FOXP1 Promotes Embryonic Neural Stem Cell Differentiation by Repressing Jagged1 Expression

Elsevier BV - Tập 9 - Trang 1530-1545 - 2017
Luca Braccioli1,2, Stephin J. Vervoort2, Youri Adolfs3, Cobi J. Heijnen4, Onur Basak5, R. Jeroen Pasterkamp3, Cora H. Nijboer1, Paul J. Coffer2
1Laboratory of Neuroimmunology and Developmental Origins of Disease (NIDOD), University Medical Center Utrecht, Utrecht 3508 AB, the Netherlands
2Center for Molecular Medicine and Regenerative Medicine Center, University Medical Center Utrecht, Utrecht 3584 CT, the Netherlands
3Department of Translational Neuroscience, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht 3584 CX, the Netherlands
4Laboratory of Neuroimmunology, Department of Symptom Research, Division of Internal Medicine, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA
5Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW) and University Medical Center Utrecht, 3584 CT Utrecht, the Netherlands

Tài liệu tham khảo

Ables, 2011, Not(ch) just development: Notch signalling in the adult brain, Nat. Rev. Neurosci., 12, 269, 10.1038/nrn3024 Araujo, 2015, FOXP1 orchestration of ASD-relevant signaling pathways in the striatum, Genes Dev., 29, 2081, 10.1101/gad.267989.115 Archer, 2011, Interaction of Sox1, Sox2, Sox3 and Oct4 during primary neurogenesis, Dev. Biol., 350, 429, 10.1016/j.ydbio.2010.12.013 Bacigaluppi, 2016, Neural stem cell transplantation induces stroke recovery by upregulating glutamate transporter GLT-1 in astrocytes, J. Neurosci., 36, 10529, 10.1523/JNEUROSCI.1643-16.2016 Bacon, 2012, The distinct and overlapping phenotypic spectra of FOXP1 and FOXP2 in cognitive disorders, Hum. Genet., 131, 1687, 10.1007/s00439-012-1193-z Bacon, 2015, Brain-specific Foxp1 deletion impairs neuronal development and causes autistic-like behaviour, Mol. Psychiatry, 20, 632, 10.1038/mp.2014.116 Basu, 2009, AutDB: a gene reference resource for autism research, Nucleic Acids Res., 37, D832, 10.1093/nar/gkn835 Bergsland, 2011, Sequentially acting Sox transcription factors in neural lineage development, Genes Dev., 25, 2453, 10.1101/gad.176008.111 Blurton-Jones, 2009, Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease, Proc. Natl. Acad. Sci. USA, 106, 13594, 10.1073/pnas.0901402106 Braccioli, 2016, Delayed administration of neural stem cells after hypoxia-ischemia reduces sensorimotor deficits, cerebral lesion size, and neuroinflammation in neonatal mice, Pediatr. Res., 81, 127, 10.1038/pr.2016.172 Carbon, 2009, AmiGO: online access to ontology and annotation data, Bioinformatics, 25, 288, 10.1093/bioinformatics/btn615 Chen, 2013, Expression analysis of the speech-related genes FoxP1 and FoxP2 and their relation to singing behavior in two songbird species, J. Exp. Biol., 216, 3682, 10.1242/jeb.085886 Chien, 2013, Increased gene expression of FOXP1 in patients with autism spectrum disorders, Mol. Autism, 4, 23, 10.1186/2040-2392-4-23 Crawford, 2007, The notch response inhibitor DAPT enhances neuronal differentiation in embryonic stem cell-derived embryoid bodies independently of sonic hedgehog signaling, Dev. Dyn., 236, 886, 10.1002/dvdy.21083 Daadi, 2010, Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic-ischemic brain injury, Stroke, 41, 516, 10.1161/STROKEAHA.109.573691 Dovey, 2001, Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain, J. Neurochem., 76, 173, 10.1046/j.1471-4159.2001.00012.x Ellis, 2004, SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult, Dev. Neurosci., 26, 148, 10.1159/000082134 Eng, 1994, GFAP