Muscarine activates a nonselective cation current through a M3 muscarinic receptor subtype in rat dorsolateral septal nucleus neurons

Journal of Neurophysiology

Volumn 76, Issue 4, 1996, Pages 2221-2230

  Hasuo, Hiroshi ^a   Akasu, Takashi ^b   Gallagher, Joel P ^b  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ATROPINE; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); METHOCTRAMINE; METHYL IODIDE; MUSCARINE; MUSCARINIC M3 RECEPTOR; OTENZEPAD; OXOTREMORINE; PERTUSSIS TOXIN; PIRENZEPINE; POTASSIUM ION; SODIUM ION; [4 [(3 CHLOROPHENYL)CARBAMOYLOXY] 2 BUTYNYL]TRIMETHYLAMMONIUM;

ANIMAL CELL; ARTICLE; CELL MEMBRANE CONDUCTANCE; CONTROLLED STUDY; DISSOCIATION CONSTANT; ION CURRENT; NONHUMAN; PRIORITY JOURNAL; RAT; SEPTUM NUCLEUS; VOLTAGE CLAMP;

EID: 0029908303     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.4.2221     Document Type: Article

References (66)

1. ALONSO, J. R. AND FROTSCHER, M. Hippocampo-septal fibers terminate on identified spiny neurons in the lateral septum: a combined Golgi/electron-microscopic and degeneration study in the rat. Cell Tissue Res. 258: 243-246, 1989.
2. ASHKENAZI, A., WINSLOW, J. W., PERALTA, E. G., PETERSON, G. L., SCHIMERLIK, M. I., CAPON, D. J., AND RAMACHANDRAN, J. An M2 muscarinic receptor subtype coupled to both adenylyl cyclase and phosphoinositide turnover. Science Wash. DC 238: 672-675, 1987.
3. BENSON, D. M., BLITZER, R. D., AND LANDAU, E. M. An analysis of the depolarization produced in guinea-pig hippocampus by cholinergic receptor stimulation. J. Physiol. Lond. 404: 479-496, 1988.
4. BIALOWAS, J. AND FROTSCHER, M. Choline acetyltransferase- immunoreactive neurons and terminals in the rat septal complex: a combined light and electron microscopic study. J. Comp. Neurol. 259: 298-307, 1987.
5. BIRDSALL, N. J. M., BURGEN, A. S. V., HULME, E. C., ZIGMOND, M. J., AND STOCKTON, J. M. The effect of McN-A-343 on muscarinic receptors in the cerebral cortex and heart. Br. J. Pharmacol. 78: 257-259, 1983.
6. BLANTON, M. G, LO TURCO, J. J., AND KRIEGSTEIN, A. R. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J. Neurosci. Methods 30: 203-210, 1989.
7. BONNER, T. I. New subtypes of muscarinic acetylcholine receptors. Trends Pharmacol. Sci. Suppl. 10: 11-15, 1989.
8. BONNER T. I., BUCKLEY, N. J., YOUNG, A. C., AND BRANN, M. R. Identification of a family of muscarinic acetylcholine receptor genes. Science Wash. DC 237: 527-532, 1987.
9. BONNER T. I., YOUNG, A. C., BRANN, M. R., AND BUCKLEY, N. J. Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Neuron 1: 403-410, 1988.
10. BRANN, M. R., BUCKLEY, N. J., AND BONNER, T. I. The striatum and cerebral cortex express different muscarinic receptor mRNAs. FEBS Lett. 230: 90-94, 1988.
11. BUCKLEY, N. J., BONNER, T. I., AND BRANN, M. R. Localization of a family of muscarinic receptor mRNAs in rat brain. J. Neurosci. 8: 4646-4652, 1988.
12. BUCKLEY, N. J., BONNER, T. I., BUCKLEY, C. M., AND BRANN, M. R. Antagonist binding properties of five cloned muscarinic receptors expressed in CHO-K1 cells. Mol. Pharmacol. 35: 469-476, 1989.
13. COLE, A. AND NICOLL, R. A. The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells. Brain Res. 305: 283-290, 1984.
