Regulation of Radial Glial Survival by Signals from the Meninges
Open accessAbstract
Radial glial cells (RGCs) in the developing cerebral cortex are progenitors for neurons and glia, and their processes serve as guideposts for migrating neurons. So far, it has remained unclear whether RGC processes also control the function of RGCs more directly. Here, we show that RGC numbers and cortical size are reduced in mice lacking beta1 integrins in RGCs. TUNEL stainings and time-lapse video recordings demonstrate that beta1-deficient RGCs processes detach from the meningeal basement membrane (BM) followed by apoptotic death of RGCs. Apoptosis is also induced by surgical removal of the meninges. Finally, mice lacking the BM components laminin alpha2 and alpha4 show defects in the attachment of RGC processes at the meninges, a reduction in cortical size, and enhanced apoptosis of RGC cells. Our findings demonstrate that attachment of RGC processes at the meninges is important for RGC survival and the control of cortical size.
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GPR56 likely influences progenitor proliferation by stabilizing the basal process of radial neuroepithelial progenitors.
“GPR56 likely influences progenitor proliferation by stabilizing the basal process of radial neuroepithelial progenitors”
From Evolutionarily Dynamic Alternative Splicing of <i>GPR56</i> Regulates Regional Cerebral Cortical Patterning (2014) · cites this paper as [22]
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Neurotrophin-regulated signalling pathways
Reichardt, L. F. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1894 · Cited by 2,195 · see citing works
The cell biology of neurogenesis
Götz, M., & Huttner, W. B. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1739 · Cited by 2,130 · see citing works
Neurons derived from radial glial cells establish radial units in neocortex
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., & Kriegstein, A. R. (2001) · Nature · doi:10.1038/35055553 · Cited by 2,016 · see citing works
Frisch, S. M., & Ruoslahti, E. I. (1997) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(97)80124-x · Cited by 1,153 · see citing works
Asymmetric Inheritance of Radial Glial Fibers by Cortical Neurons
Miyata, T., Kawaguchi, A., Okano, H., & Ogawa, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00420-2 · Cited by 892 · see citing works
Pöschl, E., Schlötzer-Schrehardt, U. M., Brachvogel, B., Saito, K., Ninomiya, Y., & Mayer, U. (2004) · Development · doi:10.1242/dev.01037 · Cited by 816 · see citing works
Post-translational disruption of dystroglycan–ligand interactions in congenital muscular dystrophies
Michele, D. E., Barresi, R., Kanagawa, M., Saito, F., Cohn, R. D., Satz, J. S., Dollar, J., Nishino, I., Kelley, R. I., Somer, H., et al. (2002) · Nature · doi:10.1038/nature00837 · Cited by 779 · see citing works
LAMININ FUNCTIONS IN TISSUE MORPHOGENESIS
Miner, J. H., & Yurchenco, P. D. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.094555 · Cited by 756 · see citing works
Radial Glial Identity Is Promoted by Notch1 Signaling in the Murine Forebrain
Gaiano, N., Nye, J. S., & Fishell, G. (2000) · Neuron · doi:10.1016/s0896-6273(00)81172-1 · Cited by 727 · see citing works
Perlecan Maintains the Integrity of Cartilage and Some Basement Membranes
Costell, M., Gustafsson, E., Aszódi, A., Mörgelin, M., Bloch, W., Hunziker, E. B., Addicks, K., Timpl, R., & Fässler, R. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.5.1109 · Cited by 672 · see citing works
Noctor, S. C., Flint, A. C., Weissman, T. A., Wong, W. S., Clinton, B. K., & Kriegstein, A. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-08-03161.2002 · Cited by 623 · see citing works
Expression and Function of Laminins in the Embryonic and Mature Vasculature
Hallmann, R., Horn, N., Selg, M., Wendler, O., Pausch, F., & Sorokin, L. M. (2005) · Physiological Reviews · doi:10.1152/physrev.00014.2004 · Cited by 575 · see citing works
Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy
Moore, S. A., Saito, F., Chen, J., Michele, D. E., Henry, M. D., Messing, A., Cohn, R. D., Ross, S. E., Westra, S., Williamson, R. A., et al. (2002) · Nature · doi:10.1038/nature00838 · Cited by 574 · see citing works
Graus-Porta, D., Blaess, S., Senften, M., Littlewood-Evans, A., Damsky, C. H., Huang, Z., Orban, P. C., Klein, R., Schittny, J. C., & Müller, U. (2001) · Neuron · doi:10.1016/s0896-6273(01)00374-9 · Cited by 559 · see citing works
Miner, J. H., Cunningham, J. M., & Sanes, J. R. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.6.1713 · Cited by 491 · see citing works
Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling
Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T., & Ghosh, A. (2002) · Development · doi:10.1242/dev.129.13.3147 · Cited by 361 · see citing works
Hand, R., Bortone, D. S., Mattar, P. A., Nguyen, L., Heng, J. I., Guerrier, S., Boutt, E., Peters, E. C., Barnes, A. P., Parras, C. M., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.032 · Cited by 350 · see citing works
Campos, L. S., Leone, D. P., Relvas, J. B., Brakebusch, C., Fässler, R., Suter, U., & ffrench‐Constant, C. (2004) · Development · doi:10.1242/dev.01199 · Cited by 313 · see citing works
Beggs, H. E., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K., Gorski, J. A., Jones, K. R., Sretavan, D. W., & Reichardt, L. F. (2003) · Neuron · doi:10.1016/s0896-6273(03)00666-4 · Cited by 305 · see citing works
Essential role of α6 integrins in cortical and retinal lamination
Georges‐Labouesse, E., Mark, M. P., Messaddeq, N., & Gansmüller, A. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70402-6 · Cited by 304 · see citing works
Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain gene to dy locus.
