Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos
Open accessAbstract
Precisely arranged cytoarchitectures such as layers and nuclei depend on neuronal migration, of which many in vitro studies have revealed the mode and underlying mechanisms. However, how neuronal migration is achieved in vivo remains unknown. Here we established an imaging system that allows direct visualization of cortical interneuron migration in living mouse embryos. We found that during nucleokinesis, translocation of the Golgi apparatus either precedes or occurs in parallel to that of the nucleus, suggesting the existence of both a Golgi/centrosome-dependent and -independent mechanism of nucleokinesis. Changes in migratory direction occur when the nucleus enters one of the leading process branches, which is accompanied by the retraction of other branches. The nucleus occasionally swings between two branches before translocating into one of them, the occurrence of which is most often preceded by Golgi apparatus translocation into that branch. These in vivo observations provide important insight into the mechanisms of neuronal migration and demonstrate the usefulness of our system for studying dynamic events in living animals.
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Interneurons born in the MGE, CGE and preoptic region use largely the same cellular mechanisms to move to the cortex and show strong transcriptional similarity at that stage.
“Interneurons from the MGE, CGE and preoptic region use essentially the same cellular mechanisms to translocate to the cortex (Marín et al., 2006; Martini et al., 2009; Yanagida et al., 2012), and it is therefore perhaps not surprising that they exhibit great transcriptional similarity at this stage (Mayer et al., 2018).”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Yanagida et al., 2012
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Cites
The Molecular Biology of Axon Guidance
Tessier‐Lavigne, M., & Goodman, C. S. (1996) · Science · doi:10.1126/science.274.5290.1123 · Cited by 3,295 · see citing works
The origin and specification of cortical interneurons
Wonders, C. P., & Anderson, S. A. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1954 · Cited by 980 · see citing works
C ELL M IGRATION IN THE F OREBRAIN
Marín, Ó., & Rubenstein, J. L. R. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131058 · Cited by 917 · see citing works
Two modes of radial migration in early development of the cerebral cortex
Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R., & Pearlman, A. L. (2001) · Nature Neuroscience · doi:10.1038/83967 · Cited by 689 · see citing works
Roles of Rho-family GTPases in cell polarisation and directional migration
Fukata, M., Nakagawa, M., & Kaibuchi, K. (2003) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(03)00097-8 · Cited by 485 · see citing works
Diverse Migratory Pathways tn the Developing Cerebral Cortex
O’Rourke, N. A., Dailey, M. E., Smith, S. J., & McConnell, S. K. (1992) · Science · doi:10.1126/science.1411527 · Cited by 458 · see citing works
Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue
Tsai, J., Bremner, K. H., & Vallee, R. B. (2007) · Nature Neuroscience · doi:10.1038/nn1934 · Cited by 442 · see citing works
Tanaka, T., Serneo, F. F., Higgins, C., Gambello, M. J., Wynshaw-Boris, A. J., & Gleeson, J. G. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200309025 · Cited by 436 · see citing works
Direct Evidence for Homotypic, Glia-Independent Neuronal Migration
Wichterle, H., García‐Verdugo, J. M., & Álvarez-Buylla, A. (1997) · Neuron · doi:10.1016/s0896-6273(00)80317-7 · Cited by 416 · see citing works
Intracellular Ca2+ Fluctuations Modulate the Rate of Neuronal Migration
Komuro, H., & RAKIC, P. T. (1996) · Neuron · doi:10.1016/s0896-6273(00)80159-2 · Cited by 406 · see citing works
Cytoskeletal coordination during neuronal migration
Schaar, B. T., & McConnell, S. K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506008102 · Cited by 364 · see citing works
Nucleokinesis in Neuronal Migration
Tsai, L., & Gleeson, J. G. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.013 · Cited by 357 · see citing works
Bellion, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1030-05.2005 · Cited by 354 · see citing works
Edmondson, J., & Hatten, M. E. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-06-01928.1987 · Cited by 347 · see citing works
A Primary Role for Golgi Positioning in Directed Secretion, Cell Polarity, and Wound Healing
Yadav, S., Puri, S., & Linstedt, A. D. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-10-1077 · Cited by 294 · see citing works
Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex
Ang, E. S. B. C., Haydar, T. F., Gluncic, V., & Rakic, P. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05805.2003 · Cited by 282 · see citing works
Par6α signaling controls glial-guided neuronal migration
Solecki, D. J., Model, L. S., Gaetz, J., Kapoor, T. M., & Hatten, M. E. (2004) · Nature Neuroscience · doi:10.1038/nn1332 · Cited by 281 · see citing works
Neuronal migration mechanisms in development and disease
Valiente, M., & Marín, Ó. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.12.003 · Cited by 255 · see citing works
Solecki, D. J., Trivedi, N., Govek, E., Kerekes, R. A., Gleason, S. S., & Hatten, M. E. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.028 · Cited by 233 · see citing works
Cell and molecular mechanisms involved in the migration of cortical interneurons
Métin, C., Baudoin, J., Rakić, S., & Parnavelas, J. G. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04630.x · Cited by 216 · see citing works
The Golgi apparatus at the cell centre
Rios, R. M., & Bornens, M. (2003) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00013-3 · Cited by 188 · see citing works
ERK regulates Golgi and centrosome orientation towards the leading edge through GRASP65
Bisel, B., Wang, Y., Wei, J.-H., Xiang, Y., Tang, D., Miron-Mendoza, M., Yoshimura, S.-I., Nakamura, N., & Seemann, J. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200805045 · Cited by 184 · see citing works
Umeshima, H., Hirano, T., & Kengaku, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708047104 · Cited by 182 · see citing works
Tanaka, D. H., Nakaya, Y., Yanagawa, Y., Obata, K., & Murakami, F. (2003) · Development · doi:10.1242/dev.00825 · Cited by 169 · see citing works
Self-citationKappeler, C., Saillour, Y., Baudoin, J., Tuy, F. P. D., Alvarez, C., Houbron, C., Gaspar, P., Hamard, G., Chelly, J., Métin, C., et al. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl062 · Cited by 163 · see citing works
Two forms of cerebellar glial cells interact differently with neurons in vitro.
