resonance imaging (MRI) scanning with T2 and DTI sequencing was performed in 12-week old mice. Although Triofl/fl; Pcp2-Cre mice showed significant impairments of spontaneous locomotion activity in both 12-week and 20-week ages, only the 20-week but not 12-week Triofl/fl; Pcp2-Cre mice showed extra mild abnormal motor, fine motor coordination, and gait. The decreased expression of Calbindin existed in both 12-week and 20-week old mice compared with control. Differentially expressed genes analysis from RNA-Seq and Gene Co-expression Network Analysis (GCNA) showed that Syne1 and its co-expressed genes were upregulated in Triofl/fl; Pcp2-Cre mice compared to controls. In addition, abnormal ADC values suggested the long-term chronic damage in the cerebellum. Together, our findings indicate that the motor dysfunction in ASD are affected by Trio deletion in PCs with delayed in onset, accompanied with alterations in MRI, histological, and epigenetic level.https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1396716/fullautism spectrum disordertriomotor dysfunctionscerebellumPurkinje cells
spellingShingle Jinxin Wang
Yimeng Li
Dai Zhang
Wenzhi Sun
Jun Li
Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairments
Frontiers in Psychiatry
autism spectrum disorder
trio
motor dysfunctions
cerebellum
Purkinje cells
title Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairments
title_full Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairments
title_fullStr Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairments
title_full_unstemmed Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairments
title_short Deficiency of autism susceptibility gene Trio in cerebellar Purkinje cells leads to delayed motor impairments
title_sort deficiency of autism susceptibility gene trio in cerebellar purkinje cells leads to delayed motor impairments
topic autism spectrum disorder
trio
motor dysfunctions
cerebellum
Purkinje cells
url https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1396716/full
work_keys_str_mv AT jinxinwang deficiencyofautismsusceptibilitygenetrioincerebellarpurkinjecellsleadstodelayedmotorimpairments
AT yimengli deficiencyofautismsusceptibilitygenetrioincerebellarpurkinjecellsleadstodelayedmotorimpairments
AT daizhang deficiencyofautismsusceptibilitygenetrioincerebellarpurkinjecellsleadstodelayedmotorimpairments
AT wenzhisun deficiencyofautismsusceptibilitygenetrioincerebellarpurkinjecellsleadstodelayedmotorimpairments
AT junli deficiencyofautismsusceptibilitygenetrioincerebellarpurkinjecellsleadstodelayedmotorimpairments