Sunada, Y., Bernier, S. M., Kozak, C. A., Yamada, Y., & Campbell, K. P. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36704-2 · Cited by 293 · see citing works
A Critical Function of the Pial Basement Membrane in Cortical Histogenesis
Halfter, W. M., Dong, S., Yip, Y.-P., Willem, M., & Mayer, U. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-14-06029.2002 · Cited by 290 · see citing works
Ephrin signalling controls brain size by regulating apoptosis of neural progenitors
Depaepe, V., Gonzalez, N. S., Dufour, A., Passante, L., Gorski, J. A., Jones, K. R., Ledent, C. A., & Vanderhaeghen, P. (2005) · Nature · doi:10.1038/nature03651 · Cited by 284 · see citing works
Radial glial cell heterogeneity—The source of diverse progeny in the CNS
Pinto, L., & GOTZ, M. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.02.010 · Cited by 259 · see citing works
Defective muscle basement membrane and lack of M-laminin in the dystrophic dy/dy mouse.
Xu, H. W., Christmas, P., Wu, X., Wewer, U. M., & Engvall, E. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.12.5572 · Cited by 252 · see citing works
Reelin signaling directly affects radial glia morphology and biochemical maturation
Hartfuss, E., Förster, E., Bock, H. H., Hack, M. A., Leprince, P., Luque, J. M., Herz, J., Frotscher, M., & Götz, M. (2003) · Development · doi:10.1242/dev.00654 · Cited by 237 · see citing works
Arcangelis, A. D., Mark, M. P., Kreidberg, J. A., Sorokin, L. M., & Georges‐Labouesse, E. (1999) · Development · doi:10.1242/dev.126.17.3957 · Cited by 231 · see citing works
Neurons from radial glia: the consequences of asymmetric inheritance
Fishell, G., & Kriegstein, A. R. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00013-8 · Cited by 224 · see citing works
Yoon, K., Koo, B., Im, S.-K., Jeong, H., Ghim, J., Kwon, M.-C., Moon, J.-S., Miyata, T., & Kong, Y. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.018 · Cited by 198 · see citing works
Properly formed but improperly localized synaptic specializations in the absence of laminin α4
Patton, B. L., Cunningham, J. M., Thyboll, J., Kortesmaa, J., Westerblad, H., Edström, L., Tryggvason, K., & Sanes, J. R. (2001) · Nature Neuroscience · doi:10.1038/88414 · Cited by 187 · see citing works
Self-citationCoordinate control of axon defasciculation and myelination by laminin-2 and -8
Yang, D., Bierman, J., Tarumi, Y. S., Zhong, Y.-P., Rangwala, R. A., Proctor, T. M., Miyagoe‐Suzuki, Y., Takeda, S., Miner, J. H., Sherman, L. S., et al. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200411158 · Cited by 171 · see citing works
Self-citationHunter, K. E., & Hatten, M. E. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.6.2061 · Cited by 167 · see citing works
Regulation of neural progenitor proliferation and survival by β1 integrins
Leone, D. P., Relvas, J. B., Campos, L. S., Hemmi, S., Brakebusch, C., Fässler, R., ffrench‐Constant, C., & Suter, U. (2005) · Journal of Cell Science · doi:10.1242/jcs.02396 · Cited by 163 · see citing works
Supèr, H. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.6.602 · Cited by 160 · see citing works
Haubst, N., Georges‐Labouesse, E., Arcangelis, A. D., Mayer, U., & Götz, M. (2006) · Development · doi:10.1242/dev.02486 · Cited by 157 · see citing works
Sievers, J., Pehlemann, F. W., Gude, S., & Berry, M. (1994) · Journal of Neurocytology · doi:10.1007/bf01183867 · Cited by 153 · see citing works
Action in the axon: generation and transport of signaling endosomes
Cosker, K., Courchesne, S. L., & Segal, R. A. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.08.005 · Cited by 149 · see citing works
Belvindrah, R., Graus-Porta, D., Goebbels, S., Nave, K., & Müller, U. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4494-07.2007 · Cited by 147 · see citing works
Self-citationBauer, H., Bauer, H. C., Lametschwandtner, A., Amberger, A., Ruiz, P., & Steiner, M. (1993) · Developmental Brain Research · doi:10.1016/0165-3806(93)90031-5 · Cited by 136 · see citing works
