Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex
Open accessAbstract
Projection neurons migrate from the ventricular zone to the neocortical plate during the development of the mouse brain. Their overall movement is radial, but they become multipolar and move nonradially in the intermediate zone. Here we show that Reelin, the Rap1 GTPase and N-cadherin (NCad) are important for multipolar neurons to polarize their migration toward the cortical plate. Inhibition and rescue experiments indicated that Reelin regulates migration through Rap1 and Akt, and that the Rap1-regulated GTPases RalA, RalB, Rac1 and Cdc42 are also involved. We found that Rap1 regulated the plasma membrane localization of NCad and NCad rescued radial polarization when Rap1 was inhibited. However, inhibition of Rap1 or NCad had little effect on glia-dependent locomotion. We propose a multistep mechanism in which Reelin activates Rap1, Rap1 upregulates NCad, and NCad is needed to orient cell migration.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Crk family proteins are important downstream components of Reelin signaling in the regulation of neocortical lamination and postnatal hippocampal dendritogenesis.
“Crk family proteins are also important downstream components of the Reelin signaling pathway in the regulation of both neocortical lamination and postnatal hippocampal dendritogenesis (12, 13) (Fig. 1E).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [13]
Independent of PI3K, Reelin stabilizes actin by triggering C3G activation of Rap1 through Crk family proteins.
“independent of PI3K, Reelin stabilizes actin by triggering C3G activation of Rap1 through Crk family proteins (Crk), which is essential for normal neocortical lamination and postnatal hippocampal dendritogenesis (12, 13).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [13]
C3G activation of Rap1 through Crk family proteins is essential for normal neocortical lamination and postnatal hippocampal dendritogenesis.
“independent of PI3K, Reelin stabilizes actin by triggering C3G activation of Rap1 through Crk family proteins (Crk), which is essential for normal neocortical lamination and postnatal hippocampal dendritogenesis (12, 13).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [13]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Cell Adhesion: The Molecular Basis of Tissue Architecture and Morphogenesis
Gumbiner, B. M. (1996) · Cell · doi:10.1016/s0092-8674(00)81279-9 · Cited by 3,471 · see citing works
Cadherin Cell Adhesion Receptors as a Morphogenetic Regulator
Takeichi, M. (1991) · Science · doi:10.1126/science.2006419 · Cited by 3,283 · see citing works
Noctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229 · see citing works
Ogawa, M., Miyata, T., Nakajimat, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., & Mikoshibat, K. (1995) · Neuron · doi:10.1016/0896-6273(95)90329-1 · Cited by 889 · see citing works
A core function for p120-catenin in cadherin turnover
Davis, M. A., Ireton, R. C., & Reynolds, A. B. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200307111 · Cited by 733 · see citing works
Tabata, H., & Nakajima, K. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00016-1 · Cited by 705 · see citing works
Two modes of radial migration in early development of the cerebral cortex
Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R., & Pearlman, A. L. (2001) · Nature Neuroscience · doi:10.1038/83967 · Cited by 689 · see citing works
Nectin and afadin: novel organizers of intercellular junctions
Takai, Y., & Nakanishi, H. (2002) · Journal of Cell Science · doi:10.1242/jcs.00167 · Cited by 602 · see citing works
Gap junction adhesion is necessary for radial migration in the neocortex
Elias, L., Wang, D. D., & Kriegstein, A. R. (2007) · Nature · doi:10.1038/nature06063 · Cited by 587 · see citing works
Multipolar Migration: The Third Mode of Radial Neuronal Migration in the Developing Cerebral Cortex
Tabata, H., & Nakajima, K. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-09996.2003 · Cited by 541 · see citing works
Grindstaff, K. K., Yeaman, C. A., Anandasabapathy, N., Hsu, S.-C., Rodriguez-Boulan, E. J., Scheller, R. H., & Nelson, W. J. (1998) · Cell · doi:10.1016/s0092-8674(00)81435-x · Cited by 527 · see citing works
Kuroda, S., Fukata, M., Nakagawa, M., Fujii, K., Nakamura, T., Ookubo, T., Izawa, I., Nagase, T., Nomura, N., Tani, H., et al. (1998) · Science · doi:10.1126/science.281.5378.832 · Cited by 499 · see citing works
The exocyst is a Ral effector complex
Moskalenko, S., Henry, D. O., Rosse, C., Mirey, G., Camonis, J. H., & White, M. A. (2002) · Nature Cell Biology · doi:10.1038/ncb728 · Cited by 423 · see citing works
Central Roles of Small GTPases in the Development of Cell Polarity in Yeast and Beyond
Park, H.-O., & Bi, E. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00028-06 · Cited by 421 · see citing works
Regulation of cell–cell adhesion by the cadherin–catenin complex
Nelson, W. J. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360149 · Cited by 411 · see citing works
Tsai, J., Chen, Y., Kriegstein, A. R., & Vallee, R. B. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200505166 · Cited by 401 · see citing works
The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity.
