Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disorders

Abstract Social dysfunction is the core syndrome of autism spectrum disorder (ASD) and lacks effective medicine. Although numerous risk genes and relevant environmental factors have been identified, the convergent molecular mechanism underlying ASD‐associated social dysfunction remains largely elusi...

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Main Authors: Mengmeng Wang, Panpan Xian, Weian Zheng, Zhenzhen Li, Andi Chen, Haoxiang Xiao, Chao Xu, Fei Wang, Honghui Mao, Han Meng, Youyi Zhao, Ceng Luo, Yazhou Wang, Shengxi Wu
Format: Article
Language:English
Published: Springer Nature 2023-04-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202217101
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author Mengmeng Wang
Panpan Xian
Weian Zheng
Zhenzhen Li
Andi Chen
Haoxiang Xiao
Chao Xu
Fei Wang
Honghui Mao
Han Meng
Youyi Zhao
Ceng Luo
Yazhou Wang
Shengxi Wu
author_facet Mengmeng Wang
Panpan Xian
Weian Zheng
Zhenzhen Li
Andi Chen
Haoxiang Xiao
Chao Xu
Fei Wang
Honghui Mao
Han Meng
Youyi Zhao
Ceng Luo
Yazhou Wang
Shengxi Wu
author_sort Mengmeng Wang
collection DOAJ
description Abstract Social dysfunction is the core syndrome of autism spectrum disorder (ASD) and lacks effective medicine. Although numerous risk genes and relevant environmental factors have been identified, the convergent molecular mechanism underlying ASD‐associated social dysfunction remains largely elusive. Here, we report aberrant activation of canonical Wnt signaling and increased glycolysis in the anterior cingulate cortex (ACC, a key brain region of social function) of two ASD mouse models (Shank3−/− and valproic acid‐treated mice) and their corresponding human neurons. Overexpressing β‐catenin in the ACC of wild‐type mice induces both glycolysis and social deficits. Suppressing glycolysis in ASD mice partially rescued synaptic and social phenotype. Axin2, a key inhibitory molecule in Wnt signaling, interacts with the glycolytic enzyme enolase 1 (ENO1) in ASD neurons. Surprisingly, an Axin2 stabilizer, XAV939, effectively blocked Axin2/ENO1 interaction, switched glycolysis/oxidative phosphorylation balance, promoted synaptic maturation, and rescued social function. These data revealed excessive neuronal Wnt‐glycolysis signaling as an important underlying mechanism for ASD synaptic deficiency, indicating Axin2 as a potential therapeutic target for social dysfunction.
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institution Kabale University
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spelling doaj-art-e52c2912ea124d4eb4fccce223ad9ddb2025-08-20T03:43:25ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842023-04-0115612010.15252/emmm.202217101Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disordersMengmeng Wang0Panpan Xian1Weian Zheng2Zhenzhen Li3Andi Chen4Haoxiang Xiao5Chao Xu6Fei Wang7Honghui Mao8Han Meng9Youyi Zhao10Ceng Luo11Yazhou Wang12Shengxi Wu13Department of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityState Key Laboratory of Military Stomatology and National Clinical Research Center for Oral Diseases and Shaanxi Engineering Research, Center for Dental Materials and Advanced Manufacture, Department of Anesthesiology, School of Stomatology, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityDepartment of Neurobiology and Institute of Neurosciences, School of Basic Medicine, Fourth Military Medical UniversityAbstract Social dysfunction is the core syndrome of autism spectrum disorder (ASD) and lacks effective medicine. Although numerous risk genes and relevant environmental factors have been identified, the convergent molecular mechanism underlying ASD‐associated social dysfunction remains largely elusive. Here, we report aberrant activation of canonical Wnt signaling and increased glycolysis in the anterior cingulate cortex (ACC, a key brain region of social function) of two ASD mouse models (Shank3−/− and valproic acid‐treated mice) and their corresponding human neurons. Overexpressing β‐catenin in the ACC of wild‐type mice induces both glycolysis and social deficits. Suppressing glycolysis in ASD mice partially rescued synaptic and social phenotype. Axin2, a key inhibitory molecule in Wnt signaling, interacts with the glycolytic enzyme enolase 1 (ENO1) in ASD neurons. Surprisingly, an Axin2 stabilizer, XAV939, effectively blocked Axin2/ENO1 interaction, switched glycolysis/oxidative phosphorylation balance, promoted synaptic maturation, and rescued social function. These data revealed excessive neuronal Wnt‐glycolysis signaling as an important underlying mechanism for ASD synaptic deficiency, indicating Axin2 as a potential therapeutic target for social dysfunction.https://doi.org/10.15252/emmm.202217101Axin2glycolysissocial dysfunctionWnt signaling
spellingShingle Mengmeng Wang
Panpan Xian
Weian Zheng
Zhenzhen Li
Andi Chen
Haoxiang Xiao
Chao Xu
Fei Wang
Honghui Mao
Han Meng
Youyi Zhao
Ceng Luo
Yazhou Wang
Shengxi Wu
Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disorders
EMBO Molecular Medicine
Axin2
glycolysis
social dysfunction
Wnt signaling
title Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disorders
title_full Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disorders
title_fullStr Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disorders
title_full_unstemmed Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disorders
title_short Axin2 coupled excessive Wnt‐glycolysis signaling mediates social defect in autism spectrum disorders
title_sort axin2 coupled excessive wnt glycolysis signaling mediates social defect in autism spectrum disorders
topic Axin2
glycolysis
social dysfunction
Wnt signaling
url https://doi.org/10.15252/emmm.202217101
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