Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS

Brain Research Reviews

Volumn 32, Issue 1, 2000, Pages 29-44

  Nagy, James I ^a   Rash, John E ^b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Astrocyte; Brain and spinal cord; Connexin; Electron microscopy; Freeze fracture; Gap junction; Glial cell; Immunocytochemistry; Immunogold labelling; Intercellular communication; Oligodendrocyte

Indexed keywords

GAP JUNCTION PROTEIN;

ASTROCYTE; CELL COMMUNICATION; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; ELECTRON MICROSCOPY; FREEZE FRACTURE; GAP JUNCTION; GLIA CELL; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD STAINING; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SHORT SURVEY; SYNCYTIUM;

EID: 0034067910     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0173(99)00066-1     Document Type: Review

References (117)

1. Anders J.J., Salopek M. Meningeal cells increase in vitro astrocytic gap junctional communication as measured by fluorescence recovery after laser photobleaching. J. Neurocytol. 18:1989;257-264.
2. Bahr M., Andres F., Timmerman V., Nelis M.E., Van Broeckhoven C., Dichgans J. Central visual, acoustic, and motor pathway involvement in a Charcot-Marie-Tooth family with an Asn205Ser mutation in the connexin 32 gene. J. Neurol. Neurosurg. Psychiatry. 66:1999;202-206.
3. Batter D.K., Corpina R., Roy C., Spray D.C., Hertzberg E.L., Kessler J.A. Heterogeneity in gap junction expression in astrocytes cultured from different brain regions. Glia. 6:1992;213-221.
4. Belliveau D.J., Naus C.C.G. Cortical type 2 astrocytes are not dye coupled nor do they express the major gap junction genes found in the central nervous system. Glia. 12:1994;24-34.
5. Belliveau D.J., Naus C.C.G. Cellular localization of gap junction mRNAs in developing rat brain. Dev. Neurosci. 17:1995;81-96.
6. +-buffer capacity, and morphology of glial cells in the corpus callosum slice. J. Neurosci. 11:1991;3008-3024.
7. Bergoffen J., Scherer S.S., Wang S., Scott M.O., Bone L.J., Paul D.L., Chen K., Lensch M.W., Chance P.F., Fischbeck K.H. Connexin mutations in X-linked Charcot-Marie-Tooth disease. Science. 262:1993;2039-2042.
8. Binmoller F.-J., Muller C.M. Postnatal development of dye-coupling among astrocytes in rat visual cortex. Glia. 6:1992;127-137.
9. Bittman K., Owens D.F., Kriegstein A.R., LoTurco J. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J. Neurosci. 15:1997;7037-7044.
10. 2+ homeostasis and cell death. J. Neurochem. 70:1998;958-970.
11. Bolanos J.P., Medina J.M. Induction of nitric oxide synthase inhibits gap junction permeability in cultured rat astrocytes. J. Neurochem. 66:1996;2091-2099.
12. Brightman M.W., Reese T.S. Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40:1969;648-677.
13. Bruzzone B., Ressot C. Connexins, gap junctions and cell-cell signalling in the nervous system. Eur. J. Neurosci. 9:1997;1-6.
14. Bruzzone B., White T.W., Goodenough D.A. The cellular internet: on-line with connexins. BioEssays. 18:1996;709-718.
15. Bruzzone B., White T.W., Paul D.L. Connections with connexins: the molecular basis of direct intercellular signalling. Eur. J. Biochem. 238:1996;1-27.
16. Butt A.M., Ransom B.R. Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of lucifer yellow and horseradish peroxidase. Glia. 2:1989;470-475.
17. Condorelli D.F., Parenti R., Spinella F., Salinaro T., Belluardo N., Cardile V., Cicirata F. Cloning of a new gap junction gene (Cx36) highly expressed in mammalian neurons. Eur. J. Neurosci. 10:1998;1202-1208.
18. Cotrina M.L., Kang J., Lin J.H.-C., Bueno E., Hansen T.W., He L., Liu Y., Nedergaard M. Astrocytic gap junctions remain open during ischemic conditions. J. Neurosci. 18:1998;2520-2537.
