Defects of the radial glial scaffold in reeler mice were detected and characterized after the radial neuronal migration defects in this mutant had been described (Caviness and Rakic, 1978; Caviness et al., 1988; Pinto-Lord et al., 1982). Based on these findings, it has been hypothesized that radial glial defects contribute to the malpositioning of radially migrating neurons. Experimental evidence that Reelin may directly influence the development of radial glial cells is quite recent (Förster et al., 2002; Weiss et al., 2003; Hartfuss et al., 2003; Luque et al., 2003). The question as to why Reelin should simultaneously act on two different cell types, neurons and radial glial cells, turned out to be a semantic problem when radial glial cells were shown to be precursors of radially migrating neurons (Malatesta et al., 2000; Noctor et al., 2001; Miyata et al., 2001). Thus, when discussing a role of Reelin in the formation of the radial glial scaffold, the changing view of radial glial cell function in cortical development has to be taken into account.
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References
Alvarez-Buylla, A., Garcia-Verdugo, J. M., and Tramóntin, A. D. (2001). A unified hypothesis on the lineage of neural stem cells. Nature Rev. Neurosci. 2:287-293.
Angevine, J. B. (1965). Time of origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. Suppl. 2:1-70.
Bayer, S. A. (1980). Development of the hippocampal region in the rat. I. Neurogenesis examined with (3H) thymidine autoradiography. J. Comp. Neurol. 190:87-114.
Berry, M., and Rogers, A. W. (1965). The migration of neuroblasts in the developing cerebral cor-tex. J. Anat. 99:691-709.
Caviness, V. S., and Sidman, R. L. (1973). Time of origin of corresponding cell classes in the cer-ebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J. Comp. Neurol. 148:141-151.
Caviness, V. S., Jr., and Rakic, P. (1978). Mechanisms of cortical development: a view from muta-tions in mice. Annu. Rev. Neurosci. 1:297-326.
Caviness, V.S., Crandall, J. E., and Edwards, M. A. (1988). The reeler malformation. Implications for neocortical histogenesis. Cereb. Cortex 7:59-89.
Cowan, W. M., Stanfield, B., and Kishi, K. (1980). The development of the dentate gyrus. Curr. Top. Dev. Biol. 15 Part 1:103-157.
Cowan, W. M., Stanfield, B. B., and Amaral, D. G. (1981). Further observations on the develop-ment of the dentate gyrus. In Cowan, W.M. (ed.), Studies in Developmental Neurobiology. Oxford University Press, New York, pp. 395-435.
Deller, T., Drakew, A., Heimrich, B., Förster, E., Tielsch, A., and Frotscher, M. (1999). The hip-pocampus of the reeler mutant mouse: fiber segregation in area CA1 depends on the position of the postsynaptic target cells. Exp. Neurol. 156:254-267.
Del Rio, J. A., Heimrich, B., Supér, H., Borrell, V., Frotscher, M., and Soriano, E. (1996). Differential survival of Cajal-Retzius cells in organotypic cultures of hippocampus and neocor-tex. J. Neurosci. 16:6896-6907.
Del Rio, J. A., Heimrich, B., Borrell, V., Förster, E., Drakew, A., Alcántara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., Derer, P., Frotscher, M., and Soriano, E. (1997). A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385:70-74.
Drakew, A., Deller, T., Heimrich, B., Gebhardt, C., Del Turco, D., Tielsch, A., Förster, E., Herz, J., and Frotscher, M. (2002). Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Exp. Neurol. 176:12-24.
Dulabon, L., Olson, E. C., Taglienti, M. G., Eisenhuth, S., McGrath, B., Walsh, C. A., Kreidberg, J. A., and Anton, E. S. (2000). Reelin binds α3β1 integrin and inhibits neuronal migration. Neuron 27:33-44.
Eckenhoff, M. F., and Rakic, P. (1984). Radial organization of the hippocampal dentate gyrus: A Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J. Comp. Neurol. 223:1-21.
Förster, E., Tielsch, A., Saum, B., Weiss, K. H., Johanssen, C., Graus-Porta, D., Müller, U., and Frotscher, M. (2002). Reelin, disabled 1, and β1-integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc. Natl. Acad. Sci. USA 99:13178-13183.
Förster, E., Zhao, S., and Frotscher, M. (2006). Laminating the hippocampus. Nature Rev. Neurosci. 7:259-267.
