Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus
Open accessAbstract
Adult hippocampal neurogenesis is thought to be essential for learning and memory, and has been implicated in the pathogenesis of several disorders. Although recent studies have identified key factors regulating neuroprogenitor proliferation in the adult hippocampus, the mechanisms that control the migration and integration of adult-born neurons into circuits are largely unknown. Reelin is an extracellular matrix protein that is vital for neuronal development. Activation of the Reelin cascade leads to phosphorylation of Disabled-1, an adaptor protein required for Reelin signaling. Here we used transgenic mouse and retroviral reporters along with Reelin signaling gain-of-function and loss-of-function studies to show that the Reelin pathway regulates migration and dendritic development of adult-generated hippocampal neurons. Whereas overexpression of Reelin accelerated dendritic maturation, inactivation of the Reelin signaling pathway specifically in adult neuroprogenitor cells resulted in aberrant migration, decreased dendrite development, formation of ectopic dendrites in the hilus, and the establishment of aberrant circuits. Our findings support a cell-autonomous and critical role for the Reelin pathway in regulating dendritic development and the integration of adult-generated granule cells and point to this pathway as a key regulator of adult neurogenesis. Moreover, our data reveal a novel role of the Reelin cascade in adult brain function with potential implications for the pathogenesis of several neurological and psychiatric disorders.
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Overexpression of reelin accelerates dendritic development of adult-born neurons and increases the number of synaptic contacts in the dentate gyrus, whereas the absence of reelin signaling reduces dendritic tree complexity on new granule neurons.
“Overexpression of reelin accelerates dendritic development of adult-born neurons and increases the number of synaptic contacts in the dentate gyrus (Pejadas et al., 2010; Teixeira et al., 2012), whereas the absence of reelin signaling reduces dendritic tree complexity on new granule neurons (Teixeira et al., 2012).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Teixeira et al., 2012
Disruption of reelin signaling in hippocampal stem cells causes aberrant migration such that new granule neurons are scattered throughout the dentate gyrus area, where they form aberrant dendrites.
“Disruption of reelin signaling in hippocampal stem cells causes aberrant migration such that new granule neurons are scattered throughout the dentate gyrus area, where they form aberrant dendrites (Teixeira et al., 2012).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Teixeira et al., 2012
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Self-citationBosch, C., Masachs, N., Exposito-Alonso, D., Martínez, A., Teixeira, C. M., Fernaud, I., Pujadas, L., Ulloa, F., Comella, J. X., DeFelipe, J., et al. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw216 · Cited by 70 · see citing works
Self-citationFenton, E. Y., Fournier, N. M., Lussier, A. L., Romay-Tallon, R., Caruncho, H. J., & Kalynchuk, L. E. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.02.001 · Cited by 69 · see citing works
Reelin proteolysis affects signaling related to normal synapse function and neurodegeneration
Lussier, A. L., Weeber, E. J., & Rebeck, G. W. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00075 · Cited by 31 · see citing works
- Authors
- Teixeira, C. M., Kron, M. M., Masachs, N., Zhang, H., Lagace, D. C., Martinez, A., Reillo, I., Duan, X., Bosch, C., Pujadas, L., Brunso, L., Song, H., Eisch, A. J., Borrell, V., Howell, B. W., Parent, J. M., & Soriano, E.
- Affiliations
- University of Michigan (US)
- University of Ottawa (CA)
- Universitat de Miguel Hernández d'Elx (ES)
- Johns Hopkins University (US)
- Instituto de Salud Carlos III (ES)
- The University of Texas Southwestern Medical Center (US)
- State University of New York (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-08-29
- Volume
- 32
- Issue
- 35
- Pages
- 12051-12065
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3475414
- OpenAlex
- W2085446287
- Cited by
- 97
- References
- 82
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 4 · 2023: 8 · 2022: 9 · 2021: 5 · 2020: 5 · 2019: 4 · 2018: 3 · 2017: 10 · 2016: 8 · 2015: 10 · 2014: 8 · 2013: 12
- FWCI
- 3.23
- 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)
- Europe PMC (PubMed Central) (acceptedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- Epilepsy Foundation
- Ministerio de Ciencia e Innovación (CSD2007-00023)
- Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas
- National Institutes of Health
- National Institute of Mental Health (R33MH087874)
- National Institute of Neurological Disorders and Stroke (R01NS073662, R56NS047344, NS-058585, R01NS058585)
- National Institute of Environmental Health Sciences (R21ES021957)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- Reelin signaling, adult hippocampal neurogenesis, Disabled-1, dendritic development, neuronal migration, granule cells, cell-autonomous signaling
- MeSH terms
- Reelin Protein, Age Factors, Aging, Animals, Cell Line, Cells, Cultured, Hippocampus, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Nerve Tissue Proteins, Serine Endopeptidases, Signal Transduction, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Rats, Sprague-Dawley, Gene Silencing, Mice, Rats, Neurogenesis
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