The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons
Open accessAbstract
In the neurological mutant mouse reeler, the histological organization of the neocortex develops abnormally and essentially results in an inversion of the relative positions of the cortical layers. The reeler mutation, therefore, provides an insight into the molecular mechanisms underlying the formation of the cortical layers. We have generated a monoclonal antibody (CR-50) that probes a distinct allelic antigen present in wild-type but not in reeler mutant mice. CR-50 reacted specifically with Cajal-Retzius neurons, one of the first cortical neurons to differentiate in the neocortex, but whose functional role is not known. When dissociated cerebral cortical cells were incubated with CR-50 in reaggregation culture, the genotype-dependent histogenetic assembly of wild-type cortical cells resembled that of reeler mutants. These findings revealed that the selective expression of a distinct molecule on Cajal-Retzius neurons is critical for the normal lamination of cortical neurons in the mammalian neocortex.
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Reelin proteins are assembled and anchored to the surface of a cell membrane of the Reelin-secreting cells.
“These data suggest that Reelin proteins are assembled and anchored to the surface of a cell membrane of the Reelin-secreting cells.”
From Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody (2000) · cites this paper as [13]
CR-50 antibody has neutralizing activity of Reelin both in vitro and in vivo.
“The CR-50 antibody has neutralizing activity of Reelin both in vitro and in vivo (13, 19–21).”
From Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody (2000) · cites this paper as [13]
CR-50 antibody shows a function-blocking effect on Reelin from around 20 μg/ml.
“CR-50 antibody shows a function-blocking effect on Reelin from around this concentration (13)”
From Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody (2000) · cites this paper as [13]
Some of the secreted Reelin is anchored to the surface of Reelin-producing cells by an unknown mechanism.
“some of the secreted Reelin is anchored to the surface of the Reelin-producing cells by an unknown mechanism.”
From Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody (2000) · cites this paper as [13]
The CR-50 epitope region is essential for Reelin functions.
“This epitope region is essential for the Reelin functions, because CR-50 antibody inhibits laminar pattern formation in cortical reaggregation cultures (13), Purkinje cell alignment in cerebellar explant cultures (20), and an axonal branching pattern in the entorhinohippocampal pathway in vitro (19) and disrupts hippocampal development in vivo (21).”
From Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody (2000) · cites this paper as [13]
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Tamamaki, N., Fujimori, K. E., & Takauji, R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08313.1997 · Cited by 394 · see citing works
“The marginal zone contains different types of cells that have functions different from those of the subplate neurons (Shatz et al., 1988; McConnell et al., 1989, 1990; D’Arcangelo et al., 1995; Ogawa et al., 1995 ).”
BackgroundReelin 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
Self-citationLi, M., & Ransohoff, R. M. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.11.003 · Cited by 352 · see citing works
Anton, E. S., Kreidberg, J. A., & RAKIC, P. T. (1999) · Neuron · doi:10.1016/s0896-6273(00)81089-2 · Cited by 351 · see citing works
Neuronal migration disorders: from genetic diseases to developmental mechanisms
Gleeson, J. G., & Walsh, C. A. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01607-6 · Cited by 344 · see citing works
Reelin gene alleles and haplotypes as a factor predisposing to autistic disorder
Persico, A. M., D'Agruma, L., Maiorano, N., Totaro, A., Militerni, R., Bravaccio, C., Wassink, T. H., Schneider, C., Melmed, R., Trillo, S., et al. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000850 · Cited by 337 · see citing works
Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex
Jossin, Y., & Cooper, J. A. (2011) · Nature Neuroscience · doi:10.1038/nn.2816 · Cited by 332 · see citing works
Lissencephaly and the molecular basis of neuronal migration
Kato, M. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg086 · Cited by 334 · 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
“Reelin is prominently expressed in the developing neocortex in Cajal-Retzius cells in the MZ (Alcántara et al., 1998; D’Arcangelo et al., 1997; Ogawa et al., 1995) and binds to the Vldlr and Apoer2 receptors (D’Arcangelo et al., 1999; Hiesberger et al., 1999), which are expressed in RGCs and…”
Pax6Modulates the Dorsoventral Patterning of the Mammalian Telencephalon
Stoykova, A., Treichel, D., Hallonet, M. E. R., & Gruß, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08042.2000 · Cited by 314 · see citing works
“We show in this work that early in development the proliferative Ne of the VP and LP in Sey/Sey expresses ectopically Dlx1, Mash1, Vax1, and Six3, whereas the restricted expression of Nkx2.”
