Calcium flux through predominantly independent purinergic ATP and nicotinic acetylcholine receptors

Journal of Neurophysiology

Volumn 77, Issue 3, 1997, Pages 1407-1417

  Rogers, Marc ^a,b   Colquhoun, Lorna M ^a   Patrick, James W ^a   Dani, John A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; NICOTINIC RECEPTOR; PURINE RECEPTOR;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; MICROFLUOROMETRY; NONHUMAN; OOCYTE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYMPATHETIC NERVE CELL; XENOPUS;

EID: 0030900294     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1997.77.3.1407     Document Type: Article

References (78)

1. ADAMS, D. J., DWYER, T. M., AND HILLE, B. The permeability of endplate channels to monovalent and divalent metal cations. J. Gen. Physiol. 75: 493-510, 1980.
2. AKASU, T. AND KOKETSU, K. Effect of adenosine trisphosphate on the sensitivity of the nicotinic acetylcholine receptor in bullfrog sympathetic ganglion. Br. J. Pharmacol. 84: 525-531, 1985.
3. AMADOR, M. A. AND DANI, J. A. Mechanism for modulation of nicotinic acetykholine receptors that can influence synaptic transmission. J. Neurosci. 15: 4525-4532, 1995.
4. BEAN, B. P. ATP-activated channels in rat and bullfrog sensory neurons: concentration dependence and kinetics. J. Neurosci. 10: 1-10, 1990a.
5. BEAN, B. P. ATP-activated channels in rat and bullfrog sensory neurons: current-voltage relation and single channel behavior. J. Neurosci. 10: 11-19, 1990b.
6. BEAN, B. P. Pharmacology and electrophysiology of ATP-activated ion channels. Trends Pharmacol. Sci. 13: 87-90, 1992.
7. BENHAM, C. D., BOLTON, T. B., BYRNE, N. G., AND LARGE, W. A. Action of externally applied adenosine triphosphate on single smooth muscle cells dispersed from rabbit ear artery. J. Physiol. Lond. 387: 473-488, 1987.
8. 2+-permeable channel activated by ATP in smooth muscle. Nature Lond. 328: 275-277, 1987.
9. BETZ, H. Glycine receptors: heterogeneous and widespread in the mammalian brain. Trends Neurosci. 14: 458-461, 1991.
10. BRAKE, A. J., WAGENBACH, M. J., AND JULIUS, D. New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor. Nature Lond. 371: 519-523, 1994.
11. BUELL, G., LEWIS, C., COLLO, G., NORTH, R. A., AND SURPRENANT, A. An antagonist-insensitive P2X receptor expressed in epithelia and brain. EMBO J. 15: 55-62, 1996.
12. CASTRO, N. G. AND ALBUQUERQUE, E. X. α-Bungarotoxin-sensitive hippocampal receptor channel has a high calcium permeability. Biophys. J. 68: 516-524, 1995.
13. CHEN, C.-C., AKOPIAN, A. N., SIVILOTTI, L., COLQUHOUN, D., BURNSTOCK, G., AND WOOD, J. N. A P2X purinoceptor expressed by a subset of sensory neurons. Nature Lond. 377: 428-431, 1995.
14. CLOUES, R., JONES, S., AND BROWN, D. Zinc potentiates ATP-activated currents in rat sympathetic neurons. Pfluegers Arch. 424: 152-158, 1993.
15. CONROY, W. G. AND BERG B. K. Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J. Biol. Chem. 270: 4424-4431, 1995.
16. CONROY, W. G., VERNALLIS, A. B., AND BERG, D. K. The α5 gene product assembles with multiple acetylcholine receptor subunits to form distinctive receptor subtypes in brain. Neuron 9: 679-691, 1992.
17. DECKER, E. R. AND DANI, J. A. Calcium permeability of the nicotinic acetylcholine receptor: the single-channel calcium influx is significant. J. Neurosci. 10: 3413-3420, 1990.
