The DOI matches its Crossref record; 61 of the 61 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“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]
Citations
Cites
Mode of cell migration to the superficial layers of fetal monkey neocortex
Rakic, P. (1972) · Journal of Comparative Neurology · doi:10.1002/cne.901450105 · Cited by 2,170
Autoradiographic Study of Cell Migration during Histogenesis of Cerebral Cortex in the Mouse
ANGEVINE, J. B., & SIDMAN, R. L. (1961) · Nature · doi:10.1038/192766b0 · Cited by 1,530
Rakic, P. (1974) · Science · doi:10.1126/science.183.4123.425 · Cited by 1,161
Altman, J. (1972) · The Journal of Comparative Neurology · doi:10.1002/cne.901450305 · Cited by 912
Kostović, I., & RAKIC, P. T. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970309 · Cited by 912
The migration of neuroblasts in the developing cerebral cortex.
Berry, M., & Rogers, A. W. (1965) · PubMed · Cited by 674
Allendoerfer, K. L., & Shatz, C. J. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.001153 · Cited by 653
Mechanisms of Cortical Development: A View From Mutations in Mice
Caviness, V. S., & RAKIC, P. T. (1978) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.01.030178.001501 · Cited by 653
Caviness, V. S. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90141-9 · Cited by 639
Falconer, D. S. (1951) · Journal of Genetics · doi:10.1007/bf02996215 · Cited by 539
Research works printed but not linked: 1
- Berry, 1965, The migration of neuroblastin the developing cerebral cortex, J. Anat., 99, 691
Cited by
Sorted by citations
Items 801–890 of 890
Neurotrophic Factors: Versatile Signals for Cell-Cell Communication in the Nervous System
Ibáñez, C. F. (2000) · Results and problems in cell differentiation · doi:10.1007/978-3-540-48002-0_7 · Cited by 1
Mouse Mutations in the Study of Cerebellar Development
Karagogeos, D., & Pavlou, O. (1999) · Springer eBooks · doi:10.1007/978-1-4615-4887-4_4 · Cited by 1
Functional Characterization of Neurexophilins in the Central Nervous system
Benglopoulos, V. (2002) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-96
Regulation of Postnatal Dentate Gyrus Neurogenesis and its Alteration in Experimental Epilepsy.
Kron, M. M. (2010) · Deep Blue (University of Michigan)
Molecular development and laminar distribution of GABAergic interneurons of the cerebral cortex
Lodato, S. (2011) · Università degli Studi di Napoli Federico II · doi:10.6092/unina/fedoa/8450
Alternative signaling pathways triggered by different mechanisms of serpin endocytosis
Li, X. (2006) · edoc (University of Basel) · doi:10.5451/unibas-003907175
“Reelin is a large extracellular protein, which is predominantly synthesized and secreted in the cerebral cortex by the Caja-Retzius cells of the marginal zone, the most outer layer of the developing cortex [D'Arcangelo et al., 1995;Ogawa et al., 1995].”
BackgroundIntegrin signaling and central nervous system development
Belvindrah, R., & Müller, U. (2005) · Advances in developmental biology · doi:10.1016/s1574-3349(05)15005-4
Daniel, A., Palacios-García, I., & González-Billault, C. E. (2013) · InTech eBooks · doi:10.5772/54038 · Cited by 1
“Additionally, migrating neurons fail to establish an inside-out pattern of cortical layers [26].”
BackgroundBarber, M. (2009) · OpenGrey (Institut de l'Information Scientifique et Technique)
Examining Hippocampal Reelin Expression and Neural Plasticity in an Animal Model of Depression
Fenton, E. Y. (2013) · University Library - University of Saskatchewan (University of Saskatchewan)
Parrini, E., & Guerrini, R. (2008) · Springer eBooks · doi:10.1007/978-0-387-76761-1_21
“In this animal model, the cortical layering appears inverted (Caviness, 1976; Ogawa et al., 1995 ).”
BackgroundAssessing cognitive function in animal models of mental retardation
Strupp, B. J., & Diamond, A. D. (1996) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/(sici)1098-2779(1996)2:4 · Cited by 12
A transgene insertion at perinatal lethality (ple) is associated with abnormalities of the cortex
Beier, D. R., Dushkin, H., Stone, L. V., & Sherman, G. F. (1996) · Brain Research · doi:10.1016/0006-8993(96)00380-0
Reelin-Disabled1 signaling in the mature rat cochlear nucleus
Inagaki, A., Ugawa, S., Safwat, M., Keceli, S., Shimada, S., Motohiko, S., & Murakami, S. (2009) · Acta Oto-Laryngologica · doi:10.1080/00016480902911961
“Reelin was originally found as the responsible protein for reeler mice, autosomal recessive spontaneous model characterized by ataxic gait [1,2].”