Schwamborn, J. C., & Püschel, A. W. (2004) · Nature Neuroscience · doi:10.1038/nn1295 · Cited by 385 · see citing works
Rice, D. S., Sheldon, M., D’Arcangelo, G., Nakajima, K., Goldowitz, D., & Curran, T. (1998) · Development · doi:10.1242/dev.125.18.3719 · Cited by 378 · see citing works
Franco, S. J., Martínez‐Garay, I., Gil, C., Harkins-Perry, S. R., & Müller, U. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.003 · Cited by 329 · see citing works
Kawauchi, T., Sekine, K., Shikanai, M., Chihama, K., Tomita, K., Kubo, K., Nakajima, K., Nabeshima, Y.-I., & Hoshino, M. (2010) · Neuron · doi:10.1016/j.neuron.2010.07.007 · Cited by 328 · see citing works
Rap1: a key regulator in cell-cell junction formation
Kooistra, M. R. H., Dubé, N., & Bos, J. L. (2006) · Journal of Cell Science · doi:10.1242/jcs.03306 · Cited by 321 · see citing works
Reelin-mediated Signaling Locally Regulates Protein Kinase B/Akt and Glycogen Synthase Kinase 3β
Beffert, U., Morfini, G., Bock, H. H., Reyna, H., Brady, S. T., & Herz, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m209205200 · Cited by 306 · see citing works
N-cadherin mediates cortical organization in the mouse brain
Kadowaki, M., Nakamura, S., Machoň, O., Krauss, S. J. K., Radice, G. L., & Takeichi, M. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.12.014 · Cited by 298 · see citing works
Qin, Y., Capaldo, C., Gumbiner, B. M., & Macara, I. G. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200506094 · Cited by 285 · see citing works
Control of cell adhesion dynamics by Rap1 signaling
Boettner, B., & Aelst, L. V. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.06.004 · Cited by 270 · see citing works
Chen, X., Kojima, S.-I., Borisy, G. G., & Green, K. J. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200305137 · Cited by 259 · see citing works
Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors
Arthur, W. T., Quilliam, L. A., & Cooper, J. A. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200404068 · Cited by 252 · see citing works
Self-citationSemaphorin-3A guides radial migration of cortical neurons during development
Chen, G., Sima, J., Jin, M., Wang, K.-Y., Xue, X.-J., Zheng, W., Ding, Y., & Yuan, X. (2007) · Nature Neuroscience · doi:10.1038/nn2018 · Cited by 251 · see citing works
Molecular cloning of a GTPase activating protein specific for the Krev-1 protein p21rap1
Rubinfeld, B., Munemitsu, S. M., Clark, R., Conroy, L., Watt, K. W. K., Crosier, W. J., McCormick, F. P., & Polakis, P. G. (1991) · Cell · doi:10.1016/0092-8674(91)90555-d · Cited by 243 · see citing works
Jossin, Y., & Goffinet, A. M. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00928-07 · Cited by 235 · see citing works
Self-citationActivation of a Dab1/CrkL/C3G/Rap1 Pathway in Reelin-Stimulated Neurons
Ballif, B. A., Arnaud, L., Arthur, W. T., Guris, D. L., Imamoto, A., & Cooper, J. A. (2004) · Current Biology · doi:10.1016/j.cub.2004.03.038 · Cited by 208 · see citing works
Self-citationRap1 up-regulation and activation on plasma membrane regulates T cell adhesion
Bivona, T. G., Wiener, H. H., Ahearn, I. M., Silletti, J., Chiu, V. K., & Philips, M. R. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200311093 · Cited by 170 · see citing works
Zhang, J., Woodhead, G. J., Swaminathan, S. K., Noles, S. R., McQuinn, E. R., Pisarek-Horowitz, A., Stocker, A. M., Mutch, C. A., Funatsu, N., & Chenn, A. (2010) · Developmental Cell · doi:10.1016/j.devcel.2009.12.025 · Cited by 168 · see citing works
Regulation of Protein Tyrosine Kinase Signaling by Substrate Degradation during Brain Development
Arnaud, L., Ballif, B. A., & Cooper, J. A. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.24.9293-9302.2003 · Cited by 164 · see citing works
