Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons

Experimental Neurology

Volumn 157, Issue 1, 1999, Pages 43-57

  Leavitt, Blair R ^a   Hernit Grant, Cynthia S ^a   Macklis, Jeffrey D ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Apoptosis; Astrocyte; Migration; Neocortex; Neuronal degeneration; Radial glia; RC2; Transplantation

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN SLICE; CELL DIFFERENTIATION; CELL MATURATION; CELL TRANSPLANTATION; EMBRYO DEVELOPMENT; GENE TARGETING; GLIA CELL; MOUSE; NEOCORTEX; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION;

EID: 0032912512     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.6982     Document Type: Article

References (90)

1. Aebischer P., Winn S. R., Tresco P. A., Jaeger C. B., Greene L. A. Transplantation of polymer encapsulated neurotransmitter secreting cells: Effect of the encapsulation technique. J. Biomech. Eng. 112:1991;178-183.
2. Alvarez-Buylla A., Nottebohm F. Migration of young neurons in adult avian brain. Nature. 335:1988;353-354.
3. Angevine J. B., Sidman R. L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature. 192:1961;766-768.
4. Ashley D. M., Bol S. J., Waugh C., Kannourakis G. A novel approach to the measurement of differentin vitro. Leukemia Res. 17:1993;873-882.
5. Aubert I., Ridet J., Gage F. H. Regeneration in the adult mammalian CNS: Guided by development. Curr. Opin. Neurobiol. 5:1995;625-635.
6. Barbe M. F., Leavitt P. Age-dependent specification of corticocortical connections of cerebral grafts. J. Neurosci. 15:1995;513-538.
7. Bignami A., Dahl D. Astrocyte-specific protein and radial glia in the cerebral cortex of newborn rat. Nature. 252:1974;55-56.
8. Bjorklund A. Dopaminergic transplants in experimental parkinsonism: Cellular mechanisms of graft-induced recovery. Curr. Opin. Neurobiol. 2:1992;683-689.
9. Bonhoeffer T. Formation of target-specific neuronal projections in organotypic slice cultures from rat visual cortex. Nature. 346:1990;359-362.
10. Bredesen D. E. Neural apoptosis. Ann. Neurol. 38:1995;839-851.
11. Brenner M., Kisseberth W. C., Su Y., Besnard F., Messing A. GFAP pomoter directs astrocyte-specific expression in transgenic mice. J. Neurosci. 14:1994;1030-1037.
12. Castro A. J., Tonder N., Sunde N. A., Zimmer J. Fetal neocortical transplants grafted to the cerebral cortex of newborn rats receive afferents from the basal forebrain, locus coeruleus, and midline raphe. Exp. Brain Res. 69:1988;613-622.
13. Castro A. J., Hogan T. P., Sorensen J. C., Klausen B. S., Danielson E. H., Zimmer J., Neafsey E. J. Heterotopic neocortical transplants: An anatomical and electrophysiological analysis of host projections to occipital cortex grafts placed into sensorimotorlesions made in newborn rats. Dev. Brain Res. 58:1991;231-236.
14. Cameron R. S., Rakic P. Glial cell lineage in the cerebral cortex: A review and synthesis. Glia. 4:1991;124-137.
15. Canning D. R., Hoke A., Malemud C. J., Silver J. A potent inhibitor of neurite outgrowth that predominates in the extracellular mattix of reactive astrocytes. Int. J. Dev. Neurosci. 14:1996;153-175.
16. Culican S. M., Baumrind N. L., Yamamoto M., Pearlman A. L. Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J. Neurosci. 10:1990;684-692.
17. Davies S. J., Fitch M. T., Memberg S. P., Hall A. K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature. 390:1997;680-683.
18. Dumesnil-Bousez N., Sotelo C. Partial reconstruction of the adult Lurcher cerebellar circuitry by neural grafting. Neuroscience. 55:1993;1-21.
19. Edwards M. A., Tamamoto M., Caviness V. S. Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience. 36:1990;121-144.
20. Eng L. F., Vanderhagen V. J., Bignami A., Gerstl B. An acidic protein isolated from fibrous astrocytes. Brain Res. 28:1971;351-354.
21. Fisher L. J., Gage F. H. Intracerebral transplantation: Basic and clinical applications to the neostriatum. Faseb J. 8:1994;486-496.