Frotscher, M., Haas, C., and Förster, E. (2003). Reelin controls granule cell migration in the den-tate gyrus by acting on the radial glial scaffold. Cereb. Cortex 13:634-640.
Gebhardt, C., del Turco, D., Drakew, A., Tielsch, A., Herz, J., Frotscher, M., and Deller, T. (2002). Abnormal positioning of granule cells alters afferent fiber distribution in the mouse fascia dentata: morphologic evidence from reeler, apolipoprotein E receptor 2-, and very low density lipoprotein receptor knockout mice. J. Comp. Neurol. 445:278-292.
Hartfuss, E., Förster, E., Bock, H. H., Hack, M. A., Leprince, P., Luque, J. M., Herz, J., Frotscher, M., and Götz, M. (2003). Reelin signaling directly affects radial glial morphology and biochemical maturation. Development 130:4597-4609.
Hartmann, D., Sievers, J., Pehlemann, F. W., and Berry, M. (1992). Destruction of meningeal cells over the medial cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus. J. Comp. Neurol. 320:33-61.
Hiesberger, T., Trommsdorff, M., Howell, B. W., Goffinet, A., Mumby, M. C., Cooper, J. A., and Herz, J. (1999). Direct binding of reelin to VLDL receptor and ApoE receptor 2 induces tyro-sine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481-489.
His, W. (1889). Die Neuroblasten und deren Entstehung im embryonalen Marke. Abh. Math. Phys. Cl. Kgl. Sächs. Ges. Wiss. 15:313-372.
Howell, B. W., Hawkes, R., Soriano, P., and Cooper, J. A. (1997). Neuronal positioning in the developing brain is regulated by mouse disabled-1. Nature 389:733-737.
Hunter-Schaedle, K. E. (1997). Radial glial cell development and transformation are disturbed in the reeler forebrain. J. Neurobiol. 33:459-472.
Jacobson, M. (1991). Developmental Neurobiology, 2nd ed. Plenum Press, New York.
Kölliker, A. (1896). Handbuch der Gewebelehre des Menschen, 6th ed. W. Engelmann, Leipzig.
Levitt, P., and Rakic, P. (1980). Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey. J. Comp. Neurol. 193:815-840.
Luque, J. M., Morante-Oria, J., and Fairen, A. (2003). Localization of ApoER2, VLDLR and Dab1 in radial glia: groundwork for a new model of reelin action during cortical development. Dev. Brain Res. 140:195-203.
Magdaleno, S., Keshvara, L., and Curran, T. (2002). Rescue of ataxia and preplate splitting by ectopic expression of reelin in reeler mice. Neuron 33:573-586.
Magini, J. (1888a). Sur la névroglie et les cellules nerveuses cerebrales chez les fœtus. Arch. Ital. Biol. 9:59-60.
Magini, J. (1888b). Nouvelles recherches histologiques sur le cerveau du foetus. Arch. Ital. Biol. 10:384-387.
Malatesta, P., Hartfuss, E., and Götz, M. (2000). Isolation of radial glial cells by fluorescent-acti-vated cell sorting reveals a neuronal lineage. Development 127:5253-5263.
Mission, J. P., Takahashi, T., and Caviness, V. S. (1991). Ontogeny of radial and other astroglial cells in the murine cerebral cortex. Glia 4:138-148.
Miyata, T., Kawaguchi, A., Okano, H., and Ogawa, M. (2001). Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727-741.
Morest, D. K. (1970). A study of neurogenesis in the forebrain of opossum pouch young. Z. Anat. Entwicklungsgesch. 130:265-305.
Nadarajah, B., and Parnavelas, J. G. (2002). Modes of neuronal migration in the developing cere-bral cortex. Nature Rev. Neurosci. 3:423-432.
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., and Kriegstein, A. R. (2001). Neurons derived from radial units in neocortex. Nature 409:714-720.
Noctor, S. C., Flint, A. C., Weissman, T. A., Wong, W. S., Clinton, B. K., and Kriegstein, A. R. (2002). Dividing precursor cells of the embryonic cortical ventricular zone have morphologi-cal and molecular characteristics of radial glia. J. Neurosci. 22:3161-3173.
Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., and Mikoshiba, K. (1995). The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899-912.
Pinto-Lord, M. C., Evrard, P., and Caviness, V. S. (1982). Obstructed neuronal migration along radial glia fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Dev. Brain Res. 4:379-393.