Self-citationInvasive cell migration is initiated by guided growth of long cellular extensions
Fulga, T. A., & Rørth, P. (2002) · Nature Cell Biology · doi:10.1038/ncb848 · Cited by 152 · 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
Jossin, Y., Gui, L., & Goffinet, A. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0023-07.2007 · Cited by 143 · see citing works
Self-citationCentrosome Motility Is Essential for Initial Axon Formation in the Neocortex
de Anda, F. C., Meletis, K., Ge, X., Rei, D., & Tsai, L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0381-10.2010 · Cited by 137 · see citing works
CORTICAL NEURONAL MIGRATION MUTANTS SUGGEST SEPARATE BUT INTERSECTING PATHWAYS
Bielas, S. L., Higginbotham, H., Koizumi, H., Tanaka, T., & Gleeson, J. G. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.082503.103047 · Cited by 133 · see citing works
Yang, X., Chrisman, H., & Weijer, C. J. (2008) · Development · doi:10.1242/dev.023416 · Cited by 107 · see citing works
An early development defect in the cerebral cortex of the reeler mouse
Goffinet, A. M. (1979) · Anatomy and Embryology · doi:10.1007/bf00305160 · Cited by 93 · see citing works
Cadherin-2 Controls Directional Chain Migration of Cerebellar Granule Neurons
Rieger, S., Senghaas, N., Walch, A. K., & Köster, R. W. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000240 · Cited by 87 · see citing works
Jossin, Y., Ogawa, M., Métin, C., Tissir, F., & Goffinet, A. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09953.2003 · Cited by 74 · see citing works
Self-citationSimó, S., Jossin, Y., & Cooper, J. A. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.0035-10.2010 · Cited by 72 · see citing works
Self-citationUchida, T., Baba, A., Pérez-Martínez, F. J., Hibi, T., Miyata, T., Luque, J. M., Nakajima, K., & Hattori, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0345-09.2009 · Cited by 67 · see citing works
Neuronal Migration and the Role of Reelin During Early Development of the Cerebral Cortex
Jossin, Y. (2004) · Molecular Neurobiology · doi:10.1385/mn:30:3:225 · Cited by 63 · see citing works
Self-citationRas Is Required for the Cyclic AMP-Dependent Activation of Rap1 via Epac2
Liu, C., Takahashi, M., Li, Y., Song, S., Dillon, T. J., Shinde, U. P., & Stork, P. A. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01060-08 · Cited by 62 · see citing works
Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain
Taniguchi, H., Kawauchi, D., Nishida, K., & Murakami, F. (2006) · Development · doi:10.1242/dev.02354 · Cited by 59 · see citing works
Morimura, T., & Ogawa, M. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.087 · Cited by 22 · see citing works
Comparison of slow and fast neocortical neuron migration using a new in vitromodel
Nichols, A. J., Carney, L. H., & Olson, E. C. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-50 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cho, A.-N., Jin, Y., An, Y., Kim, J., Choi, Y. S., Lee, J. S., Kim, J., Choi, W.-Y., Koo, D.-J., Yu, W., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24775-5 · Cited by 397 · see citing works
Cadherins and neuropsychiatric disorders
Redies, C., Hertel, N., & Hübner, C. A. (2012) · Brain Research · doi:10.1016/j.brainres.2012.06.020 · Cited by 257 · see citing works
Jossin, Y. (2020) · Biomolecules · doi:10.3390/biom10060964 · Cited by 208 · see citing works
Self-citationReelin and neuropsychiatric disorders
Ishii, K., Kubo, K.-I., & Nakajima, K. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00229 · Cited by 185 · see citing works
Sekine, K., Kawauchi, T., Kubo, K., Honda, T., Herz, J., Hattori, M., Kinashi, T., & Nakajima, K. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.020 · Cited by 180 · see citing works
