Neuronal position in the developing brain is regulated by mouse disabled-1
Abstract
During mammalian brain development, immature neurons migrate radially from the neuroectoderm to defined locations, giving rise to characteristic cell layers. Here we show that targeted disruption of the mouse disabled1 (mdab1) gene disturbs neuronal layering in the cerebral cortex, hippocampus and cerebellum. The gene encodes a cytoplasmic protein, mDab1 p80, which is expressed and tyrosine-phosphorylated in the developing nervous system. It is likely to be an adaptor protein, docking to others through its phosphotyrosine residues and protein-interacting domain. The mdab1 mutant phenotype is very similar to that of the reeler mouse. The product of the reeler gene, Reelin, is a secreted protein that has been proposed to act as an extracellular signpost for migrating neurons. Because mDab1 is expressed in wild-type cortical neurons, and Reelin expression is normal in mdab1 mutants, mDab1 may be part of a Reelin-regulated or parallel pathway that controls the final positioning of neurons.
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VLDLR and ApoER2 have a critical role in the neuronal Reelin pathway essential for proper neuronal positioning and brain development.
“studies in recent years have established a critical role for VLDLR and ApoER2 in the neuronal Reelin pathway that is essential for proper neuronal positioning and brain development (16–19).”
From The E3 ubiquitin ligase IDOL induces the degradation of the low density lipoprotein receptor family members VLDLR and ApoER2 (2010) · cites this paper as [18]
Cites
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 · cited 1× · see citing works
“The product of the reeler gene, Reelin, is a secreted protein that has been proposed to act as an extracellular signpost for migrating neuron”
BackgroundA role for Cajal–Retzius cells and reelin in the development of hippocampal connections
Del Río, J. A., Heimrich, B., Borrell, V., Förster, E., Drakew, A., Alcántara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., et al. (1997) · Nature · doi:10.1038/385070a0 · Cited by 472 · see citing works
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Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., & Herz, J. (1999) · Cell · doi:10.1016/s0092-8674(00)80782-5 · Cited by 1,261 · see citing works
Hiesberger, T., Trommsdorff, M., Howell, B. W., Goffinet, A., Mumby, M. C., Cooper, J. A., & Herz, J. (1999) · Neuron · doi:10.1016/s0896-6273(00)80861-2 · Cited by 916 · see citing works
Self-citationReelin Is a Ligand for Lipoprotein Receptors
D'Arcangelo, G., Homayouni, R., Keshvara, L., Rice, D. S., Sheldon, M., & Curran, T. (1999) · Neuron · doi:10.1016/s0896-6273(00)80860-0 · Cited by 808 · see citing works
Role of the Reelin Signaling Pathway in Central Nervous System Development
Rice, D. S., & Curran, T. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1005 · Cited by 667 · see citing works
Scrambler and yotari disrupt the disabled gene and produce a reeler -like phenotype in mice
Sheldon, M., Rice, D. S., D'Arcangelo, G., Yoneshima, H., Nakajima, K., Mikoshiba, K., Howell, B. W., Cooper, J. A., Goldowitz, D., & Curran, T. (1997) · Nature · doi:10.1038/39601 · Cited by 638 · see citing works
Self-citationReelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning
Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Förster, E., Sweatt, J. D., & Herz, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205147200 · Cited by 623 · see citing works
Distinct Profiles of Myelin Distribution Along Single Axons of Pyramidal Neurons in the Neocortex
Tomassy, G. S., Berger, D. R., Chen, H.-H., Kasthuri, N., Hayworth, K. J., Vercelli, A., Seung, H. S., Lichtman, J. W., & Arlotta, P. (2014) · Science · doi:10.1126/science.1249766 · Cited by 600 · see citing works
Reelin Binds α3β1 Integrin and Inhibits Neuronal Migration
Dulabon, L., Olson, E. C., Taglienti, M. G., Eisenhuth, S., McGrath, B., Walsh, C. A., Kreidberg, J. A., & Anton, E. S. (2000) · Neuron · doi:10.1016/s0896-6273(00)00007-6 · Cited by 577 · see citing works
Localizing Recent Adaptive Evolution in the Human Genome.
