Quantitative measurement of calcium flux through muscle and neuronal nicotinic acetylcholine receptors

Journal of Neuroscience

Volumn 14, Issue 9, 1994, Pages 5514-5524

  Vernino, Steven ^a   Rogers, Marc ^a   Radcliffe, Kristofer A ^a   Dani, John A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

cholinergic; fura 2; ion channel; patch clamp; permeability; selectivity; synaptic transmission

Indexed keywords

CHOLINERGIC RECEPTOR; NICOTINIC RECEPTOR;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM TRANSPORT; CATTLE; CHROMAFFIN CELL; MUSCLE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

EID: 0027937263     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.14-09-05514.1994     Document Type: Article

References (80)

1. Adams DJ, Dwyer TM, Hille B (1980) The permeability of endplate channels to monovalent and divalent metal cations. J Gen Physiol 75:493-510.
2. Adams DJ, Nonner W, Dwyer TM, Hille B (1981) Block of endplate channels by permeant cations in frog skeletal muscle. J Gen Physiol 78:593-615.
3. Akaike A, Mine Y, Sasa M, Takaori S (1990) Voltage and current clamp studies of muscarinic and nicotinic excitation of the rat adrenal chromaffin cells. J Pharmacol Exp Ther 255:333-339.
4. Alkondon M, Albuquerque EX (1991) Initial characterization of the nicotinic acetylcholine receptors in rat hippocampal neurons. J Recept Res 11:1001-1021.
5. Amador M, Dani JA (1991) MK-801 inhibition of nicotinic acetylcholine receptor channels. Synapse 7:207-215.
6. Amador M,Vernino S, Luetje C,Patrick J, Dani JA (1991) Modulation of neuronal nicotinic acetylcholine receptors by calcium. Soc Neurosci Abstr 17:960.
7. Ascher P, Large WA, Rang HP (1979) Studies on the mechanism of action of acetylcholine antagonists on rat parasympathetic ganglion cells. J Physiol (Lond) 295:139.
8. Belleroche J, Bradford HF (1978) Biochemical evidence for the presence of presynaptic receptors on dopaminergic nerve terminals. Brain Res 142:53-68.
9. Berg DK, Boyd RT, Halvorsen SW, Higgins LS, Jacob MH, Margiotta JF (1989) Regulating the number and function of neuronal acetylcholine receptors. Trends Neurosci 12:16-21.
10. 2+ in BC3H-1 muscle cells with fura-2: relationship to acetylcholine receptor synthesis. Cell Calcium 11: 371-384.
11. Bloch RJ, Steinbach JH (1981) Reversible loss of acetylcholine receptor clusters at the developing rat neuromuscular junction. Dev Biol 81:386-391.
12. Boulter J, Connolly J, Deneris ES, Goldman D, Heinemann S, Patrick J (1987) Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family. Proc Natl Acad Sci USA 84:7763-7767.
13. Bowman WC, Prior C, Marshall IG (1990) Presynaptic receptors in the neuromuscular junction. Ann NY Acad Sci 603:69-81.
14. Brown DA, Docherty RJ, Halliwell JV (1984) The action of cholinomimetic substances on impulse conduction in the habenulointerpeduncular pathway of the rat. J Physiol (Lond) 353:101-109.
15. Carbonetto ST, Fambrough DM, Muller KJ (1978) Nonequivalence of α-bungarotoxin receptors and acetylcholine receptors in chick sympathetic neurons. Proc Natl Acad Sci USA 75:1016-1020.
16. 125I-α-bungarotoxin. J Neurosci 5:1307-1315.
17. Conti-Tronconi BA, Dunn SMJ, Barnard EA, Dolly OJ, Lai FA, Ray N, Raftery MA (1985) Brain and muscle nicotinic acetylcholine receptors are different but homologous proteins. Proc Natl Acad Sci USA 82:5208-5212.
18. Couturier S, Bertrand D, Matter J-M, Hernandez M-C, Bertrand S, Millar N, Valera S, Barkas T, Balli vet M (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-bungarotoxin. Neuron 5:847-856.
19. Criado M, Alamo L, Navarro A (1992) Primary structure of an agonist binding subunit of the nicotinic acetylcholine receptor from bovine adrenal chromaffin cells. Neurochem Res 17:281-287.
20. Dani JA (1986) Ion-channel entrances influence permeation. Net charge, size, shape, and binding considerations. Biophys J 49:607-618.
21. Dani JA (1989) Open channel structure and ion binding sites of the nicotinic acetylcholine receptor channel. J Neurosci 9:882-890.