and astrogliosis, Brain Pathol., 4, 229, 10.1111/j.1750-3639.1994.tb00838.x Englund, 2005, Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex, J. Neurosci., 25, 247, 10.1523/JNEUROSCI.2899-04.2005 Fishell, 2003, Neurons from radial glia: the consequences of asymmetric inheritance, Curr. Opin. Neurobiol., 13, 34, 10.1016/S0959-4388(03)00013-8 Frohlich, 2017, Foxp1 expression is essential for sex-specific murine neonatal ultrasonic vocalization, Hum. Mol. Genet., 26, 1511, 10.1093/hmg/ddx055 Gaiano, 2002, The role of notch in promoting glial and neural stem cell fates, Annu. Rev. Neurosci., 25, 471, 10.1146/annurev.neuro.25.030702.130823 Gotz, 2005, The cell biology of neurogenesis, Nat. Rev. Mol. Cell Biol., 6, 777, 10.1038/nrm1739 Hamdan, 2010, De novo mutations in FOXP1 in cases with intellectual disability, autism, and language impairment, Am. J. Hum. Genet., 87, 671, 10.1016/j.ajhg.2010.09.017 Horn, 2010, Identification of FOXP1 deletions in three unrelated patients with mental retardation and significant speech and language deficits, Hum. Mutat., 31, E1851, 10.1002/humu.21362 Imayoshi, 2013, Oscillatory control of factors determining multipotency and fate in mouse neural progenitors, Science, 342, 1203, 10.1126/science.1242366 Islam, 2015, TLX: a master regulator for neural stem cell maintenance and neurogenesis, Biochim. Biophys. Acta, 1849, 210, 10.1016/j.bbagrm.2014.06.001 Kaushik, 2016, Prenatal neurogenesis in autism spectrum disorders, Front. Chem., 4, 12, 10.3389/fchem.2016.00012 Kopan, 2009, The canonical Notch signaling pathway: unfolding the activation mechanism, Cell, 137, 216, 10.1016/j.cell.2009.03.045 Kriegstein, 2009, The glial nature of embryonic and adult neural stem cells, Annu. Rev. Neurosci., 32, 149, 10.1146/annurev.neuro.051508.135600 Ladi, 2005, The divergent DSL ligand Dll3 does not activate Notch signaling but cell autonomously attenuates signaling induced by other DSL ligands, J. Cell Biol., 170, 983, 10.1083/jcb.200503113 Lavado, 2014, Jagged1 is necessary for postnatal and adult neurogenesis in the dentate gyrus, Dev. Biol., 388, 11, 10.1016/j.ydbio.2014.02.004 Le Fevre, 2013, FOXP1 mutations cause intellectual disability and a recognizable phenotype, Am. J. Med. Genet. A, 161A, 3166, 10.1002/ajmg.a.36174 Lendahl, 1990, CNS stem cells express a new class of intermediate filament protein, Cell, 60, 585, 10.1016/0092-8674(90)90662-X Leone, 2008, The determination of projection neuron identity in the developing cerebral cortex, Curr. Opin. Neurobiol., 18, 28, 10.1016/j.conb.2008.05.006 Li, 2015, Foxp1 regulates cortical radial migration and neuronal morphogenesis in developing cerebral cortex, PLoS One, 10, e0127671, 10.1371/journal.pone.0127671 Louvi, 2006, Notch signalling in vertebrate neural development, Nat. Rev. Neurosci., 7, 93, 10.1038/nrn1847 Lozano, 2015, A de novo FOXP1 variant in a patient with autism, intellectual disability and severe speech and language impairment, Eur. J. Hum. Genet., 23, 1702, 10.1038/ejhg.2015.66 Martino, 2006, The therapeutic potential of neural stem cells, Nat. Rev. Neurosci., 7, 395, 10.1038/nrn1908 Memberg, 1995, Dividing neuron precursors express neuron-specific tubulin, J. Neurobiol., 27, 26, 10.1002/neu.480270104 Mendoza, 2015, Differential coexpression of FoxP1, FoxP2, and FoxP4 in the Zebra Finch (Taeniopygia guttata) song system, J. Comp. Neurol., 523, 1318, 10.1002/cne.23731 Nijboer, 2008, Low endogenous G-protein-coupled receptor kinase 2 sensitizes the immature brain to hypoxia-ischemia-induced