22. Fitch M. T., Silver J. Glial cell extracellular matrix: Boundaries for axon growth in development and regeneration. Cell Tissue Res. 290:1997;379-384.
23. Gage F. H., Ray J., Fisher L. J. Isolation, characterization and use of stem cells from the CNS. Annu. Rev. Neurosci. 18:1995;159-192.
24. Gasser U. E., Hatten M. E. Central nervous system neurons migrate on astroglial fibers from heterotypic brain regions in vitro. Proc. Natl. Acad. Sci. USA. 87:1990;4543-4547.
25. Gasser U. E., Hatten M. E. Neuron glial interactions of rat hippocampal cells in vitro: Glial guided neuronal migration and neuronal regulation of glial differentiation. J. Neurosci. 10:1990;1276-1285.
26. Gates M. A., Laywell E. D., Filmore H., Steindler D. A. Astrocytes and extracellular matrix following intracerebral transplantation of embryonic ventral mesencephalon or lateral ganglionic eminence. Neuroscience. 74:1996;579-597.
27. Goetz C. G., Tanner C. M., Penn R. D., Stebbins G. T., Gilley D. W., Shannon K. M., Klawans H. K., Comella C. L., Wilson R. S., Witt T. Adrenal medullary transplants to the striatum of patients with advanced Parkinson's disease: 1 year motor and psychomotor data. Neurology. 40:1990;273-276.
28. Gotz M., Bolz J. Formation and preservation of cortical layers in slice cultures. J. Neurobiol. 23:1992;783-802.
29. Gray G. E., Leber S. M., Sanes J. R. Migratory patterns of clonally related cells in the developing nervous system. Experientia. 46:1990;929-940.
30. Hatten M. E., Liem R. K. H., Mason C. A. Two forms of cerebellar glial cells interact differently with neurons in vitro. J. Cell Biol. 98:1984;193-204.
31. Hatten M. E. Riding the glial monorail: A common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci. 13:1990;179-184.
32. Hatten M. E. The role of migration in central nervous system neuronal development. Curr. Opin. Neurobiol. 3:1993;38-44.
33. Hernit-Grant C. S., Macklis J. D. Re-expression of the radial glial marker RC2 in young adult mouse cortex following targeted neuronal death. Soc. Neurosci. Abs. 20:1994;682.6.
34. Hernit-Grant C. S., Macklis J. D. Embryonic neurons transplanted to regions of targeted photolytic cell death in adult mouse somatosensory cortex re-form specific callosal projections. Exp. Neurol. 139:1996;131-142.
35. Hicks S. P., D'Amato C. J. Cell migrations to the isocortex in the rat. Anat. Rec. 160:1968;619-634.
36. Hoke A., Silver J. Proteoglycans and other repulsive molecules in glial boudaries during development and regeneration of the nervous system. Prog. Brain Res. 108:1996;149-163.
37. Honig M. G., Hume R. I. DiI and DiO: Versatile fluorescent dyes for neuronal labeling and pathway tracing. Trends Neurosci. 12:1989a;333-335.
38. Honig M. G., Hume R. I. Carbocyanine dyes. Novel markers for labeling neurons. Trends Neurosci. 12:1989b;336-338.
39. Hunter K. E., Hatten M. E. Radial glial cell transformation to astrocytes is bidirectional: Regulation by a diffusible factor in embryonic forebrain. Proc. Natl. Acad. Sci. USA. 92:1995;2061-2065.
40. Hunter K. E., Hatten M. E. The novel astroglial differentiation factor RF60 limits gliosis when infused into adult cortical stab wounds. Soc. Neurosci. Abst. 1997;449.4.
41. Hunter-Schaedie K. E. Radial glial cell development and transformation are disturbed in reeler forebrain. J. Neurobiol. 33:1997;459-472.
42. Isacson O., Deacon T. W. Neural Transplantation studies reveal the brain's capacity for continuous reconstruction. Trends Neurosci. 20:1997;477-482.
43. Leavitt B. R., Canales M., Snyder E. Y., Macklis J. D. Multipotent neural precursors transplanted to regions of targeted neuronal apoptosis in adult mouse somatosensory cortex differentiate into neurons and reform callosal projections. Soc. Neurosci. Abs. 24:1996;205.11.
44. Lindvall O., Brundin P., Widner H., Rehncrona S., Gustavii B., Frackowiak R. Grafts of fetal dopaminergic neurons survive and improve motor function in Parkinson's disease. Science. 247:1990;574-577.