Soriano, E., Alvarado‐Mallart, R. M., Dumesnil, N., del Rı́o, J. A., & Sotelo, C. (1997) · Neuron · doi:10.1016/s0896-6273(00)80298-6 · Cited by 132 · see citing works
β1-Integrins Are Critical for Cerebellar Granule Cell Precursor Proliferation
Blaess, S., Graus-Porta, D., Belvindrah, R., Radakovits, R., Pons, S., Littlewood-Evans, A., Senften, M., Guo, H., Li, Y., Miner, J. H., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5241-03.2004 · Cited by 130 · see citing works
Self-citationNiewmierzycka, A., Mills, J., St‐Arnaud, R., Dedhar, S., & Reichardt, L. F. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1695-05.2005 · Cited by 115 · see citing works
Developmental morphology of the subarachnoid space and contiguous structures in the mouse
McLone, D. G., & Bondareff, W. (1975) · American Journal of Anatomy · doi:10.1002/aja.1001420302 · Cited by 104 · see citing works
Perlecan controls neurogenesis in the developing telencephalon
Girós, A., Morante, J., Gil, C., Fairén, A., & Costell, M. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-29 · Cited by 101 · see citing works
Doeberitz, C. V. K., Sievers, J., Sadler, M., Pehlemann, F. W., Berry, M., & Halliwell, P. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90256-3 · Cited by 66 · see citing works
Meningeal cells influence cerebellar development over a critical period
Sievers, J., Doeberitz, C. V. K., Pehlemann, F. W., & Berry, M. (1986) · Anatomy and Embryology · doi:10.1007/bf00315459 · Cited by 64 · see citing works
Hartmann, D., Sievers, J., Pehlemann, F. W., & Berry, M. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903200103 · Cited by 63 · see citing works
Pehlemann, F.-W., Sievers, J., & Berry, M. (1985) · Developmental Biology · doi:10.1016/0012-1606(85)90071-5 · Cited by 58 · see citing works
Supèr, H., Martı́nez, A., & Soriano, E. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(96)00155-1 · Cited by 49 · see citing works
Influence of meningeal cells on the proliferation and maturation of rat neuroblasts in culture
Gensburger, C., Labourdette, G., & Sensenbrenner, M. (1986) · Experimental Brain Research · doi:10.1007/bf00236849 · Cited by 45 · see citing works
Sievers, J., Pehlemann, F. W., Baumgarten, H., & Berry, M. (1985) · Developmental Biology · doi:10.1016/0012-1606(85)90070-3 · Cited by 35 · see citing works
Hartfuss, E., Förster, E., Bock, H. H., Hack, M. A., Leprince, P., Luque, I. M., Herz, J., Frotscher, M., & Götz, M. (2003) · Cited by 31 · see citing works
Influence of Meningeal Cells on the Proliferation of Neuroblasts in Culture
Barakat, I., Wittendorp, E., Rechenmann, R. V., & Sensenbrenner, M. (2007) · Developmental Neuroscience · doi:10.1159/000112776 · Cited by 28 · see citing works
Reelin signaling directly affects radial glia morphology and biochemical maturation
(2003) · Development · doi:10.1242/dev.130.21.5291 · Cited by 11 · see citing works
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A developmental and genetic classification for malformations of cortical development: update 2012
Barkovich, A. J., Guerrini, R., Kuzniecky, R., Jackson, G. D., & Dobyns, W. B. (2012) · Brain · doi:10.1093/brain/aws019 · Cited by 1,110 · see citing works
OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling
Fietz, S. A., Kelava, I., Vogt, J., Wilsch-Bräuninger, M., Stenzel, D., Fish, J. L., Corbeil, D., Riehn, A., Distler, W., Nitsch, R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2553 · Cited by 830 · see citing works
Extracellular Matrix: Functions in the Nervous System
Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506 · see citing works
Self-citationNeurogenesis during development of the vertebrate central nervous system
Paridaen, J. T. M. L., & Huttner, W. Β. (2014) · EMBO Reports · doi:10.1002/embr.201438447 · Cited by 390 · see citing works
Cortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective
