Intrinsic and extrinsic mechanisms control the termination of cortical interneuron migration
Open accessAbstract
During development, neurons migrate from their site of origin to their final destinations. Upon reaching this destination, the termination of their migration is crucial for building functional architectures such as laminated structures and nuclei. How this termination is regulated, however, is not clear. Here, we investigated the contribution of cell-intrinsic mechanisms and extrinsic factors. Using GAD67-GFP knock-in mice and in utero electroporation cell labeling, we visualized GABAergic neurons and analyzed their motility in vitro. We find that the motility of GABAergic neurons in cortical slices gradually decreases as development proceeds and is almost abolished by the end of the first postnatal week. Consistent with this, a reduction of embryonic interneuron motility occurred in dissociated cultures. This is in part due to cell-intrinsic mechanisms, as a reduction in motility is observed during long-term culturing on glial feeder cells. Cell-intrinsic regulation is further supported by observations that interneurons labeled in early stages migrated more actively than those labeled in late stages in the same cortical explant. We found evidence suggesting that upregulation of the potassium-chloride cotransporter KCC2 underlies this intrinsic regulation. Reduced motility is also observed when embryonic interneurons are plated on postnatal cortical feeder cells, suggesting extrinsic factors derived from the postnatal cortex too contribute to termination. These factors should include secreted molecules, as cultured postnatal cortical cells could exercise this effect without directly contacting the interneuron. These findings suggest that intrinsic mechanisms and extrinsic factors coordinate to reduce the motility of migrating neurons, thereby leading to the termination of migration.
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KCC2 upregulation appears to be part of an intrinsic maturation program that may be common to all interneuron classes.
“Upregulation of KCC2 seems to be part of an intrinsic program of maturation that might be common to all classes of interneurons (Inamura et al., 2012).”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Inamura et al., 2012
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Development and Functional Diversification of Cortical Interneurons
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- Authors
- Inamura, N., Kimura, T., Tada, S., Kurahashi, T., Yanagida, M., Yanagawa, Y., Ikenaka, K., & Murakami, F.
- Affiliations
- National Institute for Physiological Sciences (JP)
- The University of Osaka (JP)
- Gunma University (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-04-25
- Volume
- 32
- Issue
- 17
- Pages
- 6032-6042
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6703612
- OpenAlex
- W2039940084
- Cited by
- 43
- References
- 32
- Citations by year
- 2026: 1 · 2024: 1 · 2023: 2 · 2022: 2 · 2021: 6 · 2020: 7 · 2019: 1 · 2018: 7 · 2017: 1 · 2016: 2 · 2015: 7 · 2014: 1 · 2013: 5
- FWCI
- 1.40
- 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
- Ministry of Education, Culture, Sports, Science and Technology
- Japan Society for the Promotion of Science (24650166)
- 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
- cortical interneuron migration, GABAergic neurons, neuronal motility, KCC2, potassium-chloride cotransporter, cell-intrinsic regulation, external factors, in utero electroporation, cortical lamination
- MeSH terms
- K Cl- Cotransporters, Age Factors, Analysis of Variance, Animals, Animals, Newborn, Cell Movement, Cells, Cultured, Cerebral Cortex, Embryo, Mammalian, Glutamate Decarboxylase, Interneurons, Mice, Transgenic, Neuroglia, Organ Culture Techniques, Time Factors, Electroporation, Gene Expression Regulation, Developmental, Microscopy, Confocal, Statistics, Nonparametric, Symporters, Green Fluorescent Proteins, Mice
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