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Human Molecular Genetics Advance Access published online on February 12, 2009

Human Molecular Genetics, doi:10.1093/hmg/ddp047
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© The Author 2009. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

DYRK1A interacts with the REST/NRSF-SWI/SNF chromatin remodelling complex to deregulate gene clusters involved in the neuronal phenotypic traits of Down syndrome

Aude-Marie Lepagnol-Bestel1, Agnes Zvara2, Gilles Maussion1, Frédérique Quignon3, Bedel Ngimbous1, Nicolas Ramoz1, Sandrine Imbeaud4, Yann Loe-Mie1, Karim Benihoud5, Nicolas Agier4, Paul A. Salin6, Ana Cardona7, Suonavy Khung-Savatovsky8, Pekka Kallunki9, Jean-Maurice Delabar10, Laszlo G. Puskas2, Hervé Delacroix4, Lawrence Aggerbeck4, Anne-Lise Delezoide8, Olivier Delattre3, Philip Gorwood1, Jean-Marie Moalic1 and Michel Simonneau1,*

1 INSERM U675, IFR02, Faculté de Médecine Xavier Bichat, Université Paris VII, Paris, France 2 Laboratory for Functional Genomics, Biological Research Center, HAS, Szeged, Hungary 3 INSERM U830, Institut Curie, Paris, France 4 Centre de Génétique Moléculaire, UPR 2167, CNRS and Gif/Orsay DNA Microarray Platform (GODMAP), Gif sur Yvette, France 5 UMR CNRS 8121, IGR, Villejuif, France 6 UMR CNRS 5167, Lyon, France 7 Institut Pasteur, Paris, France 8 Service de Biologie du Développement/ Foetopathologie, Hôpital Robert Debré, Paris, France 9 H. Lundbeck A/S, 2500 Valby, Denmark 10 EA 3508, Université Paris Diderot - Paris 7, Paris, France

* corresponding author: michel.simonneau{at}bichat.inserm.fr

Received October 13, 2008; Revised January 22, 2009; Accepted January 22, 2009

The molecular mechanisms that lead to the cognitive defects characteristic of Down syndrome (DS), the most frequent cause of mental retardation, have remained elusive. Here we use a transgenic DS mouse model (152F7 line) to show that DYRK1A gene dosage imbalance deregulates chromosomal clusters of genes located near neuron-restrictive silencer factor (REST/NRSF) binding sites. We found that Dyrk1a binds the SWI/SNF-complex known to interact with REST/NRSF. Mutation of a REST/NRSF binding site in the promoter of the REST/NRSF target gene L1cam modifies the transcriptional effect of Dyrk1a-dosage imbalance on L1cam. Dyrk1a dosage imbalance perturbs Rest/Nrsf levels with decreased Rest/Nrsf expression in embryonic neurons and increased expression in adult neurons. Using transcriptome analysis of embryonic brain subregions of transgenic 152F7 mouse line, we identified a coordinated deregulation of multiple genes that are responsible for dendritic growth impairment present in DS. Similarly, Dyrk1a overexpression in primary mouse cortical neurons induced severe reduction of the dendritic growth and dendritic complexity. We propose that DYRK1A overexpression-related neuronal gene deregulation via disturbance of REST/NRSF levels, and the REST/NRSF-SWI/SNF chromatin remodelling complex, significantly contributes to the neural phenotypic changes that characterize DS.


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