A radialization factor in normal cortical plate restores disorganized radial glia and disrupted migration in a model of cortical dysplasia

European Journal of Neuroscience

Volumn 17, Issue 3, 2003, Pages 467-480

  Hasling, Thomas A ^a   Gierdalski, Marcin ^a   Jablonska, Beata ^a   Juliano, Sharon L ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Cajal Retzius; Cortical dysplasia; Ferret; Neocortical development; Neuronal migration

Indexed keywords

DEXTRAN; FLUORESCENT DYE; METHYLAZOXYMETHANOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; CELL LABELING; CELL MIGRATION; COCULTURE; CONTROLLED STUDY; CORTICAL DYSPLASIA; EXPLANT; FEMALE; FERRET; GLIA CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; TISSUE CULTURE;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; ANTIMETABOLITES; BRAIN; BROMODEOXYURIDINE; CELL COUNT; CELL MOVEMENT; CEREBRAL CORTEX; CILIARY NEUROTROPHIC FACTOR; COCULTURE TECHNIQUES; FEMALE; FERRETS; FLUORESCENT DYES; IMAGE PROCESSING, COMPUTER-ASSISTED; METHYLAZOXYMETHANOL ACETATE; MODELS, NEUROLOGICAL; NEUROGLIA; ORGAN CULTURE TECHNIQUES; PREGNANCY; TERATOGENS;

EID: 0037330606     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02468.x     Document Type: Article

References (53)

