Cited by 276Genetics and Neurodevelopmental DisordersNeurogenesis and neuroplasticity mechanismsAxon Guidance and Neuronal Signaling

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Foxp2 Regulates Gene Networks Implicated in Neurite Outgrowth in the Developing Brain

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Vernes, Sonja C., Oliver, Peter L., Spiteri, Elizabeth, Lockstone, Helen E., Puliyadi, Rathi, Taylor, Jennifer M., Ho, Joses, Mombereau, Cedric, Brewer, Ariel, Lowy, Ernesto, Nicod, Jérôme, Groszer, Matthias, Baban, Dilair, Sahgal, Natasha, Cazier, Jean-Baptiste, Ragoussis, Jiannis, Davies, Kay E., Geschwind, Daniel H., Fisher, Simon E.·2011·PLoS Genetics

DOI 10.1371/journal.pgen.1002145PMC PMC3131290

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Abstract

Forkhead-box protein P2 is a transcription factor that has been associated with intriguing aspects of cognitive function in humans, non-human mammals, and song-learning birds. Heterozygous mutations of the human FOXP2 gene cause a monogenic speech and language disorder. Reduced functional dosage of the mouse version (Foxp2) causes deficient cortico-striatal synaptic plasticity and impairs motor-skill learning. Moreover, the songbird orthologue appears critically important for vocal learning. Across diverse vertebrate species, this well-conserved transcription factor is highly expressed in the developing and adult central nervous system. Very little is known about the mechanisms regulated by Foxp2 during brain development. We used an integrated functional genomics strategy to robustly define Foxp2-dependent pathways, both direct and indirect targets, in the embryonic brain. Specifically, we performed genome-wide in vivo ChIP-chip screens for Foxp2-binding and thereby identified a set of 264 high-confidence neural targets under strict, empirically derived significance thresholds. The findings, coupled to expression profiling and in situ hybridization of brain tissue from wild-type and mutant mouse embryos, strongly highlighted gene networks linked to neurite development. We followed up our genomics data with functional experiments, showing that Foxp2 impacts on neurite outgrowth in primary neurons and in neuronal cell models. Our data indicate that Foxp2 modulates neuronal network formation, by directly and indirectly regulating mRNAs involved in the development and plasticity of neuronal connections.

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Authors: Vernes, S. C., Oliver, P. L., Spiteri, E., Lockstone, H. E., Puliyadi, R., Taylor, J. M., Ho, J., Mombereau, C., Brewer, A., Lowy, E., Nicod, J., Groszer, M., Baban, D., Sahgal, N., Cazier, J.-B., Ragoussis, J., Davies, K. E., Geschwind, D. H., & Fisher, S. E.
Affiliations: Centre for Human Genetics (GB)
University of Oxford (GB)
University of California, Los Angeles (US)
Inserm (FR)
Corresponding author: Fisher, Simon E.
ORCID: Vernes, Sonja C.
Oliver, Peter L.
Lockstone, Helen E.
Puliyadi, Rathi
Taylor, Jennifer M.
Ho, Joses
Lowy, Ernesto
Nicod, Jérôme
Groszer, Matthias
Cazier, Jean-Baptiste
Ragoussis, Jiannis
Geschwind, Daniel H.
Fisher, Simon E.
Venue: PLoS Genetics
Publisher: Public Library of Science (PLoS)
Published: 2011-07-07
Volume: 7
Issue: 7
Pages: e1002145
ISSN: 1553-7390 (ISSN-L)
1553-7404
DOI: 10.1371/journal.pgen.1002145
PMC: PMC3131290
OpenAlex: W2010016215
Cited by: 276
References: 69
Citations by year: 2026: 9 · 2025: 14 · 2024: 10 · 2023: 11 · 2022: 13 · 2021: 12 · 2020: 19 · 2019: 27 · 2018: 26 · 2017: 19 · 2016: 21 · 2015: 16 · 2014: 26 · 2013: 29 · 2012: 21
FWCI: 15.76
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Genetics (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
eScholarship (California Digital Library) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
Max Planck Digital Library (submittedVersion, other-oa)
Figshare (submittedVersion, cc-by)
University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders: Autism Speaks
Simons Foundation
Wellcome Trust (075491, 080971, 075491/Z/04,)
Simons Foundation Autism Research Initiative
Royal Society
Institut National de la Santé et de la Recherche Médicale
Max-Planck-Gesellschaft
National Institutes of Health (080971, 075491/Z/04)
Directorate for Biological Sciences
National Institute of Mental Health (R21MH075028, R37MH060233)
National Institute of General Medical Sciences (T32GM008243)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
Keywords: FOXP2, transcription factors, neurite outgrowth, embryonic brain development, gene regulatory networks, ChIP-chip, neuronal network formation, synaptic plasticity, speech and language disorders, corticostriatal synapses, motor skill learning, vocal learning
MeSH terms: Animals, Brain, Corpus Striatum, Mice, Inbred C57BL, Models, Biological, Mutation, Repressor Proteins, RNA, Messenger, Neurites, Gene Expression Regulation, Developmental, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Cell Line, Tumor, Chromatin Immunoprecipitation, Mice, Forkhead Transcription Factors, Gene Regulatory Networks, Primary Cell Culture

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Foxp2 Regulates Gene Networks Implicated in Neurite Outgrowth in the Developing Brain

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