Dynamic transformation of Bergmann glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells

Journal of Comparative Neurology

Volumn 418, Issue 1, 2000, Pages 106-120

  Yamada, Keiko ^a   Fukaya, Masahiro ^a   Shibata, Takashi ^a   Kurihara, Hideo ^a   Tanaka, Kohichi ^b   Inoue, Yoshiro ^a   Watanabe, Masahiko ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Bergmann fibers; Cerebellum; Electron microscopy; Glutamate transporter GLAST; Mouse; Neuron glial relationship

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE TRANSPORTER;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL STRUCTURE; CEREBELLUM; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; GLIA CELL; GRANULE CELL; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SYNAPSE;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; ATP-BINDING CASSETTE TRANSPORTERS; CELL SIZE; CEREBELLUM; DENDRITES; EMBRYO; MICE; MICE, INBRED C57BL; PURKINJE CELLS; RNA, MESSENGER; SYNAPSES; TIME FACTORS;

EID: 0034723714     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000228)418:1<106::AID-CNE8>3.0.CO;2-N     Document Type: Article

References (76)

1. Altman J. 1972. Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol 145:399-463.
2. Altman J. 1975. Postnatal development of the cerebellar cortex in the rat. IV. Spatial organization of bipolar cells, parallel fibers and glial palisades. J Comp Neurol 163:427-448.
3. Altman J, Anderson WK. 1972. Experimental reorganization of the cerebellar cortex. I. Morphological effects of elimination of all microneurons with prolonged x-irradiation started at birth. J Comp Neurol 146:355-406.
4. Altman J, Bayer SA. 1997. Development of the cerebellar system: in relation to its evolution, structure, and functions. Boca Raton, New York, London, Tokyo: CRC press.
5. Baptista CA, Hatten ME, Blazeski R, Mason CA. 1994. Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron 12:243-260.
6. Bignami A, Dahl D. 1973. Differentiation of astrocytes in the cerebellar cortex and the pyramidal tracts of the newborn rat: an immunofluorescence study with antibodies to a protein specific to astrocytes. Brain Res 49:393-402.
7. Bovolenta P, Liem RK, Mason CA. 1984. Development of cerebellar astroglia: transitions in form and cytoskeletal content. Dev Biol 102:248-259.
8. Bravin M, Morando L, Vercelli A, Rossi F. 1999. Control of spine formation by electrical activity in the adult rat cerebellum. Proc Natl Acad Sci USA 96:1704-1709.
9. Chaudhry FA, Lehre KP, van Lockeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. 1995. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
10. Choi BH, Lapham LW. 1980. Evolution of Bergmann glia in developing human fetal cerebellum: a Golgi, electron microscopic and immunofluorescent study. Brain Res 190:369-383.
11. Crépel F. 1982. Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci 5:266-269.
12. Das GD. 1976. Differentiation of Bergmann glia cells in the cerebellum: a Golgi study. Brain Res 110:199-213.
13. de Kort EJM, Gribnau AAM, van Aanholt HTH, Nieuwenhuys R. 1985. On the development of the pyramidal tract in the rat. I. The morphology of the growth zone. Anat Embryol 172:195-204.
14. Delaney CL, Brenner M, Messing A. 1996. Conditional ablation of cerebellar astrocytes in postnatal transgenic mice. J Neurosci 16:6908-6918.
15. Edwards MA, Yamamoto M, Caviness VS Jr. 1990. Organization of radial glia and related cells in the developing murine CNS: an analysis based upon a new monoclonal antibody marker. Neuroscience 36:121-144.
16. Feng L, Hatten ME, Heinz N. 1994. Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12:895-908.
17. Fukaya M, Yamada K, Nagashima M, Tanaka K, Watanabe M. 1999. Down-regulated expression of glutamate transporter GLAST in Purkinje cell-associated astrocytes of reeler and weaver mutant cerebella. Neurosci Res 34:165-175.
18. Furuta A, Rothstein JD, Martin LJ. 1997. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363-8375.
19. Grosche JG, Matyash V, Möller T, Verkhratsky A, Reichenbach A, Kettenmann H. 1999. Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2:139-143.
20. Gregory WA, Edmondson JC, Hatten ME, Mason CA. 1988. Cytology and neuron-glial apposition of migrating cerebellar granule cells in vitro. J Neurosci 8:1728-1738.
