Abstract
Although Ramón y Cajal suggested that cellular contiguity was the basis of neural function, it was only by the mid-1950s that the detailed morphology of synapses were unveiled by electron microscopy. As a result, the term “synapse” (from Greek synapsis meaning “to clasp”) has been widely used to designate specialized sites of transmission that can be either chemically or electrotonically mediated between cells. While discussion about the relative contribution of these forms of cellular interactions in the developing brain has been controversial, electrotonic coupling among neurons seems to diminish greatly at the time when chemical synaptic interactions are established. Electrotonic synapses have thus been suggested to provide the interactions necessary for neuronal pathfinding, chemical synaptogenesis and establishment of neuronal circuitry. Nevertheless, the mechanisms of progression between these types of synaptic interactions during development remains unclear. From the standpoint of function, although fast transmission is best achieved throughout gap junction channels, inhibitory modulation is best regulated chemically; thus, coexistence of mixed synapses could offer distinct advantageous performances during brain ontogeny. One recent example of coexistence of these modes of synaptic interaction is neurons cultured from second trimester human fetal brain, where the high level of coupling among neurons appears to compensate for the poor expression of chemical synaptic inputs1 (Fig. 16.1).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Chiu F-C, Rozental R, Bassallo C et al. Human fetal neurons in culture: Intercellular communication and voltage-and ligand-gated responses. J Neurosci Res 1994; 38: 687–697.
Rozental R, Gebhard D, Padin C et al. Purification of cell populations from human fetal brain using flow cytometric techniques. Dev Brain Res 1995; 85: 161–170.
Rozental R, Padin C, Spray DC et al. Purification of human fetal neurons from primary dissociated cultures. 1995: (submitted).
Kita H, Armstrong W. A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin. J Neurosci Methods 1991; 37: 141–150.
Lo Turco JJ, Kriegstein AR. Clusters of coupled neuroblasts in embryonic neocortex. Science 1991; 252: 563–566.
Peinado A, Yuste R, Katz LC. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 1993; 10: 103–114.
Rozental R, Mehler, MF, Morales, M et al. Differentiation of hippocampal progenitor cells in vitro: Temporal expression of intercellular coupling and voltage-and ligand-gated responses. Dev Biol 1995; 167: 350–362.
Shiosaka S, Yamamoto T, Hertzberg EL et al. Gap junction protein in rat hippocampus: correlative light and electron microscope immunohistochemical localization. J Comp Neurol 1989; 281: 282–297.
Stewart WW. Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 1978; 14: 741–759.
Vaney DI. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neurosci Lett 1991; 125: 187–190.
Yamamoto T, Shiosaka S, Whittaker ME et al. Gap junction protein in rat hippocampus: light microscope immunohistochemical localization. J Comp Neurol 1989; 281: 269–281.
Naus CCG, Bechberger, JF, Paul DL. Gap junction gene expression in human seizure disorder. Exp Neurol 1991; 111: 198–203.
Perez-Velazquez JL, Valiante TA, Carlen PL. Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. J Neurosci 1994; 14: 4308–4317.
Caveney S. The role of gap junctions in development. Annu Rev Physiol 1985; 47: 319–335.
Loewenstein WR. Junctional communication and the control of growth. Biochem Biophy Acta 1979; 560: 1–65.
Loewenstein WR, Kanno Y. Intercellular communication and the control of tissue growth. Lack of communication between cancer cells. Nature 1966; 209: 1248–1249.
Mehta PP, Bertram JS, Loewenstein WR. Growth inhibition of transformed cells correlates with their junctional communication with normal cells. Cell 1986; 44: 187–196.
Morales M, Rozental R, Mehler MF et al. Changes in gap junction properties of an immortalized hippocampal cell line induced by differentiation. ( 1996, submitted).
Rozental R, Urban M, Fishman GI et al. Gap junction downregulation is required for neuronal differentiation. Soc Neurosci Abst 1995; 21: 2000.
Loewenstein WR, Kanno Y. Intercellular communication and tissue growth. I. Cancerous growth. J Cell Biol 1967; 33: 225–234.
Bennett MVL, Spray DC, Harris AL. Electrical coupling in development. Am Zool 1981; 21: 413–427.
Warner AE, Guthrie SC, Gilula NB. Antibodies to gap junctional protein selectively disrupt junctional communication in early amphibian embryo. Nature 1984; 311: 127–131.
Lee S, Gilula NB, Warner AE. Gap junctional communication and compaction during preimplantation stages of mouse development. Cell 1987; 51: 851–860.
