Chromatin remodeling inactivates activity genes and regulates neural coding

Activity-dependent transcription influences neuronal connectivity, but the roles and mechanisms of inactivation of activity-dependent genes have remained poorly understood. Genome-wide analyses in the mouse cerebellum revealed that the nucleosome remodeling and deacetylase (NuRD) complex deposits th...

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Published inScience (American Association for the Advancement of Science) Vol. 353; no. 6296; p. 300
Main Authors Yang, Yue, Yamada, Tomoko, Hill, Kelly K, Hemberg, Martin, Reddy, Naveen C, Cho, Ha Y, Guthrie, Arden N, Oldenborg, Anna, Heiney, Shane A, Ohmae, Shogo, Medina, Javier F, Holy, Timothy E, Bonni, Azad
Format Journal Article
LanguageEnglish
Published United States 15.07.2016
Subjects
Animals
Cerebellum - physiology
Chromatin Assembly and Disassembly
Dendrites - physiology
DNA Helicases - metabolism
Gene Knockout Techniques
Gene Silencing
Genome-Wide Association Study
Histones - metabolism
Mi-2 Nucleosome Remodeling and Deacetylase Complex - metabolism
Mice
Mice, Knockout
Neurons - physiology
Nucleosomes - metabolism
Promoter Regions, Genetic
Transcription, Genetic
Online AccessGet more information
ISSN1095-9203
DOI10.1126/science.aad4225

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Abstract Activity-dependent transcription influences neuronal connectivity, but the roles and mechanisms of inactivation of activity-dependent genes have remained poorly understood. Genome-wide analyses in the mouse cerebellum revealed that the nucleosome remodeling and deacetylase (NuRD) complex deposits the histone variant H2A.z at promoters of activity-dependent genes, thereby triggering their inactivation. Purification of translating messenger RNAs from synchronously developing granule neurons (Sync-TRAP) showed that conditional knockout of the core NuRD subunit Chd4 impairs inactivation of activity-dependent genes when neurons undergo dendrite pruning. Chd4 knockout or expression of NuRD-regulated activity genes impairs dendrite pruning. Imaging of behaving mice revealed hyperresponsivity of granule neurons to sensorimotor stimuli upon Chd4 knockout. Our findings define an epigenetic mechanism that inactivates activity-dependent transcription and regulates dendrite patterning and sensorimotor encoding in the brain.
AbstractList Activity-dependent transcription influences neuronal connectivity, but the roles and mechanisms of inactivation of activity-dependent genes have remained poorly understood. Genome-wide analyses in the mouse cerebellum revealed that the nucleosome remodeling and deacetylase (NuRD) complex deposits the histone variant H2A.z at promoters of activity-dependent genes, thereby triggering their inactivation. Purification of translating messenger RNAs from synchronously developing granule neurons (Sync-TRAP) showed that conditional knockout of the core NuRD subunit Chd4 impairs inactivation of activity-dependent genes when neurons undergo dendrite pruning. Chd4 knockout or expression of NuRD-regulated activity genes impairs dendrite pruning. Imaging of behaving mice revealed hyperresponsivity of granule neurons to sensorimotor stimuli upon Chd4 knockout. Our findings define an epigenetic mechanism that inactivates activity-dependent transcription and regulates dendrite patterning and sensorimotor encoding in the brain.
Author Medina, Javier F
Cho, Ha Y
Ohmae, Shogo
Holy, Timothy E
Yamada, Tomoko
Guthrie, Arden N
Heiney, Shane A
Bonni, Azad
Hemberg, Martin
Reddy, Naveen C
Yang, Yue
Hill, Kelly K
Oldenborg, Anna
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  organization: Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA
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  surname: Bonni
  fullname: Bonni, Azad
  organization: Department of Neuroscience, Washington University School of Medicine, St. Louis, MO 63110, USA
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Snippet Activity-dependent transcription influences neuronal connectivity, but the roles and mechanisms of inactivation of activity-dependent genes have remained...
SourceID pubmed
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StartPage 300
SubjectTerms Animals
Cerebellum - physiology
Chromatin Assembly and Disassembly
Dendrites - physiology
DNA Helicases - metabolism
Gene Knockout Techniques
Gene Silencing
Genome-Wide Association Study
Histones - metabolism
Mi-2 Nucleosome Remodeling and Deacetylase Complex - metabolism
Mice
Mice, Knockout
Neurons - physiology
Nucleosomes - metabolism
Promoter Regions, Genetic
Transcription, Genetic
Title Chromatin remodeling inactivates activity genes and regulates neural coding
URI https://www.ncbi.nlm.nih.gov/pubmed/27418512
Volume 353
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