Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model mice

Summary: Angelman syndrome (AS) is a severe neurological disorder characterized by intellectual disability, absence of speech, spontaneous seizure, and motor dysfunction. The absence of functional maternally derived UBE3A protein is considered the primary cause of AS, yet the downstream signaling pa...

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Main Authors: Jia-Hua Hu, Cole Malloy, Ying Liu, Jung M. Park, Ashley Pratt, Meghyn Welch, Jonathan G. Murphy, Daniel Abebe, Rose-Marie Karlsson, Heather A. Cameron, Dax A. Hoffman
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725003547
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author Jia-Hua Hu
Cole Malloy
Ying Liu
Jung M. Park
Ashley Pratt
Meghyn Welch
Jonathan G. Murphy
Daniel Abebe
Rose-Marie Karlsson
Heather A. Cameron
Dax A. Hoffman
author_facet Jia-Hua Hu
Cole Malloy
Ying Liu
Jung M. Park
Ashley Pratt
Meghyn Welch
Jonathan G. Murphy
Daniel Abebe
Rose-Marie Karlsson
Heather A. Cameron
Dax A. Hoffman
author_sort Jia-Hua Hu
collection DOAJ
description Summary: Angelman syndrome (AS) is a severe neurological disorder characterized by intellectual disability, absence of speech, spontaneous seizure, and motor dysfunction. The absence of functional maternally derived UBE3A protein is considered the primary cause of AS, yet the downstream signaling pathways remain elusive. Here, we show the voltage-gated K+ channel Kv4.2 as an activity-dependent substrate for UBE3A. We show that UBE3A binding of Kv4.2 at its N terminus, ubiquitinating residue K103, induces activity-induced Kv4.2 protein loss. In a mouse model of AS, we observe elevated Kv4.2 protein level and abolished kainic acid-induced Kv4.2 protein loss. Moreover, deficits in mEPSC frequency and spike-timing-dependent long-term potentiation, as well as certain behaviors including cognitive inflexibility found in AS mice, are rescued when bred with Kv4.2 conditional knockout mice. These findings indicate a UBE3A downstream pathway regulating plasticity and cognitive behaviors and provide potential targets for the treatment of AS.
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spelling doaj-art-28948102fa3b4be7bcfcc8f3081d76ef2025-08-20T03:48:31ZengElsevierCell Reports2211-12472025-05-0144511558310.1016/j.celrep.2025.115583Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model miceJia-Hua Hu0Cole Malloy1Ying Liu2Jung M. Park3Ashley Pratt4Meghyn Welch5Jonathan G. Murphy6Daniel Abebe7Rose-Marie Karlsson8Heather A. Cameron9Dax A. Hoffman10Molecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USA; Corresponding authorMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USAMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USAMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USAMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USAMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USAMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USAMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USASection on Neuroplasticity, National Institute of Mental Health, Bethesda, MD 20892, USASection on Neuroplasticity, National Institute of Mental Health, Bethesda, MD 20892, USAMolecular Neurophysiology and Biophysics Section, The Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892, USA; Corresponding authorSummary: Angelman syndrome (AS) is a severe neurological disorder characterized by intellectual disability, absence of speech, spontaneous seizure, and motor dysfunction. The absence of functional maternally derived UBE3A protein is considered the primary cause of AS, yet the downstream signaling pathways remain elusive. Here, we show the voltage-gated K+ channel Kv4.2 as an activity-dependent substrate for UBE3A. We show that UBE3A binding of Kv4.2 at its N terminus, ubiquitinating residue K103, induces activity-induced Kv4.2 protein loss. In a mouse model of AS, we observe elevated Kv4.2 protein level and abolished kainic acid-induced Kv4.2 protein loss. Moreover, deficits in mEPSC frequency and spike-timing-dependent long-term potentiation, as well as certain behaviors including cognitive inflexibility found in AS mice, are rescued when bred with Kv4.2 conditional knockout mice. These findings indicate a UBE3A downstream pathway regulating plasticity and cognitive behaviors and provide potential targets for the treatment of AS.http://www.sciencedirect.com/science/article/pii/S2211124725003547CP: NeuroscienceCP: Molecular biology
spellingShingle Jia-Hua Hu
Cole Malloy
Ying Liu
Jung M. Park
Ashley Pratt
Meghyn Welch
Jonathan G. Murphy
Daniel Abebe
Rose-Marie Karlsson
Heather A. Cameron
Dax A. Hoffman
Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model mice
Cell Reports
CP: Neuroscience
CP: Molecular biology
title Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model mice
title_full Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model mice
title_fullStr Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model mice
title_full_unstemmed Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model mice
title_short Activity-dependent degradation of Kv4.2 contributes to synaptic plasticity and behavior in Angelman syndrome model mice
title_sort activity dependent degradation of kv4 2 contributes to synaptic plasticity and behavior in angelman syndrome model mice
topic CP: Neuroscience
CP: Molecular biology
url http://www.sciencedirect.com/science/article/pii/S2211124725003547
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