Reelin-Nrp1 Interaction Regulates Neocortical Dendrite Development in a Context-Specific Manner
Open accessAbstract
Reelin plays versatile roles in neocortical development. The C-terminal region (CTR) of Reelin is required for the correct formation of the superficial structure of the neocortex; however, the mechanisms by which this position-specific effect occurs remain largely unknown. In this study, we demonstrate that Reelin with an intact CTR binds to neuropilin-1 (Nrp1), a transmembrane protein. Both male and female mice were used. Nrp1 is localized with very-low-density lipoprotein receptor (VLDLR), a canonical Reelin receptor, in the superficial layers of the developing neocortex. It forms a complex with VLDLR, and this interaction is modulated by the alternative splicing of VLDLR. Reelin with an intact CTR binds more strongly to the VLDLR/Nrp1 complex than to VLDLR alone. Knockdown of Nrp1 in neurons leads to the accumulation of Dab1 protein. Since the degradation of Dab1 is induced by Reelin signaling, it is suggested that Nrp1 augments Reelin signaling. The interaction between Reelin and Nrp1 is required for normal dendritic development in superficial-layer neurons. All of these characteristics of Reelin are abrogated by proteolytic processing of the six C-terminal amino acid residues of Reelin (0.17% of the whole protein). Therefore, Nrp1 is a coreceptor molecule for Reelin and, together with the proteolytic processing of Reelin, can account for context-specific Reelin function in brain development. SIGNIFICANCE STATEMENT Reelin often exhibits a context-dependent function during brain development; however, its underlying mechanism is not well understood. We found that neuropilin-1 (Nrp1) specifically binds to the CTR of Reelin and acts as a coreceptor for very-low-density lipoprotein receptor (VLDLR). The Nrp1/VLDLR complex is localized in the superficial layers of the neocortex, and its interaction with Reelin is essential for proper dendritic development in superficial-layer neurons. This study provides the first mechanistic evidence of the context-specific function of Reelin (>3400 residues) regulated by the C-terminal residues and Nrp1, a component of the canonical Reelin receptor complex.
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Neuropilin 1 (NRP1) was identified as a coreceptor via binding to a fragment of CTR-RELN consisting of the last six amino acids.
“Recently, neuropilin 1 (NRP1) was identified as a coreceptor via binding to a fragment of CTR-RELN consisting of the last six amino acids. This fragment is removed by furin protease. The uncleaved ‘long’ CTR-RELN interacts with NRP1 and the cleaved ‘short’ CTR-RELN does not11.”
From Resilience to autosomal dominant Alzheimer’s disease in a Reelin-COLBOS heterozygous man (2023) · cites this paper as [11]
The Discussion identifies Nrp1 as a Reelin coreceptor and says the terminal six amino acids are required for their interaction. The Results show binding by Reelin with those residues intact, but do not show that an isolated six-amino-acid fragment binds Nrp1. They describe cleavage by a proprotein convertase family, without identifying furin specifically as the protease. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe uncleaved 'long' CTR-RELN interacts with NRP1 and the cleaved 'short' CTR-RELN does not.
“Recently, neuropilin 1 (NRP1) was identified as a coreceptor via binding to a fragment of CTR-RELN consisting of the last six amino acids. This fragment is removed by furin protease. The uncleaved ‘long’ CTR-RELN interacts with NRP1 and the cleaved ‘short’ CTR-RELN does not11.”
From Resilience to autosomal dominant Alzheimer’s disease in a Reelin-COLBOS heterozygous man (2023) · cites this paper as [11]
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van Battum, E. Y., van den Munkhof, M. H., & Pasterkamp, R. J. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.103012 · Cited by 11 · see citing works
Regulatory mechanism of Reelin activity: a platform for exploiting Reelin as a therapeutic agent
Hattori, M. (2025) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2025.1546083 · Cited by 10 · see citing works
Self-citationREELIN ameliorates Alzheimer's disease, but how?
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Self-citationVisualization of Reelin Secretion from Primary Cultured Neurons by Bioluminescence Imaging
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Self-citationYuasa‐Kawada, J., Kinoshita-Kawada, M., Hiramoto, M., Yamagishi, S., Mishima, T., Yasunaga, S., Tsuboi, Y., Hattori, N., & Wu, J. Y. (2025) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-01330 · Cited by 8 · see citing works
Reelin regulates the migration of late-born hippocampal CA1 neurons via cofilin phosphorylation
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Self-citationRiva, M., Ferreira, S., Medvedeva, V. P., Causeret, F., Henry, O. J., Roux, C., Bellesme, C., Freri, E., Parrini, E., Josifova, D. J., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.25.445586 · Cited by 6 · see citing works
Ishii, K., Kohno, T., & Hattori, M. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.03.004 · Cited by 4 · see citing works
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EphA4 Induces the Phosphorylation of an Intracellular Adaptor Protein Dab1 via Src Family Kinases
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Self-citationBartkowska, K., Koguc-Sobolewska, P., Djavadian, R. L., & Turlejski, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031476 · Cited by 3 · see citing works
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Takekoshi, Y., Ando, H., Kohno, T., Takase, H., Taguchi, T., Arita, M., Kobayashi, T., & Hattori, M. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70225 · Cited by 1 · see citing works
Self-citationStructure of Reelin repeat 8 and the adjacent C-terminal region
Turk, L. S., Currie, M. J., Dobson, R. C. J., & Comoletti, D. (2022) · Biophysical Journal · doi:10.1016/j.bpj.2022.06.002 · Cited by 1 · see citing works
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Self-citationEpilepsy genetics in clinical practice today and for the future
Goldman, A. M., & Noebels, J. L. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-19176-3.00033-9
Cajal-Retzius cells and Reelin in mouse cortical development and human pathologies
Riva, M. (2021) · theses.fr (ABES) · doi:10.70675/b321eca5ze455z480bzb6d4z43505d8c9faf
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Kohno, T., Okino, R., Li, M., & Hattori, M. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.2137-25.2026
Self-citationAashaq, S., Rakhshan, R., Rafiq, A., Ali, M., & Beigh, M. A. (2026) · Gene · doi:10.1016/j.gene.2026.150400
- Authors
- Kohno, T., Ishii, K., Hirota, Y., Honda, T., Makino, M., Kawasaki, T., Nakajima, K., & Hattori, M.
- Affiliations
- Nagoya City University (JP)
- Keio University (JP)
- National Institute of Genetics (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2020-10-02
- Volume
- 40
- Issue
- 43
- Pages
- 8248-8261
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC7577592
- OpenAlex
- W3091003608
- Cited by
- 30
- References
- 78
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 8 · 2023: 6 · 2022: 4 · 2021: 5
- FWCI
- 1.72
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (JP20K07051, JP17K08281, JP18K06508, JP16H06482, JP17H03985)
- Nagoya City University (1922006)
- Takeda Science Foundation
- Keio Gijuku Academic Development Funds
- Keio Gijuku Fukuzawa Memorial Fund for the Advancement of Education and Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- reelin, neuropilin-1, VLDLR, dendrite formation, neocortex development, co-receptors, alternative splicing, Dab1, proteolytic processing, superficial cortical layers, sex differences, Reelin signaling
- MeSH terms
- Reelin Protein, Animals, Cell Line, Dendrites, DNA, Female, Male, Mice, Inbred ICR, Nerve Tissue Proteins, Receptors, LDL, Serine Endopeptidases, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Neocortex, Neuropilin-1, Mice, Gene Knockdown Techniques
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