Mechanisms of cell migration in the nervous system
Cooper, J. A. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201305021 · Cited by 168 · see citing works
Self-citationPioneering Axons Regulate Neuronal Polarization in the Developing Cerebral Cortex
Namba, T., Kibe, Y., Funahashi, Y., Nakamuta, S., Takano, T., Ueno, T., Shimada, A., Kozawa, S., Okamoto, M., Shimoda, Y., et al. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.015 · Cited by 164 · see citing works
Kawauchi, T. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms13044564 · Cited by 156 · see citing works
Integrative Mechanisms of Oriented Neuronal Migration in the Developing Brain
Evsyukova, I. Y., Plestant, C., & Anton, E. S. (2013) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101512-122400 · Cited by 143 · see citing works
Developmental disruptions underlying brain abnormalities in ciliopathies
Guo, J., Higginbotham, H., Li, J., Nichols, J., Hirt, J., Ghukasyan, V., & Anton, E. S. (2015) · Nature Communications · doi:10.1038/ncomms8857 · Cited by 140 · see citing works
New insights into Reelin-mediated signaling pathways
Lee, G. H., & D’Arcangelo, G. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00122 · Cited by 144 · see citing works
Gil, C., Franco, S. J., Martínez‐Garay, I., Espinosa, A., Harkins-Perry, S. R., & Müller, U. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.040 · Cited by 143 · see citing works
Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition–like mechanism
Itoh, Y., Moriyama, Y., Hasegawa, T., Endo, T. A., Toyoda, T., & Gotoh, Y. (2013) · Nature Neuroscience · doi:10.1038/nn.3336 · Cited by 142 · see citing works
FMRP regulates multipolar to bipolar transition affecting neuronal migration and cortical circuitry
Fata, G. L., Gärtner, A., Domıńguez-Iturza, N., Dresselaers, T., Dawitz, J., Poorthuis, R. B., Averna, M., Himmelreich, U., Meredith, R. M., Achsel, T., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3870 · Cited by 142 · see citing works
Takano, T., Xu, C., Funahashi, Y., Namba, T., & Kaibuchi, K. (2015) · Development · doi:10.1242/dev.114454 · Cited by 132 · see citing works
Genetics and mechanisms leading to human cortical malformations
Romero, D. M., Bahi‐Buisson, N., & Francis, F. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.031 · Cited by 126 · see citing works
Sekine, K., Kubo, K.-I., & Nakajima, K. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.06.004 · 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
Baek, S. T., Copeland, B. R., Yun, E.-J., Kwon, S., Guemez‐Gamboa, A., Schaffer, A. E., Kim, S., Kang, H., Song, S., Mathern, G. W., et al. (2015) · Nature Medicine · doi:10.1038/nm.3982 · Cited by 122 · see citing works
Reelin in the years: controlling neuronal migration and maturation in the mammalian brain
D'Arcangelo, G. (2014) · Advances in Neuroscience · doi:10.1155/2014/597395 · Cited by 120 · see citing works
Control of Neuronal Migration and Aggregation by Reelin Signaling in the Developing Cerebral Cortex
Hirota, Y., & Nakajima, K. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2017.00040 · Cited by 116 · see citing works
N‐cadherin specifies first asymmetry in developing neurons
Gärtner, A., Fornasiero, E. F., Munck, S., Vennekens, K., Seuntjens, E., Huttner, W. Β., Valtorta, F., & Dotti, C. G. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.41 · Cited by 113 · see citing works
Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses
Wasser, C. R., & Herz, J. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.766782 · Cited by 111 · see citing works
“natal hippocampal dendritogenesis (12, 13).”