22. Dani JA, Eisenman G (1987) Monovalent and divalent cation permeation in acetylcholine receptor channels: ion transport related to structure. J Gen Physiol 89:959-983.
23. Dani JA, Levitt DG (1990) Diffusion and kinetic approaches to describe permeation in ion channels. J Theor Biol 146:289-301.
24. Decker ER, Dani JA (1990) Calcium permeability of the nicotinic acetylcholine receptor: the single-channel calcium influx is significant. J Neurosci 10:3413-3420.
25. Dwyer TM, Farley JM (1984) Permeability properties of chick myotube acetylcholine-activated channels. Biophys J 45:529-539.
26. Fabiato A (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol 157:378-417.
27. Fenwick EM, Marty A, Neher E, Sakmann B, Sigworth FJ (1982) Sodium and calcium channels in bovine chromaffin cells. J Physiol (Lond) 331:599-635.
28. Fieber LA, Adams DJ (1991) Acetylcholine-evoked currents in cultured neurones dissociated from rat parasympathetic cardiac ganglia. J Physiol (Lond) 434:215-237.
29. Fuchs PA, Murrow BW (1992) Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J Neurosci 12:800-809.
30. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
31. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recordings from cells and cell-free membrane patches. Pfluegers Arch 391:85-100.
32. Heinemann U, Stabel J, Rausche G (1990) Activity-dependent ionic changes and neuronal plasticity in rat hippocampus. Prog Brain Res 83:197-214.
33. Hille B (1975) Ionic selectivity of Na and K channels of nerve membranes. In: Membranes-a series of advances, Vol 3, Lipid bilayers and biological membranes: dynamic properties (G Eisenman, ed), pp 255-323. New York: Dekker.
34. Hille B (1992) Ionic channels in excitable membranes. Sunderland, MA: Sinauer.
35. Huganir RL (1988) Regulation of the nicotinic acetylcholine receptor channel by protein phosphorylation. Curr Top Membr Transpl 33: 147-163.
36. Hussy N, Bertrand D (1991) Single channel currents through α-bungarotoxin-sensitive neuronal nicotinic acetylcholine receptors. Soc Neurosci Abstr 17:249.
37. 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.
38. Katz B, Miledi R (1969) Spontaneous and evoked activity of motor nerve endings in calcium ringer. J Physiol (Lond) 203:689-706.
39. Lapchak PA, Araujo DM, Quirion R, Collier B (1989) Presynaptic mechanisms in the rat cerebellum: evidence for nicotinic, but not muscarinic autoreceptors. J Neurochem 53:1843-1851.
40. Leonard JP, Salpeter MM (1979) Agonist-induced myopathy at the neuromuscular junction is mediated by calcium. J Cell Biol 82:811-819.
41. Levitt DG (1986) Interpretation of biological ion channel flux data: reaction-rate versus continuum theory. Annu Rev Biophys Biophys Chem 15:29-57.
42. Lewis CA (1979) Ion-concentration dependence of the reversal potential and the single channel conductance of ion channels at the frog neuromuscular junction. J Physiol (Lond) 286:417-455.
43. 2+ channels in sympathetic neurons. Neuron 1:355-365.
44. Lipton SA, Aizenman E, Loring RH (1987) Neural nicotinic acetylcholine responses in solitary mammalian retinal ganglion cells. Pfluegers Arch 410:37-43.
45. Luetje CW, Patrick J (1991) Both alpha and beta subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J Neurosci 11:837-845.
46. Luetje CW, Wada K, Rogers S, Abramson SN, Tsuji K, Heinemann S, Patrick J (1990) Neurotoxins distinguish between different neuronal nicotinic acetylcholine receptor subunit combinations. J Neurochem 55:632-640.
47. 2+ store. J Biol Chem 265:3005-3012.
48. Mathie A, Cull-Candy SG, Colquhoun D (1987) Single-channel and whole-cell currents evoked by acetylcholine in dissociated sympathetic neurons of the rat. Proc R Soc Lond [Biol] 232:239-248.
49. McCormick DA, Prince DA (1987) Acetylcholine causes rapid nicotinic excitation in the medial habenular nucleus of guinea pig, in vitro. J Neurosci 7:742-752.
50. McManaman JL, Blosser JC, Appel SH (1981) The effect of calcium of acetylcholine receptor synthesis. J Neurosci 1:771-776.
51. Messing RO, Stevens AM, Kiyasu E, Sneade AB (1989) Nicotinic and muscarinic agonists stimulate rapid protein kinase C translocation in PC12 cells. J Neurosci 9:507-512.