Bevilacqua A, Loch-Caruso R, Erickson RP. Abnormal development and dye coupling produced by antisense RNA to gap junction protein in mouse preimplantation embryos. Proc Natl Acad Sci USA 1989; 86: 5444–5558.
DeSousa PA, Valimarsson G, Nicholson BJ et al. Connexin trafficking and the control of gap junction asssembly in mouse preimplantation embryos. Development 1993; 117: 1355–1367.
Reaume AG, DeSousa PA, Kulkarni S. Cardiac malformation in neonatal mice lacking connexin43. Science 1995; 267: 1831–1834.
Nelles E, Jung D, Gabriel HD. Characterization of connexin32 deficient mice generated by gene targeting. In: The Role of Connexin Diversity. Gap Junction International Conference, L’Ile des Embiez, France, 1995.
Davids M, Heydrich U, Hofer A et al. Microinjection of antibody to connexin43 into early Xenopus embryo results in specific defects during development. (Submitted).
Britz-Cunningham SH, Shah BSMM, Zuppan BSCW et al. Mutations of the connexin43 gap junction gene in patients with heart malformations and defects of laterality. New England J Medicine 1995; 332: 1323–1329.
Batter DK, Corpina RA, Roy C et al. Heterogeneity gap junction expression in astrocytes cultured from different brain regions. Glia 1992; 6: 213–221.
Dermietzel R, Traub O, Hwang TK. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc Natl Acad Sci USA 1989; 86: 10148–10152.
Dermietzel R, Hertzberg EL, Kessler JA et al. Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis. J Neurosci 1991; 11: 1421–1432.
Dermietzel R, Spray DC. Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 1993; 16: 186–192.
Spray DC, Moreno AP, Kessler JA. Characterization of gap junctions between cultured leptomeningeal cells. Brain Res 1991; 568: 1–14.
Spray DC, Peinado A, Dermietzel R et al. Interactive Panel: Gap Junctions in the nervous system: What’s new and what do they do. 28th Winter Conference on Brain Research Abst. 1995; 28: 68.
Connors BW, Bernardo LS, Prince DA. Coupling between neurons of the developing rat neocortex. J Neurosci 1983; 3: 773–782.
Harrison RG. Observations on the living developing nerve fiber. Anat Rec 1907; 1“116–118.
Harrison RG. The outgrowth of the nerve fiber as a mode of protoplasmic movement. J Exp Zool 1910; 9: 787–846.
Harrison RG. The cultivation of tissues in extraneous media as a method of morpho-genetic study. Anat Rec 1912; 6: 181–193.
Banker G, Goslin K. Culturing Nerve Cells. MIT Press, MA, 1992.
Eves EM, Tucker MS, Roback JD et al. Immortal rat hippocampal cell lines exhibit neuronal and glial lineages and neurotrophin gene expression. Proc Natl Acad Sci 1992; 89: 4373–4377.
Frederiksen K, Jat PS, Valtz N. Immortalization of precursor cells from the mammalian CNS. Neuron 1988; 1: 439–448.
Mehler MF, Rozental R, Dougherty M et al. Cytokine regulation of neuronal differentiation of hippocampal progenitor cells. Nature 1993; 362: 62–65.
Jacks T, Fazeli A, Schmitt EA. Effects of an Rb mutation in the mouse. Nature 1992; 359: 295–300.
Lee EY-H, Chang C-Y, Nanopin H et al. Mice deficient for Rb are noviable and show defects in neurogenesis and haematopoiesis. Nature 1992; 359: 288–330.
Michaelson MD, Xu H, Mehler MF et al. Interleukin-7 is a neuronal growth factor. Soc Neurosci Abstr 1993; 19: 1102.
Cattaneo E, McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 1990; 347: 762–765.
Lazar LM, Blum M. Regional distribution and developmental expression of epidermal growth factor and transforming growth factor-a mRNA in mouse brain by a quantitative nuclease protection assay. J Neurosci 1992; 12: 1688–1697.
Baker RE, Corner MA, Habets AMMC. Effects of chronic supression of bioelectric activity on the development of sensory ganglion evoked responses in spinal cord ex-plants. J Neurosci 1984; 4: 1187–1192.
Bergey GK, Fitzgerald SC, Schrier B. et al. Neuronal maturation in mammalian cell cultures is dependent on spontaneous bio-electric activity. Brain Res 1981; 207: 49–58.
Corner MA. Localization of the capacities for functional development in the neural plate of Xenopus. J Comp Neurol 1964; 123: 243–255.
Corner MA, Crain SM. Patterns of spontaneous bioelectric activity during maturation in culture of fetal rodent medulla and spinal cord tissues. J Neurobiol 1972; 3: 25–45.
