Extracellular calcium regulates responses of both α3- and α7- containing nicotinic receptors on chick ciliary ganglion neurons

Journal of Neurophysiology

Volumn 82, Issue 3, 1999, Pages 1124-1132

  Liu, Qing Song ^a   Berg, Darwin K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARIUM; CALCIUM; NICOTINIC AGENT; NICOTINIC RECEPTOR; STRONTIUM;

ANIMAL CELL; ARTICLE; CHICK EMBRYO; CILIARY GANGLION; EMBRYO; EXTRACELLULAR SPACE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; RECEPTOR SENSITIVITY; REGULATORY MECHANISM;

EID: 0032824274     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.82.3.1124     Document Type: Article

References (68)

1. ALKONDON, M. AND ALBUQUERQUE, E. X. Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J. Pharmacol. Exp. Ther. 265: 1455-1473, 1993.
2. ALKONDON, M., PEREIRA, E.F.R., CORTES, W. S., MAELICKE, A., AND ALBUQUERQUE, E. X. Choline is a selective agonist of α7 nicotinic acetylcholine receptors in the rat brain neurons. Eur. J. Neurosci. 9: 2734-2742, 1997.
3. AMADOR, M. AND DANI, J. A. Mechanism for modulation of nicotinic acetylcholine receptors that can influence synaptic transmission. J. Neurosci. 15: 4525-4532, 1995.
4. ANAND, R., PENG, X., AND LINDSTROM, J. 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, 1993.
5. ARAMAKIS, V. B. AND METHERATE, R. Nicotine selectively enhances NMDA receptor-mediated synaptic transmission during postnatal development in sensory neocortex. J. Neurosci. 18: 8485-8495, 1998.
6. BENNINGER, C., KADIS, J., AND PRINCE, D. A. Extracellular calcium and potassium changes in hippocampal slices. Brain Res. 187: 165-182, 1980.
7. BERTRAND, D., GALZI, J. L., DEVILLERS-THIERY, A., BERTRAND, S., AND CHANGEUX, J. P. 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, 1993.
8. ++. J. Pharmacol. Exp. Ther. 277: 432-444, 1996.
9. BOOKER, T. K., SMITH, K. W., DODRILL, C., AND COLLINS, A. C. Calcium modulation of activation and desensitization of nicotinic receptors from mouse brain. J. Neurochem. 71: 1490-1500, 1998.
10. CHAN, J. AND QUIK, M. A role for nicotinic α-bungarotoxin receptor in neurite outgrowth in PC12 cells. Neuroscience 56: 441-451, 1993.
11. CHIAPPINELLI, V. A. Kappa-bungarotoxin: a probe for the neuronal nicotinic receptor in the avian ciliary ganglion. Brain Res. 277: 9-21, 1983.
12. CHIAPPINELLI, V. A. AND GIACOBINI, E. Time course of appearance of α-bungarotoxin binding sites during development of chick CG and iris. Neurochem. Res. 3: 465-478, 1978.
13. COGGAN, J. S., PAYSAN, J., CONROY, W. G., AND BERG, D. K. Direct recording of nicotinic responses in presynaptic nerve terminals. J. Neurosci. 17: 5798-5806, 1997.
14. CONROY, W. G. AND BERG, D. K. Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J. Biol. Chem. 270: 4424-4431, 1995.
15. CONROY, W. G. AND BERG, D. K. 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, 1998.
16. CORRIVEAU, R. A. AND BERG, D. K. Neurons in culture maintain acetylcholine receptor levels with far fewer transcripts than in vivo. J. Neurobiol. 25: 1579-1592, 1994.
17. COUTURIER, S., BERTRAND, D., MATTER, J.-M., HERNANDEZ, M.-C., BERTRAND, S., MILLAR, N., VALERA, S., BARKAS, T., AND BALLIVET, M. A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5: 847-856, 1990.
18. CUEVAS, J. AND BERG, D. K. Mammalian nicotinic receptors with α7 subunits that slowly desensitize and rapidly recover from α-bungarotoxin blockade. J. Neurosci. 18: 10335-10344, 1998.
19. DRYER, S. E. 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, 1994.
20. EISELE, J.-L., BERTRAND, S., GALZI, J.-L., DEVILLERS-THIERY, A., CHANGEUX, J.-P., AND BERTRAND, D. Chimaeric nicotinic-serotonergic receptor combines distinct ligand binding and channel specificities. Nature 366: 479-483, 1993.
21. FENSTER, C. P., RAINS, M. F., NOERAGER, B., QUICK, M. W., AND LESTER, R. A. Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J. Neurosci. 17: 5747-5759, 1997.
