Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain
Open accessAbstract
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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FOXP2, ROBO1, and ROBO2 have long been implicated in brain wiring processes critical for vocal learning in several species, including humans.
“Among the genes downstream of BAZ1B that we uncovered in this study, FOXP2, ROBO1, and ROBO2 have long been implicated in brain wiring processes critical for vocal learning in several species (50, 51), including humans”
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Genetics and the Language Sciences
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FOXP2 drives neuronal differentiation by interacting with retinoic acid signaling pathways
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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
- 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
- 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
- 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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