DREAM Controls the On/Off Switch of Specific Activity-Dependent Transcription Pathways
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Published in | Molecular and Cellular Biology Vol. 34; no. 5; pp. 877 - 887 |
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Main Authors | , , , , , , , , , , , , , , , , , , |
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American Society for Microbiology
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AbstractList | Changes in nuclear Ca(2+) homeostasis activate specific gene expression programs and are central to the acquisition and storage of information in the brain. DREAM (downstream regulatory element antagonist modulator), also known as calsenilin/KChIP-3 (K(+) channel interacting protein 3), is a Ca(2+)-binding protein that binds DNA and represses transcription in a Ca(2+)-dependent manner. To study the function of DREAM in the brain, we used transgenic mice expressing a Ca(2+)-insensitive/CREB-independent dominant active mutant DREAM (daDREAM). Using genome-wide analysis, we show that DREAM regulates the expression of specific activity-dependent transcription factors in the hippocampus, including Npas4, Nr4a1, Mef2c, JunB, and c-Fos. Furthermore, DREAM regulates its own expression, establishing an autoinhibitory feedback loop to terminate activity-dependent transcription. Ablation of DREAM does not modify activity-dependent transcription because of gene compensation by the other KChIP family members. The expression of daDREAM in the forebrain resulted in a complex phenotype characterized by loss of recurrent inhibition and enhanced long-term potentiation (LTP) in the dentate gyrus and impaired learning and memory. Our results indicate that DREAM is a major master switch transcription factor that regulates the on/off status of specific activity-dependent gene expression programs that control synaptic plasticity, learning, and memory. OA Classifications Services MCB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue MCB About MCB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy MCB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0270-7306 Online ISSN: 1098-5549 Copyright © 2014 by the American Society for Microbiology. For an alternate route to MCB .asm.org, visit: MCB Changes in nuclear Ca(2+) homeostasis activate specific gene expression programs and are central to the acquisition and storage of information in the brain. DREAM (downstream regulatory element antagonist modulator), also known as calsenilin/KChIP-3 (K(+) channel interacting protein 3), is a Ca(2+)-binding protein that binds DNA and represses transcription in a Ca(2+)-dependent manner. To study the function of DREAM in the brain, we used transgenic mice expressing a Ca(2+)-insensitive/CREB-independent dominant active mutant DREAM (daDREAM). Using genome-wide analysis, we show that DREAM regulates the expression of specific activity-dependent transcription factors in the hippocampus, including Npas4, Nr4a1, Mef2c, JunB, and c-Fos. Furthermore, DREAM regulates its own expression, establishing an autoinhibitory feedback loop to terminate activity-dependent transcription. Ablation of DREAM does not modify activity-dependent transcription because of gene compensation by the other KChIP family members. The expression of daDREAM in the forebrain resulted in a complex phenotype characterized by loss of recurrent inhibition and enhanced long-term potentiation (LTP) in the dentate gyrus and impaired learning and memory. Our results indicate that DREAM is a major master switch transcription factor that regulates the on/off status of specific activity-dependent gene expression programs that control synaptic plasticity, learning, and memory. This work was supported by grants from Spanish Ministry of Health and Science, Madrid Community, La Marató, La Caixa, Reina Sofía and Areces Foundations, the EU 6th Framework Program (NeuroNE, CureFXS), the ERA-NET Program (Neuron and E-Rare), and the Medical Research Council. S.K. has a postdoctoral contract from the Ramón y Cajal Program of the Ministry of Science and Innovation. Changes in nuclear Ca 2+ homeostasis activate specific gene expression programs and are central to the acquisition and storage of information in the brain. DREAM ( d ownstream r egulatory e lement a ntagonist m odulator), also known as calsenilin/KChIP-3 ( K + ch annel i nteracting p rotein 3), is a Ca 2+ -binding protein that binds DNA and represses transcription in a Ca 2+ -dependent manner. To study the function of DREAM in the brain, we used transgenic mice expressing a Ca 2+ -insensitive/CREB-independent dominant active mutant DREAM (daDREAM). Using genome-wide analysis, we show that DREAM regulates the expression of specific activity-dependent transcription factors in the hippocampus, including Npas4, Nr4a1, Mef2c, JunB, and c-Fos. Furthermore, DREAM regulates its own expression, establishing an autoinhibitory feedback loop to terminate activity-dependent transcription. Ablation of DREAM does not modify activity-dependent transcription because of gene compensation by the other KChIP family members. The expression of daDREAM in the forebrain resulted in a complex phenotype characterized by loss of recurrent inhibition and enhanced long-term potentiation (LTP) in the dentate gyrus and impaired learning and memory. Our results indicate that DREAM is a major master switch transcription factor that regulates the on/off status of specific activity-dependent gene expression programs that control synaptic plasticity, learning, and memory. |
Author | Michael L. Errington Jose R. Naranjo Alejandro Higuera-Matas Rosa Gomez-Villafuertes Patricia Murtra Tim V. P. Bliss John G. R. Jefferys Britt Mellström Ignasi Sahún Rafael Maldonado Paz Gonzalez Asta Kastanauskaite Ana Ruiz-Nuño Javier DeFelipe Magali Savignac Shira Knafo Juan C. Oliveros Min Zhuo Mara Dierssen |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24366545$$D View this record in MEDLINE/PubMed |
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Mendeley... Changes in nuclear Ca 2+ homeostasis activate specific gene expression programs and are central to the acquisition and storage of information in the brain.... Changes in nuclear Ca(2+) homeostasis activate specific gene expression programs and are central to the acquisition and storage of information in the brain.... |
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SubjectTerms | Animals Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Calcium - metabolism Cells, Cultured Cervell Cyclic AMP Response Element-Binding Protein - genetics Cyclic AMP Response Element-Binding Protein - metabolism Dentate Gyrus - metabolism Down-Regulation - genetics GABAergic Neurons - metabolism Genètica Hippocampus - metabolism Kv Channel-Interacting Proteins - genetics Kv Channel-Interacting Proteins - metabolism Learning Mice Mice, Transgenic Promoter Regions, Genetic - genetics Prosencephalon - metabolism Proteïnes Repressor Proteins - genetics Repressor Proteins - metabolism Transcription Factors - genetics Transcription Factors - metabolism Transcription, Genetic - genetics |
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Title | DREAM Controls the On/Off Switch of Specific Activity-Dependent Transcription Pathways |
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