19. Cravatt B.F., Giang D.K., Mayfield S.P., Goger D.L., Lerner R.A., Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature. 384:1996;83-87.
20. Dahl E., Manthey D., Chen Y., Schwarz H.-J., Chang S., Lalley P.A., Nicholson B.J., Willecke K. Molecular cloning and functional expression of mouse connexin30, a gap junction gene highly expressed in adult brain and skin. J. Biol. Chem. 271:1996;17903-17910.
21. Dermietzel R. The oligodendrocytic junctional complex. Cell Tiss. Res. 193:1978;61-72.
22. Dermietzel R., Farooq M., Kessler J.A., Althaus H., Hertzberg E.L., Spray D.C. Oligodendroytes express gap junction proteins connexin32 and connexin45. Glia. 20:1997;101-114.
23. Dermietzel R., Hertzberg E.L., Kessler J.A., Spray D.C. Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis. J. Neurosci. 11:1991;1421-1432.
24. Dermietzel R., Traub O., Hwang T.K., Beyer E., Bennett M.V.L., Spray D.C., Willecke K. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc. Natl. Acad. Sci. U. S. A. 86:1989;10148-10152.
25. Elfgang C., Eckert R., Lichtenberg-Frate H., Butterweck A., Traub O., Klein R.A., Hulser D.F., Willecke K. Specific permeability and selective formation of gap junction channels in connexin-transfected Hela cells. J. Cell Biol. 129:1995;805-817.
26. Elisevich K., Rempel S.A., Smith B.J., Edvardsen K. Hippocampal connexin43 expression in human complex partial seizure disorder. Exp. Neurol. 145:1997;154-164.
27. Enkvist M.O.K., McCarthy K.D. Activation of protein kinase C blocks astroglial gap junction communication and inhibits the spread of calcium waves. J. Neurochem. 59:1992;519-526.
28. + concentration. J. Neurochem. 62:1994;489-495.
29. Fischer G., Kettenmann H. Cultured astrocytes form a syncytium after maturation. Exp. Cell Res. 159:1985;273-279.
30. Giaume C., Cordier J., Glowinski J. Endothelins inhibit junctional permeability in cultured mouse astrocytes. Eur. J. Neurosci. 4:1992;877-881.
31. Giaume C., Fromaget C., Aoumari A.E., Cordier J., Glowinski J., Gros D. Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron. 6:1991;133-143.
32. Giaume C., Marin P., Cordier J., Glowinski J., Premont J. Adrenergic regulation of intercellular communications between cultured striatal astrocytes from the mouse. Proc. Natl. Acad. Sci. U. S. A. 88:1991;5577-5581.
33. Giaume C., McCarthy K.D. Control of gap junctional communication in astrocytic networks. Trends Neurosci. 8:1996;319-325.
34. Giaume C., Tabernero A., Medina J.M. Metabolic trafficking through astrocytic gap junctions. Glia. 21:1997;114-123.
35. Goodenough D.A., Goliger J.A., Paul D.L. Connexins, connexons and intercellular communication. Annu. Rev. Biochem. 65:1996;475-502.
36. Hossain M.Z., Murphy L.J., Hertzberg E.L., Nagy J.I. Phosphorylated forms of connexin43 predominate in rat brain: demonstration by rapid inactivation of brain metabolism. J. Neurochem. 62:1994;2394-2403.
37. Hossain M.Z., Peeling J., Sutherland G.R., Hertzberg E.L., Nagy J.I. Ischemia-induced cellular redistribution of the astrocytic gap junctional protein connexin43 in rat brain. Brain Res. 652:1994;311-322.
38. Hossain M.Z., Sawchuk M.A., Murphy L.J., Hertzberg E.L., Nagy J.I. Kainic acid induced alterations in antibody recognition of connexin43 and loss of astrocytic gap junctions in rat brain. Glia. 10:1994;250-265.
39. Jiang J.X., Goodenough D.A. Heteromeric connexons in lens gap junction channels. Proc. Natl. Acad. Sci. U. S. A. 93:1996;1287-1291.
40. Kardami E., Stoski R.M., Doble B.W., Yamamoto T., Hertzberg E.L., Nagy J.I. Biochemical and ultrastructural evidence for the association of basic fibroblast growth factor with cardiac gap junctions. J. Biol. Chem. 226:1991;19551-19557.
