Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development

International Journal of Developmental Neuroscience

Volumn 22, Issue 2, 2004, Pages 73-86

  Bushong, Eric A ^a   Martone, Maryann E ^a,b   Ellisman, Mark H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocytes; Maturation; Morphology

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CELL MATURATION; CELL STRUCTURE; DENDRITE; HIPPOCAMPUS; NEUROPIL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT;

EID: 1342308184     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2003.12.008     Document Type: Article

References (84)

1. Altman J., Das G.D. Autoradiographic examination of the effects of enriched environment on the rate of glial multiplication in the adult rat brain. Nature. 204:1964;1161-1163.
2. Amthor F.R., Oyster C.W. Spatial organization of retinal information about the direction of image motion. Proc. Natl. Acad. Sci. U.S.A. 92:1995;4002-4005.
3. Arai Y., Mizuguchi M., Takashima S. Developmental changes of glutamate receptors in the rat cerebral cortex and hippocampus. Anat. Embryol. 195:1997;65-70.
4. Araque A., Parpura V., Sanzgiri R.P., Haydon P.G. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 22:1999;208-215.
5. Bagri A., Cheng H.J., Yaorn A., Pleasure S.J., Tessier-Lavigne M. Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell. 113:2003;285-299.
6. Blackshaw S.E., Nicholls J.G., Parnas I. Expanded receptive fields of cutaneous mechanoreceptor cells after single neurone deletion in leech central nervous system. J. Physiol. 326:1982;261-268.
7. Blondel O., Collin C., McCarran W.J., Zhu S., Zamostiano R., Gozes I., Brenneman D.E., McKay R.D. A glia-derived signal regulating neuronal differentiation. J. Neurosci. 20:2000;8012-8020.
8. Borell V., Callaway E.M. Reorganization of exuberant axon arbors contributes to the development of laminar specificty in ferret visual cortex. J. Neurosci. 22:2002;6682-6695.
9. Bringmann A., Francke M., Pannicke T., Biedermann B., Kodal H., Faude F., Reichelt W., Reichenbach A. Role of glial K(+) channels in ontogeny and gliosis: a hypothesis based upon studies on Muller cells. Glia. 29:2000;35-44.
10. Buhl, E.H., Schwerdtfeger, W.K., Germroth, P., 1990. Intracellular injection of neurons in fixed brain tissue combined with other neuroanatomical techniques at the light and electron microscopic level. In: Bjorklund, A, Hokfelt, T, Wouterlood, FG, van den Pol, A.N. (Eds.), Handbook of Chemical Neuroanatomy: Analysis of Neuronal Microcircuits and Synaptic Interactions, vol. 8. Elsevier, New York, pp. 273-304.
11. Bushong E.A., Martone M.E., Jones Y.Z., Ellisman M.H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22:2002;183-192.
12. Cajal, S.R., 1995. Histology of the Nervous System. Oxford University Press, New York.
13. Caley D.W., Maxwell D.S. An electron microscopic study of the neuroglia during postnatal development of the rat cerebrum. J. Comp. Neurol. 133:1968;45-70.
14. Catalani A., Sabbatini M., Consoli C., Cinque C., Tomassoni D., Azmitia E., Angelucci L., Amenta F. Glial fibrillary acidic protein immunoreactive astrocytes in developing rat hippocampus. Mech. Ageing Dev. 123:2002;481-490.
15. Choi B.H., Lapham L.W. Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent, and electron microscopic study. Brain Res. 148:1978;295-311.
16. Collard K.J., Edwards R., Liu Y. Changes in synaptosomal glutamate release during postnatal development in the rat hippocampus and cortex. Brain Res. Dev. Brain Res. 71:1993;37-43.
17. Connor J.R., Berkowitz E.M. A demonstration of glial filament distribution in astrocytes isolated from rat cerebral cortex. Neuroscience. 16:1985;33-44.
18. Cornell-Bell A.H., Thomas P.G., Smith S.J. The excitatory neurotransmitter glutamate causes filopodia formation in cultured hippocampal astrocytes. Glia. 3:1990;322-334.
19. Derouiche A., Frotscher M. Peripheral astrocyte processes: monitoring by selective immunostaining for the actin-binding ERM proteins. Glia. 36:2001;330-341.
20. Dienel G.A., Cruz N.F. Neighborly interactions of metabolically- activated astrocytes in vivo. Neurochem. Int. 43:2003;339-354.
21. Durand G.M., Kovalchuk Y., Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature. 381:1996;71-75.
22. Edwards M.A., Yamamoto M., Caviness V.S. Jr. 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.
23. Eng, L.F., Lee, Y.L., 1995. Intermediate filaments in astrocytes. In: Kettenmann, H., Ransom, B.R. (Eds.), Neuroglia. Oxford University Press, New York, pp. 650-667.
