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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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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]
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Prume, M., Rollenhagen, A., & Lübke, J. H. R. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00080 · Cited by 8
“This could lead to an imbalance of intracortical vs. thalamocortical inputs and may thus contribute to either a possible impairment or more likely to facilitation of intracortical network activity resulting in epileptic seizures observed in reeler (Patrylo et al., 2006).”
BackgroundCajal-Retzius cells: organizers of cortical development
Kilb, W., & Frotscher, M. (2016) · e-Neuroforum · doi:10.1007/s13295-016-0031-5 · Cited by 8
Disrupted in Schizophrenia 1 regulates the processing of reelin in the perinatal cortex
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“Heterozygous reeler were chosen over homozygous reeler mice because DISC1 mouse models (both knockdown animals and those expressing mutant variants of the protein) show subtle behavioural and cognitive deficits (Lipina and Roder, 2014) which would likely not be detectable on the background of the gross rearrangements…”
BackgroundReelin Mediates Hippocampal Cajal-Retzius Cell Positioning and Infrapyramidal Blade Morphogenesis
Ha, S., Tripathi, P. P., Daza, R. A. M., Hevner, R. F., & Beier, D. R. (2020) · Journal of Developmental Biology · doi:10.3390/jdb8030020 · Cited by 7
Neurobiología del desarrollo temprano
Olivé, M. L. P. (2013) · Contextos Educativos Revista de Educación · doi:10.18172/con.487 · Cited by 7
Osumi, N., & Kikkawa, T. (2013) · Springer eBooks · doi:10.1007/978-4-431-54496-8_3 · Cited by 8
New Genetic Insights into Cerebral Cortical Development
Gleeson, J. G., & Walsh, C. A. (1997) · Research and perspectives in neurosciences · doi:10.1007/978-3-642-60861-2_9 · Cited by 7
The Reelin Gene and Its Functions in Brain Development
Huang, C.-C., & D’Arcangelo, G. (2008) · Springer eBooks · doi:10.1007/978-0-387-76761-1_1 · Cited by 8
Microarray Analysis of the Fetal Hippocampus in the Emx2 Mutant
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“…that the Apoe receptor Apoer2 (Lrp8) is also a receptor for the extracellular matrix protein reelin [Hiesberger et al., 1999; Trommsdorff et al., 1999], essential for hippocampal [Del Rio et al., 1997; Nakajima et al., 1997] and cortical [D’Arcangelo et al., 1995; Ogawa et al., 1995] development.”
BackgroundThe Role of Neurodevelopmental Genes in Infectious Etiology of Autism
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Polleux, F., & Anton, E. S. (2006) · Kluwer Academic Publishers-Plenum Publishers eBooks · doi:10.1007/0-387-28117-7_8 · Cited by 7
Casciano, F., Bianchi, N., Borin, M., Vellani, V., Secchiero, P., Bergamini, C. M., Capsoni, S., & Pignatelli, A. (2023) · Biology · doi:10.3390/biology12030367 · Cited by 6
“During development and maturation of the Central Nervous System (CNS), Reelin is involved in cortical and hippocampal layering [68,69], neuroblasts detachment [70], differentiation of radial cells [71], neurogenesis and gliogenesis processes [72].”
BackgroundComparative analyses of the Smith−Magenis syndrome protein RAI1 in mice and common marmoset monkeys
Chang, Y., Lee, Y., Haque, M., Chang, H., Javed, S., Lin, Y. C., Cho, Y., Abramovitz, J., Chin, G. J., Khamis, A., et al. (2024) · The Journal of Comparative Neurology · doi:10.1002/cne.25589 · Cited by 7
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“RELN has been initially studied via the characterization of the 24 reeler (rl/rl) homozygous mouse mutant (3, 29), which shows, amongst a large panel of 25 phenotypes, a profound disorganization of cortical lamination, largely due to an impairment in 26 migration of pyramidal neurons (2, 30).”