Fietz, S. A., & Huttner, W. Β. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.10.002 · Cited by 267 · see citing works
How the extracellular matrix shapes neural development
Long, K. R., & Huttner, W. Β. (2019) · Open Biology · doi:10.1098/rsob.180216 · Cited by 263 · see citing works
Bae, B.-I., Tietjen, I., Atabay, K. D., Evrony, G. D., Johnson, M. B., Asare, E., Wang, P. P., Murayama, A. Y., Im, K., Lisgo, S. N., et al. (2014) · Science · doi:10.1126/science.1244392 · Cited by 229 · see citing works
Shaping Our Minds: Stem and Progenitor Cell Diversity in the Mammalian Neocortex
Franco, S. J., & Müller, U. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.022 · Cited by 219 · see citing works
Neurogenesis at the Brain–Cerebrospinal Fluid Interface
Lehtinen, M. K., & Walsh, C. A. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154026 · Cited by 213 · see citing works
Pathogenic DDX3X Mutations Impair RNA Metabolism and Neurogenesis during Fetal Cortical Development
Lennox, A. L., Hoye, M. L., Jiang, R., Johnson-Kerner, B., Suit, L., Venkataramanan, S., Sheehan, C. J., Alsina, F. C., Fregeau, B., Aldinger, K. A., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.01.042 · Cited by 205 · see citing works
It Takes a Village: Constructing the Neurogenic Niche
Bjornsson, C. S., Apostolopoulou, M., Tian, Y. I., & Temple, S. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.010 · Cited by 210 · see citing works
The cerebrospinal fluid: regulator of neurogenesis, behavior, and beyond
Zappaterra, M., & Lehtinen, M. K. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-0957-x · Cited by 182 · see citing works
A Radial Glia-Specific Role of RhoA in Double Cortex Formation
Cappello, S., Böhringer, C., Bergami, M., Conzelmann, K., Ghanem, A., Tomassy, G. S., Arlotta, P., Mainardi, M., Allegra, M., Caleo, M., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.030 · Cited by 171 · see citing works
Segarra, M., Aburto, M. R., Cop, F., Llaó-Cid, C., Härtl, R., Damm, M., Bethani, I., Parrilla, M., Husainie, D., Schänzer, A., et al. (2018) · Science · doi:10.1126/science.aao2861 · Cited by 162 · see citing works
Kalebic, N., Gilardi, C., Stepien, B. K., Wilsch‐Bräuninger, M., Long, K. R., Namba, T., Florio, M., Langen, B., Lombardot, B., Shevchenko, A., et al. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.02.017 · Cited by 152 · see citing works
Adhesion molecules in the stem cell niche – more than just staying in shape?
Marthiens, V., Kazanis, I., Moss, L., Long, K. R., & ffrench‐Constant, C. (2010) · Journal of Cell Science · doi:10.1242/jcs.054312 · Cited by 155 · see citing works
Distinct Functions of Glial and Neuronal Dystroglycan in the Developing and Adult Mouse Brain
Satz, J. S., Ostendorf, A. P., Hou, S., Turner, A., Kusano, H., Lee, J. C., Turk, R., Nguyen, H. T., Ross, S. E., Westra, S., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3247-10.2010 · Cited by 158 · see citing works
Endogenous microglia regulate development of embryonic cortical precursor cells
Antony, J. M., Paquin, A., Nutt, S. L., Kaplan, D. R., & Miller, F. D. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22533 · Cited by 157 · see citing works
Cytomegalovirus-Induced Brain Malformations in Fetuses
Teissier, N., Fallet‐Bianco, C., Delezoide, A., Laquerrière, A., Marcorelles, P., Khung‐Savatovsky, S., Nardelli, J., Cipriani, S., Csaba, Z., Picone, O., et al. (2014) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000038 · Cited by 155 · see citing works
We have got you ‘covered’: how the meninges control brain development
Siegenthaler, J. A., & Pleasure, S. J. (2011) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2010.12.005 · Cited by 145 · see citing works
Dynamic mRNA Transport and Local Translation in Radial Glial Progenitors of the Developing Brain
Pilaz, L., Lennox, A. L., Rouanet, J. P., & Silver, D. L. (2016) · Current Biology · doi:10.1016/j.cub.2016.10.040 · Cited by 144 · see citing works
Meninges: from protective membrane to stem cell niche.