18. EDWARDS, F. A., GIBB, A. J., AND COLQUHOUN, D. ATP receptor-mediated synaptic current in the central nervous system. Nature Lond. 359: 144-147, 1992.
19. EVANS, R. J., DERKACH, V., AND SURPRENANT, A. ATP mediates fast synaptic transmission in mammalian neurons. Nature Lond. 357: 503-505, 1992.
20. EVANS, R. J. AND SURPRENANT, A. Vasoconstriction of guinea-pig submucosal arterioles following sympathetic nerve stimulation is mediated through release of ATP. Br. J. Pharmacol. 106: 242-249, 1992.
21. 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, 1991a.
22. FIEBER, L. A. AND ADAMS, D. J. Adenosine trisphosphate-evoked currents in cultured neurones dissociated from rat parasympathetic cardiac ganglia. J. Physiol. Lond. 434: 239-256, 1991b.
23. FREDHOLM, B. B., ABBRACHIO, M. A., BURNSTOCK, G., DALY, J. W., HARDEN, T. K., JACOBSON, K. A., LEFF, P. A., AND WILLIAMS, M. Nomenclature and classification of purinoceptors. Pharmacol. Rev. 46: 143-156, 1994.
24. Fu, W.-M. Potentiation by ATP of the postsynaptic acetylcholine responses at developing neuromuscular synapses in Xenopus cell cultures. J. Physiol. Lond. 477: 449-458, 1994.
25. FUCHS, P. A. AND MORROW, B. W. Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J. Neurosci. 12: 800-809, 1992.
26. GALLIGAN, J. J. AND BERTRAND, P. P. ATP mediates fast synaptic potentials in enteric neurons. J. Neurosci. 14: 7563-7571, 1994.
27. GRAY, R., RAJAN, A. S., RADCLIFFE, K. A., YAKEHIRO, M., AND DANI, J. A. Low concentrations of nicotine enhance glutamatergic synaptic transmission in the hippocampus. Nature Lond. 383: 713-716, 1996.
28. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440-3450, 1985.
29. HILLE, B. Ionic selectivity of Na and K channels of nerve membranes. In: Membranes - A Series of Advances. Lipid Bilayers and Biological Membranes: Dynamic Properties, edited by G. Eisenman. New York: Dekker, 1975, vol. 3, p. 255-323.
30. HOUSLEY, G. D., GREENWOOD, D., AND ASHMORE, J. F. Localization of cholinergic and purinergic receptors on outer hair cells isolated from guinea-pig cochlear. Proc. R. Soc. Lond. B Biol. Sci. 249: 265-273, 1992.
31. HOYLE, C., KNIGHT, G. E., AND BURNSTOCK, G. Suramin antagonizes responses to P2 purinoceptor agonists and purinergic nerve stimulation in guinea pig urinary bladder and taenia coli. Br. J. Pharmacol. 99: 617-621, 1990.
32. IGUSA, Y. Adenosine 5-trisphosphate activates acetylcholine receptor channels in cultured Xenopus myotomal muscle cells. J. Physiol. Lond. 405: 169-185, 1988.
33. KATZ, B. Nerve, Muscle and Synapse. New York: McGraw-Hill, 1966.
34. KHAKH, B. S., HUMPHREY, P.P.A., AND SURPRENANT, A. Electrophysiological properties of P2x purinoceptors in rat superior cervical, nodose and guinea-pig coeliac neurons. J. Physiol. Lond. 484: 385-395, 1995.
35. 3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature Land. 377: 432-435, 1995.
36. 2+ channels in sympathetic neurons. Neuron 1: 355-365, 1988.
37. LU, Z. AND SMITH, D. O. Adenosine 5-trisphosphate increases acetylcholine channel opening frequency in rat skeletal muscle. J. Physiol. Lond. 436: 45-56, 1991.