45. Locorazza H., Flax J. D., Snyder E. Y., Jendoubi M. Expression of human beta-hexosaminidase alpha subunit gene (the gene defect of Tay-Sachs disease) in mouse brains upon engraftment of transduced progenitor cells. Nat. Med. 2:1996;424-429.
46. Lois C., Alvarez Buylla A. Long-distance neuronal migration in the adult mammalian brain. Nature. 264:1994;1145-1148.
47. Lois C., Garcia-Verdugo J., Alvarez Buylla A. Chain migration of neuronal precursors. Science. 271:1996;978-981.
48. Macklis J. D. Transplanted neocortical neurons migrate selectively into regions of neuronal degeneration produced by chromophore-targeted laser photolysis. J. Neurosci. 13:1993;3848-3863.
49. Madison R., Macklis J. D., Thies C. Latex nanosphere delivery system (LNDS): Novel nanometer sized carriers of fluorescent dyes and active agents selectively target neuronal subpopulations via uptake and retrograde transport. Brain Res. 522:1990;90-98.
50. Markham J. A., Vaughn J. E. Migration patterns of sympathetic preganglionic neurons in embryonic rat spinal cord. J. Neurobiol. 22:1991;811-822.
51. Martinez-Serrano A., Bjorklund A. Immortalized neural progenitor cells for CNS gene transfer and repair. Trends Neurosci. 20:1997;530-538.
52. McConnell S. K. Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J. Neurosci. 8:1988;945-974.
53. McConnell S. K. Migration and differentiation of cerebral cortical neurons after transplantation into the brains of ferrets. Science. 229:1985;1268-1271.
54. McConnell S. K. Strategies for the generation of neuronal diversity in the developing central nervous system. J. Neurosci. 15:1995;6987-6998.
55. Mission J. P., Takahashi T., Caviness V. S. Ontogeny of radial and other astroglial cells in murine cerebral cortex. Glia. 4:1991;138-148.
56. Misson J. P., Edwards M. A., Yamamoto M., Caviness V. S. Jr. Identification of radial glial cells within developing murine central nervous system: Studies based upon a new immunochemical marker. Dev. Brain Res. 44:1988;95-108.
57. O'Rourke N. A., Dailey M. E., Smith S. J., McConnell S. K. Diverse migratory pathways in the developing cerebral cortex. Science. 258:1992;299-302.
58. O'Rourke N. A., Sullivan D. P., Kaznowski C. E., Jacobs A. A., McConnell S. K. Tangetial migration of neurons in the developing cerebral cortex. Development. 121:1995;2165-2176.
59. Phelps P. E., Vaughn J. E. Commissural fibers may guide cholinergic neuronal migration in developing rat cervical spinal cord. J. Comp. Neurol. 355:1995;38-50.
60. Phelps P. E., Barber R. P., Vaughn J. E. Embryonic development of rat sympathetic preganglionic neurons: Possible migratory substrates. J. Comp. Neurol. 330:1993;1-14.
61. Pixley S. K. R., DeVellis J. Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Dev. Brain Res. 15:1984;201-209.
62. Rakic P. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. 33:1971;471-476.
63. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145:1972;61-84.
64. Rakic P. Principles of neural cell migration. Experientia. 46:1990;882-891.
65. Rakic P., Cameron R. S., Komuro H. Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr. Opin. Neurobiol. 4:1990;63-69.
66. Ralph M. R., Lehman M. N. Transplantation: A new tool in the analysis of the mammalian hypothalamic circadian pacemaker. J. Biol. Rhythms Suppl. 87:1993;83-87.
67. Ridet J. L., Malhotra S. K., Privat A., Gage F. H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20:1997;570-577.
68. Sandor R., Gonzales M. F., Mosely M., Sharp F. R. Motor defecits are produced by removing some cortical transplants grafted into sensorimotor cortex of neonatal rats. J. Neural Transplant. Plast. 2:1991;221-223.
69. Schmechel D. E., Rakic P. A golgi study of radial glial cells in developing monkey telencephalon: Morphogenesis and transformation into astrocytes. Anat. Embryol. 156:1979;115-152.
