Neuronal acetylcholine receptors with α7 subunits are concentrated on somatic spines for synaptic signaling in embryonic chick ciliary ganglia

Journal of Neuroscience

Volumn 19, Issue 2, 1999, Pages 692-704

  Shoop, Richard D ^a   Martone, Maryann E ^a   Yamada, Naoko ^a   Ellisman, Mark H ^a   Berg, Darwin K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine; Calyx; Cholinergic; Ciliary ganglion; Confocal; Electron microscopy; Immunogold; Neuronal; Nicotinic; Presynaptic; Receptors; Spines; Synaptic; Tom ography; 7

Indexed keywords

ACETYLCHOLINE; NICOTINIC RECEPTOR;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CILIARY GANGLION; ELECTRON MICROSCOPY; EMBRYO; MICROSCOPIC ANATOMY; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECEPTOR DENSITY;

EID: 0033556086     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-02-00692.1999     Document Type: Article

References (49)

1. Anand R, Peng X, Lindstrom J (1993) Homomeric and native α7 acetylcholine receptors exhibit remarkably similar but non-identical pharmacological properties, suggesting that the native receptor is a heteromeric protein complex. FEBS Lett 327:241-246.
2. Bertrand D, Galzi JL, Devillers-Thiery A, Bertrand S, Changeux JP (1993) Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal α7 nicotinic receptor. Proc Natl Acad Sci USA 90:6971-6975.
3. Chen D, Patrick JW (1997) The α-bungarotoxin-binding nicotinic acetylcholine receptor from rat brain contains only the α7 subunit. J Biol Chem 272:24024-24029.
4. Chiappinelli VA, Giacobini E (1978) Time course of appearance of α-bungarotoxin binding sites during development of chick ciliary ganglion and iris. Neurochem Res 3:465-478.
5. Clements JD (1996) Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19:163-171.
6. Coggan JS, Paysan J, Conroy WG, Berg DK (1997) Direct recording of nicotinic responses in presynaptic nerve terminals. J Neurosci 17:5798-5806.
7. Conroy WG, Berg DK (1995) Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J Biol Chem 270:4424-4431.
8. Conroy WG, Berg DK (1998) Nicotinic receptor subtypes in the developing chick brain: appearance of a species containing the α4, β2, and α5 gene products. Mol Pharmacol 53:392-401.
9. Corriveau RA, Berg DK (1993) Co-expression of multiple acetylcholine receptor genes in neurons: quantification of transcripts during development. J Neurosci 13:2662-2671.
10. Corriveau RA, Berg DK (1994) Neurons in culture maintain acetylcholine receptor levels with far fewer transcripts than in vivo. J Neurobiol 25:1579-1592.
11. Couturier S, Bertrand D, Matter J-M, Hernandez M-C, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-Btx. Neuron 5:847-856.
12. Dryer S (1994) Functional development of the parasympathetic neurons of the avian ciliary ganglion: a classic model system for the study of neuronal differentiation and development. Prog Neurobiol 43:281-322.
13. Fertuck HC, Salpeter MM (1976) Quantitation of junctional and extrajunctional acetylcholine receptors by electron microscope autoradiography after I-125-α-bungarotoxin binding at mouse neuromuscular junctions. J Cell Biol 69:144-158.
14. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
15. Guo J-Z, Tredway TL, Chiappinelli VA (1998) Glutamate and GABA release are enhanced by different subtypes of presynaptic nicotinic receptors in the lateral geniculate nucleus. J Neurosci 18:1963-1969.
16. Harris KM, Kater SB (1994) Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
17. Hess A (1965) Developmental changes in the structure of the synapse on the myelinated cell bodies of the chicken ciliary ganglion. J Cell Biol 25:1-19.
18. Hessler D, Young SJ, Carragher BO, Martone M, Lamont S, Whittaker M, Milligan RA, Masliah E, Hinshaw JE, Ellisman MH (1992) Programs for visualization in 3-dimensional microscopy. NeuroImage 1:55-67.
19. Jacob MH, Berg DK (1983) The ultrastructural localization of α-bungarotoxin binding sites in relation to synapses on chick ciliary ganglion neurons. J Neurosci 3:260-271.
20. Jacob MH, Berg DK, Lindstrom JM (1984) Shared antigenic determinant between the Electrophorus acetylcholine receptor and a synaptic component on chicken ciliary ganglion neurons. Proc Natl Acad Sci USA 81:3223-3227.
21. Koch C, Zador A (1993) The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization. J Neurosci 13:413-422.