38. MANDELZYS, A., PIE, B., DENERIS, E. S., AND COOPER, E. The developmental increase in ACh current densities on rat sympathetic neurons correlates with changes in nicotinic ACh receptor α-subunit gene expression and occurs independent of innervation. J. Neurosci. 14: 2357-2364, 1994.
39. MATHIE, A., CULL-CANDY, S. G., AND COLQUHOUN, D. Single-channel and whole-cell currents evoked by acetylcholine in dissociated sympathetic neurons of the rat. Proc. R. Soc. Lond. B Biol. Sci. 232: 239-248, 1987.
40. MCGEHEE, D. S., HEATH, M.J.S., GELBER, S., DEVAY, P., AND ROLE, L. W. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors Science Wash. DC 269: 1692-1696, 1995.
41. MCGEHEE, D. S. AND ROLE, L. W. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu. Rev. Physiol. 57: 521-546 1995.
42. MCMAHON, L. L., YOON, K.-W., AND CHIAPZNELLI, V. A. Electrophysiological evidence for presynaptic nicotinic receptors in the avian ventral lateral geniculate nucleus. J. Neurophysiol. 71: 826-829, 1994.
43. MOZRZYMAS, J. W. AND RUZZIER, F. ATP activates junctional and extrajunctional acetylcholine receptor channels in isolated adult rat muscle fibres. Neurosci. Lett. 139: 217-220, 1992.
44. 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, 1992.
45. NABEKURA, J., UENO, S., OGAWA, T., AND AKAIKE, N. Colocalization of ATP and nicotinic ACh receptors in the identified vagal preganglionic neuron of rat. J. Physiol. Lond. 489: 519-527, 1995.
46. NAKAGAWA, T., AKAIKE, N., KJMITSUKI, T., KOMUNE, S., AND ARIMA, T. ATP-induced current in isolated outer hair cells of guinea pig cochlea. J. Neurophysiol. 63: 1068-1074, 1990.
47. NAKAZAWA, K. ATP-activated current and its interaction with acetylchohone-activated currents in rat sympathetic neurons. J. Neurosci. 14: 740-750, 1994.
48. NAKAZAWA, K., FUJIMORI, K., TAKANAKA, A., AND INOUE, K. Comparison of adenosine triphosphate- and nicotine-activated inward currents in rat pheochromocytoma cells. J. Physiol. Lond. 434: 647-660, 1991.
49. NEELY, A. AND LINGLE, C. J. Trapping of an open-channel blocker at the frog neuromuscular acetylcholine channel. Biophys. J. 50: 981-986, 1986.
50. NEHER, E. AND AUGUSTINE, G. J. Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. Lond. 450: 273-301, 1992.
51. PELLEG, A. AND HURT, C. M. Mechanism of action of ATP on canine pulmonary vagal C fibre nerve terminals. J. Physiol. Lond. 490: 265-275, 1996.
52. RAMIREZ-LATORRE, J., YU, C. R., QU, X., PERIN, F., KARLIN, A., AND ROLE, L. Functional contributions of α5 subunit to neuronal acetylcholine receptor channels. Nature Lond. 380: 347-351, 1996.
53. RAYMOND, L. A., BLACKSTONE, C. D., AND HUGANIR, R. L. Phosphorylation of amino acid neurotransmitter receptors in synaptic plasticity. Trends Neurosci. 16: 147-153, 1993.
54. ROGERS, M. AND DANI, J. A. Comparison of quantitative calcium flux through NMDA, ATP and ACh receptor channels. Biophys. J. 68: 501-506, 1995.
55. SARGENT, P. The diversity of neuronal nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 16: 403-443, 1993.
56. SCHNEGGENBURGER, R., ZHOU, Z., KONNERTH, A., AND NEHER, E. Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron 11: 133-143, 1993.
57. Ca in myocytes from guinea-pig urinary bladder. J. Physiol. Lond. 440: 479-496, 1991.
58. SCHRATTENHOLZ, A., ROTH, U., SCHUHEN, A., SCHAFER, H. J., GODOVAC- ZIMMERMAN, J., ALBUQUERQUE, E. X., AND MAELICKE, A. Identification of purine binding sites on Torpedo acetylcholine receptor. J. Recept. Res. 14: 197-208, 1994.