Hatten, M. E., Liem, R. K. H., & Mason, C. A. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.1.193 · Cited by 148 · see citing works
Komuro, H., & RAKIC, P. T. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-02-01110.1995 · Cited by 147 · see citing works
Martini, F. J., Valiente, M., López Bendito, G., Szabó, G., Moya, F., Valdeolmillos, M., & Marín, O. (2009) · Development · doi:10.1242/dev.025502 · Cited by 147 · see citing works
Centrosome Motility Is Essential for Initial Axon Formation in the Neocortex
de Anda, F. C., Meletis, K., Ge, X., Rei, D., & Tsai, L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0381-10.2010 · Cited by 137 · see citing works
Direct imaging of in vivo neuronal migration in the developing cerebellum
Köster, R. W., & Fraser, S. E. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00585-1 · Cited by 136 · see citing works
A role for mDia, a Rho-regulated actin nucleator, in tangential migration of interneuron precursors
Shinohara, R., Thumkeo, D., Kamijo, H., Kaneko, N., Sawamoto, K., Watanabe, K., Takebayashi, H., Kiyonari, H., Ishizaki, T., Furuyashiki, T., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3020 · Cited by 131 · see citing works
Distel, M., Hocking, J. C., Volkmann, K., & Köster, R. W. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201004154 · Cited by 129 · see citing works
Tanaka, D. H., Maekawa, K., Yanagawa, Y., Obata, K., & Murakami, F. (2006) · Development · doi:10.1242/dev.02382 · Cited by 128 · see citing works
Self-citationYokota, Y., Ghashghaei, H. T., Han, C., Watson, H., Campbell, K., & Anton, E. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000794 · Cited by 127 · see citing works
Martini, F. J., & Valdeolmillos, M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1962-10.2010 · Cited by 125 · see citing works
Tanaka, D. H., Yanagida, M., Zhu, Y., Mikami, S., Nagasawa, T., Miyazaki, J., Yanagawa, Y., Obata, K., & Murakami, F. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5446-08.2009 · Cited by 107 · see citing works
Self-citationLeading Tip Drives Soma Translocation via Forward F-Actin Flow during Neuronal Migration
He, M., Zhang, Z., Guan, C.-B., Xia, D., & Yuan, X. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0240-10.2010 · Cited by 93 · see citing works
SDF1 Regulates Leading Process Branching and Speed of Migrating Interneurons
Lysko, D. E., Putt, M. E., & Golden, J. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3118-10.2011 · Cited by 83 · see citing works
Higginbotham, H., Tanaka, T., Brinkman, B. C., & Gleeson, J. G. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.03.003 · Cited by 68 · see citing works
Köster, R. W., & Fraser, S. E. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0095-06.2006 · Cited by 60 · see citing works
Ohata, S., Kinoshita, S., Aoki, R., Tanaka, H., Wada, H., Tsuruoka-Kinoshita, S., Tsuboi, T., Watabe, S., & Okamoto, H. (2009) · Development · doi:10.1242/dev.033290 · Cited by 40 · see citing works
Ward, M. E., Jiang, H., & Rao, Y. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.08.002 · Cited by 32 · see citing works
Real time analysis of pontine neurons during initial stages of nucleogenesis
Watanabe, H., & Murakami, F. (2009) · Neuroscience Research · doi:10.1016/j.neures.2009.01.007 · Cited by 29 · see citing works
Self-citationHayashi, K., Kawai‐Hirai, R., Harada, A., & Takata, K. (2003) · Journal of Cell Science · doi:10.1242/jcs.00762 · Cited by 26 · see citing works
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Development and Functional Diversification of Cortical Interneurons
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- Authors
- Yanagida, M., Miyoshi, R., Toyokuni, R., Zhu, Y., & Murakami, F.
- Affiliations
- The University of Osaka (JP)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-09-24
- Volume
- 109
- Issue
- 41
- Pages
- 16737-16742
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3478636
- OpenAlex
- W1970232029
- Cited by
- 58
- References
- 44
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 3 · 2023: 4 · 2022: 4 · 2021: 3 · 2020: 10 · 2019: 1 · 2018: 4 · 2017: 5 · 2016: 4 · 2015: 7 · 2014: 6 · 2013: 3
- FWCI
- 1.73
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (24650166, 23570226)
- 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
- neuronal migration, cortical interneurons, leading process, centrosome, migratory direction, mouse embryo, in vivo imaging
- MeSH terms
- Animals, Cell Movement, Cell Nucleus, Cerebral Cortex, Embryo, Mammalian, Female, Golgi Apparatus, Immunohistochemistry, Interneurons, Kinetics, Male, Mice, Inbred ICR, Pregnancy, Time Factors, Centrosome, Microscopy, Confocal, Microscopy, Fluorescence, Multiphoton, Green Fluorescent Proteins, Mice
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