41. Kettenmann H., Orkand R.K., Schachner M. Coupling among identified cells in mammalian nervous system cultures. J. Neurosci. 3:1983;506-516.
42. Kettenmann H., Ransom B.R. Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures. Glia. 1:1988;64-73.
43. - solution. Glia. 3:1990;110-117.
44. Konietzko U., Muller C.M. Astrocytic dye coupling in rat hippocampus: topography, developmental onset, and modulation by protein kinase C. Hippocampus. 4:1994;297-306.
45. S.W. Kuffler, J.G. Nicholls (Eds.), From Neuron to Brain, Sinauer Assoc., Sunderland, 1977.
46. Kunzelmann P., Blümcke I., Traub O., Dermietzel R., Willecke K. Coexpression of connexin45 and -32 in oligodendrocytes of rat brain. J. Neurocytol. 26:1997;17-22.
47. Kunzelmann P., Schrder W., Traub O., Steinhäuser C., Dermietzel R., Willecke K. Late onset and increasing expression of the gap junction protein connexin30 in adult murine brain and long-term cultured astrocytes. Glia. 25:1999;111-119.
48. Laskawi R., Rohlmann A., Landgrebe M., Wolff J.R. Rapid astroglial reactions in the motor cortex of adult rats following peripheral facial nerve lesions. Eur. Arch. Oto.-Rhino.-Laryngol. 254:1997;81-85.
49. Lau A.F., Kurata W.E., Kanemitsu M.Y., Loo L.W.M., Warn-Cramer B.J., Eckhart W., Lampe P.D. Regulation of connexin43 function by activated tyrosine protein kinases. J. Bioenerg. Biomembr. 28:1996;359-368.
50. Lavado E., Sanchez-Abarca L.I., Tabernero A., Bolanos J.P., Medina J.M. Oleic acid inhibits gap junction permeability and increases glucose uptake in cultured rat astrocytes. J. Neurochem. 69:1997;721-728.
51. Lee S.H., Magge S., Spencer D.D., Sontheimer H., Cornell-Bell A.H. Human epileptic astrocytes exhibit increased gap junction coupling. Glia. 15:1995;195-202.
52. Lee S.H., Kim W.T., Cornell-Bell A.H., Sontheimer H. Astrocytes exhibit regional specificity in gap junction coupling. Glia. 11:1994;315-325.
53. Lehmenkuhler A., Sykova E., Svoboda J., Zilles K., Nicholson C. Extracellular space parameters in the rat neocortex and subcortical white matter during postnatal development determined by diffusion analysis. Neuroscience. 55:1993;339-351.
54. Li J., Hertzberg E.L., Nagy J.L. Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. J. Comp. Neurol. 379:1997;571-591.
55. Li W.E.I., Ochalski P.A.Y., Hertzberg E.L., Nagy J.I. Immunorecognition, ultrastructure and phosphorylation of astrocytic gap junctions and connexin43 in rat brain after cerebral focal ischemia. Eur. J. Neurosci. 10:1998;2444-2463.
56. Lo Turco J.J., Kriegstein A.R. Clusters of coupled neuroblasts in embryonic neocortex. Science. 252:1991;563-566.
57. Lynn B.D., Marotta C.A., Nagy J.I. Propagation of intercellular calcium waves in PC12 cells overexpressing a carboxy-terminal fragment of amyloid precursor protein. Neurosci. Lett. 199:1995;21-24.
58. Marrero H., Orkand R.K. Nerve impulses increase glial intercellular permeability. Glia. 16:1996;285-289.
59. Massa P.T., Mugnaini E. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze fracture study. Neuroscience. 7:1982;523-538.
60. Massa P.T., Szuchet S., Mugnaini E. Cell-cell interactions of isolated and cultured oligodendrocytes: formation of linear occluding junctions and expression of peculiar intramembrane particles. J. Neurosci. 4:1984;3128-3139.
61. McKhann G.M., D'Ambrosio R., Janigro D. Heterogeneity of astrocyte resting membrane potentials and intercellular coupling revealed by whole-cell and gramicidin-perforated patches from cultured neocortical and hippocampal slice astrocytes. J. Neurosci. 17:1997;6850-6863.