Decimo, I., Fumagalli, G. F., Berton, V., Krampera, M., & Bifari, F. (2012) · Europe PMC (PubMed Central) · Cited by 135 · see citing works
Extracellular matrix and the neural stem cell niche
Kazanis, I., & ffrench‐Constant, C. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20970 · Cited by 124 · see citing works
Cell migration promotes dynamic cellular interactions to control cerebral cortex morphogenesis
Silva, C. G., Peyre, E., & Nguyen, L. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0148-y · Cited by 117 · see citing works
Polymicrogyria: pathology, fetal origins and mechanisms
Squier, W., & Jansen, A. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0080-3 · Cited by 122 · see citing works
Cerebral cortex development: an outside‐in perspective
Agirman, G., Broix, L., & Nguyen, L. (2017) · FEBS Letters · doi:10.1002/1873-3468.12924 · Cited by 120 · see citing works
Franco, S. J., & Müller, U. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20946 · Cited by 117 · see citing works
Hashimoto‐Torii, K., Torii, M., Fujimoto, M., Nakai, A., Fatimy, R. E., Mezger, V., Ju, M. J., Ishii, S., Chao, S.-H., Brennand, K., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.002 · Cited by 118 · see citing works
The extracellular matrix compartment of neural stem and glial progenitor cells
Faissner, A., & Reinhard, J. (2015) · Glia · doi:10.1002/glia.22839 · Cited by 114 · see citing works
Decimo, I., Bifari, F., Rodríguez, F. J., Malpeli, G., Dolci, S., Lavarini, V., Pretto, S., Vásquez, S., Sciancalepore, M., Montalbano, A., et al. (2011) · Stem Cells · doi:10.1002/stem.766 · Cited by 117 · see citing works
Integrin αvβ3 and thyroid hormones promote expansion of progenitors in embryonic neocortex
Stenzel, D., Wilsch‐Bräuninger, M., Wong, F. K., Heuer, H., & Huttner, W. Β. (2014) · Development · doi:10.1242/dev.101907 · Cited by 115 · see citing works
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Canonical and non-canonical Reelin signaling
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Genes and Mechanisms Involved in the Generation and Amplification of Basal Radial Glial Cells
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Self-citationGlia unglued: How signals from the extracellular matrix regulate the development of myelinating glia
Colognato, H., & Tzvetanova, I. D. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20966 · Cited by 90 · see citing works
3D culture of murine neural stem cells on decellularized mouse brain sections
Waele, J. D., Reekmans, K., Daans, J., Goossens, H., Berneman, Z. N., & Ponsaerts, P. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.11.025 · Cited by 92 · see citing works
Segklia, A., Seuntjens, E., Elkouris, M., Tsalavos, S., Stappers, E., Mitsiadis, T. A., Huylebroeck, D., Remboutsika, E., & Graf, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034088 · Cited by 88 · see citing works
The histopathology of polymicrogyria: a series of 71 brain autopsy studies
Jansen, A., Robitaille, Y., Honavar, M., Mullatti, N., Leventer, R. J., Andermann, E., Andermann, F., & Squier, W. (2015) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.12840 · Cited by 86 · see citing works
Lei, W., Xing, S., Deng, C.-Y., Ju, X.-C., Jiang, X., & Luo, Z. (2012) · Cell Research · doi:10.1038/cr.2012.40 · Cited by 86 · see citing works
Neurogenesis in Neurodegenerative Diseases: Role of MFG-E8
Cheyuo, C., Aziz, M., & Wang, P. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00569 · Cited by 75 · see citing works
The regulation of cortical neurogenesis
Villalba, A., Götz, M., & Borrell, V. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.10.003 · Cited by 74 · see citing works
Laminin α1 is essential for mouse cerebellar development
Ichikawa‐Tomikawa, N., Ogawa, J., Douet, V., Xu, Z., Kamikubo, Y., Sakurai, T., Kohsaka, S., Chiba, H., Hattori, N., Yamada, Y., et al. (2011) · Matrix Biology · doi:10.1016/j.matbio.2011.09.002 · Cited by 72 · see citing works
Long, K. R., Moss, L., Laursen, L. S., Boulter, L., & ffrench‐Constant, C. (2016) · Nature Communications · doi:10.1038/ncomms10354 · Cited by 69 · see citing works
Ulhaq, Z. S., & Kishida, M. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00230 · Cited by 69 · see citing works