52. Moss BL, Schuetze SM, Role LW (1989) Functional properties and developmental regulation of nicotinic acetylcholine receptors on embryonic chicken sympathetic neurons. Neuron 3:597-607.
53. Mulle C, Changeux JP (1990) A novel type of nicotinic receptor in the rat central nervous system characterized by patch-clamp techniques. J Neurosci 10:169-175.
54. Mulle C, Choquet D, Korn H, Changeux JP (1992a) Calcium influx through nicotinic receptor in rat central neurons: its relevance to cellular regulation. Neuron 8:135-143.
55. Mulle C, Lena C, Changeux JP (1992b) Potentiation of nicotinic receptor response by external calcium in rat central neurons. Neuron 8:937-945.
56. Nestler EJ, Greengard P, eds (1984) Protein phosphorylation in the nervous system. New York: Wiley.
57. Papke RL, Boulter J, Patrick J, Heinemann S (1989) Single-channel currents of rat neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes. Neuron 3:589-596.
58. 2+ influx associated with muscle activity. Nature 349:337-339.
59. 3H-acetylcholine release from mouse cerebral cortical synaptosomes. J Neurochem 43:1593-1598.
60. 5H]metabolites in rat striatum by nicotinic drugs. Brain Res 242:99-106.
61. Sánchez JA, Dani JA, Siemen D, Hille B (1986) Slow permeation of organic cations in acetylcholine receptor channels. J Gen Physiol 87: 985-1001.
62. Sands SB, Barish ME (1991) Calcium permeability of neuronal nicotinic acetylcholine receptor channels in PC-12 cells. Brain Res 560: 38-42.
63. Sargent P (1993) The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci 16:403-443.
64. Schneggenburger R, Zhou Z, Konnerth A, Neher, E (1993) Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron 11:133-143.
65. Schoepfer R, Conroy W, 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 gen superfamily. Neuron 5:35-48.
66. 125I-neuronal bungarotoxin. J Neurosci 11:287-297.
67. Séguéla P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional expression and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604.
68. Thayer SA, Miller RJ (1990) Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurones in vitro. J Physiol (Lond) 425:85-115.
69. Thayer SA, Hirning LD, Miller RJ (1988a) The role of caffeine-sensitive calcium stores in the regulation of the intracellular free calcium concentration in rat sympathetic neurons in vitro. Mol Pharmacol 34: 664-673.
70. 2+ transients using simultaneous microfluorimetry and electrophysiology. J Physiol (Lond) 412:216-223.
71. Tokimasa T, North RA (1984) Calcium entry through acetylcholine channels can activate potassium conductance in bullfrog sympathetic neurons. Brain Res 295:364-367.
72. Trouslard J, Marsh SJ, Brown DA (1993) Calcium entry through nicotinic receptor channels and calcium channels in cultured rat superior cervical ganglion cells. J Physiol (Lond) 468:53-71.
73. Vernino S, Amador M, Luetje CW, Patrick J, Dani JA (1992) Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron 8:127-135.
74. Vijayaraghavan S, Pugh PC, Zhang Z, Rathouz MM, Berg DK (1992) Nicotinic receptors that bind α-bungarotoxin on neurons raise intracellular free calcium. Neuron 8:353-362.
75. Vizi ES, Somogyi GT (1989) Prejunctional modulation of acetylcholine release from the skeletal neuromuscular junction: link between positive (nicotinic)- and negative (muscarinic)-feedback mechanisms. Br J Pharmacol 97:65-70.
76. Wong LS, Gallagher JP (1991) Pharmacology of nicotinic receptormediated inhibition in rat dorsolateral septal neurones. J Physiol (Lond) 436:325-346.
77. Wonnacott S, Drasdo A, Sanderson E, Rowell P (1990) Presynaptic nicotinic receptors and the modulation of transmitter release. In: The Biology of nicotine dependence (Bock G, Marsh J, eds), pp 87-105. New York: Wiley.
78. 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.
79. Zhou Z, Neher E (1993) Calcium permeability of nicotinic acetylcholine receptor channels in bovine adrenal chromaffin cells. Pfluegers Arch 425:511-517.
80. Zorumski CF, Thio LL, Isenberg KE, Clifford DB (1992) Nicotinic acetylcholine currents in cultured postnatal rat hippocampal neurons. Mol Pharmacol 41:931-936.