62. Micevych P.E., Abelson L. Distribution of mRNA coding for liver and heart gap junction proteins in the rat central nervous system. J. Comp. Neurol. 305:1991;96-118.
63. E. Mugnaini, Cell junctions of astrocytes, ependyma, and related cells in the mammalian central nervous system, with emphasis on the hypothesis of a generalized functional syncytium of supporting cells, in: Astrocytes, Vol. 1., Academic Press, 1986, pp. 329-371.
64. Muller T., Moller T., Neuhaus J., Kettenmann H. Electrical coupling among Bergmann glial cells and it modulation by glutamate receptor activation. Glia. 17:1996;274-284.
65. Nadarajah B., Jones A.M., Evans W.H., Parnavelas J.G. Differential expression of connexins during neocortical development and neuronal circuit formation. J. Neurosci. 17:1997;3096-3111.
66. Nadarajah B., Thomaidou D., Evans W.H., Parnavelas J.G. Gap junctions in the adult cerebral cortex: regional differences in their distribution and cellular expression of connexins. J. Comp. Neurol. 376:1996;326-342.
67. J.I. Nagy, R. Dermietzel, Gap junctions and connexins in the mammalian central nervous system, in: E.L. Hertzberg (Ed.), Advances in Molecular and Cell Biology, JAI Press, New York, 1999, in press.
68. Nagy J.I., Hossain M.Z., Hertzberg E.L., Marotta C.A. Induction of connexin43 and gap junctional communication in PC12 cells overexpressing the carboxy terminal region of amyloid precursor protein. J. Neurosci. Res. 44:1996;124-132.
69. Nagy J.I., Li W., Hertzberg E.L., Marotta C.A. Elevated connexin43 immunoreactivity at sites of amyloid plaques in Alzheimer's disease. Brain Res. 717:1996;173-178.
70. Nagy J.I., Li W.E.I., Doble B.W., Hochman S., Hertzberg E.L., Kardami E. Detection of dephosphorylated Cx43 in brain, heart and in spinal cord after nerve stimulation. Soc. Neurosci. Abstr. 22:1996;1023.
71. Nagy J.I., Li W.E.I., Roy C., Doble B.W., Gilchrist J.S., Kardami E., Hertzberg E.L. Selective monoclonal antibody recognition and cellular localization of an unphosphorylated form of connexin43. Exp. Cell Res. 236:1997;127-136.
72. Nagy J.I., Ochalski P.A.Y., Li J., Hertzberg E.L. Evidence for the co-localization of another connexin with connexin43 at astrocytic gap junctions in rat brain. Neuroscience. 78:1997;533-548.
73. Nagy J.I., Patel D., Ochalski P.A.Y., Stelmack G.L. Connexin30 in rodent, cat and human brain: selective expression in gray matter astrocytes, co-localization with connexin30 at gap junctions and late developmental appearance. Neuroscience. 88:1999;447-468.
74. Nagy J.I., Yamamoto T., Sawchuk M.A., Nance D.M., Hertzberg E.L. Quantitative immunohistochemical and biochemical correlates of connexin43 localization in rat brain. Glia. 5:1992;1-9.
75. Naus C.C.G., Bechberger J.F., Paul D.L. Gap junction gene expression in human seizure disorder. Exp. Neurol. 111:1991;198-203.
76. Naus C.C.G., Bechberger J.F., Zhang Y., Venance L., Yamasaki H., Juneja S.C., Kidder G.M., Giaume C. Altered gap junctional communication, intercellular signalling, and growth in cultured astrocytes deficient in connexin43. J. Neurosci. Res. 49:1997;528-540.
77. Newman E.A. High potassium conductance in astrocyte endfeet. Nature. 233:1986;453-454.
78. + and pH by polarized ion fluxes in glial cells: the retinal Muller cell. Neuroscientist. 2:1996;109-117.
79. Ochalski P.A.Y., Frankenstein U.N., Hertzberg E.L., Nagy J.I. Connexin43 in rat spinal cord: localization in astrocytes and identification of heterotypic astro-oligodendrocytic gap junctions. Neuroscience. 76:1997;931-945.
