Cited by 890Neurogenesis and neuroplasticity mechanismsAxon Guidance and Neuronal SignalingDevelopmental Biology and Gene Regulation

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The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons

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Ogawa, Masaharu, Miyata, Takaki, Nakajimat, Kazunori, Yagyu, Kenichi, Seike, Masahiro, Ikenaka, Kazuhiro, Yamamoto, Hiroshi, Mikoshibat, Katsuhiko·1995·Neuron

DOI 10.1016/0896-6273(95)90329-1

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Abstract

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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BackgroundInfluential
The Reeler Mouse: Anatomy of a Mutant
D’Arcangelo, G. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)71016-3 · Cited by 80
“Reelin is abundantly and selectively expressed by Cajal-Retzius cells in the marginal zone of the embryonic cortex and hippocampus (Alcantara et al., 1998; D’Arcangelo et al., 1995; Ogawa et al., 1995) (Fig.”
Background
The functions of Reelin in membrane trafficking and cytoskeletal dynamics: implications for neuronal migration, polarization and differentiation
Santana, J., & Marzolo, M. (2017) · Biochemical Journal · doi:10.1042/bcj20160628 · Cited by 76
Genomic Organization of the MouseReelinGene
Royaux, I. E., de Rouvroit, C. L., D’Arcangelo, G., Demirov, D. G., & Goffinet, A. M. (1997) · Genomics · doi:10.1006/geno.1997.4983 · Cited by 79
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
Ectopic Reelin Induces Neuronal Aggregation with a Normal Birthdate-Dependent “Inside-Out” Alignment in the Developing Neocortex
Kubo, K., Honda, T., Tomita, K., Sekine, K., Ishii, K., Uto, A., Kobayashi, K., Tabata, H., & Nakajima, K. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0486-10.2010 · Cited by 78
Importance of Reelin C-Terminal Region in the Development and Maintenance of the Postnatal Cerebral Cortex and Its Regulation by Specific Proteolysis
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
Developmental distribution of a reeler gene-related antigen in the rat hippocampal formation visualized by CR-50 immunocytochemistry
Drakew, A., Frotscher, M., Deller, T., Ogawa, M., & Heimrich, B. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00326-6 · Cited by 77
Self-citation
The Synaptic Pathology of Schizophrenia: Is Aberrant Neurodevelopment and Plasticity to Blame?
Eastwood, S. L. (2004) · International review of neurobiology · doi:10.1016/s0074-7742(04)59003-7 · Cited by 75
Cortical development: Layers of complexity
Gilmore, E. C., & Herrup, K. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00108-4 · Cited by 81
“The product of the reeler gene, now known as Reelin, is a 385 kDa secreted glycoprotein produced by cells in the marginal zone known as CajalRetzius cells [8–10].”
A leucine‐rich repeat membrane protein, 5T4, is expressed by a subtype of granule cells with dendritic arbors in specific strata of the mouse olfactory bulb
Imamura, F., Nagao, H., Naritsuka, H., Murata, Y., Taniguchi, H., & Mori, K. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20896 · Cited by 78
Subpallial origin of a population of projecting pioneer neurons during corticogenesis
Morante, J., Carleton, A., Ortino, B., Kremer, E. J., Fairén, A., & Lledo, P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1633692100 · Cited by 78
BDNF-modulated Spatial Organization of Cajal–Retzius and GABAergic Neurons in the Marginal Zone Plays a Role in the Development of Cortical Organization
Alcántara, S., Pozas, E., Ibañez, C. F., & Soriano, E. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhi128 · Cited by 71
“The gene disrupted in reeler mice codes for a large extracellular matrix glycoprotein, reelin, which is secreted by Cajal--Retzius (CR) cells (D’Arcangelo et al., 1995; Ogawa et al., 1995).”