gray and white matter damage, J. Neurosci., 28, 3324, 10.1523/JNEUROSCI.4769-07.2008 Nyfeler, 2005, Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self-renewal, EMBO J., 24, 3504, 10.1038/sj.emboj.7600816 Ottone, 2014, Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells, Nat. Cell Biol., 16, 1045, 10.1038/ncb3045 Palumbo, 2013, 3p14.1 de novo microdeletion involving the FOXP1 gene in an adult patient with autism, severe speech delay and deficit of motor coordination, Gene, 516, 107, 10.1016/j.gene.2012.12.073 Park, 2002, The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue, Nat. Biotechnol., 20, 1111, 10.1038/nbt751 Peeters, 2015, Inhibition of super-enhancer activity in autoinflammatory site-derived T cells reduces disease-associated gene expression, Cell Rep., 12, 1986, 10.1016/j.celrep.2015.08.046 Polito, 2005, NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system, J. Anat., 207, 707 Precious, 2016, FoxP1 marks medium spiny neurons from precursors to maturity and is required for their differentiation, Exp. Neurol., 282, 9, 10.1016/j.expneurol.2016.05.002 Raponi, 2007, S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage, Glia, 55, 165, 10.1002/glia.20445 Renault, 2009, FoxO3 regulates neural stem cell homeostasis, Cell Stem Cell, 5, 527, 10.1016/j.stem.2009.09.014 Schallert, 2000, CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury, Neuropharmacology, 39, 777, 10.1016/S0028-3908(00)00005-8 Shimojo, 2008, Oscillations in notch signaling regulate maintenance of neural progenitors, Neuron, 58, 52, 10.1016/j.neuron.2008.02.014 Shu, 2001, Characterization of a new subfamily of winged-helix/forkhead (Fox) genes that are expressed in the lung and act as transcriptional repressors, J. Biol. Chem., 276, 27488, 10.1074/jbc.M100636200 Sin, 2015, Transcriptional regulation by FOXP1, FOXP2, and FOXP4 dimerization, J. Mol. Neurosci., 55, 437, 10.1007/s12031-014-0359-7 Sollis, 2016, Identification and functional characterization of de novo FOXP1 variants provides novel insights into the etiology of neurodevelopmental disorder, Hum. Mol. Genet., 25, 546, 10.1093/hmg/ddv495 Subramanian, 2005, Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles, Proc. Natl. Acad. Sci. USA, 102, 15545, 10.1073/pnas.0506580102 Teramitsu, 2004, Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction, J. Neurosci., 24, 3152, 10.1523/JNEUROSCI.5589-03.2004 van Boxtel, 2013, FOXP1 acts through a negative feedback loop to suppress FOXO-induced apoptosis, Cell Death Differ., 20, 1219, 10.1038/cdd.2013.81 van der Kooij, 2010, Mild neonatal hypoxia-ischemia induces long-term motor- and cognitive impairments in mice, Brain Behav. Immun., 24, 850, 10.1016/j.bbi.2009.09.003 van Velthoven, 2010, Repeated mesenchymal stem cell treatment after neonatal hypoxia-ischemia has distinct effects on formation and maturation of new neurons and oligodendrocytes leading to restoration of damage, corticospinal motor tract activity, and sensorimotor function, J. Neurosci., 30, 9603, 10.1523/JNEUROSCI.1835-10.2010 Wang, 2016, The orphan nuclear receptor TLX/NR2E1 in neural stem cells and diseases, Neurosci. Bull., 32, 108, 10.1007/s12264-015-0004-7 Xiao, 2014, Involvement of aquaporin 4 in astrocyte function and neuropsychiatric disorders, CNS Neurosci. Ther., 20, 385, 10.1111/cns.12267 Zhao, 2009, The N-Myc-DLL3 cascade is suppressed by the ubiquitin ligase Huwe1 to inhibit proliferation and promote neurogenesis in the developing brain, Dev. Cell, 17, 210, 10.1016/j.devcel.2009.07.009