59. SÉGUÉLA, P., HAGHIGHI, A., SOGHOMONIAN, J.-J., AND COOPER, E. A novel neuronal P2X ATP receptor ion channel with widespread distribution in the brain. J. Neurosci. 15: 448-455, 1995,
60. SÉGUÉLA, P., WADICHE, J., DINELEY-MILLER, K., DANI, J. A., AND PATRICK, J. W. Molecular cloning, functional expression and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 13: 596-604, 1993.
61. SILINSKY, E. AND GERZANICH, V. On the excitatory effects of ATP and its role as a neurotransmitter in coeliac neurons of the guinea-pig. J. Physiol. Lond. 464: 197-212, 1993.
62. SMITH, K. E. AND KESSLER, J. A. Non-neuronal cell conditioned medium regulates muscarinic receptor expression in cultured sympathetic neurons. J. Neurosci. 8: 2406-2413, 1988.
63. SURPRENANT, A., BUELL, G., AND NORTH, R. A. P2x receptors bring new structure to ligand-gated ion channels. Trends Neurosci. 18: 224-229, 1995.
64. 2+-ATPase. Proc. Natl. Acad. Sci. USA 87: 2466-2470, 1990.
65. THAYER, S. A., HIRNING, L. D., AND MILLER, R. J. 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, 1988.
66. THAYER, S. A. AND MILLER, R. J. Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurones in vitro. J. Physiol. Lond. 425: 85-115, 1990.
67. TOKIMASA, T. AND NORTH, R. A. Calcium entry through acetylcholine channels can activate potassium conductance in bullfrog sympathetic neurons. Brain Res. 295: 364-367, 1984.
68. TROUSLARD, J., MARSH, S. J., AND BROWN, D. A. Calcium entry through nicotinic receptor channels and calcium channels in cultured rat superior cervical ganglion cells. J. Physiol. Lond. 468: 53-71, 1993.
69. VALERA, S., HUSSY, N., EVANS, R. J., ADAMI, N., NORTH, R. A., SURPRENANT, A., AND BUELL, G. A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP. Nature Lond. 371: 516-519, 1994.
70. 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: 127-135, 1992.
71. VERNENO, 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.
72. VIJAYARAGHAVAN, S., HUANG, B., BLUMENTAL, M., AND BERG, D. K. Ara- chidonic acid as a possible negative feedback inhibitor of nicotinic acetyl- choline receptors on neurons. J. Neurosci. 15: 3679-3687, 1995.
73. VIZI, E. S. AND SOMOGYI, G. T. 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, 1989.
74. WANG, F., GERAZNICH, V., WELLS, G. B., ANAND, R., PENG, X., KEYSER, K., AND LINDSTROM, J. Assembly of human neuronal nicotinic receptor α5 subunits with α3, β2, and β4 subunits. J. Biol. Chem. 271: 17656-17665, 1996.
75. WONG, L. S. AND GALLAGHER, J. P. Pharmacology of nicotinic receptor-mediated inhibition in rat dorsolateral septal neurones. J. Physiol. Lond. 436: 325-346, 1991.
76. WONNACOTT, S., DRASDO, A., SANDERSON, E., AND ROWELL, P. Presynaptic nicotinic receptors and the modulation of transmitter release. In: The Biology of Nicotine Dependence, edited by G. Bock and J. Marsh. New York: Wiley, 1990, p. 87-105.
77. ZHOU, Z. AND NEHER, E. Calcium permeability of nicotinic acetylcholine receptor channels in bovine adrenal chromaffin cells. Pfluegers Arch. 425: 511-517, 1993.
78. ZIMMERMANN, H. Signalling via ATP in the nervous system. Trends Neurosci. 17: 420-426, 1994.