24. Fiala J.C., Feinberg M., Popov V., Harris K.M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18:1998;8900-8911.
25. Gao F.-B., Kohwi M., Brenman J.E., Jan L.Y., Jan Y.N. Control of dendritic field formation in Drosophila: the roles of Flamingo and competition between homologous neurons. Neuron. 28:2000;91-101.
26. Gasser U.E., Hatten M.E. Neuron-glia interactions of rat hippocampal cells in vitro: glial-guided neuronal migration and neuronal regulation of glial differentiation. J. Neurosci. 10:1990;1276-1285.
27. Ghandour M.S., Langley O.K., Clos J. Immunohistochemical and biochemical approaches to the development of neuroglia in the CNS, with special reference to cerebellum. Int. J. Dev. Neurosci. 1:1983;411-425.
28. Grosche J., Kettenmann H., Reichenbach A. Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J. Neurosci. Res. 68:2002;138-149.
29. Grueber W.B., Graubard K., Truman J.W. Tiling of the body wall by multidendritic sensory neurons in Manduca sexta. J. Comp. Neurol. 440:2001;271-283.
30. Grueber W.B., Jan L.Y., Jan Y.N. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development. 129:2002;2867-2878.
31. Grueber W.B., Ye B., Moore A.W., Jan L.Y., Jan Y.N. Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr. Biol. 13:2003;618-626.
32. Hall A. Rho GTPases and the actin cytoskeleton. Science. 279:1998;509-514.
33. Harlow, E., Lane, D., 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor.
34. Harris K.M., Jensen F.E., Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12:1992;2685-2705.
35. Harris K.M., Teyler T.J. Developmental onset of long-term potentiation in area CA1 of the rat hippocampus. J. Physiol. 346:1984;27-48.
36. Hatten M.E. Neuronal regulation of astroglial morphology and proliferation in vitro. J. Cell. Biol. 100:1985;384-396.
37. Honda H. Geometrical models for cells in tissues. Int. Rev. Cytol. 81:1983;191-248.
38. Ichikawa M., Hirata Y. Morphology and distribution of postnatally generated glial cells in the somatosensory cortex of the rat: an autoradiographic and electron microscopic study. Brain Res. 256:1982;369-377.
39. Jones T.A., Greenough W.T. Ultrastructural evidence for increased contact between astrocytes and synapses in rats reared in a complex environment. Neurobiol. Learn. Mem. 65:1996;48-56.
40. Koguchi K., Nakatsuji Y., Nakayama K.-I., Sakoda S. Modulation of astrocyte proliferation by cyclin-dependent kinase inhibitor p27Kip1. Glia. 37:2002;93-104.
41. Kudryashov I.E., Kudryashova I.V. Ontogeny of synaptic transmission in the rat hippocampus. Brain Res. 892:2001;263-286.
42. Lehre K.P., Rusakov D.A. Asymmetry of glia near central synapses favors presynaptically directed glutamate escape. Biophys. J. 83:2002;125-134.
43. MacNeil M.A., Masland R.H. Extreme diversity among amacrine cells: implications for function. Neuron. 20:1998;971-982.
44. Maslim J., Stone J. Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Brain Res. Dev. Brain Res. 44:1988;87-93.
45. Mason C.A., Edmondson J.C., Hatten M.E. The extending astroglial process: development of glial cell shape, the growing tip, and interactions with neurons. J. Neurosci. 8:1988;3124-3134.
46. Matsutani S., Yamamoto N. Neuronal regulation of astrocyte morphology in vitro is mediated by GABAergic signaling. Glia. 20:1997;1-9.
47. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4:2001;1086-1092.
48. Mauch D.H., Nagler K., Schumacher S., Goritz C., Muller E.C., Otto A., Pfrieger F.W. CNS synaptogenesis promoted by glia-derived cholesterol. Science. 294:2001;1354-1357.
49. Meyer G., Feldman E.L. Signaling mechanisms that regulate actin-based motility in the nervous system. J. Neurochem. 83:2002;490-503.
50. Michelson H.B., Lothman E.W. An in vivo electrophysiological study of the ontogeny of excitatory and inhibitory processes in the rat hippocampus. Brain Res. Dev. Brain Res. 47:1989;113-122.
51. Missler M., Eins S., Bottcher H., Wolff J.R. Postnatal development of glial fibrillary acidic protein, vimentin and S100 protein in monkey visual cortex: evidence for a transient reduction of GFAP immunoreactivity. Brain Res. Dev. Brain Res. 82:1994;103-117.
52. Muller D., Oliver M., Lynch G. Developmental changes in synaptic properties in hippocampus of neonatal rats. Brain Res. Dev. Brain Res. 49:1989;105-114.
53. Müller C.M. Astrocytes in cat visual cortex studied by GFAP and S-100 immunocytochemistry during postnatal development. J. Comp. Neurol. 317:1992a;309-323.