BackgroundOhtaka‐Maruyama, C., & Okado, H. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00447 · Cited by 111 · see citing works
miR379–410 cluster miRNAs regulate neurogenesis and neuronal migration by fine‐tuning N‐cadherin
Rago, L., Beattie, R., Taylor, V., & Winter, J. (2014) · The EMBO Journal · doi:10.1002/embj.201386591 · Cited by 110 · see citing works
Canonical and non-canonical Reelin signaling
Bock, H. H., & May, P. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00166 · Cited by 107 · see citing works
Barnat, M., Friec, J. L., Benstaali, C., & Humbert, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.035 · Cited by 105 · see citing works
Bcl11a (Ctip1) Controls Migration of Cortical Projection Neurons through Regulation of Sema3c
Wiegreffe, C., Simon, R., Peschkes, K., Kling, C., Strehle, M., Cheng, J., Srivatsa, S., Liu, P., Jenkins, N. A., Copeland, N. G., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.023 · Cited by 100 · see citing works
Revisiting the Relationship Between Autism and Schizophrenia: Toward an Integrated Neurobiology
de Lacy, N., & King, B. H. (2013) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050212-185627 · Cited by 98 · see citing works
Extracellular and Intracellular Signaling for Neuronal Polarity
Namba, T., Funahashi, Y., Nakamuta, S., Xu, C., Takano, T., & Kaibuchi, K. (2015) · Physiological Reviews · doi:10.1152/physrev.00025.2014 · Cited by 101 · see citing works
Leeb, C., Eresheim, C., & Nimpf, J. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.529271 · Cited by 99 · see citing works
Molecules and mechanisms that regulate multipolar migration in the intermediate zone
Cooper, J. A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00386 · Cited by 97 · see citing works
Self-citationEstablishing Neuronal Polarity with Environmental and Intrinsic Mechanisms
Yogev, S., & Shen, K. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.021 · Cited by 96 · see citing works
FOXG1 Orchestrates Neocortical Organization and Cortico-Cortical Connections
Cargnin, F., Kwon, J.-S., Katzman, S. J., Chen, B., Lee, J. W., & Lee, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.016 · Cited by 91 · see citing works
A temporary compendium of thyroid hormone target genes in brain
Chatonnet, F., Flamant, F., & Morte, B. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.05.023 · Cited by 93 · see citing works
Motor neuron position and topographic order imposed by β- And γ-catenin activities
Demireva, E. Y., Shapiro, L. S., Jessell, T. M., & Zampieri, N. (2011) · Cell · doi:10.1016/j.cell.2011.09.037 · Cited by 85 · see citing works
Dab1 Is Required for Synaptic Plasticity and Associative Learning
Trotter, J. H., Lee, G. H., Kazdoba, T. M., Crowell, B., Domogauer, J., Mahoney, H. L., Franco, S. J., Müller, U., Weeber, E. J., & D’Arcangelo, G. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2010-13.2013 · Cited by 87 · see citing works
Ito, H., Fujita, K., Tagawa, K., Chen, X., Homma, H., Sasabe, T., Shimizu, J., Shimizu, S., Tamura, T., Muramatsu, S., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201404392 · Cited by 85 · see citing works
RAP1-mediated MEK/ERK pathway defects in Kabuki syndrome
Bögershausen, N., Tsai, I.-C., Pohl, E., Şimşek‐Kiper, P. Ö., Beleggia, F., Perçin, E. F., Keupp, K., Matchan, A., Milz, E., Alanay, Y., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci80102 · Cited by 86 · see citing works
Wnt Signaling Regulates Multipolar-to-Bipolar Transition of Migrating Neurons in the Cerebral Cortex
Boitard, M., Bocchi, R., Egervari, K., Petrenko, V., Viale, B., Gremaud, S., Zgraggen, E., Salmon, P., & Kiss, J. Z. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.061 · Cited by 83 · see citing works
Kawauchi, T. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00394 · Cited by 83 · see citing works
Kann, A. P., Hung, M., Wang, W., Nguyen, J., Gilbert, P. M., Wu, Z., & Krauss, R. S. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.04.016 · Cited by 78 · see citing works
Thyroid Hormones in the Brain and Their Impact in Recovery Mechanisms After Stroke
Talhada, D., Santos, C. R. A., Gonçalves, I., & Ruscher, K. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.01103 · Cited by 83 · see citing works
Regulation of Neuronal Migration by Dchs1-Fat4 Planar Cell Polarity