22. FIEBER, L. A. AND ADAMS, D. J. Acetylcholine-evoked currents in cultured neurones dissociated from rat parasympathetic cardiac ganglia. J. Physiol. (Lond.) 434: 215-237, 1991.
23. FU, W.-M., LIOU, H.-C., AND CHEN, Y.-H. Nerve terminal currents induced by autoreception of acetylcholine release. J. Neurosci. 18: 9954-9961, 1998.
24. FU, W.-M. AND LIU, J.-J. Regulation of acetylcholine release by presynaptic nicotinic receptors at developing neuromuscular synapses. Mol. Pharmacol. 51: 390-398, 1997.
25. GALZI, J.-L., BERTRAND, S., CORRINGER, P.-J., CHANGEUX, J.-P., AND BERTRAND, D. Identification of calcium binding sites that regulate potentiation of a neuronal nicotinic acetylcholine receptor. EMBO J. 15: 5824-5832, 1996.
26. GRAY, R., RAJAN, A. S., RADCLIFFE, K. A., YAKEHIRO, M., AND DANI, J. A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713-716, 1996.
27. GUO, J.-Z., TREDWAY, T. L., AND CHIAPPINELLI, V. A. Glutamate and GABA release are enhanced by different subtypes of presynaptic nicotinic receptors in the lateral geniculate nucleus. J. Neurosci. 18: 1963-1969, 1998.
28. HAMILL, O. P., MARTY, A., NEHER, E., SAKMANN, B., AND SIGWORTH, F. J. Improved patch-clamp techniques for high-resolution current recordings from cells and cell-free membrane patches. Pflügers Arch. 391: 85-100, 1981.
29. HEINEMANN, U., STABEL, J., AND RAUSCHE, G. Activity-dependent ionic changes and neuronal plasticity in rat hippocampus. Prog. Brain Res. 83: 197-214, 1990.
30. HORN, R. AND MARTY, A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J. Gen. Physiol. 92: 145-159, 1988.
31. JACOB, M. H. AND BERG, D. K. The ultrastructural localization of α-bungarotoxin binding sites in relation to synapses on chick CG neurons. J. Neurosci. 3: 260-271, 1983.
32. JACOB, M. H., BERG, D. K., AND LINDSTROM, J. M. A shared antigenic determinant between the Electrophorus acetylcholine receptor and a synaptic component on chick CG neurons. Proc. Natl. Acad. Sci. U SA 81: 3223-3227, 1984.
33. KASSNER, P. D. AND BERG, D. K. Differences in the fate of neuronal acetylcholine receptor protein expressed in neurons and stably transfected cells. J. Neurobiol. 33: 968-982, 1997.
34. LANDMESSER, L. AND PILAR, G. Synapse formation during embryogenesis on ganglion cells lacking a periphery. J. Physiol. (Lond.) 241: 715-736, 1974.
35. LI, X., RAINNIE, D. G., MCCARLEY, R. W., AND GREENE, R. W. Presynaptic nicotinic receptors facilitate monoaminergic transmission. J. Neurosci. 18: 1904-1912, 1998.
36. LIVSEY, C. T., HUANG, B., XU, J., AND KARWOSKI, C. J. Light-evoked changes in extracellular calcium concentration in frog retina. Vision Res. 6: 853-861, 1990.
37. LORING, R. H., CHIAPPINELLI, V. A., ZIGMOND, R. E., AND COHEN, J. B. Characterization of a snake venom neurotoxin which blocks nicotinic transmission in the avian ciliary ganglion. Neuroscience 11: 989-999, 1984.
38. LORING, R. H., DAHM, R. H., AND ZIGMOND, R. E. 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, 1985.
39. 125I-toxin F binding sites on chick ciliary neurons: synaptic localization of a toxin that blocks ganglionic nicotinic receptors. J. Neurosci. 7: 2153-2162, 1987.
40. MARGIOTTA, J. F. AND GURANTZ, D. Changes in the number, function, and regulation of nicotinic acetylcholine receptors during neuronal development. Dev. Biol. 135: 326-339, 1989.
41. MCGEHEE, D., HEATH, M., GELBER, S., AND ROLE, L. W, Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269: 1692-1697, 1995.
42. MCGEHEE, D. S. AND ROLE, L. W. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu. Rev. Physiol. 57: 521-546, 1995.
43. MULLE, C., CHOQUET, D., KORN, H., AND CHANGEUX, J.-P. Calcium influx through nicotinic receptor in rat central neurons: its relevance to cellular regulation. Neuron 8: 135-143, 1992a.
44. MULLE, C., LENA, C., AND CHANGEUX, J.-P. Potentiation of nicotinic receptor response by external calcium in rat central neurons. Neuron 8: 937-945, 1992b.
