Nicotinic acetylcholine receptors containing α7 subunits are required for reliable synaptic transmission in situ

Journal of Neuroscience

Volumn 19, Issue 10, 1999, Pages 3701-3710

  Chang, Karen T ^a   Berg, Darwin K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine; Calyx; Ciliary; Ganglion; Neuronal; Nicotinic; Patch clamp; Postsynaptic; Receptors; Synaptic; Transmission; bungarotoxin; 7

Indexed keywords

NICOTINIC RECEPTOR;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CHICKEN; EMBRYO DEVELOPMENT; EVOKED RESPONSE; NONHUMAN; POSTGANGLIONIC NERVE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

EID: 0033562868     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-10-03701.1999     Document Type: Article

References (54)

1. Alkondon M, Pereira EF, Wonnacott S, Albuquerque EX (1992) Blockade of nicotinic currents in hippocampal neurons defines methyllycaconitine as a potent and specific receptor antagonist. Mol Pharmacol 41:802-808.
2. 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.
3. 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.
4. 2+ transients and their transmission in the developing chick retina. Curr Biol 8:283-286.
5. 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.
6. Chiappinelli VA (1983) Kappa-bungarotoxin: a probe for the neuronal nicotinic receptor in the avian ciliary ganglion. Brain Res 277:9-21.
7. 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.
8. Coggan JS, Paysan J, Conroy WG, Berg DK (1997) Direct recording of nicotinic responses in presynaptic nerve terminals. J Neurosci 17:5798-5806.
9. 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.
10. 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.
11. Corriveau RA, Berg DK (1994) Neurons in culture maintain acetylcholine receptor levels with far fewer transcripts than in vivo. J Neurobiol 25:1579-1592.
12. 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.
13. Cuevas J, Harper AA, Trequattrini C, Adams DJ (1997) Passive and active membrane properties of isolated rat intracardiac neurons: regulation by H- and M-currents. J Neurophysiol 78:1890-1902.
14. Dahm LM, Landmesser LT (1991) The regulation of synaptogenesis during normal development and following activity blockade. J Neurosci 11:238-255.
15. Ding R, Jansen JKS, Laing NG, Tonnesen H (1983) The innervation of skeletal muscles in chickens curarized during early development. J Neurocytol 12:887-919.
16. 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.
17. Dryer SE, Chiappinelli VA (1987) Analysis of quantal content and quantal conductance in two populations of neurons in the avian ciliary ganglion. Neuroscience 20:905-910.
18. Feller MB, Wellis DP, Stellwagen D, Werblin FS, Shatz CJ (1996) Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272:1182-1187.
19. Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV (1998) Synaptic potentials mediated via α-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 18:8228-8235.
20. Fu W-M, Liu J-J (1997) Regulation of acetylcholine release by presynaptic nicotinic receptors at developing neuromuscular synapses. Mol Pharmacol 51:390-398.
21. Galli L, Maffei L (1988) Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242:90-91.
22. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
23. 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.
24. 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.
25. 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.
26. Landmesser L, Pilar G (1974) Synapse formation during embryogenesis on ganglion cells lacking a periphery. J Physiol (Lond) 241:715-736.
27. Li X, Rainnie DG, McCarley RW, Greene RW (1998) Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 18:1904-1912.
28. Link BA, Nishi R (1998) Development of the avian iris and ciliary body: mechanisms of cellular differentiation during the smooth-to-striated muscle transition. Dev Biol 203:163-176.
29. 125I-toxin F binding sites on chick ciliary neurons: synaptic localization of a toxin that blocks ganglionic nicotinic receptors. J Neurosci 7:2153-2162.
30. Loring RH, Chiappinelli VA, Zigmond RE, Cohen JB (1984) Characterization of a snake venom neurotoxin which blocks nicotinic transmission in the avian ciliary ganglion. Neuroscience 11:989-999.
31. Marwitt G, Pilar G, Weakly JN (1971) Characterization of two ganglion cell populations in avian ciliary ganglia. Brain Res 25:317-334.
32. 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.
33. Meriney SD, Pilar G, Ogaswa M, Nunez R (1987) Differential neuronal survival in the avian ciliary ganglion after chronic acetylcholine receptor blockade. J Neurosci 7:3840-3849.
34. Mooney R, Penn AA, Gallego R, Shatz CJ (1996) Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17:863-874.
35. O'Donovan MJ, Landmesser L (1987) The development of hindlimb motor activity studied in the isolated spinal cord of the chick embryo. J Neurosci 7:3256-3264.
36. Penn AA, Riquelme PA, Feller MB, Shatz CJ (1998) Competition in retinogeniculate patterning driven by spontaneous activity. Science 279:2108-2112.
37. Pilar G, Landmesser L, Burnstein L (1980) Competition for survival among developing ciliary ganglion cells. J Neurophysiol 43:233-254.
38. Pugh PC, Berg DK (1994) Neuronal acetylcholine receptors that bind α-bungarotoxin mediate neurite retraction in a calcium-dependent manner. J Neurosci 14:889-896.
39. Rae J, Cooper K, Gates P, Watsky M (1991) Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37:15-26.
40. Ruthazer ES, Stryker MP (1996) The role of activity in the development of long-range horizontal connections in area 17 of the ferret. J Neurosci 16:7253-7269.
41. 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.
42. 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.
43. Shatz CJ, Stryker MP (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87-89.
44. Shoop RD, Martone ME, Yamada N, Ellisman MH, Berg DK (1999) Neuronal acetylcholine receptors with α7 subunits are concentrated on somatic spines for synaptic signaling. J Neurosci 19:692-704.
45. Thompson WJ (1985) Activity and synapse elimination at the neuromuscular junction. Cell Mol Neurobiol 5:167-182.
46. 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.
47. 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.
48. Vijayaraghavan S, Huang B, Blumenthal EM, Berg DK (1995) Arachidonic acid as a possible negative feedback inhibitor of nicotinic acetylcholine receptors on neurons. J Neurosci 15:3679-3687.
49. Ward JM, Cockcroft VB, Lunt GG, Smillie FS, Wonnacott S (1990) Methyllycaconitine: a selective probe for neuronal α-bungarotoxin binding sites. FEBS Lett 270:45-48.
50. Weliky M, Katz LC (1997) Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386:680-685.
51. 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.
52. Yawo H, Chuhma N (1994) ω-Conotoxin-sensitive and -resistant transmitter release from the chick ciliary presynaptic terminal. J Physiol (Lond) 477:437-448.
53. Yawo H, Momiyama A (1993) Re-evaluation of calcium currents in preand postsynaptic neurones of the chick ciliary ganglion. J Physiol (Lond) 460:153-172.
54. Zhang Z-w, Coggan JS, Berg DK (1996) Synaptic currents generated by neuronal acetylcholine receptors sensitive to α-bungarotoxin. Neuron 17:1231-1240.