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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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“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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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Scrambler and yotari disrupt the disabled gene and produce a reeler -like phenotype in mice
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Self-citationCadherin superfamily genes: functions, genomic organization, and neurologic diversityPreprint
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BackgroundSearching for ways out of the autism maze: genetic, epigenetic and environmental clues
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Reelin Binds α3β1 Integrin and Inhibits Neuronal Migration
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The Adult Ventricular–Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis
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“We therefore searched for other markers and discovered, by using the CR50 antibody (Ogawa et al., 1995), that the glycoprotein Reelin is expressed in a large percentage of CGEderived interneurons (Fig.”
BackgroundReelin Is a Secreted Glycoprotein Recognized by the CR-50 Monoclonal Antibody
D’Arcangelo, G., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., & Curran, T. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-01-00023.1997 · Cited by 515
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Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506
“Reelin has variably been proposed to be a chemoattractant (Gilmore and Herrup 2000), repellent (Ogawa et al. 1995; Schiffmann et al. 1997), stop (Sheppard and Pearlman 1997), or detachment (Sheppard and Pearlman 1997; Dulabon et al. 2000; Sanada et al. 2004) signal for migrating neurons.”
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Self-citationMultiple origins of Cajal-Retzius cells at the borders of the developing pallium
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BackgroundLKB1 and SAD Kinases Define a Pathway Required for the Polarization of Cortical Neurons
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“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…”
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“These cells express the calcium-binding protein CR and the extracellular matrix protein, reelin (Ogawa et al., 1995).”
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“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 285
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“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
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Self-citationHow the extracellular matrix shapes neural development
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“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
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Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons
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“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-citationDab1 tyrosine phosphorylation sites relay positional signals during mouse brain development
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“secreted by specialized early neurons that appear to serve as guideposts for subsequent migrations [19,31,32].”
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Reelin glycoprotein: structure, biology and roles in health and disease
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“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 234
“…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
“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 235
Distribution of the uncoupling protein 2 mRNA in the mouse brain
Richard, D., Rivest, R., Huang, Q., Bouillaud, F., Sanchı́s, D., Champigny, O., & Ricquier, D. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980810)397:4 · Cited by 108
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
“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 228
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 222
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 232
“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 221
“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
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 228
“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 209
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 212
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
“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 201
“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 204
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 202
“, 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 199
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
“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
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 196
“…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
“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
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 192
“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 190
“, 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
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 185
“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
“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
“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 186
“Reelin is an extracellular protein secreted from the Cajal-Retzius cells in the MZ (D’Arcangelo et al., 1995; Ogawa et al., 1995).”
de Bergeyck, V., Naerhuyzen, B., Goffinet, A. M., & de Rouvroit, C. L. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(98)00024-7 · Cited by 183
Metadata
- 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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