Zakaria, S., Mao, Y., Kuta, A., de Sousa, C. F., Gaufo, G. O., McNeill, H., Hindges, R., Guthrie, S., Irvine, K. D., & Francis‐West, P. H. (2014) · Current Biology · doi:10.1016/j.cub.2014.05.067 · Cited by 80 · see citing works
Sticky situations: recent advances in control of cell adhesion during neuronal migration
Solecki, D. J. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.04.010 · Cited by 77 · see citing works
Santana, J., & Marzolo, M. (2017) · Biochemical Journal · doi:10.1042/bcj20160628 · Cited by 74 · see citing works
Kohno, T., Honda, T., Kubo, K., Nakano, Y., Tsuchiya, A., Murakami, T., Banno, H., Nakajima, K., & Hattori, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4119-14.2015 · Cited by 76 · see citing works
Colorectal Cancer Cells Adhere to and Migrate Along the Neurons of the Enteric Nervous System
Duchalais, É., Guilluy, C., Nédellec, S., Touvron, M. S., Bessard, A., Touchefeu, Y., Bossard, C., Boudin, H., Louarn, G., Neunlist, M., et al. (2017) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.10.002 · Cited by 75 · see citing works
Beyond Axon Guidance: Roles of Slit-Robo Signaling in Neocortical Formation
Gonda, Y., Namba, T., & Hanashima, C. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.607415 · Cited by 75 · see citing works
Xu, C., Funahashi, Y., Watanabe, T., Takano, T., Nakamuta, S., Namba, T., & Kaibuchi, K. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1266-15.2015 · Cited by 75 · see citing works
Tao, Y., Ip, J. P. K., Fu, A. K. Y., & Ip, N. Y. (2014) · Nature Communications · doi:10.1038/ncomms5826 · Cited by 74 · see citing works
Focal Adhesion Kinase Modulates Radial Glia-Dependent Neuronal Migration through Connexin-26
Valiente, M., Ciceri, G., Rico, B., & Marín, Ó. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2678-11.2011 · Cited by 73 · see citing works
Szczurkowska, J., Pischedda, F., Pinto, B., Managò, F., Haas, C. A., Summa, M., Bertorelli, R., Papaleo, F., Schäfer, M. K. E., Piccoli, G., et al. (2018) · Brain · doi:10.1093/brain/awy190 · Cited by 75 · see citing works
Gil, C., Landeira, B. S., Ramos, C., Costa, M. R., & Müller, U. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1793-14.2014 · Cited by 66 · see citing works
Neurogenesis, neuronal migration, and axon guidance
Accogli, A., Addour-Boudrahem, N., & Srour, M. (2020) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64150-2.00004-6 · Cited by 72 · see citing works
Inside-Out Radial Migration Facilitates Lineage-Dependent Neocortical Microcircuit Assembly
He, S., Li, Z., Ge, S., Yu, Y., & Shi, S. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.002 · Cited by 70 · see citing works
Reelin through the years: From brain development to inflammation
Alexander, A., Herz, J., & Calvier, L. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112669 · Cited by 71 · see citing works
Dimidschstein, J., Passante, L., Dufour, A., van den Ameele, J., Tiberi, L., Hrechdakian, T., Adams, R. H., Klein, R., Lie, D. C., Jossin, Y., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.015 · Cited by 65 · see citing works
Self-citationNeuronal Polarity: Positive and Negative Feedback Signals
Takano, T., Funahashi, Y., & Kaibuchi, K. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00069 · Cited by 65 · see citing works
Linking Cell Polarity to Cortical Development and Malformations
Hakanen, J., Ruiz-Reig, N., & Tissir, F. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00244 · Cited by 65 · see citing works
Fan, L., Lu, Y., Shen, X., Shao, H., Suo, L., & Wu, Q. (2018) · eLife · doi:10.7554/elife.35242 · Cited by 67 · see citing works
Foxp1 Regulates Cortical Radial Migration and Neuronal Morphogenesis in Developing Cerebral Cortex
Li, X., Xiao, J., Fröhlich, H., Tu, X., Li, L., Xu, Y., Cao, H., Qu, J., Rappold, G., & Chen, J.-G. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127671 · Cited by 65 · see citing works
Llgl1 Connects Cell Polarity with Cell-Cell Adhesion in Embryonic Neural Stem Cells
Jossin, Y., Lee, M., Klezovitch, O., Kon, E., Cossard, A., Lien, W., Fernandez, T. E., Cooper, J. A., & Vasioukhin, V. I. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.05.002 · Cited by 64 · see citing works
Self-citationCollazos-Castro, J. E., Hernández-Labrado, G. R., Polo, J. L., & García‐Rama, C. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.01.097 · Cited by 60 · see citing works