22. Landmesser L, Pilar G (1972) The onset and development of transmission in the chick ciliary ganglion. J Physiol (Lond) 222:691-713.
23. Landmesser L, Pilar G (1974) Synapse formation during embryogenesis on ganglion cells lacking a periphery. J Physiol (Lond) 241:715-736.
24. Li X, Rainnie DG, McCarley RW, Greene RW (1998) Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 18:1904-1912.
25. 125I-toxin F binding sites on chick ciliary neurons: synaptic localization of a toxin that blocks ganglionic nicotinic receptors. J Neurosci 7:2153-2162.
26. Loring RH, Dahm LM, Zigmond RE (1985) Localization of α-bungarotoxin binding sites in the ciliary ganglion of the embryonic chick: an autoradiographic study at the light and electron microscopic level. Neuroscience 14:645-660.
27. Loring RH, Sah DWY, Landis SC, Zigmond RE (1988) The ultrastructural distribution of putative nicotinic receptors on cultured neurons from the rat superior cervical ganglion. Neuroscience 24:1071-1080.
28. McGehee D, Heath M, Gelber S, Role LW (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1697.
29. Palma E, Bertrand S, Binzoni T, Bertrand D (1996) Neuronal nicotinic α7 receptor expressed in Xenopus oocytes presents five putative binding sites for methyllycaconitine. J Physiol (Lond) 491:151-161.
30. Perkins GA, Renken CW, Song JY, Frey TG, Young SJ, Lanont S, Marione ME, Lindsey S, Ellisman MH (1997) Electron tomography of large multicomponent biological structures.
31. Piezzi RS, Rodriguez-Echandia EL (1968) Studies on the pararenal ganglion of the Bufo arenarum Hensel. I. Its normal fine structure and histochemical characteristics. Z Zellforsch Mikrosk Anat 88:180-186.
32. Pilar G, Tuttle JB (1982) A simple neuronal system with a range of uses: the avian ciliary ganglion. In: Progress in cholinergic biology (Hanin I, Goldberg AM, eds), pp 213-247. New York: Raven.
33. Plonsey R, Barr R (1989) Bioelectricity. New York: Plenum.
34. Pugh PC, Corriveau RA, Conroy WG, Berg DK (1995) A novel subpopulation of neuronal acetylcholine receptors among those binding α-bungarotoxin. Mol Pharmacol 47:717-725.
35. Robertson GN, Jackson PC (1996) Axosomatic synapses of the rat ciliary ganglion. Synapse 22:269-280.
36. Schoepfer R, Conroy WG, Whiting P, Gore M, Lindstrom J (1990) Brain α-bungarotoxin binding protein cDNAs and mAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 5:35-48.
37. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604.
38. Smith MA, Margiotta JF, Berg DK (1983) Differential regulation of acetylcholine sensitivity and α-bungarotoxin-binding sites on ciliary ganglion neurons in cell culture. J Neurosci 3:2395-2402.
39. Smith MA, Stollberg J, Lindstrom JM, Berg DK (1985) Characterization of a component in chick ciliary ganglia that cross-reacts with monoclonal antibodies to muscle and electric organ acetylcholine receptor. J Neurosci 5:2726-2731.
40. Smolen A (1988) Morphology of synapses in the autonomic nervous system. J Electron Microsc Tech 10:187-204.
41. Soto GE, Young SJ, Marione ME, Deerinck TJ, Lamont S, Carragher BO, Hama K, Ellisman MH (1994) Serial section electron tomography: a method for three-dimensional reconstruction of large structures. NeuroImage 1:230-243.
42. Szentagothai J (1964) The structure of the autonomic interneuronal synapse. Acta Neurovegetativa 26:338-359.
43. Takahashi K (1967) Special somatic spine synapses in the ciliary ganglion of the chick. Z Zellforsch Mikrosk Anat 83:70-75.
44. Ullian EM, McIntosh JM, Sargent PB (1997) Rapid synaptic transmission in the avian CG is mediated by two distinct classes of nicotinic receptors. J Neurosci 17:7210-7219.
45. Vernallis AB, Conroy WG, Berg DK (1993) Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10:451-464.
46. Watanabe H (1971) Adrenergic nerve elements in the hypogastric ganglion of the guinea pig. Am J Anat 130:305-330.
47. Wilson Horch HL, Sargent PB (1995) Perisynaptic surface distribution of multiple classes of nicotinic acetylcholine receptors on neurons in the chicken ciliary ganglion. J Neurosci 15:7778-7795.
48. Zhang Z-w, Vijayaraghavan S, Berg DK (1994) Neuronal acetylcholine receptors that bind α-bungarotoxin with high affinity function as ligand-gated ion channels. Neuron 12:167-177.
49. Zhang Z-w, Coggan JS, Berg DK (1996) Synaptic currents generated by neuronal acetylcholine receptors sensitive to α-bungarotoxin. Neuron 17:1231-1240.