Background
Regulation of Cortical Neuron Migration by the Reelin Signaling Pathway
Honda, T., Kobayashi, K., Mikoshiba, K., & Nakajima, K. (2011) · Neurochemical Research · doi:10.1007/s11064-011-0407-4 · Cited by 77
“Thus, Ogawa, in collaboration with Miyata and Nakajima, worked hard to obtain monoclonal antibodies and finally obtained 3 clones, including CR-50, over the course of approximately 3 years [ 23 , 24].”
BackgroundInfluential
Cellular dynamics of neuronal migration in the hippocampus
Hayashi, K., Kubo, K., Kitazawa, A., & Nakajima, K. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00135 · Cited by 80
“Reelin is a giant glycoprotein secreted from Cajal–Retzius cells in the MZ during development (D’Arcangelo et al., 1995; Hirotsune et al., 1995; Ogawa et al., 1995).”
Background
An increase of hippocampal calretinin-immunoreactive neurons correlates with early febrile seizures in temporal lobe epilepsy
Blümcke, I., Beck, H., Suter, B., Hoffmann, D., Födisch, H. J., Wolf, H. K., Schramm, J., Elger, C. E., & Wiestler, O. D. (1999) · Acta Neuropathologica · doi:10.1007/s004010050952 · Cited by 77
“Mice with a mutation in the reelin gene show a severely altered organization of the cerebral cortex [13, 33 ].”
Background
Neurons tend to stop migration and differentiate along the cortical internal plexiform zones in the Reelin signal‐deficient mice
Tabata, H., & Nakajima, K. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10345 · Cited by 74
“Reelin is a huge extracellular matrix protein secreted by Cajal-Retzius neurons in the MZ (D’Arcangelo et al., 1995; Hirotsune et al., 1995; Ogawa et al., 1995).”
Background
Neocortical neurogenesis and neuronal migration
Tan, X., & Shi, S. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.88 · Cited by 85
Involvement of Cajal-Retzius Neurons in Spontaneous Correlated Activity of Embryonic and Postnatal Layer 1 from Wild-Type and Reeler Mice
Aguiló, A., Schwartz, T. H., Kumar, V. S., Peterlin, Z. A., Tsiola, A., Soriano, E., & Yuste, R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-10856.1999 · Cited by 73
“As the cortex develops, the marginal zone becomes layer 1 and CR cells disappear, by either apoptosis or differentiation into nonpyramidal cells (Marı́n-Padilla, 1972; Parnavelas and Edmunds, 1983; Derer and Derer, 1990; Del Rı́o et al., 1995).”
Background
The Early Differentiation of the Neocortex: a Hypothesis on Neocortical Evolution
Supèr, H. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.12.1101 · Cited by 73
Reelin provides an inhibitory signal in the migration of gonadotropin-releasing hormone neurons
Cariboni, A. M., Rakić, S., Liapi, A., Maggi, R., Goffinet, A. M., & Parnavelas, J. G. (2005) · Development · doi:10.1242/dev.02033 · Cited by 74
“For the reelin-blocking experiments, monoclonal anti-reelin antibody (clone CR-50; kindly provided by Kazunori Nakajima, Keio University, Japan) was added to the culture medium every 6 hours at a dilution of 1:100 (Ogawa et al., 1995; Miyata et al., 1997; Nakajima et al., 1997).”
BackgroundMethodInfluential
Neurogenesis and Commitment of Corticospinal Neurons inreeler
Polleux, F., Dehay, C., & Kennedy, H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-23-09910.1998 · Cited by 74
Developmental anatomy of reeler mutant mouse
Katsuyama, Y., & Terashima, T. (2009) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01102.x · Cited by 80
“…in reeler and the preplate remains as a single superficial layer intermingling with Cajal-Retzius cells, which becomes the structure called superplate in the subsequent embryonic stages (Goffinet 1979; Caviness 1982; Derer 1985; Hoffarth et al. 1995; Ogawa et al. 1995; Sheppard and Pearlman 1997).”
Background