21. Hama K, Kosaka T. 1979. Purkinje cell and related neurons and glia cell under high-voltage electron microscopy. In: Zimmerman HM, editor. Progress in neuropathology, Vol. 4. New York: Raven Press. p 61-67.
22. Hanke S, Reichenbach A. 1987. Quantitative-morphometric aspects of Bergmann glial (Golgi epithelial) cell development in rats. Anat Embryol 177:183-188.
23. Hatten ME, Mason CA. 1990. Mechanisms of glial-guided neuronal migration in vitro and in vivo. Experientia 46:907-916.
24. Hillman DE, Chen S, Ackman J. 1988. Perinatal methylazoxymethanol acetate uncouples coincidence of orientation of cerebellar folia and parallel fibers. Neuroscience 24:99-110.
25. Hirano A, Dembitzer HM. 1973. Cerebellar alterations in the weaver mouse. J Cell Biol 56:478-486.
26. Hockfield S, McKay RD. 1985. Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328.
27. Ito M. 1989. Long-term depression. Annu Rev Neurosci 12:85-102.
28. Jeffrey PL, Meaney J, Tolhurst O, Weinberger RP. 1996. Epigenetic factors controlling the development of avian Purkinje neurons. J Neurosci Methods 67:163-175.
29. Kano M, Hashimoto K, Kurihara H, Watanabe M, Inoue Y, Aiba A, Tonegawa S. 1997. Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18:71-79.
30. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y, Aizawa S, Mishina M. 1995. Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluRδ2 mutant mice. Cell 81: 245-252.
31. Keinänen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH. 1990. A family of AMPA-selective glutamate receptors. Science 249:556-560.
32. Komuro H, Rakic P. 1993. Modulation of neuronal migration by NMDA receptors. Science 260:95-98.
33. Kurihara H, Hashimoto K, Kano M, Takayama C, Sakimura K, Mishina M, Inoue Y, Watanabe M. 1997. Impaired parallel fiber-Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor δ2 subunit. J Neurosci 17:9613-9623.
34. Landis SC. 1983. Neuronal growth cones. Annu Rev Physiol 45:567-580.
35. Landis DMD, Sidman RL. 1978. Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice. J Comp Neurol 179:831-864.
36. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC. 1995. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci 15:1835-1853.
37. Levitt P, Rakic P. 1980. Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol 193:815-840.
38. Linden DJ, Smeyne M, Conner JA. 1994. Trans-ACPD, a metabotropic receptor agonist, produces calcium mobilization and an inward current in cultured cerebellar Purkinje neurons. J Neurophysiol 71:1992-1998.
39. Mariani J. 1982. Extent of multiple innervation of Purkinje cells by climbing fibers in the olivocerebellar system of weaver, reeler, and staggerer mutant mice. J Neurobiol 13:119-126.
40. Mariani J, Crepel F, Mikoshiba K, Changeux JP, Sotelo C. 1977. Anatomical, physiological and biochemical studies of the cerebellum from reeler mutant mouse. Philos Trans R Soc Lond B 281:1-28.
41. Mattson MP. 1988. Neurotransmitters in the regulation of neuronal cyto-architecture. Brain Res Rev 13:179-212.
42. Mattson MP, Dou P, Kater SB. 1988. Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J Neurosci 8:2087-2100.
43. Metzger F, Weise S, Sendtner M. 1998. Effect of glutamate on dendritic growth in embryonic rat motoneurons. J Neurosci 18:1735-1742.
44. Misson JP, Edwards ME, Yamamoto M, Caviness VS Jr. 1988. Identification of radial glial cells within the developing murine central nervous system: studies based upon a new histochemical marker. Dev Brain Res 44:95-108.
45. Mitoma J, Furuya S, Hirabayashi Y. 1998. A nonessential amino acid L-serine released from astrocytes promotes the survival and neurite outgrowth of cultured hippocampal and cerebellar neurons. Soc Neurosci Abstr 24:546.
46. Muller T, Kettenmann H. 1995. Physiology of Bergmann glial cells. Int Rev Neurobiol 38:341-359.
47. Nakagawa S, Watanabe M, Isobe T, Kondo H, Inoue Y. 1998. Cytological compartmentalization in the staggerer cerebellum, as revealed by calbindin immunohistochemistry for Purkinje cells. J Comp Neurol 395: 112-120.
48. Nicholls D, Attwell D. 1990. The release and uptake of excitatory amino acids. Trends Pharmacol Sci 11:462-468.
49. O'Hearn E, Molliver ME. 1997. The olivocerebellar projection mediates ibogaine-induced degeneration of Purkinje cells: a model of indirect, transsynaptic excitotoxicity. J Neurosci 17:8828-8841.
