Modes of neuronal migration in the developing cerebral cortex (original) (raw)
References
Gleeson, J. G. & Walsh, C. A. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci.23, 352–359 (2000). CASPubMed Google Scholar
Lambert de Rouvroit, C. & Goffinet, A. M. Neuronal migration. Mech. Dev.105, 47–56 (2001). CASPubMed Google Scholar
Ross, M. E. & Walsh, C. A. Human brain malformations and their lessons for neuronal migration. Annu. Rev. Neurosci.24, 1041–1070 (2001).A review of studies that point to neuronal migration disorders in human brain malformations. CASPubMed Google Scholar
Hatten, M. E. Central nervous system neuronal migration. Annu. Rev. Neurosci.22, 511–539 (1999). CASPubMed Google Scholar
Parnavelas, J. G. The origin and migration of cortical neurones: new vistas. Trends Neurosci.23, 126–131 (2000). CASPubMed Google Scholar
Marin, O. & Rubenstein, J. L. A long, remarkable journey: tangential migration in the telencephalon. Nature Rev. Neurosci.2, 780–790 (2001).A comprehensive review of the genetic mechanisms involved in the tangential migration of cortical interneurons from the ventral telencephalon. CAS Google Scholar
Wilson, S. W. & Rubenstein, J. L. Induction and dorsoventral patterning of the telencephalon. Neuron28, 641–651 (2000). CASPubMed Google Scholar
Uylings, H. B., Van Eden, C. G., Parnavelas, J. G. & Kalsbeek, A. in The Cerebral Cortex of the Rat (eds Kolb, B. & Tees, R. C.) 35–76 (MIT Press, Cambridge, Massachusetts, 1990). Google Scholar
Angevine, J. B. & Sidman, R. L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature192, 766–768 (1961). PubMed Google Scholar
Berry, M. & Rogers, A. W. The migration of neuroblasts in the developing cerebral cortex. J. Anat.99, 691–709 (1965). CASPubMedPubMed Central Google Scholar
Rakic, P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol.145, 61–83 (1972). CASPubMed Google Scholar
Rakic, P., Stensas, L. J., Sayre, E. & Sidman, R. L. Computer-aided three-dimensional reconstruction and quantitative analysis of cells from serial electron microscopic montages of foetal monkey brain. Nature250, 31–34 (1974). CASPubMed Google Scholar
Walsh, C. & Cepko, C. L. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature362, 632–635 (1993). CASPubMed Google Scholar
Mione, M. C., Cavanagh, J. F., Harris, B. & Parnavelas, J. G. Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J. Neurosci.17, 2018–2029 (1997). CASPubMedPubMed Central Google Scholar
Tan, S. S. et al. Cell dispersion patterns in different cortical regions studied with an X-inactivated transgenic marker. Development121, 1029–1039 (1995). CASPubMed Google Scholar
Tan, S. S. et al. Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex. Neuron21, 295–304 (1998). CASPubMed Google Scholar
Nadarajah, B., Alifragis, P., Wong, R. O. & Parnavelas, J. G. Ventricle-directed migration in the developing cerebral cortex. Nature Neurosci.5, 218–224 (2002).The first evidence of ventricle-directed migration in the developing cortex. CASPubMed Google Scholar
Morest, D. K. A study of neurogenesis in the forebrain of opossum pouch young. Z. Anat. Entwicklungsgesch.130, 265–305 (1970).The first anatomical evidence of somal translocation as a distinct mode of migration in the developing cortex. CASPubMed Google Scholar
Brittis, P. A., Meiri, K., Dent, E. & Silver, J. The earliest patterns of neuronal differentiation and migration in the mammalian central nervous system. Exp. Neurol.134, 1–12 (1995). CASPubMed Google Scholar
Sidman, R. L. & Rakic, P. Neuronal migration, with special reference to developing human brain: a review. Brain Res.62, 1–35 (1973). CASPubMed Google Scholar
O'Rourke, N. A., Dailey, M. E., Smith, S. J. & McConnell, S. K. Diverse migratory pathways in the developing cerebral cortex. Science258, 299–302 (1992).The first direct evidence of tangential movement of cortical neuronsin vitro. CASPubMed Google Scholar