Characterization of Lhx9, a novel LIM/homeobox gene expressed by the pioneer neurons in the mouse cerebral cortex
Bertuzzi, S., Porter, F. D., Pitts, A., Kumar, M. E., Agulnick, A. D., Wassif, C. A., & Westphal, H. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00233-0 · Cited by 72
“onset of Lhx9 expression coincides with the initial specification of Cajal-Retzius neurons (Ogawa et al., 1995).”
Increased Excitability and Decreased Sensitivity to GABA in an Animal Model of Dysplastic Cortex
Benardete, E. A., & Kriegstein, A. R. (2002) · Epilepsia · doi:10.1046/j.1528-1157.2002.40901.x · Cited by 73
Evidence for a Cell-Specific Action of Reelin in the Spinal Cord
Phelps, P. E., Rich, R. A., Dupuy, S. T., Ríos, Y., & Wong, T. W. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0580 · Cited by 72
“Some investigators have proposed that Reelin may act to signal radially directed neurons to disengage from the glial fiber, possibly by changing the adhesive interactions or surface properties between the migrating cells and their guidance substrates (Dulabon et al., 2000; Lambert de Rouvrout and Goffinet, 1998; Ogawa…”
Background
Girdin Is an Intrinsic Regulator of Neuroblast Chain Migration in the Rostral Migratory Stream of the Postnatal Brain
Wang, Y., Kaneko, N., Asai, N., Enomoto, A., Isotani-Sakakibara, M., Kato, T., Asai, M., Murakumo, Y., Ota, H., Hikita, T., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1130-11.2011 · Cited by 72
“…anti- -galactosidase antibody (1:5000; Abcam), anti-Reelin monoclonal antibody (G10, 1:1000; Calbiochem), anti-Reelin antibody (CR-50, 1:1000) (Ogawa et al., 1995), anticalretinin polyclonal antibody (1:500; Millipore), anti-parvalbumin monoclonal antibody (1:2000; Sigma),…”
Neuronal Death Resulting from Targeted Disruption of the Snf2 Protein ATRX Is Mediated by p53
Seah, C., Levy, M. A., Jiang, Y. Y., Mokhtarzada, S., Higgs, D. R., Gibbons, R. J., & Bérubé, N. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4048-08.2008 · Cited by 74
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 74
Tangential migration of glutamatergic neurons and cortical patterning during development: Lessons from Cajal‐Retzius cells
Barber, M., & Pierani, A. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22363 · Cited by 76
“…where they are best known for regulating the radial migration of pyramidal neurons and the formation of cortical layers through their secretion of the extracellular matrix protein Reelin (Falconer, 1951; D’Arcangelo et al., 1995; Ogawa et al., 1995; D’Arcangelo, 2006; Sekine et al., 2014).”
Background
Consequences of prenatal cocaine exposure in nonhuman primates
Lidow, M. S. (2003) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.09.001 · Cited by 70
Protein kinase C and receptor kinase gene expression in olfactory receptor neurons
Bruch, R. C., Kang, J., Moore, M. L., & Medler, K. F. (1997) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199710)33:4 · Cited by 17
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 76
Neuroanatomical phenotypes in the Reeler mouse
Badea, A., NICHOLLS, P. J., Johnson, G. A., & Wetsel, W. C. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.053 · Cited by 70
“Subsequently, reelin was found to be an extracellular matrix glycoprotein that is secreted by certain neurons (D’Arcangelo et al., 1995;Ogawa et al., 1995), such as Cajal-Retzius cells in the cortical marginal zones and granule cells in cerebellum (Tissir and Goffinet, 2003).”
BackgroundInfluential
Comparative aspects of p73 and Reelin expression in Cajal-Retzius cells and the cortical hem in lizard, mouse and human
Cabrera‐Socorro, A., Hernandez-Acosta, N. C., González‐Gómez, M., & Meyer, G. (2007) · Brain Research · doi:10.1016/j.brainres.2006.11.015 · Cited by 70
Abnormal laminar position and dendrite development of interneurons in the reeler forebrain
