title: Neurogenic Radial Glia-like Cells in Meninges Migrate and Differentiate into Functionally Integrated Neurons in the Neonatal Cortex.
abstract: Whether new neurons are added in the postnatal cerebral cortex is still debated. Here, we report that the meninges of perinatal mice contain a population of neurogenic progenitors formed during embryonic development that migrate to the caudal cortex and differentiate into Satb2+neurons in cortical layers II-IV. The resulting neurons are electrically functional and integrated into local microcircuits. Single-cell RNA sequencing identified meningeal cells with distinct transcriptome signatures characteristic of (1) neurogenic radial glia-like cells (resembling neural stem cells in the SVZ), (2) neuronal cells, and (3) a cell type with an intermediate phenotype, possibly representing radial glia-like meningeal cells differentiating to neuronal cells. Thus, we have identified a pool of embryonically derived radial glia-like cells present in the meninges that migrate and differentiate into functional neurons in the neonatal cerebral cortex.
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium.
authors.forename: Francesco
authors.initials: F
authors.lastname: Bifari
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium; Department of Diagnostics and Public Health, University of Verona, 37134 Verona, Italy.
authors.forename: Ilaria
authors.initials: I
authors.lastname: Decimo
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium; Department of Diagnostics and Public Health, University of Verona, 37134 Verona, Italy.
authors.forename: Annachiara
authors.initials: A
authors.lastname: Pino
authors.affiliation: Molecular Neurobiology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
authors.forename: Enric
authors.initials: E
authors.lastname: Llorens-Bobadilla
authors.affiliation: Molecular Neurobiology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
authors.forename: Sheng
authors.initials: S
authors.lastname: Zhao
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium.
authors.forename: Christian
authors.initials: C
authors.lastname: Lange
authors.affiliation: Theoretical Neurobiology and Neuroengineering Laboratory, Department of Biomedical Sciences, Antwerp University, 2610 Wilrijk, Belgium.
authors.forename: Gabriella
authors.initials: G
authors.lastname: Panuccio
authors.affiliation: Laboratory for Translational Genetics, Vesalius Research Center, VIB, 3000 Leuven, Belgium; Laboratory for Translational Genetics, Department of Oncology, KU Leuven, 3000 Leuven, Belgium.
authors.forename: Bram
authors.initials: B
authors.lastname: Boeckx
authors.affiliation: Laboratory for Translational Genetics, Vesalius Research Center, VIB, 3000 Leuven, Belgium; Laboratory for Translational Genetics, Department of Oncology, KU Leuven, 3000 Leuven, Belgium.
authors.forename: Bernard
authors.initials: B
authors.lastname: Thienpont
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium.
authors.forename: Stefan
authors.initials: S
authors.lastname: Vinckier
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium.
authors.forename: Sabine
authors.initials: S
authors.lastname: Wyns
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium.
authors.forename: Ann
authors.initials: A
authors.lastname: Bouché
authors.affiliation: Laboratory for Translational Genetics, Vesalius Research Center, VIB, 3000 Leuven, Belgium; Laboratory for Translational Genetics, Department of Oncology, KU Leuven, 3000 Leuven, Belgium.
authors.forename: Diether
authors.initials: D
authors.lastname: Lambrechts
authors.affiliation: Theoretical Neurobiology and Neuroengineering Laboratory, Department of Biomedical Sciences, Antwerp University, 2610 Wilrijk, Belgium; Brain Mind Institute, Swiss Federal Institute of Technology, 1015 Lausanne, Switzerland; Department of Computer Science, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Michele
authors.initials: M
authors.lastname: Giugliano
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium. Electronic address: mieke.dewerchin@vib-kuleuven.be.
authors.forename: Mieke
authors.initials: M
authors.lastname: Dewerchin
authors.affiliation: Molecular Neurobiology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany. Electronic address: a.martin-villalba@dkfz-heidelberg.de.
authors.forename: Ana
authors.initials: A
authors.lastname: Martin-Villalba
authors.affiliation: Laboratory of Angiogenesis and Vascular Metabolism, Department of Oncology, KU Leuven, 3000 Leuven, Belgium; Laboratory of Angiogenesis and Vascular Metabolism, Vesalius Research Center, VIB, 3000 Leuven, Belgium. Electronic address: peter.carmeliet@vib-kuleuven.be.
authors.forename: Peter
authors.initials: P
authors.lastname: Carmeliet
mesh_terms: D000818:Animals; D000831:Animals, Newborn; D002454:Cell Differentiation; D019070:Cell Lineage; D002465:Cell Movement; D002540:Cerebral Cortex / Q000166:cytology*; D004622:Embryo, Mammalian / Q000166:cytology; D027341:Excitatory Amino Acid Transporter 1 / Q000378:metabolism; D020869:Gene Expression Profiling; D057809:HEK293 Cells; D006801:Humans; D008578:Meninges / Q000166:cytology*; D008810:Mice, Inbred C57BL; D064231:Nestin / Q000378:metabolism; D055495:Neurogenesis; D009457:Neuroglia / Q000166:cytology*; D009474:Neurons / Q000166:cytology*; D020797:Receptor, Platelet-Derived Growth Factor beta / Q000378:metabolism; D015203:Reproducibility of Results; D059010:Single-Cell Analysis; D018874:Spheroids, Cellular / Q000166:cytology; D013194:Staining and Labeling; D059467:Transcriptome / Q000235:genetics
chemical_list: D027341:Excitatory Amino Acid Transporter 1; D064231:Nestin; C493393:Slc1a3 protein, mouse; D020797:Receptor, Platelet-Derived Growth Factor beta
keywords: PDGFRβ; electrophysiology; lineage tracing; meninges; neonatal cerebral cortex; neural progenitors; neurogenesis; radial glia cells; single-cell RNA sequencing