BackgroundInfluentialReelin is a detachment signal in tangential chain-migration during postnatal neurogenesis
Hack, I., Bancila, M., Loulier, K., Carroll, P., & Cremer, H. (2002) · Nature Neuroscience · doi:10.1038/nn923 · Cited by 313 · see citing works
Cyclin-Dependent Kinase 5-Deficient Mice Demonstrate Novel Developmental Arrest in Cerebral Cortex
Gilmore, E. C., Ohshima, T., Goffinet, A. M., Kulkarni, A. B., & Herrup, K. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-16-06370.1998 · Cited by 312 · see citing works
“Examination of cresyl violet-stained sections of embryonic Cdk5 Ϫ/Ϫ brains reveals a disruption in cerebral cortical morphology (Ohshima et al., 1996).”
BackgroundMethodHeinrich, C., Nitta, N., Flubacher, A., Müller, M., Fahrner, A., Kirsch, M., Freiman, T. M., Suzuki, F., Depaulis, A., Frotscher, M., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5516-05.2006 · Cited by 303 · see citing works
“CR-50 has been shown to effectively neutralize reelin function in a variety of experimental approaches during development (Ogawa et al., 1995; Nakajima et al., 1997).”
BackgroundMethodFatemi, S. H., Stary, J. M., Earle, J. A., Araghi‐Niknam, M., & Eagan, E. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2004.02.017 · Cited by 300 · see citing works
Patterning of the Dorsal Telencephalon and Cerebral Cortex by a Roof Plate-Lhx2 Pathway
Monuki, E. S., Porter, F. D., & Walsh, C. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00504-9 · Cited by 294 · see citing works
Preferential Origin and Layer Destination of GAD65-GFP Cortical Interneurons
López‐Bendito, G. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh072 · Cited by 288 · see citing works
“These cells express the calcium-binding protein CR and the extracellular matrix protein, reelin (Ogawa et al., 1995).”
BackgroundCortical development: View from neurological mutants two decades later
Rakic, P., & Caviness, V. S. (1995) · Neuron · doi:10.1016/0896-6273(95)90258-9 · Cited by 287 · see citing works
Stoykova, A., Götz, M., Gruss, P., & Price, J. (1997) · Development · doi:10.1242/dev.124.19.3765 · Cited by 284 · see citing works
Reelin signaling is impaired in autism
Fatemi, S. H., Snow, A. V., Stary, J. M., Araghi-Niknam, M., Reutiman, T. J., Lee, S., Brooks, A. I., & Pearce, D. A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.018 · Cited by 280 · see citing works
Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling
Borrell, V., & Marín, Ó. (2006) · Nature Neuroscience · doi:10.1038/nn1764 · Cited by 279 · see citing works
Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order
Yoshida, M., Assimacopoulos, S., Jones, K. R., & Grove, E. A. (2006) · Development · doi:10.1242/dev.02209 · Cited by 275 · see citing works
“Since the identification of reelin, and the observation that it is robustly produced by Cajal-Retzius (CR) cells in the marginal zone (MZ) of the cortical primordium (D’Arcangelo et al., 1995; Meyer et al., 1999; Ogawa et al., 1995), CR neurons have been thought to be essential for laminar organization (Bielas et al.”
BackgroundInfluentialCajal—Retzius cells, Reelin, and the formation of layers
Frotscher, M. (1998) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(98)80082-2 · Cited by 275 · see citing works
Prenatal stress: Role in psychotic and depressive diseases
Markham, J. A., & Koenig, J. I. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2035-0 · Cited by 274 · see citing works
“Early in brain development, during the embryonic stage, Reelin is first expressed by the transient GABAergic Cajal–Retzius neurons and is crucial for establishing neocortical and allocortical laminar structure (Ogawa et al. 1995).”
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
Self-citationBrn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons
Sugitani, Y., Nakai, S., Minowa, O., Nishi, M., Jishage, K.-I., Kawano, H., Mori, K., Ogawa, M., & Noda, T. (2002) · Genes & Development · doi:10.1101/gad.978002 · Cited by 259 · see citing works
“1994), and CR-50 for Cajal-Retzius neurons in the marginal zone (MZ; Fig. 3O; Ogawa et al. 1995; D’Arcangelo et al. 1997).”