Multisensory cortical processing and dysfunction across the neuropsychiatric spectrum
Hornix, B., Havekes, R., & Kas, M. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.02.010 · Cited by 60 · see citing works
Hirota, Y., Kubo, K., Katayama, K., Honda, T., Fujino, T., Yamamoto, T. T., & Nakajima, K. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23691 · Cited by 59 · see citing works
Reelin Induces Branching of Neurons and Radial Glial Cells during Corticogenesis
Chai, X., Fan, L., Shao, H., Lu, X., Zhang, W., Li, J., Wang, J., Chen, S., Frotscher, M., & Zhao, S. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu216 · Cited by 59 · see citing works
Horn, Z., Behesti, H., & Hatten, M. E. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1811100115 · Cited by 59 · see citing works
Reelin Induces Erk1/2 Signaling in Cortical Neurons Through a Non-canonical Pathway
Lee, G. H., Chhangawala, Z., von Daake, S., Savas, J. N., Yates, J. R., Comoletti, D., & D’Arcangelo, G. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.576249 · Cited by 57 · see citing works
Luccardini, C., Hennekinne, L., Viou, L., Yanagida, M., Murakami, F., Kessaris, N., Ma, X., Adelstein, R. S., Mège, R., & Métin, C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0593-13.2013 · Cited by 56 · see citing works
Reelin transiently promotes N-cadherin–dependent neuronal adhesion during mouse cortical development
Matsunaga, Y., Noda, M., Murakawa, H., Hayashi, K., Nagasaka, A., Inoue, S., Miyata, T., Miura, T., Kubo, K., & Nakajima, K. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1615215114 · Cited by 55 · see citing works
Singh, S. T., & Solecki, D. J. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00062 · Cited by 54 · see citing works
Rbx2 Regulates Neuronal Migration through Different Cullin 5-RING Ligase Adaptors
Simó, S., & Cooper, J. A. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.09.022 · Cited by 53 · see citing works
Self-citationNguyen, T., & Mège, R. (2016) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2016.05.002 · Cited by 53 · see citing works
Neuronal Polarity in the Embryonic Mammalian Cerebral Cortex
Kon, E., Cossard, A., & Jossin, Y. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00163 · Cited by 52 · see citing works
Self-citationZhao, X., Kohen, R., Parent, R., Duan, Y., Fisher, G. L., Korn, M. J., Ji, L., Wan, G., Jin, J., Püschel, A. W., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.044 · Cited by 50 · see citing works
Du, Y., Song, W., Chen, J., Chen, H. H., Xuan, Z., Zhao, L., Chen, J., Jin, C., Zhou, M., Tuo, B., et al. (2019) · International Journal of Cancer · doi:10.1002/ijc.32121 · Cited by 52 · see citing works
RalA promotes a direct exocyst-Par6 interaction to regulate polarity in neuronal development
Das, A. K., Gajendra, S., Falenta, K., Oudin, M. J., Peschard, P., Feng, S., Wu, B., Marshall, C. J., Doherty, P., Guo, W., et al. (2013) · Journal of Cell Science · doi:10.1242/jcs.145037 · Cited by 50 · see citing works
Regulation of cerebral cortex development by Rho GTPases: insights from in vivo studies
Azzarelli, R., Kerloch, T., & Pacary, E. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00445 · Cited by 50 · see citing works
Reelin-Disabled-1 signaling in neuronal migration: splicing takes the stage
Gao, Z., & Godbout, R. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1171-6 · Cited by 50 · see citing works
Itoh, Y., Higuchi, M., Oishi, K., Kishi, Y., Okazaki, T., Sakai, H., Miyata, T., Nakajima, K., & Gotoh, Y. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516321113 · Cited by 50 · see citing works
Astrocyte-induced Reelin expression drives proliferation of Her2+ breast cancer metastases
Jandial, R., Choy, C., Levy, D. M., Chen, M. Y., & Ansari, K. I. (2017) · Clinical & Experimental Metastasis · doi:10.1007/s10585-017-9839-9 · Cited by 50 · see citing works
Kon, E., Calvo-Jiménez, E., Cossard, A., Na, Y., Cooper, J. A., & Jossin, Y. (2019) · eLife · doi:10.7554/elife.47673 · Cited by 50 · see citing works
Self-citationLászló, Z. I., & Lele, Z. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.972059 · Cited by 49 · see citing works
Molecular Pathways Controlling the Sequential Steps of Cortical Projection Neuron Migration