BackgroundMethodDifferent activity patterns control various stages of Reelin synthesis in the developing neocortex
Engeroff, K., Warm, D., Bittner, S., & Blanquie, O. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad210 · Cited by 5
“In accordance with previous reports (Ogawa et al. 1995; Alcántara et al. 1998; Chowdhury et al. 2010; Ma et al. 2014; Ledonne et al. 2016), we show that CRs represent the main source of Reelin at birth and”
BackgroundResultHormonal and morphological study of the pituitaries in reeler mice
Lombardero, M., Kovács, K., Horváth, É., & Salazar, I. (2007) · International Journal of Experimental Pathology · doi:10.1111/j.1365-2613.2007.00528.x · Cited by 5
“The Reelin protein is synthesized mainly in the Cajal-Retzius neurons of the brain (Ogawa et al. 1995; Schiffmann et al. 1997) but it is also expressed in the spinal cord and retina (Schiffmann et al. 1997) and outside the nervous system, mainly in the liver but also in spleen, thymus, kidney,…”
BackgroundRadial Migration of Neurons in the Cerebral Cortex
Stanco, A., & Anton, E. S. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00028-4 · Cited by 5
Genetics of Central Nervous System Developmental Disorders
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Neuronal Migration of Guidepost Cells
Bielle, F., & Garel, S. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00037-5 · Cited by 5
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RAKIC, P. T. (2000) · Results and problems in cell differentiation · doi:10.1007/978-3-540-48002-0_1 · Cited by 5
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Gumnit, E., Gattoni, G., Woych, J., Deryckere, A., Bhattarai, P., Gillis, J. A., Kızıl, Ç., & Tosches, M. A. (2026) · Current Biology · doi:10.1016/j.cub.2026.03.082 · Cited by 4
Repurposing Reelin: The new role of radial glia, Reelin and Notch in motor neuron migration
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Safety of Anti-Reelin Therapeutic Approaches for Chronic Inflammatory Diseases
Calvier, L., Alexander, A., Marckx, A. T., Kounnas, M. Z., Durakoglugil, M. S., & Herz, J. (2024) · Cells · doi:10.3390/cells13070583 · Cited by 6
“The same year, a mouse monoclonal anti-Reelin antibody was developed [110], having the remarkable ability to block Reelin function [110–116], but also to deplete it from the circulation when administered by intravenous or intraperitoneal injection [53,72,74].”
BackgroundBrain Malformations Associated with Cell Migration
Nasrallah, I. M., & Golden, J. A. (2006) · Pediatric and Developmental Pathology · doi:10.2350/06-04-0077.1 · Cited by 4
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García‐Moreno, F., & Molnár, Z. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814407-7.00025-0 · Cited by 4
Reelin inhibits migration of sympathetic preganglionic neurons in the spinal cord of the chick
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“…1982; Miyata et al., 1997; Frotscher, 1997; Dulabon et al., 2002; Hack et al., 2002), an attractive signal (Goffinet, 1997), a repulsive signal (Ogawa et al., 1995; Schiffmann et al., 1997), a cofactor for other guidance cues (Magdaleno et al., 2002), a signal that allows migrating neurons to…”
BackgroundResultInfluentialHumphreys, P., & Hendelman, W. J. (2000) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(00)00002-2 · Cited by 4
“mation in culture include growth factor de®ciencies in the various culture media used (whether de®ned [26] or serum-supplemented), lack of incoming axonal growth cones normally present in the CP in late neuronal migration, or a disturbance in the expression of morphoregulatory molecules such as reelin [20], a-integrin…”
BackgroundGilerovich, E. G., & Grigor’ev, I. P. (2005) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-005-0140-z · Cited by 4
“In mammals, the leading role in the process of the controlled migration of neuroblasts is played by neurons in layer I [1, 3], especially Cajal–Retzius cells [14], which are located in the upper part of layer I.”
BackgroundOrigin and Migration of Olfactory Cajal-Retzius Cells
Frade-Pérez, M. D., Miquelajáuregui, A., & Varela‐Echavarría, A. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00097 · Cited by 4
“…cytomorphology, early birthdate, localization in the neocortical marginal zone, an excitatory (glutamatergic) profile, and expression of the markers Reelin and Calretinin (D’Arcangelo et al., 1995; Ogawa et al., 1995; Grkovic and Anderson, 1997; Meyer et al., 1999; Hevner et al., 2001, 2003a,b).”
BackgroundYabut, O., Renfro, A., Niu, S., Swann, J. W., Marín, Ó., & D’Arcangelo, G. (2005) · Molecular Brain Research · doi:10.1016/j.molbrainres.2005.09.015 · Cited by 4
Cdk5, a Journey from Brain to Pain: Lessons from Gene Targeting
Pareek, T. K., & Kulkarni, A. B. (2008) · Springer eBooks · doi:10.1007/978-0-387-78887-6_15 · Cited by 4
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Differential contribution of P73+ Cajal-Retzius cells and Reelin to cortical morphogenesis
Elorriaga, V., Bouloudi, B., Saillour, Y., Morel, J. S., Delberghe, E., Azzam, P., Moreau, M. X., Stottmann, R. W., Bahi‐Buisson, N., Pierani, A., et al. (2025) · Development · doi:10.1242/dev.204451 · Cited by 4
Morphological study of the postnatal hippocampal development in the TRPV1 knockout mice
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Reelin promotes oligodendrocyte precursors migration via the Wnt/β-catenin signaling pathway
Liu, Y., Wang, Y. Y., Yuan, W., Dong, F., Zhen, F., Liu, J., Yang, L., Qu, X., & Yao, R. (2021) · Neurological Research · doi:10.1080/01616412.2021.1888604 · Cited by 4
“CajalRetzius cells, which are located in the forebrain, secrete high levels of Reelin in the marginal zone during embryonic development [4,5], they also regulate neuron migration and cell layer formation [6], and disappear from the new cortex once neuron migration is complete.”