70. Schultz M. K., McNulty J. A., Handa R. J., Hogan T. P., Tillotson G. L., Shaw P. L., Zimmer J., Castro A. J. Fetal neocortical transplants grafted into neocortical lesion cavities made in newborn rats: An analysis of transplant integration with the host brain. Cell Transplant. 4:1995;123-132.
71. Sheen V. L., Macklis J. D. Apoptotic mechanisms in targeted neuronal cell death by chromophore-activated photolysis. Exp. Neurol. 130:1994;67-81.
72. Sheen V. L., Macklis J. D. Targeted neocortical cell death in adult mice guides migration and differentiation of transplanted embryonic neurons. J. Neurosci. 15:1995;8378-8392.
73. Snyder E. Y., Deitcher D. L., Walsh C., Arnold-Aldea S., Hartwieg E. A., Cepko C. L. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell. 68:1992;35-51.
74. Snyder E. Y., Taylor R. M., Wolfe J. H. Neural progenitor cell engraftment corrects lysosomal storage throughout MPS VII mouse brain. Nature. 374:1995;367-370.
75. Snyder E. Y., Wittemore S. Physiological relevance and functional potential of central nervous system-derived cell lines. Mol. Neurobiol. 12:1996;13-38.
76. Snyder E. Y., Yoon C., Flax J. D., Macklis J. D. Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse cortex. Proc. Natl. Acad. Sci. USA. 94:1997;11663-11668.
77. Sorenson J. C., Wanner-Olsen H., Tonder N., Danielsen E., Castro A. J., Zimmer J. Axotomized adult basal forebrain neurons can innervate fetal frontal cortex grafts: A double fluorescent tracer study in the rat. Exp. Brain Res. 81:1990;545-551.
78. Sorenson J. C., Castro A. J., Klausen B., Zimmer J. Projections from fetal neocortical transplants placed in the frontal cortex of newborn rats: A Phaseolus vulgaris-leucoagglutanin tracing study. Exp. Brain Res. 92:1992;299-309.
79. Soriano E., Dumesnil N., Auladell C., Cohen-Tannoudji M., Sotelo C. Molecular heterogeneity of progenitors and radial migration in the developing cerebral cortex revealed by transgene expression. Proc. Natl. Acad. Sci. USA. 92:1995;11676-11680.
80. Soriano E., Alvarado-Mallart R. M., Dumesnil N., Del Rio J. A., Sotelo C. Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron. 18:1997;563-577.
81. Sotelo C., Alvarado-Mallart R. M. Embryonic and adult neurons interact to allow Purkinje cell replacement in mutant cerebellum. Nature. 327:1987;421-423.
82. Sotelo C., Alvarado-Mallart M., Frain M., Vernet M. Molecular plasticity of adult Bergmann fibers is associated with radial migration of grafted Purkinje cells. J. Neurosci. 14:1994;124-133.
83. Steindler D. A. Glial boundries in the developing nervous system. Annu. Rev. Neurosci. 16:1993;445-470.
84. Stitt T. N., Gasser U. E., Hatten M. E. Molecular mechanisms of glial-guided neuronal migration. Ann. N.Y. Acad. Sci. 633:1991;113-121.
85. Szele F. G., Chesselet M. F. Cortical lesions induce an increase in cell number and PSA-NCAM expression in the subventricular zone of adult rats. J. Comp. Neurol. 368:1996;439-454.
86. Triarhou L. C., Low W. C., Ghetti B. Intraparenchymal grafting of cerebellar cell suspensions to the deep cerebellar nuclei of pcd mutant mice, with particular emphasis on reestablishment of a Purkinje cell cortico-nuclear projection. Anat. Embryol. 185:1992;409-420.
87. Voight T. Development of glial cells in the cerebral walla of ferrets: Direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol. 289:1989;74-88.
88. Wang Y., Sheen V. L., Macklis J. D. Cortical interneurons upregulate neurotrophins in vivo in response to targeted apoptotic degeneration of neighboring pyramidal neurons. Exp. Neurol. 154:1998;389-402.
89. Zhou F. C., Buchwald N., Hull C., Towle A. Neuronal and glial elements of fetal neostriatal grafts in the adult neostriatum. Neuroscience. 30:1989;19-31.
90. Zhou H. F., Lee L. H.-C., Lund R. D. Timing and patterns of astrocyte migration from xenogeneic transplants of the cortex and corpus callosum. J. Comp. Neurol. 292:1990;320-330.