1. Allendoerfer, K.L. & Shatz, C.J. (1994) The subplate, a transient neocortical structure: Its role in the development of connections between thalamus and cortex. Annu. Rev. Neurosci., 17, 185-218.
2. Anton, E.S., Marchionni, M.A., Lee, K.-F. & Rakic, P. (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development, 124, 3501-3510.
3. Bayer, S.A. & Altman, J. (1991) Neocortical Development. Raven Press, New York.
4. Canoll, P.D., Kraemer, R., Teng, K.K., Marchionni, M.A. & Salzer, J.L. (1999) GGF/neuregulin induces a phenotypic reversion of oligodendrocytes. Mol. Cell. Neurosci., 13, 79-94.
5. Canoll, P.D., Musacchio, J.M., Hardy, R., Reynolds, R., Marchionni, M.A. & Salzer, J.L. (1996) GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron, 17, 229-243.
6. Cattabeni, F. & Di Luca, M. (1997) Developmental models of brain dysfunctions induced by targeted cellular ablations with methylazoxymethanol. Physiol. Rev., 77, 199-214.
7. Caviness, V.S. Jr, & Rakic, P. (1978) Mechanisms of cortical development: a view from mutations in mice. Annu. Rev. Neurosci., 1, 297-326.
8. D'Arcangelo, G., Homayouni, R., Keshvara, L., Rice, D.S., Sheldon, M. & Curran, T. (1999) Reelin is a ligand for lipoprotein receptors. Neuron, 24, 471-479.
9. D'Arcangelo, G., Miao, G.G., Chen, S.C., Soares, H.D., Morgan, J.I. & Curran, T. (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature, 374, 719-723.
10. De Carlos, J.A. & O'Leary, D.D.M. (1992) Growth and targeting of subplate axons and establishment of major cortical pathways. J. Neurosci., 12, 1194-1211.
11. Derer, P. & Derer, M. (1990) Cajal-Retzius cell ontogenesis and death in the mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience, 36, 839-856.
12. Dulabon, L., Olson, E.C., Taglienti, M.G., Eisenhuth, S., McGrath, B., Walsh, C.A., Kreidberg, J.A. & Anton, E.S. (2000) Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron, 27 (1), 33-44.
13. Erzurumlu, R.S. & Jhaveri, S. (1992) Emergence of connectivity in the embryonic rat parietal cortex. Cerebral Cortex, 2, 336-352.
14. Evans, L.A. & Jenkins, E.C. (1976) PHA response and methylazoxy methanol acetate. Chem. Biol. Inter., 14, 135-140.
15. Ghosh, A., Antonini, A., McConnell, S.K. & Shatz, C.J. (1990) Requirement for subplate neurons in the formation of thalamocortical connections. Nature, 347, 179-181.
16. Ghosh, A. & Shatz, C.J. (1992a) Involvement of subplate neurons in the formation of ocular dominance columns. Science, 255, 1441-1443.
17. Ghosh, A. & Shatz, C.J. (1992b) Pathfinding and target selection by developing geniculocortical axons. J. Neurosci., 12, 39-55.
18. Ghosh, A. & Shatz, C.J. (1994) Segregation of geniculocortical afferents during the critical period: a role for subplate neurons. J. Neurosci., 14, 3862-3880.
19. Hiesberger, T., Trommsdorff, M., Howell, B.W., Goffinet, A., Mumby, M.C., Cooper, J.A. & Herz, J. (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron, 24, 481-489.
20. Hunter, K.E. & Hatten, M.E. (1995) Radial glial cell transformation to astrocytes is bidirectional: Regulation by a diffusable factor in embryonic forebrain. Proc. Natl. Acad. Sci., USA, 92, 2061-2065.
21. Hunter-Schaedle, K.E. (1997) Radial glial development and transformation are disturbed in reeler forebrain. J. Neurobiol., 33, 459-472.
22. Jackson, C.A., Peduzzi, J.D. & Hickey, T.L. (1989) Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons. J. Neurosci., 9, 1242-1253.
23. Johnston, M.V., Grzanna, R. & Coyle, J.T. (1981) Methylazoxymethanol treatment of fetal rats results in abnormally dense noradrenergic innervation of neocortex. Science, 203, 369-371.
24. Jones, E.G., Valentino, K.L. & Fleshman, J.W. (1982) Adjustment of connectivity in rat neocortex after prenatal destruction of precursor cells of layers II-IV. Dev. Brain Res., 2, 425-431.
25. Juliano, S.L., Palmer, S.L., Noctor, S.C., Sonty, R. & Hill, G. (1996) Development of local connections in ferret somatosensory cortex. J. Comp. Neurol., 374, 259-277.
26. Kind, P., Sengpiel, F., Engelage, J. & Blakemore, C. (1992) Interference with generation of layer 4 prevents the formation of ocular dominance columns. Soc. Neurosci. Abstr., 18, 1314.
27. Leavitt, B.R., Hernit-Grant, C.S. & Macklis, J.D. (1999) Mature astrocytes transform into transitional radial glia withing adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp. Neurol., 157 (1), 43-57.
28. Leprince, P. & Chanas-Sacre, G. (2001) Regulation of radial glia phenotype. Prog. Brain Res., 132, 13-22.
29. Magdaleno, S.M. & Curran, T. (2001) Brain development: Integrins and the Reelin pathway. Current Biol., 11, R1032-R1035.
30. Magdaleno, S.M., Keshvara, L. & Curran, T. (2002) Rescue of ataxia and preplate splitting by ectopic expression of Reelim in reeler mice. Neuron, 331, 573-586.
31. Malatesta, P., Hartfuss, E. & Gotz, M. (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development, 127, 5253-5263.
32. Matsumoto, H. & Higa, H.H. (1966) Studies on methylazoxymethanol, the algycone of cycasin: methylation of nucleic acids in vitro. Biochem. J., 98, 20C-22C.
33. Matsumoto, H., Spatz, M. & Laquer, G.L. (1972) Quantitative changes with age in the DNA content of methylazoxymethanol-induced microcephalic rat brain. J. Neurochem., 19, 297-306.
34. McConnell, S.K., Ghosh, A. & Shatz, C.J. (1994) Subplate pioneers and the formation of descending connections from cerebral cortex. J. Neurosci., 14, 1892-1907.
35. McGrath, B., McCann, C., Eisenhuth, S. & Anton, E.S. (2001) Molecular mechanisms of interactions between radial glia and neurons. Prog. Brain Res., 132, 197-202.
36. Miller, M.W. & Nowakowski, R.S. (1988) Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res., 457, 44-52.
37. Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron, 31, 727-741.
38. Noctor, S.C., Scholnicoff, N.J. & Juliano, S.L. (1997) Histogenesis of ferret somatosensory cortex. J. Comp. Neurol., 387, 179-193.
39. Noctor, S.C., Palmer, S.L., Hasling, T.A. & Juliano, S.L. (1999) Interference with the development of early generated neocortex results in disruption of radial glia and abnormal formation of neocortical layers. Cereb. Cortex, 9, 121-136.
40. Noctor, S.C., Palmer, S.L. & Juliano, S.L. (2001a) Disruption of layer 4 during development leads to altered thalamocortical projections in ferret somatosensory cortex. J. Neurosci., 21, 3184-3195.
41. Noctor, S.C., Flint, A.C., Weissman, T.A., Dammerman, R.S. & Kriegstein, A.R. (2001b) Neurons derived from radial glial cells establish radial units in neocortex. Nature, 409, 714-720.
42. Park, J.K., Williams, B.P., Alberta, J.A. & Stiles, C.D. (1999) Bipotent cortical progenitor cells process conflicting cues for neurons and glia in a hierarchical manner. J. Neurosci., 19, 10383-10389.
43. Rajan, P. & McKay, R.D. (1998) Multiple routes to astrocytic differentiation in the CNS. J. Neurosci., 18, 3620-3629.
44. Rice, D.S. & Curran, T. (2001) Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci., 24, 1005-1039.
45. Senzaki, K., Ogawa, M. & Yagi, T. (1999) Proteins of the CNR family are multiple receptors for Reelin. Cell, 99, 635-647.
46. Soriano, E., Alvarado-Mallart, R.M., Dumesnil, N., Del Rio, J.A. & Sotelo, C. (1997) Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron, 18, 563-577.
47. Stoppini, L., Buchs, P.A. & Muller, D. (1991) A simple method for organotypic cultures of nervous tissue. J. Neurosci. Meth., 37, 173-182.
48. Super, H., Del Rio, J.A., Martinez, A., Perez-Sust, P. & Soriano, E. (2000) Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb. Cortex, 10, 602-613.
49. Tamamaki, N., Nakamura, K., Okamoto, K. & Kaneko, T. (2001) Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci. Res., 41, 51-60.
50. Voigt, T. (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol., 289, 74-88.
51. Woo, T.U. & Finlay, B.L. (1996) Cortical target depletion and ingrowth of geniculocortical axons: Implications for cortical specification. Cereb. Cortex, 6, 457-469.
52. Woo, T.U., Niederer, J.K. & Finlay, B.L. (1996) Cortical target depletion and the developing lateral geniculate nucleus: Implications for trophic dependence. Cereb. Cortex, 6, 446-456.
53. Zedeck, M.S., Sternberg, S.S., Poynter, R.W. & McGowan, J. (1970) Biochemical and pathological effects of methylazoxymethanol acetate, a potent carcinogen. Cancer Res., 30, 801-812.