80. Ochalski P.A.Y., Hossain M.Z., Sawchuk M.A., Hertzberg E.L., Nagy J.I. Astrocytic gap junction removal, connexin43 redistribution and epitope masking at excitatory amino acid lesion sites in rat brain. Glia. 14:1995;279-294.
81. R.K. Orkand, Glial cells, in: E.R. Kandel (Ed.), Handbook of Physiology, Section 1, Vol. 1, Part 2, Waverly Press, Baltimore, 1977, pp. 855-875.
82. Orkand R.K., Nicholls J.G., Kuffler S.W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29:1966;788-806.
83. Pastor A., Kremer M., Mller T., Kettenmann H., Dermietzel R. Dye-coupling between spinal cord oligodendrocytes is restricted to gray matter: Indication for functional autocellular territories in white matter oligodendrocytes. Glia. 24:1998;108-120.
84. Pepper M.S., Meda P. Basic fibroblast growth factor increases junctional communication and connexin43 expression in microvascular endothelial cells. J. Cell Physiol. 153:1992;196-205.
85. A. Peters, S.L. Palay, H.D. Webster (Eds.), The Fine Structure of the Nervous System. Neurons and Their Supporting Cells, Oxford Univ. Press, New York, 1991, 494 pp.
86. Ransom B.R., Kettenmann H. Electrical coupling, without dye coupling, between mammalian astrocyte and oligodendrocytes in cell culture. Glia. 3:1991;258-266.
87. Rash J.E., Dillman R.K., Bilhartz B.L., Duffy H.S., Whalen L.R., Yasumura T. Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc. Natl. Acad. Sci. U. S. A. 93:1996;4235-4239.
88. Rash J.E., Duffy H.S., Dudek F.E., Bilhartz B.L., Whalen L.R., Yasumura T. Grid-mapped freeze-fracture analysis of gap junctions in gray and white matter of adult rat central nervous system, with evidence for a "panglial syncytium" that is not coupled to neurons. J. Comp. Neurol. 388:1997;265-292.
89. Rash J.E., Yasumura T. Improved structural detail in freeze-fracture replicas: high-angle shadowing of gap junctions cooled below -170°C and protected by liquid nitrogen-cooled shrouds. J. Electron Microsc. Tech. 20:1992;187-204.
90. Rash J.E., Yasumura T. Direct immunogold labeling of connexins and aquaporin4 in freeze-fracture replicas of liver, brain and spinal cord: factors limiting quantitative analysis. Cell Tiss. Res. 296:1999;307-321.
91. J.E. Rash, T. Yasumura, F.E. Dudek, Ultrastructure, histological distribution, and freeze-fracture immunocytochemistry of gap junctions in rat brain and spinal cord, Cell Biol. Int. (1999) in press.
92. Rash J.E., Yasumura T., Hudson C.S., Agre P., Nielsen S. Direct immunogold labeling of aquaporin-4 in "square arrays" of astrocyte and ependymocyte plasma membrane in rat brain and spinal cord. Proc. Natl. Acad. Sci. U. S. A. 95:1998;11981-11986.
93. Revel J.P., Karnovsky M.J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33:1967;7-12.
94. Robinson R.R., Hampson E.C.G., Munro M.N., Vaney D.I. Unidirectional coupling of gap junctions between neuroglia. Science. 262:1993;1072-1074.
95. Rohlmann A., Laskawi R., Hofer A., Dermietzel R., Wolff J.R. Astrocytes as rapid sensors of peripheral axotomy in the facial nucleus of rats. NeuroReport. 36:1994;409-412.
96. Rohlmann A., Laskawi R., Hofer A., Dobo E., Dermietzel R., Wolff J.R. Facial nerve lesions lead to increased immunostaining of the astrocytic gap junction protein (connexin43) in the corresponding facial nucleus of rats. Neurosci. Lett. 154:1993;206-208.
97. A. Rohlmann, J.R. Wolff, Subcellular topography and plasticity of gap junction distribution on astrocytes, in: D.C. Spray, R. Dermietzel (Eds.), Gap Junctions in the Nervous System, Landes, Austin, 1996, pp. 175-192.