Williamson, S. H., Hubisz, M. J., Clark, A. G., Payseur, B. A., Bustamante, C. D., & Nielsen, R. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030090 · Cited by 507 · see citing works
Reelin, lipoprotein receptors and synaptic plasticity
Herz, J., & Chen, Y. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2009 · Cited by 524 · see citing works
Reelin-induced tryosine phosphorylation of Disabled 1 during neuronal positioning
Howell, B. W., Herrick, T. M., & Cooper, J. A. (1999) · Genes & Development · doi:10.1101/gad.13.6.643 · Cited by 411 · see citing works
Self-citationPesold, C., Impagnatiello, F., Pisu, M. G., Uzunov, D. P., Costa, E., Guidotti, A., & Caruncho, H. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3221 · Cited by 391 · see citing works
Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway
Niu, S., Renfro, A., Quattrocchi, C. C., Sheldon, M., & D'Arcangelo, G. (2004) · Neuron · doi:10.1016/s0896-6273(03)00819-5 · Cited by 375 · 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
Reelin modulates NMDA receptor activity in cortical neurons
Chen, Y., Beffert, U., Ertunc, M., Tang, T.-S., Kavalali, E. T., Bezprozvanny, I., & Herz, J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1951-05.2005 · Cited by 299 · see citing works
The Reelin signaling pathway promotes dendritic spine development in hippocampal neurons
Niu, S., Yabut, O., & D'Arcangelo, G. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1917-08.2008 · Cited by 266 · see citing works
Proteins of the CNR Family Are Multiple Receptors for Reelin
Senzaki, K., Ogawa, M., & Yagi, T. (1999) · Cell · doi:10.1016/s0092-8674(00)81552-4 · Cited by 272 · see citing works
Förster, E., Tielsch, A., Saum, B., Weiss, K. H., Johanssen, C., Graus-Porta, D., Müller, U., & Frotscher, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202035899 · Cited by 254 · see citing works
Curran, T., & D'Arcangelo, G. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00035-0 · Cited by 246 · see citing works
The reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2
Stockinger, W., Brandes, C., Fasching, D., Hermann, M., Gotthardt, M., Herz, J., Schneider, W. J., & Nimpf, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m004119200 · Cited by 239 · see citing works
Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation
Pujadas, L., Gruart, A., Bosch, C., Delgado, L., Teixeira, C. M., Rossi, D., de Lecea, L., Martínez, A., Delgado-García, J. M., & Soriano, E. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5284-09.2010 · Cited by 219 · see citing works
Chai, X., Förster, E., Zhao, S., Bock, H. H., & Frotscher, M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2934-08.2009 · Cited by 202 · see citing works
Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice
QIU, S., KORWEK, K., PRATTDAVIS, A., PETERS, M., BERGMAN, M., & WEEBER, E. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.11.001 · Cited by 202 · see citing works
Receptor Clustering Is Involved in Reelin Signaling
Strasser, V., Fasching, D., Hauser, C., Mayer, H., Bock, H. H., Hiesberger, T., Herz, J., Weeber, E. J., Sweatt, J. D., Pramatarova, A., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.3.1378-1386.2004 · Cited by 193 · see citing works
Self-citationChin, J., Massaro, C. M., Palop, J. J., Thwin, M. T., Yu, G.-Q., Bien-Ly, N., Bender, A., & Mucke, L. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3758-06.2007 · Cited by 188 · see citing works
Reelin 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
Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus
Qiu, S., Zhao, L. F., Korwek, K. M., & Weeber, E. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2561-06.2006 · Cited by 186 · see citing works
Nova2 Regulates Neuronal Migration through an RNA Switch in Disabled-1 Signaling
Yano, M., Hayakawa-Yano, Y., Mele, A., & Darnell, R. B. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.007 · Cited by 176 · see citing works
Pesold, C., Liu, W. S., Guidotti, A., Costa, E., & Caruncho, H. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.6.3217 · Cited by 160 · 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-citationSmalheiser, N. R., Costa, E., Guidotti, A., Impagnatiello, F., Auta, J., Lacor, P., Kriho, V., & Pappas, G. D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.1281 · Cited by 158 · see citing works
Role for Reelin in stabilizing cortical architecture
Frotscher, M. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.06.001 · Cited by 157 · see citing works
Fetit, R., Hillary, R. F., Price, D. J., & Lawrie, S. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.07.014 · Cited by 148 · see citing works
Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling
Pla, R., Borrell, V., Flames, N., & Marín, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0245-06.2006 · Cited by 151 · see citing works
Hong, C., Duit, S., Jalonen, P., Out, R., Scheer, L., Sorrentino, V., Boyadjian, R., Rodenburg, K. W., Foley, E., Korhonen, L., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.123729 · Cited by 142 · see citing works