Rakic, P. Neuron–glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus rhesus. J. Comp. Neurol.141, 283–312 (1971). CASPubMed Google Scholar
Nowakowski, R. S. & Rakic, P. The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J. Comp. Neurol.196, 129–154 (1981). CASPubMed Google Scholar
Shoukimas, G. M. & Hinds, J. W. The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J. Comp. Neurol.179, 795–830 (1978). CASPubMed Google Scholar
Caviness, V. S. Jr & Rakic, P. Mechanisms of cortical development: a view from mutations in mice. Annu. Rev. Neurosci.1, 297–326 (1978). PubMed Google Scholar
Sweet, H. O., Bronson, R. T., Johnson, K. R., Cook, S. A. & Davisson, M. T. Scrambler, a new neurological mutation of the mouse with abnormalities of neuronal migration. Mamm. Genome7, 798–802 (1996). CASPubMed Google Scholar
Howell, B. W., Hawkes, R., Soriano, P. & Cooper, J. A. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature389, 733–737 (1997). CASPubMed Google Scholar
Trommsdorff, M. et al. Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell97, 689–701 (1999). CASPubMed Google Scholar
Gilmore, E. C., Ohshima, T., Goffinet, A. M., Kulkarni, A. B. & Herrup, K. Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci.18, 6370–6377 (1998). ArticleCASPubMedPubMed Central Google Scholar
Chae, T. et al. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron18, 29–42 (1997). CASPubMed Google Scholar
Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R. O. & Pearlman, A. L. Two modes of radial migration in early development of the cerebral cortex. Nature Neurosci.4, 143–150 (2001).The first real-time evidence of somal translocation in the developing cortex. CASPubMed Google Scholar
Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron31, 727–741 (2001). CASPubMed Google Scholar
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. & Kriegstein, A. R. Neurons derived from radial glial cells establish radial units in neocortex. Nature409, 714–720 (2001). CASPubMed Google Scholar
Hartfuss, E., Galli, R., Heins, N. & Gotz, M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol.229, 15–30 (2001).Reference32–34provided the first direct evidence that radial glia give rise to cortical neurons. CASPubMed Google Scholar
Parnavelas, J. G. & Nadarajah, B. Radial glial cells. Are they really glia? Neuron31, 881–884 (2001). CASPubMed Google Scholar
Ridley, A. J. Rho GTPases and cell migration. J. Cell Sci.114, 2713–2722 (2001). CASPubMed Google Scholar
Morris, N. R., Efimov, V. P. & Xiang, X. Nuclear migration, nucleokinesis and lissencephaly. Trends Cell Biol.8, 467–470 (1998). CASPubMed Google Scholar
Oakley, B. R. & Morris, N. R. Nuclear movement is β-tubulin-dependent in Aspergillus nidulans. Cell19, 255–262 (1980). CASPubMed Google Scholar
Oakley, B. R. & Morris, N. R. A β-tubulin mutation in Aspergillus nidulans that blocks microtubule function without blocking assembly. Cell24, 837–845 (1981). CASPubMed Google Scholar
Xiang, X., Zuo, W., Efimov, V. P. & Morris, N. R. Isolation of a new set of Aspergillus nidulans mutants defective in nuclear migration. Curr. Genet.35, 626–630 (1999). CASPubMed Google Scholar
Xiang, X., Osmani, A. H., Osmani, S. A., Xin, M. & Morris, N. R. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell6, 297–310 (1995). CASPubMedPubMed Central Google Scholar
Dobyns, W. B., Reiner, O., Carrozzo, R. & Ledbetter, D. H. Lissencephaly. A human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13. JAMA270, 2838–2842 (1993). CASPubMed Google Scholar
Hattori, M., Adachi, H., Tsujimoto, M., Arai, H. & Inoue, K. Miller–Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase. Nature370, 216–218 (1994). CASPubMed Google Scholar
Leventer, R. J., Cardoso, C., Ledbetter, D. H. & Dobyns, W. B. LIS1: from cortical malformation to essential protein of cellular dynamics. Trends Neurosci.24, 489–492 (2001). CASPubMed Google Scholar