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“The results brought by Ramón y Cajal showed that the neurons present in the neocortex are arranged in six layers (Ogawa et al. , 1995), as well as having axons and dendrites, responsible for the nerve connections called synapses (Hawkins, 2021, p. 29).”
ResultEpilepsy-Associated Reelin Dysfunction Induces Granule Cell Dispersion in the Dentate Gyrus☆
Frotscher, M., & Haas, C. A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.00032-8 · Cited by 3
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“It is secreted by CajalRetzius cells (Ogawa et al., 1995) and has become a key focus point of study for various mental health-associated illness and conditions such as Alzheimer’s (Botella-Lopez et al., 2006), autism (Serajee, Zhong, & Mahbubul Huq, 2006), bipolar disorder, depression and…”
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“Southern blots showed the t-eGFP reporter as 1.4 kb and 0.82 kb GFP fragments in all triple transgenic mice.”
BackgroundResultInfluentialREELIN IMMUNOREACTIVITY AND MORPHOLOGICAL ANALYSIS OF THE HUMAN VISUAL CORTEX
Tsamis, K. I., Mytilinaios, D. G., Psaroulis, D., Njau, S. N., Costa, V., & Balogiannis, S. (2007) · International Journal of Neuroscience · doi:10.1080/00207450500535974 · Cited by 3
“In fetuses reelin acts on the migration of neuronal precursors, regulating their final positioning and the organization of the laminar cytoarchitecture of the cerebral cortex, the cerebellum, and the hippocampus in order to establish the “inside-out” pattern of layering, which is of highest importance for the developm…”
BackgroundInfluentialMammalian Neural Induction and brain pattern Formation.
Mikoshiba, K. (1999) · The Keio Journal of Medicine · doi:10.2302/kjm.48.111 · Cited by 3
Neuronal Migration and Brain Patterning
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Insights on nervous system biology and anatomy
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“Reelin protein is secreted from neurones in the MZ (Ogawa et al., 1995).”
BackgroundExpression of Neuronal Nitric Oxide Synthase During Embryonic Development of the Rat Optic Vesicle
Nobakht, M., Majidzadeh, S., Fattahi, M., Samadi, M., & Tabatabaee, P. (2007) · Pakistan Journal of Biological Sciences · doi:10.3923/pjbs.2007.1078.1082 · Cited by 3
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Reelin-LRP8 signaling mediates brain dissemination of breast cancer cells via abluminal migration
Huang, H., Zhang, M., Huang, E., Zhao, Y., Li, X., Qiu, P., Li, C., Tao, J., Zhang, Y., Luo, L., et al. (2025) · EMBO Molecular Medicine · doi:10.1038/s44321-025-00260-0 · Cited by 3
“This antibody targets the epitope recognized by the function-blocking CR-50 antibody (D ’ Arcangelo et al, 1997; Ogawa et al, 1995).”
A Tale of Two Genes: Reelin and BDNF
Ringstedt, T. (2008) · Springer eBooks · doi:10.1007/978-0-387-76761-1_16 · Cited by 2
Protein Kinases and Signaling Pathways that Are Activated by Reelin
Cooper, J. A., Allen, N. S., & Feng, L. (2008) · Springer eBooks · doi:10.1007/978-0-387-76761-1_13 · Cited by 2
“The discovery that Reelin is secreted (D’Arcangelo et al., 1995; Ogawa et al., 1995) and acts nonautonomously, as shown by chimera experiments (Terashima et al.”
BackgroundA Career in Child Neurology: Explorations at the Frontiers
DeLong, G. R. (2010) · Journal of Child Neurology · doi:10.1177/0883073810365738 · Cited by 2
Modern slice culture for direct observation of production and migration of brain neurons.