BackgroundMcGregor, C. (2012) · uO Research (University of Ottawa) · doi:10.20381/ruor-5975
“Most of these functions are performed by the glycoprotein Reelin which is secreted by the Cajal-Retzius cells and is a hallmark of their identity (Ogawa et al., 1995).”
BackgroundIdentification of novel ligands of WDR47, using yeast two-hybrid analysis
McGillewie, L. (2009) · SUNScholar (Stellenbosch University)
Förster, E., Zhao, S., & Frotscher, M. (2008) · Springer eBooks · doi:10.1007/978-0-387-76761-1_11
“Where may radial glial cells encounter Reelin? Immunocytochemistry with antibodies against Reelin suggests that Reelin is predominantly localized in the marginal zone ( Ogawa et al., 1995 ).”
BackgroundHammond, V. E., So, E., Cate, H. S., Britto, J. M., Gunnersen, J. M., & Tan, S.-S. (2010)
REVIEW ARTICLE Comparative aspects of cerebral cortical development
Molnár, Z., Stoykova, A., Tarabykin, V. S., Price, D. J., Francis, F., Meyer, G., Kennedy, H., Curie, M., & Paris (2006)
ALTERNATIVE SIGNALING PATHWAYS TRIGGERED BY DIFFERENT MECHANISMS OF SERPIN ENDOCYTOSIS
Fakultät, P.-N. (2006)
Gedruckt mit Genehmigung des Fachbereichs Veterinärmedizin der Freien Universität Berlin
Brunnberg, L., Staufenbiel, R., Zessin, K.-H., & Fries, R. (2009)
Davoodi, S. (2015) · cIRcle (University of British Columbia) · doi:10.14288/1.0166263
“Cajal-Retzius neurons produces RELN and they are transient neurons acting as path-finders and they become more active upon early laminar organization of cortex (D’Arcangelo et al., 1995; Ogawa et al., 1995).”
BackgroundDAB2IP regulates neuronal migration and neurite development in the developing neocortex
Lee, G. H. (2012) · Rutgers University Community Repository (Rutgers University) · doi:10.7282/t3fn1504
GENETICS OF HUMAN BRAIN MALFORMATIONS
Clark, G. (2005) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/01.con.0000293703.31088.44
Reelin et développement cérébral : état de la question depuis le clonage du gène
Bernier, B., de Bergeyck, V., de Rouvroit, C. L., Royaux, I. E., & Goffinet, A. M. (1998) · médecine/sciences · doi:10.4267/10608/1091
COPY NUMBER VARIANT ANALYSIS OF PATIENTS WITH MALFORMATIONS OF CORTICAL DEVELOPMENT
Kolb, L. E. (2009) · Europe PMC (PubMed Central)
The function of connexin43 in neuronal migration and cortical development
Cina, C. (2010) · cIRcle (University of British Columbia) · doi:10.14288/1.0069727
“This means that the first wave of neurons accumulates above the CP and the following waves of neurons end up residing beneath the previous neurons (Ogawa et al., 1995; D‟Arcangelo et al., 1995).”
BackgroundStructural functional analysis of disabled-1 in regulation of reelin signaling
Huang, Y. (2007) · OhioLink ETD Center (Ohio Library and Information Network)
The intrinsic and synaptic properties of inverted pyramidal cells within the neocortex
Steger, R. (2015) · CUNY Academic Works (City University of New York)
Review Molecular mechanisms of lipoprotein receptor signalling
Herz, J., & Bock, H. H. (2005)
Erratum to “Constructing the mammalian neocortex: the role of intrinsic factors”
Job, C., & Tan, S. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00279-3
From inside-out to outside-in: cortical lamination development in the Reelin-deficient neocortex
Mingo-Moreno, N. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7335
The role of α3β1 integrin in cortical development
Stanco, A. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/5jc4-rs44
Hatanaka, Y., Kawasaki, T., Abe, T., Shioi, G., Kohno, T., Hattori, M., Sakakibara, A., Kawaguchi, Y., & Hirata, T. (2018) · SSRN Electronic Journal · doi:10.2139/ssrn.3299432
Richards, L. J., & Gobius, I. (2011) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.11661956.12854058
Mirnics, K. (2006) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1050652.502557
Inoue, T. (2006) · Encyclopedia of Molecular Cell Biology and Molecular Medicine · doi:10.1002/3527600906.mcb.200300096
Mechanismen der Entwicklung des zerebralen Kortex
Mühlfriedel, S. (2005) · doi:10.53846/goediss-670
Schizophrenie als Gyrifikationsstörung?