50. Owen AD, Bird MM. 1997. Role of glutamate in the regulation of the outgrowth and motility of neurites from mouse spinal cord neurons in culture. J Anat 191:301-307.
51. Palay SL, Chan-Palay V. 1974. Cerebellar cortex. New York: Springer-Verlag.
52. Rakic P. 1971. Neuron-glia relationship during granule cell migration in developing cerebellar cortex: a Golgi and electron microscopic study in Macacus rhesus. J Comp Neurol 141:293-312.
53. Rakic P, Sidman RL. 1973. Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J Comp Neurol 152:103-132.
54. Ramón y Cajal S. 1911. Histologie du Systeme Nerveux de l'Homme et des Vertébrés. Tome 2. Paris Maloine. Reprinted by Consejo Superior de Investigaciones Cientificas, Madrid, 1955.
55. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW. 1994. Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
56. Sadler M, Berry M. 1989. Topological link-vertex analysis of the growth of Purkinje cell dendritic trees in normal, reeler, and weaver mice. J Comp Neurol 289:260-283.
57. Schmechel DE, Rakic P. 1979. A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol 156:115-152.
58. Shibata T, Watanabe M, Tanaka K, Wada K, Inoue Y. 1996. Dynamic changes in expression of glutamate transporter mRNAs in developing brain. Neuroreport 7:705-709.
59. Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, Tanaka K, Inoue Y. 1997. Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci 17:9212-9219.
60. Shibuki K, Gomi H, Chen L, Bao SW, Kim JSK, Watatsuki H, Fujisaki T, Fujimoto J, Katoh A, Ikeda T, Chen C, Thompson RF, Itohara S. 1996. Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron 16:587-599.
61. Shiga T, Ichikawa M, Hirata Y. 1983. A Golgi study of Bergmann glial cells in developing rat cerebellum. Anat Embryol 167:191-201.
62. Skoff RP, Hamburger V. 1974. Fine structure of dendritic and axonal growth cones in embryonic chick spinal cord. J Camp Neurol 153:107148.
63. Sotelo C. 1975. Anatomical, physiological and biochemical studies of the cerebellum from mutant mice. II. Morphological study of cerebellar cortical neurons and circuits in the weaver mouse. Brain Res 94:19-44.
64. Sotelo C, Alvarado-Mallart R-M, Frain M, Vernet M. 1994. Molecular plasticity of adult Bergmann fibers is associated with radial migration of grafted Purkinje cells. J Neurosci 14:124-133.
65. Spacek J. 1985. Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol 171:245-252.
66. Storck T, Schulte S, Hofmann K, Stoffel W. 1992. Structure, expression, and functional analysis of a Na+-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci USA 89:10955-10959.
67. Terashima T, Inoue K, Inoue Y, Mikoshiba K, Tsukada Y. 1985. Observations on Golgi epithelial cells and granule cells in the cerebellum of the reeler mutant mouse. Dev Brain Res 18:103-112.
68. Torp R, Danbolt NC, Babaie E, Bjørås M, Seeberg E, Storm-Mathisen J, Ottersen OP. 1994. Differential expression of two glial glutamate transporters in the rat brain: an in situ hybridization study. Eur J Neurosci 6:936-942.
69. Trenkner E, Sidman RL. 1977. Histogenesis of mouse cerebellum in microwell culture. J Cell Biol 75:915-940.
70. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC. 1997. Differential developmental expression of the two rat brain glutamate transporter protein GLAST and GLT. Eur J Neurosci 9:1646-1655.
71. 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.
72. Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y. 1998. Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fiber-recipient layer) of the hippocampal CA3 subfield. Eur J Neurosci 10:478-487.
73. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M, Inoue Y, Okuyama S, Sakagawa T, Ogawa S, Kawashima N, Hori S, Takimoto M, Wada K, Tanaka K. 1998. Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10:976-988.
74. Wilson MT, Keith CH. 1998. Glutamate modulation of dendritic outgrowth: alterations in the distribution of dendritic microtubules. J Neurosci Res 52:599-611.
75. Yamada K, Watanabe M, Shibata T, Tanaka K, Wada K, Inoue Y. 1996. EAAT4 is a post-synaptic glutamate transporter at Purkinje cell synapses. Neuroreport 7:2013-2017.
76. Yuasa S. 1996. Bergmann glial development in the mouse cerebellum as revealed by tenascin expression. Anat Embryol 194:223-234.