Ferent, J., Zaidi, D., & Francis, F. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.578341 · Cited by 64 · see citing works
TGF-β1 promotes cerebral cortex radial glia-astrocyte differentiation in vivo
Stipursky, J., Francis, D., Dezonne, R. S., de AraÃojo, A. P. B., Souza, L., Moraes, C. A., & Gomes, F. C. A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00393 · Cited by 62 · see citing works
Foxc1 dependent mesenchymal signalling drives embryonic cerebellar growth
Haldipur, P., Gillies, G. S., Janson, O. K., Chizhikov, V. V., Mithal, D. S., Miller, R. J., & Millen, K. J. (2014) · eLife · doi:10.7554/elife.03962 · Cited by 62 · see citing works
The Extracellular Matrix in the Evolution of Cortical Development and Folding
Amin, S., & Borrell, V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.604448 · Cited by 58 · see citing works
Regulation of the neural stem cell compartment by extracellular matrix constituents
Theocharidis, U., Long, K. R., ffrench‐Constant, C., & Faissner, A. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63486-3.00001-3 · Cited by 57 · see citing works
Long, K. R., & Huttner, W. Β. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.804649 · Cited by 57 · see citing works
Cell fate control in the developing central nervous system
Guérout, N., Li, X., & Barnabé‐Heider, F. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.10.003 · Cited by 52 · see citing works
Morphological and functional aspects of progenitors perturbed in cortical malformations
Bizzotto, S., & Francis, F. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00030 · Cited by 52 · see citing works
Meningeal and choroid plexus cells—Novel drug targets for CNS disorders
Dragunow, M. (2013) · Brain Research · doi:10.1016/j.brainres.2013.01.013 · Cited by 50 · see citing works
Meninges harbor cells expressing neural precursor markers during development and adulthood
Bifari, F., Berton, V., Pino, A., Kusalo, M., Malpeli, G., Chio, M. D., Bersan, E., Amato, E., Scarpa, A., Krampera, M., et al. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00383 · Cited by 50 · see citing works
Marchetti, G., Escuin, S., van der Flier, A., Arcangelis, A. D., Hynes, R. O., & Georges‐Labouesse, E. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07072.x · Cited by 50 · see citing works
Meninges: A Widespread Niche of Neural Progenitors for the Brain
Decimo, I., Dolci, S., Panuccio, G., Riva, M., Fumagalli, G. F., & Bifari, F. (2020) · The Neuroscientist · doi:10.1177/1073858420954826 · Cited by 45 · see citing works
β1‐integrin restricts astrocytic differentiation of adult hippocampal neural stem cells
Brooker, S. M., Bond, A. M., Peng, C., & Kessler, J. A. (2016) · Glia · doi:10.1002/glia.22996 · Cited by 43 · see citing works
Vascular Regulation of Developmental Neurogenesis
Vogenstahl, J., Parrilla, M., Acker‐Palmer, A., & Segarra, M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.890852 · Cited by 40 · see citing works
Radial glial cell: Critical functions and new perspective as a steroid synthetic cell
Xing, L., Goswami, M., & Trudeau, V. L. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.03.010 · Cited by 40 · see citing works
Gorter, R. P., & Baron, W. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.134980 · Cited by 35 · see citing works
Brunken, W. J., Varshney, S., & Hunter, D. (2015) · Journal of Ophthalmic and Vision Research · doi:10.4103/2008-322x.170354 · Cited by 35 · see citing works
Pilaz, L., Liu, J., Joshi, K., Tsunekawa, Y., Musso, C. M., D’Arcy, B. R., Suzuki, I., Alsina, F. C., Pratiksha, K. C., Sethi, S., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.02.023 · Cited by 33 · see citing works
Progenitor genealogy in the developing cerebral cortex
Laguesse, S., Peyre, E., & Nguyen, L. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-1979-5 · Cited by 33 · see citing works
Pilaz, L., & Silver, D. L. (2017) · FEBS Letters · doi:10.1002/1873-3468.12626 · Cited by 32 · see citing works
Mithal, D. S., Ren, D., & Miller, R. J. (2013) · Glia · doi:10.1002/glia.22515 · Cited by 31 · see citing works
Abnormal development of the human cerebral cortex
Squier, W., & Jansen, A. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01288.x · Cited by 31 · see citing works
Cell Polarity and Neurogenesis in Embryonic Stem Cell-Derived Neural Rosettes