Schulenberg, W. (2010) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-794
WDFY3 cell autonomously controls neuronal migrationPreprint
Schaaf, Z. A., Tat, L., Cannizzaro, N., Green, R., Rülicke, T., Hippenmeyer, S., & Zarbalis, K. S. (2022) · Research Square · doi:10.21203/rs.3.rs-1316167/v1
“produced by Cajal-Retzius cells occupying the marginal zone during development [52].”
BackgroundRadial migration in the developing cerebral cortex
Noctor, S. C., Cunningham, C. L., & Kriegstein, A. R. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814407-7.00015-8 · Cited by 2
Topical Review: Neuronal Migration in Cortical Development
Kanatani, S., Tabata, H., & Nakajima, K. (2004) · Journal of Child Neurology · doi:10.1177/08830738040190030201
Marín‐Padilla, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01423-x
Neuronal migration of guidepost cells
Bielle, F., & Garel, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814407-7.00020-1
Noguchi, H., Li, G., & Pleasure, S. J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814407-7.00017-1
Ventriculo-Pial Patterning of Neural Tube
Ishikawa, Y., Yamamoto, N., & Hagio, H. (2022) · Springer eBooks · doi:10.1007/978-981-19-4324-9_7
Cortical Neuron Migration in Health and Disease
Javier‐Torrent, M., & Nguyen, L. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch17
Cell behaviors that pattern developing tissues: the case of the vertebrate nervous system
Rocha-Martins, M. (2023) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2023.11.003
Tesfaye, M., Jaholkowski, P. P., Hindley, G., Shadrin, A. A., Rahman, Z., Bahrami, S., Lin, A., Holen, B., Parker, N., Cheng, W., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23819884
Tesfaye, M., Jaholkowski, P. P., Hindley, G., Shadrin, A. A., Rahman, Z., Bahrami, S., Lin, A., Holen, B., Parker, N., Cheng, W., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23819890
Tesfaye, M., Jaholkowski, P. P., Hindley, G., Shadrin, A. A., Rahman, Z., Bahrami, S., Lin, A., Holen, B., Parker, N., Cheng, W., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23819893
Ichikawa, R. (2025) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2025.1560972
Utilizing cues from developmental neurogenesis and gliogenesis for better in vitro brain models
Gallagher, M. L., Parri, H. R., Ross, E. A., & Hill, E. J. (2025) · Artificial Cells Nanomedicine and Biotechnology · doi:10.1080/21691401.2025.2562828
“Axial alignment is a key feature of corticogenesis in vivo , with an amalgamation of signalling and transcription factors as well as architecture to guide the building of complex cortical layers [31–33].”
Sommer, N., Pacheco, A., Jorge Carvajal, C., Olguín, H. C., Leiva, A., Gutiérrez, J., & Marzolo, M. (2025) · Research Square · doi:10.21203/rs.3.rs-7934067/v1
Moan, K., Machold, R. P., & Quattrocolo, G. (2025) · The Journal of Comparative Neurology · doi:10.1002/cne.70106
“This regulation of PN migration by CR cells is required for the formation of the six-layered isocortex (D’Arcangelo et al. 1995; Ogawa et al. 1995).”
Zhu, Y., Kitagawa, K., Mori, D., Matsuzaki, T., Nagai, T., Nabeshima, T., Takemoto‐Kimura, S., Ikesue, H., Ozaki, N., Mizoguchi, H., et al. (2025) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2025.178407 · Cited by 1
Transcriptional Regulation of the Tbr1-CASK-CINAP Protein Complex in Response to Neuronal Activity
Hsueh, Y. (2007) · Springer eBooks · doi:10.1007/978-0-387-73609-9_3
Tesfaye, M., Jaholkowski, P., Hindley, G., Shadrin, A. A., Rahman, Z., Bahrami, S., Lin, A., Holen, B., Parker, N., Cheng, W., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23819881
Tesfaye, M., Jaholkowski, P., Hindley, G., Shadrin, A. A., Rahman, Z., Bahrami, S., Lin, A., Holen, B., Parker, N., Cheng, W., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23819878
Tesfaye, M., Jaholkowski, P., Hindley, G., Shadrin, A. A., Rahman, Z., Bahrami, S., Lin, A., Holen, B., Parker, N., Cheng, W., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23819887
van Bruggen, R., Freyre, K. M., Vasanthkumar, S., Wang, M., & Tan, Q. (2026) · eNeuro · doi:10.1523/eneuro.0245-25.2025
“CR cells are best known for their production of reelin, an extracellular glycoprotein critical for cortical lamination (Ogawa et al., 1995; Vilchez-Acosta et al., 2022).”