Moody WJ, Simoncini L, Coombs JL et al. Development of ion channels in early embryos. J Neurobiol 1991; 22: 674–684.
Spitzer NC. Ion channels in development. Ann Rev Neurosci 1979; 2: 363–397.
Spitzer NC. Development of voltage-dependent and ligand-gated channels in excitable membranes. In: van Pelt J, Corner MA, Uylings HBM, Lopes da Silva FH, eds. Progress in Brain Research. Elsevier Science BV, 1994: 169–179.
Spitzer NC, Lamborghini JE. The development of the action potential mechanism of amphibian neurons isolated in cell culture. Proc Natl Acad Sci USA 1976; 73: 1641–1645.
Xie H, Ziskind-Conhaim L. Blocking CaZ+dependent synaptic release delays motoneuron differentiation in the rat spinal cord. J Neurosci 1995; 15: 5900–5911.
Mattson MP. Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Res Rev 1988; 13: 179–212.
Rashid NA, Cambray-Deakin MA. N-Methyl-D-Aspartate effects on the growth, morphology and cytoskeleton of individual neurons in vitro. Dev Brain Res 1992; 67: 301–308.
Pereira EFR, Reinhardt-Maelicke S, Schrattenholz A et al. Identification and functional characterization of a new agonist site on nicotinic acetylcholine receptors of cultured hippocampal neurons. J Pharmacol Exp Ther 1993; 265: 1474–1491.
Laurie DJ, Wisden W, Seeburg PH. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 1992; 12: 4151–4172.
Alger BE, Nicoll RA. Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied in vitro. J Physiol (Lond) 1982; 328: 125–141.
Yagodin S, Holtzclaw LA, Barker JL et al. GABA-A receptor mediated Cl-flux induces intracellular calcium increase in LHRH secreting neuronal cell line. Biophy Soc Abstr 1993; 64, A325.
Garyantes TK, Regehr WG. Electrical activity increases growth cone calcium but fails to inhibit neurite outgrowth from rat sympathetic neurons. J Neurosci 1992; 12: 96–103.
Kater SB, Mattson MP, Cohan CS et al. Calcium regulation of the neuronal growth cone. Trends Neurosci 1988; 11: 315–321.
Kater SB, Mills LR. Regulation of growth cone behavior by calcium. J Neurosci 1991; 11: 891–899.
Mattson MP, Kater SB. Calcium regulation of neurite elongation and growth cone motility. J Neurosci 1987; 7: 4034–4043.
Chang M, Dahl G, Werner R. A role for an inhibitory connexin is testis? Dev Biol 1996; 175: 50–56.
Rozental R, Giaume C, Nedergaard M et al. Understanding the function of gap junction signalling in the CNS: New insights for brain development and dysfunction. 29th Winter Conference on Brain Res 1996: 29: 55.
Davies AM. The Bcl-2 family of proteins, and the regulation of neuronal survival. Trends Neurosci 1995; 18: 355–358.
McBurney MW, Reuhl KR, Ally AI et al. Differentiation and maturation of embryonal carcinoma-derived neurons in cell culture. J Neurosci 1988; 8: 1063–1073.
Eves EM, Boise LH, Thompson CB et al. Bcl-xL inhibits apoptosis induced differentiation in an immortalized central nervous system cell line. J Neurochem, in press.
Chalfie M, Tu Y, Euskirchen G et al. Green fluorescent protein as a marker for gene expression. Science 1994; 263: 802–805.
Fishman G, Spray DC, Leinwand LA. Molecular characterization and functional expression of the human cardiac gap junction channel. J Cell Biol 1990; 111: 589–598.
Friedrich G, Soriano P. Insertional mutagenesis by retroviruses and promoter traps in embryonic stem cells. Methods Enzymol 1993; 225: 681–701.
Hem WM. Correlation of fetal age and measurements between 10 and 26 weeks of gestation. J Obstet Gynecol 1994; 63: 26–32.
Grynkiewicz G, Poenie M, Tsien, RY. A new generation of Cat+ indicators with greatly improved fluorescence properties. J Biol Chem 1985; 260: 3440–3450.
Rights and permissions
Copyright information
© 1996 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Rozental, R., Spray, D.C. (1996). Temporal Expression of Gap Junctions During Neuronal Ontogeny. In: Gap Junctions in the Nervous System. Neuroscience Intelligence Unit. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-21935-5_16
Download citation
DOI: https://doi.org/10.1007/978-3-662-21935-5_16
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-662-21937-9
Online ISBN: 978-3-662-21935-5
eBook Packages: Springer Book Archive