54. Müller C.M. A role for glial cells in activity-dependent central nervous plasticity? Review and hypothesis. Int. Rev. Neurobiol. 34:1992b;215-281.
55. Murai K.K., Nguyen L.N., Irie F., Yamaguchi Y., Pasquale E.B. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6:2003;153-160.
56. Nakatsuji Y., Miller R.H. Density dependent modulation of cell cycle protein expression in astrocytes. J. Neurosci. Res. 66:2001;487-496.
57. Nixdorf-Bergweiler B.E., Albrecht D., Heinemann U. Developmental changes in the number, size, and orientation of GFAP-positive cells in the CA1 region of rat hippocampus. Glia. 12:1994;180-195.
58. Ogata K., Kosaka T. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience. 113:2002;221-233.
59. Parnavelas J.G., Luder R., Pollard S.G., Sullivan K., Lieberman A.R. A qualitative and quantitative ultrastructural study of glial cells in the developing visual cortex of the rat. Philos. Trans. R. Soc. Lond., Ser. B. 301:1983;55-84.
60. Petralia R.S., Esteban J.A., Wang Y.-X., Partridge J.G., Zhao H.-M., Wenthold R.J., Malinow R. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat. Neurosci. 2:1999;31-36.
61. Pfrieger F.W. Role of glia in synapse development. Curr. Opin. Neurobiol. 12:2002;486-490.
62. Pfrieger F.W., Barres B.A. New views on synapse-glia interactions. Curr. Opin. Neurobiol. 6:1996;615-621.
63. Pixley S.K., de Vellis J. Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res. 317:1984;201-209.
64. Privat A. Postnatal gliogenesis in the mammalian brain. Int. Rev. Cytol. 40:1975;281-323.
65. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J. Comp. Neurol. 141:1971;283-312.
66. Reichelt W., Dettmer D., Bruckner G., Brust P., Eberhardt W., Reichenbach A. Potassium as a signal for both proliferation and differentiation of rabbit retinal (Muller) glia growing in cell culture. Cell. Signal. 1:1989;187-194.
67. Ritter L.M., Vazquez D.M., Meador-Woodruff J.H. Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res. Dev. Brain Res. 139:2002;227-236.
68. Runquist M., Alonso G. Gabaergic signaling mediates the morphological organization of astrocytes in the adult rat forebrain. Glia. 41:2003;137-151.
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. Senft S.L., Woolsey T.A. Mouse barrel cortex viewed as Dirichlet domains. Cereb. Cortex. 1:1991;348-363.
71. Setkowicz Z., Pawlinski R., Ziaja M., Janeczko K. Spatiotemporal pattern of the postnatal astrogliogenesis in the rat hippocampal formation. Int. J. Dev. Neurosci. 17:1999;215-224.
72. Sircar R. Developmental maturation of the N-methyl-D-aspartic acid receptor channel complex in postnatal rat brain. Int. J. Dev. Neurosci. 18:2000;121-131.
73. Spacek J. Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat. Embryol. 171:1985;245-252.
74. Stichel C.C., Müller C.M., Zilles K. Distribution of glial fibrillary acidic protein and vimentin immunoreactivity during rat visual cortex development. J. Neurocytol. 20:1991;97-108.
75. Takahashi T., Mission J.P., Caviness V.S. Jr. Glial process elongation and branching in the developing murine neocortex: a qualitative and quantitative immunohistochemical analysis. J. Comp. Neurol. 302:1990;15-28.
76. Ullian E.M., Sapperstein S.K., Christopherson K.S., Barres B.A. Control of synapse number by glia. Science. 291:2001;657-661.
77. Vaughn J.E., Peters A. The morphology and development of neuroglial cells. UCLA Forum Med. Sci. 14:1971;103-140.
78. Ventura R., Harris K.M. Three-dimensional relationships between hippocampal synapses and astrocytes. J. Neurosci. 19:1999;6897-6906.
79. Voigt T. Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol. 289:1989;74-88.
80. Wässle H., Peichl L., Boycott B.B. Morphology and topography of on- and off-alpha cells in the cat retina. Proc. R. Soc. Lond., Ser. B. 212:1981;157-175.
81. Wolff J.R., Rickmann M. Cytological characteristics of early stages of glial differentiation in the neocortex. Folia Morphol. 25:1976;235-237.
82. Woodhams P.L., Bascó E., Hajós F., Csillág A., Balázs R. Radial glia in the developmental mouse cerebral cortex and hippocampus. Anat. Embryol. 163:1981;331-343.
83. Yamada K., Fukaya M., Shibata T., Kurihara H., Tanaka K., Inoue Y., Watanabe M. Dynamic transformation of Bergmann glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells. J. Comp. Neurol. 418:2000;106-120.
84. Yuasa S. Development of astrocytes in the mouse hippocampus as tracked by tenascin-C gene expression. Arch. Histol. Cytol. 64:2001;149-158.