Banda, E. C., McKinsey, A. G., Germain, N. D., Carter, J., Anderson, N. C., & Grabel, L. B. (2014) · Stem Cells and Development · doi:10.1089/scd.2014.0415 · Cited by 33 · see citing works
The role of integrins in brain health and neurodegenerative diseases
Cui, Y., Rõlova, T., & Fagerholm, S. C. (2024) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2024.151441 · Cited by 30 · see citing works
Tsunekawa, Y., Kikkawa, T., & Osumi, N. (2014) · Development Growth & Differentiation · doi:10.1111/dgd.12135 · Cited by 30 · see citing works
Fukutin-Related Protein Alters the Deposition of Laminin in the Eye and Brain
Ackroyd, M. R., Whitmore, C. L., Prior, S., Kaluarachchi, M. R., Nikolić, M., Mayer, U., Francesco Muntoni, A., & Brown, S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2301-11.2011 · Cited by 28 · see citing works
Astrocytes in rare neurological conditions: Morphological and functional considerations
Ravi, K., Paidas, M. J., Saad, A. G., & Jayakumar, A. R. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25118 · Cited by 27 · see citing works
Shah, B., Lutter, D., Bochenek, M. L., Kato, K., Tsytsyura, Y., Glyvuk, N., Sakakibara, A., Klingauf, J., Adams, R. H., & Püschel, A. W. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154174 · Cited by 27 · see citing works
Meninges-derived cues control axon guidance
Suter, T. A. C. S., DeLoughery, Z. J., & Jaworski, A. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.08.005 · Cited by 27 · see citing works
Shaping the cerebral cortex by cellular crosstalk
Stoufflet, J., Tielens, S., & Nguyen, L. (2023) · Cell · doi:10.1016/j.cell.2023.05.040 · Cited by 25 · see citing works
van Diepen, L., Buettner, F. F. R., Hoffmann, D., Thiesler, C. T., Halbach, O. V. B. U., Halbach, V. V. B. U., Jensen, L. R., Steinemann, D., Edvardson, S., Elpeleg, O. N., et al. (2018) · European Journal of Human Genetics · doi:10.1038/s41431-018-0220-5 · Cited by 24 · see citing works
Meyerink, B. L., Tiwari, N. K., & Pilaz, L. (2020) · Cells · doi:10.3390/cells10010003 · Cited by 23 · see citing works
Neural Progenitor Cells Survival and Neuronal Differentiation in Peptide-Based Hydrogels
Song, Y., Li, Y., Zheng, Q., Wu, K., Guo, X., Wu, Y., Yin, M., Wu, Q. H., & Fu, X. (2010) · Journal of Biomaterials Science Polymer Edition · doi:10.1163/092050610x487756 · Cited by 23 · see citing works
Kridsada, K., Niu, J., Haldipur, P., Wang, Z., Ding, L., Li, J. J., Lindgren, A., Herrera, E., Thomas, G. M., Chizhikov, V. V., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.025 · Cited by 18 · see citing works
Fonte, D. F. D., Xing, L., Mikwar, M., & Trudeau, V. L. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.04.014 · Cited by 17 · see citing works
The development and origins of vertebrate meninges
Batarfi, M. A., Valášek, P., Krejčí, E., Huang, R., & Patel, K. (2017) · Biological Communications · doi:10.21638/11701/spbu03.2017.203 · Cited by 17 · see citing works
Indirect neurogenesis in space and time
Thor, S. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00833-x · Cited by 16 · see citing works
Fstl1 is involved in the regulation of radial glial scaffold development
Liu, R., Yang, Y., Shen, J., Chen, H., Zhang, Q., Ba, R., Wei, Y., Li, K., Zhang, X., & Zhao, C. (2015) · Molecular Brain · doi:10.1186/s13041-015-0144-8 · Cited by 16 · see citing works
New spin on an old transition: epithelial parallels in neuronal adhesion control
Famulski, J. K., & Solecki, D. J. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.10.002 · Cited by 15 · see citing works
McGowan, L. D., Alaama, R. A., Freise, A. C., Huang, J. C., Charvet, C. J., & Striedter, G. F. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201875109 · Cited by 15 · see citing works
Tsukada, T., Sakata‐Haga, H., Shimada, H., Shoji, H., & Hatta, T. (2021) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2021.07.003 · Cited by 14 · see citing works
Non-muscle myosins control radial glial basal endfeet to mediate interneuron organization
D’Arcy, B. R., Lennox, A. L., Musso, C. M., Bracher, A., Escobar-Tomlienovich, C. F., Perez-Sanchez, S., & Silver, D. L. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3001926 · Cited by 14 · see citing works