BackgroundSelf-citationHow 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
Comparative aspects of cerebral cortical development
Molnár, Z., Métin, C., Stoykova, A., Tarabykin, V. S., Price, D. J., Francis, F., Meyer, G., Dehay, C., & Kennedy, H. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04611.x · Cited by 266 · see citing works
“The most prominent pre-plate components are the Cajal-Retzius (CR) cells, which secrete high levels of Reelin (D ́Arcangelo et al., 1995; Ogawa et al., 1995), and the aforementioned subplate cells (Allendoerfer and Shatz, 1994).”
BackgroundSoft Matter Models of Developing Tissues and Tumors
Gonzalez‐Rodriguez, D., Guevorkian, K., Douezan, S., & Brochard‐Wyart, F. (2012) · Science · doi:10.1126/science.1226418 · Cited by 265 · see citing works
Fatemi, S. H., Emamian, E. S., Kist, D. A., Sidwell, R. W., Nakajima, K., Akhter, P., Shier, A. C., Sheikh, S. A., & Bailey, K. W. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000520 · Cited by 259 · see citing works
Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development
Howell, B. W., Herrick, T. M., Hildebrand, J. D., Zhang, Y., & Cooper, J. A. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00608-4 · Cited by 258 · see citing works
“secreted by specialized early neurons that appear to serve as guideposts for subsequent migrations [19,31,32].”
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
Zimmer, C. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh102 · Cited by 240 · see citing works
Reelin glycoprotein: structure, biology and roles in health and disease
Fatemi, S. H. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001613 · Cited by 241 · see citing works
“1 Reelin protein product has a relative molecular mass of 388 kDa”
BackgroundReelin Regulates Neuronal Progenitor Migration in Intact and Epileptic Hippocampus
Gong, C., Wang, T., Huang, H. S., & Parent, J. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3111-06.2007 · Cited by 233 · see citing works
“…upregulated subgranular zone (SGZ) cell proliferation or DGC neurogenesis (Bengzon et al., 1997; Parent et al., 1997, 1998; Gray and Sundstrom, 1998; Scott et al., 1998; Nakagawa et al., 2000; Hattiangady et al., 2004; Mohapel et al., 2004; Jessberger et al., 2005; Overstreet-Wadiche et al., 2006).”
BackgroundTakiguchi‐Hayashi, K., Sekiguchi, M., Ashigaki, S., Takamatsu, M., Hasegawa, H., Suzuki-Migishima, R., Yokoyama, M., Nakanishi, S., & Tanabe, Y. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4671-03.2004 · Cited by 231 · see citing works
“The analyses of reeler mutant mice (Ogawa et al., 1995; Meyer et al., 1999; Rice and Curran, 2001; Tissir and Goffinet, 2003), together with studies in human congenital lissencephaly (Gleeson and Walsh, 2000), led to the suggestion that the neocortical neural organization depends on the activities…”
BackgroundReelin mRNA Expression During Mouse Brain Development
Schiffmann, S. N., Bernier, B., & Goffinet, A. M. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01456.x · Cited by 227 · see citing works
Meyer, G., Soria, J. M., Martinez-Galan, J. R., Mart�n-Clemente, B., & Fair�n, A. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980810)397:4 · Cited by 228 · see citing works
Groc, L., Choquet, D., Stephenson, F. A., Verrier, D., Manzoni, O. J., & Chavis, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1772-07.2007 · Cited by 225 · see citing works
“We chronically treated 10 –12 div neurons (see Materials and Methods) with the CR-50 antibody that has function-interfering activity of Reelin both in vivo and in vitro (Ogawa et al., 1995; Miyata et al., 1997; Nakajima et al., 1997).”
MethodThe functions of the preplate in development and evolution of the neocortex and hippocampus
Supèr, H., Soriano, E., & Uylings, H. B. M. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00005-8 · Cited by 221 · see citing works
Wang, L., Andersson, S., Warner, M. N., & Gustafsson, J.-Α. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242735799 · Cited by 220 · see citing works
Bayatti, N., Moss, J. A., Sun, L. Y., Ambrose, P. M., Ward, J. F. H., Lindsay, S., & Clowry, G. J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm184 · Cited by 227 · see citing works
“These neurons secrete reelin, a signaling molecule important in ordering the migration of cells into the cortical plate (Ogawa et al. 1995).”