45. NISHI, R. AND BERG, D. K. Two components from eye tissue that differentially stimulate the growth and development of CG neurons in cell culture. J. Neurosci. 1: 505-513, 1981.
46. PUGH, P. C. AND BERG, D. K. Neuronal acetylcholine receptors that bind α-bungarotoxin mediate neurite retraction in a calcium-dependent manner. J. Neurosci. 14: 889-896, 1994.
47. PUGH, P. C., CORRIVEAU, R. A., CONROY, W. G., AND BERG, D. K. A novel subpopulation of neuronal acetylcholine receptors among those binding a-bungarotoxin. Mol. Pharmacol. 47: 717-725, 1995.
48. PUMAIN, R. AND HEINEMANN, U. Stimulus-and amino acid-induced calcium and potassium changes in the rat neocortex. J. Neurophysiol. 53: 1-16, 1985.
49. RADCLIFFE, K. A. AND DANI, J. A. Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J. Neurosci. 18: 7075-7083, 1998.
50. RAE, J., COOPER, K., GATES, P., AND WATSKY, M. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods 37: 15-26, 1991.
51. RATHOUZ, M. M. AND BERG, D. K. Synaptic-type acetylcholine receptors raise intracellular calcium levels in neurons by two mechanisms. J. Neurosci. 14: 6935-6945, 1994.
52. RATHOUZ, M. M., VUAYARAGHAVAN, S., AND BERG, D. K. Elevation of intracellular calcium levels in neurons by nicotinic acetylcholine receptors. Mol. Neurobiol. 12: 117-131, 1996.
53. SARGENT, P. B. The diversity of neuronal nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 16: 403-443, 1993.
54. SCHOEPFER, R., CONROY, W. G., WHITING, P., GORE, M., AND LINDSTROM, J. 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, 1990.
55. SEGUELA, P., WADICHE, J., DINELEY-MILLER, K., DANI, J. A., AND PATRICK, J. W. Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 13: 596-604, 1993.
56. SHOOP, R. D., MARTONE, M. E., YAMADA, N., ELLISMAN, M. H., AND BERG, D. K. Neuronal acetylcholine receptors with α7 subunits are concentrated on somatic spines for synaptic signaling in embryonic chick ciliary ganglia. J. Neurosci. 19: 692-704, 1999.
57. ULLIAN, E. M, MCINTOSH, J. M., AND SARGENT, P. B. Rapid synaptic transmission in the avian CG is mediated by two distinct classes of nicotinic receptors. J. Neurosci. 17: 7210-7219, 1997.
58. VERNALLIS, A. B., CONROY, W. G., AND BERG, D. K. Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10: 451-464, 1993.
59. VERNINO, S., AMADOR, M., LUETJE, C. W., PATRICK, J., AND DANI, J. A. Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron 8: 127-134, 1992.
60. VERNINO, S., ROGERS, M., RADCLIFFE, K. A., AND DANI, J. A. Quantitative measurement of calcium flux through muscle and neuronal nicotinic acetylcholine receptors. J. Neurosci. 14: 5514-5524, 1994.
61. VIJAYARAGHAVAN, S., HUANG, B., BLUMENTHAL, E. M., AND BERG, D. K. Arachidonic acid as a possible negative feedback inhibitor of nicotinic acetylcholine receptors on neurons. J. Neurosci. 15: 3679-3687, 1995.
62. ++. Neuron 8: 353-362, 1992.
63. WILSON HORCH, H. L. AND SARGENT, P. B. Perisynaptic surface distribution of multiple classes of nicotinic acetylcholine receptors on neurons in the chicken CG. J. Neurosci. 15: 7778-7795, 1995.
64. YU, C. R. AND ROLE, L. W. Functional contribution of the α7 subunit to multiple subtypes of nicotinic receptors in embryonic chick sympathetic neurones. J. Physiol. (Lond.) 509: 651-665, 1998.
65. ZHANG, Z.-W. AND BERG, D. K. Patch-clamp analysis of glycine-induced currents in chick CG neurons. J. Physiol. (Lond.) 487: 395-405, 1995.
66. ZHANG, Z.-W., COGGAN, J. S., AND BERG, D. K. Synaptic currents generated by neuronal acetylcholine receptors sensitive to α-bungarotoxin. Neuron 17: 1231-1240, 1996.
67. ZHANG, Z.-W., VIJAYARAGHAVAN, S., AND BERG, D. K. Neuronal acetylcholine receptors that bind α-bungarotoxin with high affinity function as ligandgated ion channels. Neuron 12: 167-177, 1994.
68. ZORUMSKI, C. F., THIO, L. L., ISENBERG, K. E., AND CLIFFORD, D. B. Nicotinic acetylcholine currents in cultured postnatal rat hippocampal neurons. Mol. Pharmacol. 41: 931-936, 1992.