Rakic, P. (1971). Neuron-glia relationship during granule cell migration in the developing cere-bellar cortex. A Golgi and electron microscopic study in Macacus rhesus. J. Comp. Neurol. 141:283-312.
Rakic, P. (1972). Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145:61-84.
Rakic, P. (1988). Specification of cerebral cortical areas. Science 241:170-176.
Ramón y Cajal, S. (1911). Histologie du Système Nerveux de l’Homme et des Vertébrés, Vol. 2. Maloine, Paris.
Retzius, G. (1893). Die Cajalschen Zellen der Grosshirnrinde beim Menschen und bei Säugetieren. Biol. Unters. 5:1-9.
Rickmann, M., Amaral, D. G., and Cowan, M. (1987). Organization of radial glia cells during the development of the rat dentate gyrus. J. Comp. Neurol. 264:449-479.
Schlessinger, A. R., Cowan, W. M., and Gottlieb, D. I. (1975). An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol. 159:149-176.
Schmechel, S. E., and Rakic, P. (1979). A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat. Embryol. 156:115-152.
Sheldon, M., Rice, D. S., d’Arcangelo, G., Yoneshima, H., Nakajima, M., Mikoshiba, K., Howell, B. W., Cooper, J. A., Goldowitz, D., and Curran, T. (1997). Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730-733.
Sidman, R. L., and Rakic, P. (1973). Neuronal migration with special reference to developing human brain. Brain Res. 62:1-35.
Stanfield, B. B., and Cowan, W. M. (1979a). The development of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185:423-460.
Stanfield, B. B., and Cowan, W. M. (1979b). The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185:393-422.
Supér, H., Martinez, A., and Soriano, E. (1997). Degeneration of Cajal-Retzius cells in the devel-oping cortex of the mouse after ablation of meningeal cells by 6-hydroxydopamine. Dev. Brain Res. 98:15-20.
Supér, H., Del Rio, J. A., Martinez, A., Perez-Sust, P., and Soriano, E. (2000). Disruption of neu-ronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb. Cortex 10:602-613.
Sweet, H. O., Bronson, R. T., Johnson, K. R., Cook, S. A., and Davisson, M. T. (1996). Scrambler, a new neurological mutation of the mouse with abnormalities of neuronal migration. Mamm. Genome 7:798-802.
Utsunomiya-Tate, N., Kubo, K., Tate, S., Kainosho, M., Katayama, E., Nakajima, K., and Mikoshiba, K. (2000). Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody. Proc. Natl. Acad. Sci. USA 97:9729-9734.
Ware, M. L., Fox, J. W., Gonzalez, J. L., Davis, N. M., Lambert de Rouvroit, C., Russo, C. J., Chua, S. C., Jr., Goffinet, A. M., and Walsh, C. A. (1997). Aberrant splicing of a mouse disa-bled homolog, mdab1, in the scrambler mouse. Neuron 19:239-249.
Weiss, K.-H., Johanssen, C., Tielsch, A., Saum, B., Frotscher, M., and Förster, E. (2003). Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice and ApoER2/VLDLR deficient mice. J. Comp. Neurol. 460:56-65.
Woodhams, E. B., Basco, E., Hajos, F., Csillag, A., and Balazs, R. (1981). Radial glia in the developing mouse cerebral cortex and hippocampus. Anat. Embryol. 163:331-343.
Yuasa, S., Kitoh, J., Oda, S., and Kawamura, K. (1993). Obstructed migration of Purkinje cells in the developing cerebellum of the reeler mutant mouse. Anat. Embryol. 188:317-329.
Zhao, S., Chai, X., Förster, E., and Frotscher, M. (2004). Reelin is a positional signal for dentate granule cells. Development 131:5117-5125.
Zhao, S., Chai, X., Bock, H., Brunne, B., Förster, E., and Frotscher, M. (2006). Rescue of the reeler phenotype in the dentate gyrus by wildtype coculture is mediated by lipoprotein receptors for reelin and disabled1. J. Comp. Neurol. 495:1-9.
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Förster, E., Zhao, S., Frotscher, M. (2008). Reelin and Radial Glial Cells. In: Fatemi, S.H. (eds) Reelin Glycoprotein. Springer, New York, NY. https://doi.org/10.1007/978-0-387-76761-1_11
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