Wynshaw-Boris, A. & Gambello, M. J. LIS1 and dynein motor function in neuronal migration and development. Genes Dev.15, 639–651 (2001). CASPubMed Google Scholar
Hirotsune, S. et al. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nature Genet.19, 333–339 (1998). CASPubMed Google Scholar
Cahana, A. et al. Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization. Proc. Natl Acad. Sci. USA98, 6429–6434 (2001).References47and48provided the first evidence for an involvement of LIS1 in neuronal migration. CASPubMedPubMed Central Google Scholar
Rivas, R. J. & Hatten, M. E. Motility and cytoskeletal organization of migrating cerebellar granule neurons. J. Neurosci.15, 981–989 (1995). CASPubMedPubMed Central Google Scholar
Fox, J. W. et al. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron21, 1315–1325 (1998). CASPubMed Google Scholar
Loo, D. T., Kanner, S. B. & Aruffo, A. Filamin binds to the cytoplasmic domain of the β1-integrin. Identification of amino acids responsible for this interaction. J. Biol. Chem.273, 23304–23312 (1998). CASPubMed Google Scholar
Sharma, C. P., Ezzell, R. M. & Arnaout, M. A. Direct interaction of filamin (ABP-280) with the β2-integrin subunit CD18. J. Immunol.154, 3461–3470 (1995). CASPubMed Google Scholar
Anton, E. S., Kreidberg, J. A. & Rakic, P. Distinct functions of α3 and αv integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron22, 277–289 (1999). CASPubMed Google Scholar
Fox, J. W. & Walsh, C. A. Periventricular heterotopia and the genetics of neuronal migration in the cerebral cortex. Am. J. Hum. Genet.65, 19–24 (1999). CASPubMedPubMed Central Google Scholar
Nikolic, M., Chou, M. M., Lu, W., Mayer, B. J. & Tsai, L. H. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature395, 194–198 (1998). CASPubMed Google Scholar
Kwon, Y. T., Gupta, A., Zhou, Y., Nikolic, M. & Tsai, L. H. Regulation of N-cadherin-mediated adhesion by the p35–Cdk5 kinase. Curr. Biol.10, 363–372 (2000). CASPubMed Google Scholar
Redies, C. & Takeichi, M. Expression of N-cadherin mRNA during development of the mouse brain. Dev. Dyn.197, 26–39 (1993). CASPubMed Google Scholar
Rakic, P., Knyihar-Csillik, E. & Csillik, B. Polarity of microtubule assemblies during neuronal cell migration. Proc. Natl Acad. Sci. USA93, 9218–9222 (1996). CASPubMedPubMed Central Google Scholar
Feng, Y. et al. LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron28, 665–679 (2000). CASPubMed Google Scholar
Niethammer, M. et al. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron28, 697–711 (2000). CASPubMed Google Scholar
Feng, Y. & Walsh, C. A. Protein–protein interactions, cytoskeletal regulation and neuronal migration. Nature Rev. Neurosci.2, 408–416 (2001). CAS Google Scholar
Rio, C., Rieff, H. I., Qi, P., Khurana, T. S. & Corfas, G. Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron19, 39–50 (1997). CASPubMed Google Scholar
Anton, E. S., Marchionni, M. A., Lee, K. F. & Rakic, P. Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development124, 3501–3510 (1997). CASPubMed Google Scholar
Pearlman, A. L., Faust, P. L., Hatten, M. E. & Brunstrom, J. E. New directions for neuronal migration. Curr. Opin. Neurobiol.8, 45–54 (1998). CASPubMed Google Scholar
Rice, D. S. & Curran, T. Mutant mice with scrambled brains: understanding the signaling pathways that control cell positioning in the CNS. Genes Dev.13, 2758–2773 (1999). CASPubMed Google Scholar
Rice, D. S. & Curran, T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci.24, 1005–1039 (2001).References65and66are comprehensive reviews of the role of reelin and its signalling pathways in the developing nervous system. CASPubMed Google Scholar
D'Arcangelo, G. & Curran, T. Reeler: new tales on an old mutant mouse. Bioessays20, 235–244 (1998). CASPubMed Google Scholar