Glotzbach, K., Stamm, N., Weberskirch, R., & Faissner, A. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00475 · Cited by 13 · see citing works
The Control of Cortical Folding: Multiple Mechanisms, Multiple Models
Moffat, A., & Schuurmans, C. J. (2023) · The Neuroscientist · doi:10.1177/10738584231190839 · Cited by 12 · see citing works
Homemade: building the structure of the neurogenic niche
Valamparamban, G. F., & Spéder, P. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1275963 · Cited by 13 · see citing works
Regulation of Cell Delamination During Cortical Neurodevelopment and Implication for Brain Disorders
Sokpor, G., Brand‐Saberi, B., Nguyen, H. P., & Tuoc, T. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.824802 · Cited by 12 · see citing works
Pilaz, L., Joshi, K., Liu, J., Tsunekawa, Y., Alsina, F. C., Sethi, S., Suzuki, I., Vanderhaeghen, P., Polleux, F., & Silver, D. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.30.229724 · Cited by 12 · see citing works
Bioengineering innovations for neural organoids with enhanced fidelity and function
Sun, Y., Ikeuchi, Y., Guo, F., Hyun, I., Ming, G., & Fu, J. (2025) · Cell stem cell · doi:10.1016/j.stem.2025.03.014 · Cited by 14 · see citing works
100 plus years of stem cell research—20 years of ISSCR
Lendahl, U. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.04.004 · Cited by 14 · see citing works
Polylaminin recognition by retinal cells
Hochman‐Mendez, C., Menezes, J. R. L., Sholl‐Franco, A., & Coelho‐Sampaio, T. (2013) · Journal of Neuroscience Research · doi:10.1002/jnr.23298 · Cited by 11 · see citing works
Willis, C. M., & Crocker, S. J. (2016) · InTech eBooks · doi:10.5772/62706 · Cited by 11 · see citing works
McMurtrey, R. J. (2016) · Journal of Tissue Engineering · doi:10.1177/2041731416671926 · Cited by 13 · see citing works
In VivoAnalysis of the Neurovascular Niche in the DevelopingXenopusBrain
Lau, M., Li, J., & Cline, H. T. (2017) · eNeuro · doi:10.1523/eneuro.0030-17.2017 · Cited by 11 · see citing works
The roles of immune factors in neurodevelopment
Wang, C., He, T., Qin, J., Jiao, J., & Ji, F. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1451889 · Cited by 11 · see citing works
Radial glia progenitor polarity in health and disease
Viola, V., Chinnappa, K., & Francis, F. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1478283 · Cited by 10 · see citing works
Zander, M. A., Cancino, G. I., Gridley, T., Kaplan, D. R., & Miller, F. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104767 · Cited by 9 · see citing works
- Authors
- Radakovits, R., Barros, C. S., Belvindrah, R., Patton, B., & Muller, U.
- Affiliations
- Scripps Research Institute (US)
- Oregon Health & Science University (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-06-17
- Volume
- 29
- Issue
- 24
- Pages
- 7694-7705
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2738639
- OpenAlex
- W1977060481
- Cited by
- 135
- References
- 54
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 5 · 2023: 6 · 2022: 5 · 2021: 5 · 2020: 15 · 2019: 6 · 2018: 9 · 2017: 8 · 2016: 8 · 2015: 8 · 2014: 16 · 2013: 9 · 2012: 8
- FWCI
- 2.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- PEARL (University of Plymouth) (submittedVersion)
- Funders
- Christopher and Dana Reeve Foundation
- California Institute of Regenerative Medicine
- National Institutes of Health
- National Institute of Mental Health (MH078833, U01MH078833)
- National Institute of Neurological Disorders and Stroke (NS046456, R01NS046456)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- radial glia, beta1 integrin, apoptosis, laminin alpha 2, laminin α4, cortical development, neuronal migration, glial progenitors
- MeSH terms
- PAX6 Transcription Factor, Animals, Animals, Newborn, Bromodeoxyuridine, Cell Differentiation, Cell Survival, Cerebral Cortex, Embryo, Mammalian, Eye Proteins, Intermediate Filament Proteins, Laminin, Meninges, Mice, Transgenic, Nerve Tissue Proteins, Neuroglia, Repressor Proteins, Stem Cells, Signal Transduction, Electroporation, Homeodomain Proteins, Gene Expression Regulation, Developmental, Integrin beta1, Integrases, In Situ Nick-End Labeling, Cell Proliferation, Green Fluorescent Proteins, Mice, Paired Box Transcription Factors, Neurogenesis, Nestin, In Vitro Techniques
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