BackgroundDCX, a new mediator of the JNK pathway
Gdalyahu, A., Ghosh, I., Levy, T., Sapir, T., Sapoznik, S., Fishler, Y., Azoulai, D., & Reiner, O. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600079 · Cited by 218 · see citing works
“Mutations in either reelin (D’Arcangelo et al, 1995; Hirotsune et al, 1995; Ogawa et al, 1995) or in its receptors—the very low-density lipoprotein receptor (VLDLR) and the apoE receptor 2 (ApoER2) (D’Arcangelo et al, 1999; Hiesberger et al, 1999)- or in the intracellular signaling molecule Dab1…”
BackgroundDysregulation of Reelin and Bcl-2 Proteins in Autistic Cerebellum
Fatemi, S. H., Stary, J. M., Halt, A. R., & Realmuto, G. R. (2001) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1013234708757 · Cited by 212 · see citing works
The brain interstitial system: Anatomy, modeling, in vivo measurement, and applications
Lei, Y., Han, H., Yuan, F., Javeed, A., & Zhao, Y. L. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.12.007 · Cited by 215 · see citing works
“Reelin can modulate[32_TD$DIFF] synaptic plasticity and [519_TD$DIFF]contributes to the dendrites development, [500_TD$DIFF]and short-term and long-term potentiation (Ogawa et al., 1995; Stranahan et al., 2013).”
Eastwood, S. L., & Harrison, P. J. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001399 · Cited by 208 · see citing works
Activation 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
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
“Reelin is a large extracellular matrix glycoprotein that is secreted by cortical Cajal–Retzius cells located in the marginal zone during embryonic development and serves as a positioning cue for the ventricular migrating neurons (Ogawa et al., 1995; SchiVmann, Bernier, & GoYnet, 1997).”
BackgroundJossin, Y., Ignatova, N. G., Hiesberger, T., Herz, J., de Rouvroit, C. L., & Goffinet, A. M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3408-03.2004 · Cited by 198 · see citing works
“The N-terminal region of Reelin is considered important, because it contains the epitope of the function-blocking CR50 antibody ( Ogawa et al., 1995; Miyata et al., 1997; Nakajima et al., 1997).”
InfluentialAnalysis of the RELN gene as a genetic risk factor for autism
Skaar, D. A., Shao, Y., Haines, J. L., Stenger, J. E., Jaworski, J. M., Martin, E. R., DeLong, G. R., Moore, J. H., McCauley, J. L., Sutcliffe, J. S., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001614 · Cited by 197 · see citing works
Hevner, R. F., Neogi, T., Englund, C., Daza, R. A. M., & Fink, A. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00641-7 · Cited by 197 · see citing works
“, tein that acts as a signal in the marginal zone, to regulate who proposed that C–R neurons may be produced and the migrations of cortical plate neurons, which express the added to the marginal zone continuously throughout receptor molecules VLDLR and ApoER2 [12,13,23,40].”
BackgroundIguchi, T., Sakata, K., Yoshizaki, K., Tago, K., Mizuno, N., & Itoh, H. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m708919200 · Cited by 195 · see citing works
Hedgehog signaling is involved in development of the neocortex
Komada, M., Saitsu, H., Kinboshi, M., Miura, T., Shiota, K., & Ishibashi, M. (2008) · Development · doi:10.1242/dev.015891 · Cited by 195 · see citing works
“CR neurons express reelin, a large secreted protein that is associated with extracellular matrix (Ogawa et al., 1995; Schiffmann et al., 1997), and calretinin, a Ca2+-binding protein (Alcantara et al., 1998; del Rio et al., 1995).”
BackgroundCosta, E., Davis, J. M., Grayson, D. R., Guidotti, A., Pappas, G. D., & Pesold, C. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2001.0436 · Cited by 197 · see citing works
Borrell, V., del Rı́o, J. A., Alcántara, S., Derer, M., Martı́nez, A., D’Arcangelo, G., Nakajima, K., Mikoshiba, K., Derer, P., Curran, T., et al. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-04-01345.1999 · Cited by 195 · see citing works
“…wt/ rl , Wild-type/ reeler pattern: co-cultures showing intermediate ( rl ) or (wt) pattern of termination. neuronal migration resembling those of reeler mice (Ohshima et al., 1996; Chae et al., 1997; Goldowitz et al., 1997; Gonza´lez et al., 1997; Howell et al., 1997a; Sheldon et al., 1997).”