Reelin regulates the migration and differentiation of extravillous trophoblastic cells
Sommer, N., Alarcón-Godoy, C., Pizarro, H., Pacheco, A., Carvajal, J. A., Olguín, H. C., Gutiérrez, J., Leiva, A., & Marzolo, M. (2026) · Biological Research · doi:10.1186/s40659-026-00690-1 · Cited by 1
“Reelin is a large extracellular matrix glycoprotein secreted during central nervous system (CNS) development [1–3], which regulates neuronal migration and positioning in the cortex, hippocampus and cerebellum.”
Bouamrane, L. (2015) · theses.fr (ABES) · doi:10.70675/00597159za953z4221z95b8z57a6c1d48c8e
Donato, V. D. (2016) · theses.fr (ABES) · doi:10.70675/822ddbd4zef67z4ba8za80bz1f051bf30dda
Cohen, R. (2018) · theses.fr (ABES) · doi:10.70675/759ed785ze142z4504za8abzd5cf222c1a59
Assembling layer 1 of the neocortex : roles of Cajal-Retzius cells
Genescu, I. (2020) · theses.fr (ABES) · doi:10.70675/3fe1b21cz5c6bz4150z94e6zd77163aba0ad
Leprince, E. (2021) · theses.fr (ABES) · doi:10.70675/ea9385dbz28a4z4b9ez8a79zabae124a5f5b
Reelin in vulnerability and sex-dependent maturational trajectories of the prefrontal cortex
Silva-Hurtado, T. J. (2021) · theses.fr (ABES) · doi:10.70675/ecf0031ez1ac8z4688za735za4cd9acfc52c
Cajal-Retzius cells and Reelin in mouse cortical development and human pathologies
Riva, M. (2021) · theses.fr (ABES) · doi:10.70675/b321eca5ze455z480bzb6d4z43505d8c9faf
Gènes cibles des hormones thyroïdiennes, un regard nouveau par le prisme des analyses pangénomiques
Zekri, Y. (2022) · theses.fr (ABES) · doi:10.70675/f8d646ffzf184z40e1z848az174a3d652f5d
Kohno, T., Okino, R., Li, M., & Hattori, M. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.2137-25.2026
Abnormal dispersion of a purkinje cell subset in the mouse mutant cerebellar deficient folia (cdf)
Beierbach, E., Park, C., Ackerman, S. L., Goldowitz, D., & Hawkes, R. B. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1052
“The perinatal Purkinje cell clusters in the AZ seem to transform 1:1 into the zebrin II1/zebrin II2 bands (for example, the three subdivisions of P12 appear to derive from three discrete embryonic Purkinje cell clusters (mouse: Ozol and Hawkes, 1997; rat: Ji and Hawkes, 1995).”
BackgroundSalin (1998) · doi:10.1002/(sici)1096-9861(19980720)397:1
Elmquist (1998) · doi:10.1002/(sici)1096-9861(19980615)395:4
Broca's region revisited: Cytoarchitecture and intersubject variability
Amunts, K., Schleicher, A., B�rgel, U., Mohlberg, H., Uylings, H. B. M., & Zilles, K. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990920)412:2
Herman (2000) · doi:10.1002/1096-9861(20000703)422:3
Diagnostic criteria for primary progressive mutiple sclerosis: a position paper.
(2000) · Pure Amsterdam UMC · doi:10.1002/1531-8249(200006)47:6 · Cited by 2
Yeterian (1998) · doi:10.1002/(sici)1096-9861(19980928)399:3
Day, H. E. W., Curran, E. J., Watson, S. J., & Akil, H. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991011)413:1
Ciliax (1999) · doi:10.1002/(sici)1096-9861(19990621)409:1
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
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