Hippenmeyer, S. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-7687-6_1 · Cited by 46 · see citing works
N-cadherin and β1-integrins cooperate during the development of the enteric nervous system
Broders, F., Paul‐Gilloteaux, P., Carlier, C., Radice, G. L., & Dufour, S. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.02.001 · Cited by 48 · see citing works
Kawauchi, T., Shikanai, M., & Kosodo, Y. (2013) · Genes to Cells · doi:10.1111/gtc.12029 · Cited by 47 · see citing works
Meseke, M., Rosenberger, G., & Förster, E. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12153 · Cited by 46 · see citing works
Winter, J. (2015) · Neurogenesis · doi:10.1080/23262133.2015.1004970 · Cited by 44 · see citing works
Acute inactivation of the serine-threonine kinase Stk25 disrupts neuronal migration
Matsuki, T., Chen, J., & Howell, B. W. (2013) · Neural Development · doi:10.1186/1749-8104-8-21 · Cited by 45 · see citing works
RareRELNvariants affect Reelin-DAB1 signal transduction in autism spectrum disorder
Sánchez-Sánchez, S. M., Magdalon, J., Griesi‐Oliveira, K., Yamamoto, G. L., Santacruz-Pérez, C., Fogo, M. S., Passos‐Bueno, M. R., & Sertie, A. L. (2018) · Human Mutation · doi:10.1002/humu.23584 · Cited by 45 · see citing works
Shikanai, M., Nishimura, Y. V., Sakurai, M., Nabeshima, Y.-I., Yuzaki, M., & Kawauchi, T. (2018) · iScience · doi:10.1016/j.isci.2018.08.014 · Cited by 45 · see citing works
The Dynamics of Neuronal Migration
Wu, Q., Liu, J., Fang, A., Li, R., Bai, Y., Kriegstein, A. R., & Wang, X. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-7687-6_2 · Cited by 45 · see citing works
Hara, Y., Fukaya, M., Hayashi, K., Kawauchi, T., Nakajima, K., & Sakagami, H. (2016) · eNeuro · doi:10.1523/eneuro.0148-16.2016 · Cited by 44 · see citing works
Chang, Y. C., Daza, R. A. M., Hevner, R. F., Costa, L. G., & Cole, T. B. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.01.013 · Cited by 44 · see citing works
Lau, O.-C., Damiani, D., Chehade, G., Ruiz-Reig, N., Saade, R., Jossin, Y., Aittaleb, M., Schakman, O., Tajeddine, N., Gailly, P. L., et al. (2021) · eLife · doi:10.7554/elife.61974 · Cited by 44 · see citing works
Self-citationReelin, neuronal polarity and process orientation of cortical neurons
Förster, E. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.03.004 · Cited by 43 · see citing works
Chai, X., Zhao, S., Fan, L., Zhang, W., Lu, X., Shao, H., Wang, S., Song, L., Failla, A. V., Zobiak, B., et al. (2016) · Development · doi:10.1242/dev.134163 · Cited by 42 · see citing works
Vinopal, S., Dupraz, S., Alfadil, E., Pietralla, T., Bendre, S., Stieß, M., Falk, S., Ortega, G. C., Maghelli, N., Tolić, I. M., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.01.020 · Cited by 44 · see citing works
Rap1 GTPases Are Master Regulators of Neural Cell Polarity in the Developing Neocortex
Shah, B., Lutter, D., Tsytsyura, Y., Glyvuk, N., Sakakibara, A., Klingauf, J., & Püschel, A. W. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv341 · Cited by 42 · see citing works
- Authors
- Jossin, Y., & Cooper, J. A.
- Affiliations
- Fred Hutch Cancer Center (US)
- Corresponding author
- Jossin, Yves
- Cooper, Jonathan A
- Venue
- Nature Neuroscience
- Published
- 2011-04-24
- Volume
- 14
- Issue
- 6
- Pages
- 697-703
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3102785
- OpenAlex
- W2118947728
- Cited by
- 332
- References
- 50
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 19 · 2023: 15 · 2022: 17 · 2021: 14 · 2020: 24 · 2019: 26 · 2018: 34 · 2017: 26 · 2016: 27 · 2015: 35 · 2014: 31 · 2013: 24 · 2012: 20
- FWCI
- 8.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion, other-oa)
- Funders
- National Cancer Institute (R37CA041072, CA41072, R01CA041072)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- reelin, Rap1 GTPase, N-cadherin, neuronal migration, multipolar neurons, cortical plate, neocortex development, projection neurons, Akt signaling, RalA, RalB, Rac1, Cdc42, cell polarity, intermediate zone
- MeSH terms
- Reelin Protein, Animals, Cell Differentiation, Cell Movement, Mice, Inbred Strains, Nerve Tissue Proteins, Neurons, Serine Endopeptidases, Cell Adhesion Molecules, Neuronal, Cadherins, Extracellular Matrix Proteins, Neocortex, rap1 GTP-Binding Proteins, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review