Utsunomiya-Tate, N., Kubo, K.-I., Tate, S.-I., Kainosho, M., Katayama, E., Nakajima, K., & Mikoshiba, K. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.160272497 · Cited by 131 · 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
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
Reelin deficiency causes granule cell dispersion in epilepsy
Haas, C. A., & Frotscher, M. (2010) · Experimental Brain Research · doi:10.1007/s00221-009-1948-5 · Cited by 96 · see citing works
<i>Gli3</i>Is Required for Maintenance and Fate Specification of Cortical Progenitors
Wang, H., Ge, G., Uchida, Y., Luu, B., & Ahn, S. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4892-10.2011 · Cited by 93 · see citing works
Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus
Teixeira, C. M., Kron, M. M., Masachs, N., Zhang, H., Lagace, D. C., Martinez, A., Reillo, I., Duan, X., Bosch, C., Pujadas, L., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1857-12.2012 · Cited by 97 · see citing works
Self-citationAge-related accumulation of Reelin in amyloid-like deposits
Knuesel, I., Nyffeler, M., Mormède, C., Muhia, M., Meyer, U., Pietropaolo, S., Yee, B. K., Pryce, C. R., LaFerla, F. M., Marighetto, A., et al. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.08.011 · Cited by 94 · see citing works
Leemhuis, J., Bouché, E., Frotscher, M., Henle, F., Hein, L., Herz, J., Meyer, D. K., Pichler, M., Roth, G., Schwan, C., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4036-10.2010 · Cited by 80 · see citing works
Koch, S., Strasser, V., Hauser, C., Fasching, D., Brandes, C., Bajari, T. M., Schneider, W. J., & Nimpf, J. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf599 · Cited by 80 · see citing works
Role for Reelin in neurotransmitter release
Hellwig, S., Hack, I., Kowalski, J., Brunne, B., Jarowyj, J., Unger, A., Bock, H. H., Junghans, D., & Frotscher, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3984-10.2011 · Cited by 74 · see citing works
Bosch, C., Masachs, N., Exposito-Alonso, D., Martínez, A., Teixeira, C. M., Fernaud, I., Pujadas, L., Ulloa, F., Comella, J. X., DeFelipe, J., et al. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw216 · Cited by 70 · see citing works
Elsen, G. E., Choi, L. Y., Prince, V. E., & Ho, R. K. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.08.024 · Cited by 64 · see citing works
Dey, N., De, P. K., Wang, M., Zhang, H., Dobrota, E. A., Robertson, K. A., & Durden, D. L. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01352-06 · Cited by 62 · see citing works
Differential gene expression in migratory streams of cortical interneurons
Antypa, M., Faux, C., Eichele, G., Parnavelas, J. G., & Andrews, W. D. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07896.x · Cited by 49 · see citing works
ApoER2 processing by presenilin-1 modulates reelin expression
Balmaceda, V., Cuchillo‐Ibáñez, I., Pujadas, L., García‐Ayllón, M., Saura, C. A., Nimpf, J., Soriano, E., & Sáez‐Valero, J. (2014) · The FASEB Journal · doi:10.1096/fj.13-239350 · Cited by 40 · see citing works
Reelin proteolysis affects signaling related to normal synapse function and neurodegeneration
Lussier, A. L., Weeber, E. J., & Rebeck, G. W. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00075 · Cited by 31 · see citing works
Wang, S., Brunne, B., Zhao, S., Chai, X., Li, J., Lau, J., Failla, A. V., Zobiak, B., Sibbe, M., Westbrook, G. L., et al. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0988-17.2017 · Cited by 26 · see citing works
Laminar distribution of neurotransmitter receptors in different reeler mouse brain regions
Cremer, C. M., Lübke, J. H. R., Palomero-Gallagher, N., & Zilles, K. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0303-3 · Cited by 17 · see citing works
- Authors
- Howell, B. W., Hawkes, R., Soriano, P., & Cooper, J. A.
- Affiliations
- Fred Hutch Cancer Center (US)
- University of Calgary (CA)
- Venue
- Nature
- Published
- 1997-10
- Volume
- 389
- Issue
- 6652
- Pages
- 733-737
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1667992367
- Cited by
- 692
- References
- 2
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 6 · 2023: 6 · 2022: 12 · 2021: 16 · 2020: 14 · 2019: 9 · 2018: 11 · 2017: 21 · 2016: 16 · 2015: 14 · 2014: 15 · 2013: 28 · 2012: 24
- FWCI
- 13.29
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- 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
- Disabled-1, neuronal migration, cerebral cortex, hippocampus, cerebellum, reelin, reeler mice, tyrosine phosphorylation, adaptor proteins, gene targeting, brain development
- MeSH terms
- Reelin Protein, Animals, Brain, Cell Line, Cell Movement, Cerebellum, Mice, Neurologic Mutants, Nerve Tissue Proteins, Neurons, Serine Endopeptidases, Signal Transduction, Cell Adhesion Molecules, Neuronal, Mutagenesis, Extracellular Matrix Proteins, Gene Targeting, Neocortex, Mice
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