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Self-citationRadial Migration in the Developing Cerebral Cortex
Noctor, S. C., Cunningham, C. L., & Kriegstein, A. R. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00027-2 · Cited by 2
Models of Neurotoxicity Provide Unique Insight into Normal Development
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Lineage-Dependent Electrical Synapse Formation in the Mammalian Neocortex
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Calcium Signaling during Cortical Apical Dendrite Initiation: A Role for Cajal-Retzius Neurons
Enck, J. R., & Olson, E. C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612965 · Cited by 2
Birth, Migration and Function of SVZ-derived Neurons in the Adult Brain
Kohwi, M., Galvão, R. P., & Álvarez-Buylla, A. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/0-387-31389-3_3 · Cited by 2
“What regulates this change in migratory behavior? Reelin is a protein crucial for the laminar organization of the cortex by regulating the final steps in radial migration of cortical neurons (Ogawa et al., 1995).”
BackgroundReelin and Cajal-Retzius Cells
Mienville, J. (2008) · Springer eBooks · doi:10.1007/978-0-387-76761-1_18 · Cited by 2
“The discovery of this protein and of its key function in cortical lamination was made possible by the availability of the reeler mutant mouse (D’Arcangelo et al., 1995; Ogawa et al., 1995 ).”
BackgroundInfluentialCell Fate and Cell Migration in the Developing Cerebral Cortex
Ware, M. L., & Walsh, C. A. (1999) · Elsevier eBooks · doi:10.1016/b978-012505255-9/50037-7 · Cited by 2
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“Interestingly, this mouse has a very prominent cortical phenotype as the layering of the cortex is inverted [13].”
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Sobierajski, E., González‐Gómez, M., González‐Arnay, E., Wahle, P., & Meyer, G. (2025) · Brain Structure and Function · doi:10.1007/s00429-025-02958-w · Cited by 1
“CRc secrete the extracellular matrix protein Reelin (D'Arcangelo et al.1995; Ogawa et al. 1995) that initiates a signaling cascade via the lipoprotein receptors ApoER2 and VLDLR responsible for the laminar positioning of neurons through tyrosine phosphorylation of the adapter protein disabled 1…”
Biochemistry of autism: changes in serotonin, reelin and oxytocin
Mukaetova‐Ladinska, E. B., Westwood, J., & Perry, E. K. (2011) · Cambridge University Press eBooks · doi:10.1017/cbo9780511973918.009 · Cited by 1
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Tangential Cell Movements During Early Telencephalic Development
Carlos, J., & García‐Moreno, F. (2008) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195369007.003.0002 · Cited by 1
Neocortical Neurogenesis and Circuit Assembly
Gao, P., Sultan, K. T., Zhang, X., & Shi, S. (2013) · Springer eBooks · doi:10.1007/978-4-431-54496-8_7 · Cited by 1
Cajal-Retzius cells: organizers of cortical development
Kilb, W., & Frotscher, M. (2016) · e-Neuroforum · doi:10.1515/s13295-016-0031-5 · Cited by 1
Genetic Control of Cajal–Retzius Cell Development
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Molecular signatures of neural connectivity in the olfactory cortex
Diodato, A., de Brimont, M. R., Yim, Y. S., Dérian, N., Perrin, S., Pouch, J., Klatzmann, D., Garel, S., Choi, G. B., & Fleischmann, A. (2015) · RePEc: Research Papers in Economics · Cited by 1
Transcriptional and posttranscriptional mechanisms of neuronal migration
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Topical Review: Neuronal Migration in Developmental Disorders
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Development of the Cerebral Cortex: III. The Reeler Mutation
Lombroso, P. J. (1998) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199803000-00020 · Cited by 1
Characterization of subtypes of precursor cells in the developing central nervous system
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Neurotrophic factors in brain development
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Roles of the Nedd4 Family E3 Ligases in Glial Function and Nerve Cell Development
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Saito, K., Okamoto, M., Watanabe, Y., Noguchi, N., Nagasaka, A., Nishina, Y., Shinoda, T., Sakakibara, A., & Miyata, T. (2019) · SSRN Electronic Journal · doi:10.2139/ssrn.3377361 · Cited by 1
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Intrinsic and Input‐dependent Development of Cortical Neuron Types
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“In addition, the identification of Reln-Lrp8 interaction reinforces the hypothesis that Reelin signaling contributes to adolescent neuronal migration in a manner analogous to its well-established role in embryonic cortical layering 26,74 .”
Akter, S., Mirhosseiniardakani, S., Takekoshi, Y., Qiu, L., Baker, K., Jiang, K. W., Lyon, M., Hattori, M., & Chen, X. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.24.672028 · Cited by 1
“Reeler is a well-characterized Reelin-deficient strain that exhibits “outside-in” cortical lamination, disrupted apical-basal orientation, and a range of other cellular and behavioral abnormalities (Curran et al., 1995; D'Arcangelo et al., 1995; Falconer, 1951; Ogawa et al., 1995).”
Analysis of Reelin function in the molecular mechanisms underlying Alzheimer’s disease
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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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