Dulabon, L. et al. Reelin binds α3β1 integrin and inhibits neuronal migration. Neuron27, 33–44 (2000). ArticleCASPubMed Google Scholar
Magdaleno, S., Keshvara, L. & Curran, T. Rescue of ataxia and preplate splitting by ectopic expression of reelin in reeler mice. Neuron33, 573–586 (2002). CASPubMed Google Scholar
Goffinet, A. M., Daumerie, C., Langerwerf, B. & Pieau, C. Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J. Comp. Neurol.243, 106–116 (1986). CASPubMed Google Scholar
Tsai, H. M., Garber, B. B. & Larramendi, L. M. 3H-Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo. I. Neuronal birthdates of telencephalic compartments in situ. J. Comp. Neurol.198, 275–292 (1981). CASPubMed Google Scholar
Bar, I., Lambert de Rouvroit, C. & Goffinet, A. M. The evolution of cortical development. An hypothesis based on the role of the reelin signaling pathway. Trends Neurosci.23, 633–638 (2000). CASPubMed Google Scholar
Marin-Padilla, M. Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat. Embryol. (Berl.)152, 109–126 (1978). CAS Google Scholar
Goffinet, A. M. The embryonic development of the cortical plate in reptiles: a comparative study in Emys orbicularis and Lacerta agilis. J. Comp. Neurol.215, 437–452 (1983). CASPubMed Google Scholar
Luskin, M. B., Parnavelas, J. G. & Barfield, J. A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci.13, 1730–1750 (1993). CASPubMedPubMed Central Google Scholar
Anderson, S. A., Eisenstat, D. D., Shi, L. & Rubenstein, J. L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science278, 474–476 (1997). CASPubMed Google Scholar
Lavdas, A. A., Grigoriou, M., Pachnis, V. & Parnavelas, J. G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci.19, 7881–7888 (1999). CASPubMedPubMed Central Google Scholar
Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nature Neurosci.2, 461–466 (1999). CASPubMed Google Scholar
Sussel, L., Marin, O., Kimura, S. & Rubenstein, J. L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development126, 3359–3370 (1999). CASPubMed Google Scholar
Yuan, W. et al. The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev. Biol.212, 290–306 (1999). CASPubMed Google Scholar
Zhu, Y., Li, H., Zhou, L., Wu, J. Y. & Rao, Y. Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex. Neuron23, 473–485 (1999). CASPubMed Google Scholar
Powell, E. M., Mars, W. M. & Levitt, P. Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron30, 79–89 (2001). CASPubMed Google Scholar
Marin, O., Yaron, A., Bagri, A., Tessier-Lavigne, M. & Rubenstein, J. L. Sorting of striatal and cortical interneurons regulated by semaphorin–neuropilin interactions. Science293, 872–875 (2001). CASPubMed Google Scholar
Metin, C. & Godement, P. The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J. Neurosci.16, 3219–3235 (1996). CASPubMedPubMed Central Google Scholar
Rakic, P. Limits of neurogenesis in primates. Science227, 1054–1056 (1985). CASPubMed Google Scholar
Gray, G. E., Leber, S. M. & Sanes, J. R. Migratory patterns of clonally related cells in the developing central nervous system. Experientia46, 929–940 (1990). CASPubMed Google Scholar
Wolfer, D. P., Henehan-Beatty, A., Stoeckli, E. T., Sonderegger, P. & Lipp, H. P. Distribution of TAG-1/axonin-1 in fibre tracts and migratory streams of the developing mouse nervous system. J. Comp. Neurol.345, 1–32 (1994). CASPubMed Google Scholar
Denaxa, M., Chan, C. H., Schachner, M., Parnavelas, J. G. & Karagogeos, D. The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development128, 4635–4644 (2001). CASPubMed Google Scholar
Miller, M. W. Cogeneration of retrogradely labeled corticocortical projection and GABA-immunoreactive local circuit neurons in cerebral cortex. Brain Res.355, 187–192 (1985). CASPubMed Google Scholar
Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G. & Alvarez-Buylla, A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development128, 3759–3771 (2001). CASPubMed Google Scholar