BackgroundReceptor 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
“These results are in accordance with earlier observations that an antibody against the CR-50 epitope antagonizes Reelin function in vitro and in vivo (25, 26).”
ResultReelin 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
Self-citationMolecular neuropathology of human mesial temporal lobe epilepsy
Blümcke, I., Beck, H., Lie, A. A., & Wiestler, O. D. (1999) · Epilepsy Research · doi:10.1016/s0920-1211(99)00052-2 · Cited by 188 · see citing works
“Indeed, knockout mice deficient for the reeler gene show severely altered laminar organization of cortical neurons (D'Arcangelo et al., 1995; Ogawa et al., 1995).”
BackgroundRescue of Ataxia and Preplate Splitting by Ectopic Expression of Reelin in reeler Mice
Magdaleno, S. M., Keshvara, L. M., & Curran, T. (2002) · Neuron · doi:10.1016/s0896-6273(02)00582-2 · Cited by 186 · see citing works
“, anti-Reelin antibodies CR-50 (1:200) (Ogawa et al., 1995) and G10 Ogawa, M., and Mikoshiba, K. (1996). Detection of the reelin (1:1000) (de Bergeyck et al.”
InfluentialNova2 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
Disabled-1 Binds to the Cytoplasmic Domain of Amyloid Precursor-Like Protein 1
Homayouni, R., Rice, D. S., Sheldon, M., & Curran, T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07507.1999 · Cited by 184 · see citing works
“The gene disrupted in reeler mice, reelin (D’Arcangelo et al., 1995), encodes a large extracellular protein that is secreted by pioneer neurons in several regions of the developing brain (Ogawa et al., 1995; D’Arcangelo et al., 1997).”
BackgroundHevner, R. F., Daza, R. A. M., Englund, C., Kohtz, J., & Fink, A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.11.033 · Cited by 180 · see citing works
“Another molecule that regulates radial migration in the cortex is reelin (D’Arcangelo et al., 1995; Ogawa et al., 1995 ).”
Regulation of Purkinje Cell Alignment by Reelin as Revealed with CR-50 Antibody
Miyata, T., Nakajima, K., Mikoshiba, K., & Ogawa, M. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03599.1997 · Cited by 183 · see citing works
“In addition to its application in vitro (Ogawa et al., 1995; Del Rı́o et al., 1997), CR-50 can be used for functional experiments in vivo (Nakajima et al., 1996).”
BackgroundMethodInfluentialSelf-citationSekine, 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
“Reelin is an extracellular protein secreted from the Cajal-Retzius cells in the MZ (D’Arcangelo et al., 1995; Ogawa et al., 1995).”
Bergeyck, V. D., Naerhuyzen, B., Goffinet, A. M., & de Rouvroit, C. L. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(98)00024-7 · Cited by 180 · see citing works
- Authors
- Ogawa, M., Miyata, T., Nakajimat, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., & Mikoshibat, K.
- Affiliations
- Kochi Medical School Hospital (JP)
- National Institute for Physiological Sciences (JP)
- National Institute of Neuroscience (JP)
- Institute of Medical Science, The University of Tokyo (JP)
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1995-05
- Volume
- 14
- Issue
- 5
- Pages
- 899-912
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2036838270
- Cited by
- 889
- References
- 61
- Citations by year
- 2026: 4 · 2025: 12 · 2024: 5 · 2023: 20 · 2022: 16 · 2021: 21 · 2020: 22 · 2019: 25 · 2018: 20 · 2017: 23 · 2016: 22 · 2015: 25 · 2014: 18 · 2013: 32 · 2012: 25
- FWCI
- 10.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- 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
- Cajal-Retzius neurons, cortical lamination, neocortex development, histogenesis
- MeSH terms
- Reelin Protein, Animals, Antibodies, Monoclonal, Cell Adhesion, Cell Communication, Cerebral Cortex, Extracellular Space, Hybridomas, Immunohistochemistry, Mice, Neurologic Mutants, Mutation, Nerve Tissue Proteins, Neurons, Serine Endopeptidases, Tissue Distribution, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Mice
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