Yabut, O., Renfro, A., Niu, S., Swann, J. W., Marín, Ó., & D’Arcangelo, G. (2006) · Brain Research · doi:10.1016/j.brainres.2005.09.070 · Cited by 73
“This pattern of expression is consistent with that previously reported (Oliva et al., 2000).”
BackgroundMethodResultInfluential
Calretinin-immunoreactivity during postnatal development of the rat isocortex: a qualitative and quantitative study
Schierle, G. S. K. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.2.130 · Cited by 69
“Recent reports have demonstrated that CR-immunoreactive neurons in layer I express a specific extracellular matrix protein which is involved in the organization of layers within the developing cortex (D’Arcangelo et al., 1995, Ogawa et al., 1995).”
Background
Cyclin-Dependent Kinase 5/p35 Contributes Synergistically with Reelin/Dab1 to the Positioning of Facial Branchiomotor and Inferior Olive Neurons in the Developing Mouse Hindbrain
Ohshima, T., Ogawa, M., Takeuchi, K., Takahashi, S., Kulkarni, A. B., & Mikoshiba, K. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-10-04036.2002 · Cited by 69
“These mutant mice exhibit nearly identical phenotypes, suggesting that the gene products mutated in these mice, Reelin and Dab1, respectively, act in a common signaling pathway during cortical development (D’Arcangelo et al., 1995; Ogawa et al., 1995; Sheldon et al., 1997; Yoneshima et al., 1997; Rice et al., 1998; Ho…”
BackgroundSelf-citation
Single-cell transcriptomics of the early developing mouse cerebral cortex disentangle the spatial and temporal components of neuronal fate acquisition
Moreau, M. X., Saillour, Y., Cwetsch, A. W., Pierani, A., & Causeret, F. (2021) · Development · doi:10.1242/dev.197962 · Cited by 73
Migration Speed of Cajal-Retzius Cells Modulated by Vesicular Trafficking Controls the Size of Higher-Order Cortical Areas
Barber, M., Arai, Y., Morishita, Y., Vigier, L., Causeret, F., Borello, U., Ledonné, F., Coppola, E., Contremoulins, V., Pfrieger, F. W., et al. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.028 · Cited by 77
Cajal–Retzius cells: Update on structural and functional properties of these mystic neurons that bridged the 20th century
Kirischuk, S., Luhmann, H. J., & Kilb, W. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.009 · Cited by 72
The RELN Locus in Alzheimer's Disease
Seripa, D., Matera, M. G., Franceschi, M., Daniele, A., Bizzarro, A., Rinaldi, M., Panza, F., Fazio, V. M., Gravina, C., D’Onofrio, G., et al. (2008) · Journal of Alzheimer s Disease · doi:10.3233/jad-2008-14308 · Cited by 69
“…is an extracellular matrix serine protease that has been suggested pivotal for the normal cerebral and cerebellar cortical layer during neurodevelopment [8, 26], and several lines of evidence suggests that it is also involved in synaptogenesis and neuronal plasticity in the adult brain [18,30,31].”
Embryonic Expression of the Myelin Basic Protein Gene: Identification of a Promoter Region That Targets Transgene Expression to Pioneer Neurons
Landry, C. F., Pribyl, T. M., Ellison, J. A., Givogri, M. I., Kampf, K., Campagnoni, C. W., & Campagnoni, A. T. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07315.1998 · Cited by 67

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)
ORCID: Miyata, Takaki
Seike, Masahiro
Ikenaka, Kazuhiro
Yamamoto, Hiroshi
Venue: Neuron
Publisher: Elsevier BV
Published: 1995-05
Volume: 14
Issue: 5
Pages: 899-912
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/0896-6273(95)90329-1
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 6652 d)
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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The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons

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