98. Sandri C., Van Buren J.M., Akert K. Membrane morphology of the vertebrate nervous system. A study with freeze-etch technique. Prog. Brain Res. 46:1977;1-384.
99. Sawchuk M.A., Hossain M.Z., Hertzberg E.L., Nagy J.I. In situ transblot and immunocytochemical comparisons of astrocytic connexin43 responses to NMDA and kainic acid in rat brain. Brain Res. 683:1995;153-157.
100. Shiosaka S., Yamamoto T., Hertzberg E.L., Nagy J.I. Gap junction protein in rat hippocampus: correlative light and electron microsope immunohistochemical localization. J. Comp. Neurol. 281:1989;282-297.
101. Simon A.M., Goodenough D.A. Diverse functions of vertebrate gap junctions. Trends Cell Biol. 8:1998;477-483.
102. Sotelo C., Angaut P. The fine structure of the cerebellar central nuclei in the cat: I. Neurons and neuroglial cells. Exp. Brain Res. 28:1973;410-430.
103. Stauffer K.A. The gap junction protein β1-connexin (connexin-32) and β2-connexin (connexin26) can form heteromeric hemichannels. J. Biol. Chem. 270:1995;6768-6772.
104. Theriault E., Frankenstein U.N., Hertzberg E.L., Nagy J.I. Connexin43 and astrocytic gap junctions in the rat spinal cord after acute compression injury. J. Comp. Neurol. 382:1997;199-214.
105. Veenstra R.D. Size and selectivity of gap junction channels formed from different connexins. J. Bioenerg. Biomembr. 28:1996;327-337.
106. Velazquez J.L., Frantseva M., Naus C.C.G., Bechberger J.F., Junja S.C., Velumian A., Carlen P.L., Kidder G.M., Mills L.R. Development of astrocytes and neurons in cultured brain slices from mice lacking connexin43. Dev. Brain Res. 97:1996;293-296.
107. Venance L., Piomelli D., Glowinski J., Giaume C. Inhibition by anandamide of gap junctions and intercellular calcium signalling in striatal astrocytes. Nature. 376:1995;590-594.
108. Vukelic J.L., Yamamoto T., Hertzberg E.L., Nagy J.I. Depletion of connexin43-immunoreactivity in astrocytes after kainic acid-induced lesions in rat brain. Neurosci. Lett. 130:1991;120-124.
109. Warn-Cramer B.J., Lampe P.D., Kurata W.E., Kanemitsu M.Y., Loo L.W.M., Eckhart W., Lau A.F. Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin43 gap junction protein. J. Biol. Chem. 271:1996;3779-3786.
110. White T.W., Bruzzone R. Multiple connexin proteins in single intercellular channels: connexin compatibility and functional consequences. J. Bioenerg. Biomembr. 28:1996;339-350.
111. Wolburg H., Rohlmann A. Structure-function relationships in gap junctions. Int. Rev. Cytol. 157:1995;315-373.
112. Wolff J.R., Stuke K., Missler M., Tytko H., Schwarz P., Rohlmann A., Chao T.I. Autocellular coupling by gap junctions in cultured astrocytes: a new view on cellular autoregulation during process formation. Glia. 24:1998;121-140.
113. Yamamoto T., Kardami E., Nagy J.I. Basic fibroblast growth factor in rat brain: localization to glial gap junctions correlates with connexin 43 distribution. Brain Res. 554:1991;336-343.
114. Yamamoto T., Ochalski A., Hertzberg E.L., Nagy J.I. LM and EM immunolocalization of the gap junction protein connexin43 in rat brain. Brain Res. 508:1990;313-319.
115. Yamamoto T., Ochalski A., Hertzberg E.L., Nagy J.I. On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression. J. Comp. Neurol. 302:1990;853-883.
116. Yamamoto T., Shiosaka S., Whittaker M.E., Hertzberg E.L., Nagy J.I. Gap junction protein in rat hippocampus: light microscope immunohistochemical localization. J. Comp. Neurol. 281:1989;262-281.
117. Yamamoto T., Vukelic J., Hertzberg E.L., Nagy J.I. Differential anatomical and cellular patterns of connexin43 expression during postnatal development of rat brain. Dev. Brain Res. 66:1992;165-180.