14. COLEMAN, P. A. AND MILLER, R. F. Measurement of passive membrane parameters with whole-cell recording from neurons in the intact amphibian retina. J. Neurophysiol. 61: 218-230, 1989.
15. COLINO, A. AND HALLIWELL, J. V. Carbachol potentiates Q current and activates a calcium-dependent non-specific conductance in rat hippocampus in vitro. Eur. J. Neurosci. 5: 1198-1209, 1993.
16. CONSTANTI, A. AND SIM, J. A. Muscarinic receptors mediating suppression of the M-current in guinea-pig olfactory cortex neurones may be of the M2-subtype. Br. J. Pharmacol. 90: 3-5, 1987.
17. DEFRANCE, J. F., SHIMONO, T., AND KITAI, S. T. Anatomical distribution of the hippocampal fibers afferent to the lateral septal nucleus. Brain Res. 34: 176-180, 1971.
18. DÖRJE, F., WESS, J., LAMBRECHT, G., TACKE, R., MUTSCHLER, E., AND BRANN M. R. Antagonist binding profiles of five cloned human muscarinic receptor subtypes. J. Pharmacol. Exp. Ther. 256: 727-733, 1991.
19. 2 receptor binding. Relationship with functional efficacy. Eur. J. Pharmacol. 156: 133-142, 1988.
20. + currents of muscarinic acetylcholine receptor subtypes in NG108-15 cells. Nature Lond. 335: 355-358, 1988.
21. GILMAN, A. G. G proteins and dual control of adenylate cyclase. Cell 36: 577-579, 1984.
22. + current by metabotropic glutamate and muscarinic receptors in rat CA3 cells: mediation by G-proteins. J. Physiol. Lond. 474: 27-33, 1994.
23. HALLANGER, A. E. AND WAINER, B. H. Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine legmentum in the rat. J. Comp. Neurol. 274: 483-515, 1988.
24. HALLIWELL, J. V. AND ADAMS, P. R. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res. 250: 71-92, 1982.
25. HAMILL, O. P., MARTY, A., NEHER, E., SAKMANN, B., AND SIGWORTH, F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers Arch. 391: 85-100, 1981.
26. HAMMER, R., BERRIE, C. P., BIRDSALL, N. J. M., BURGEN, A. S. V., AND HULME, E. C. Pirenzepine distinguishes between different subclasses of muscarinic receptors. Nature Lond. 283: 90-92, 1980.
27. 4 receptor in rat dorsolateral septal nucleus neurons. Neurosci. Lett. 189: 163-166, 1995.
28. HASUO, H. AND GALLAGHER, J. P. Facilitatory action of muscarine on the slow afterdepolarization of rat dorsolateral septal nucleus neurons in vitro. Neurosci. Lett. 112: 234-238, 1990a.
29. HASUO, H. AND GALLAGHER, J. P. Actions of muscarine on dorsolateral septal neurons. In: Regulation of Potassium Transport Across Biological Membranes, edited by L. Reuss, J. M. Russell, and G. Szabo. Austin: University of Texas Press, 1990b, p. 459-476.
30. 1 muscarinic receptors. Brain Res. 438: 323-327, 1988.
31. HASUO, H., PHELAN, K. D., TWERY, M. J., AND GALLAGHER, J. P. A calcium-dependent slow afterdepolarization recorded in rat dorsolateral septal nucleus, neurons in vitro. J. Neurophysiol. 64: 1838-1846, 1990.
32. HILLE, B. Modifiers of gating. In: Ionic Channels of Excitable Membranes. Sunderland, MA: Sinaur Associates, 1992, p. 445-471.
33. HULME, E. C., BIRDSALL, N. J., AND BUCKLEY, N. J. Muscarinic receptor subtypes. Annu. Rev. Pharmacol. Toxicol. 30: 633-673, 1990.
34. 4 muscarinic receptor in guinea-pig chromaffin cells. Br. J. Pharmacol. 114: 419-427, 1995.
35. KELLY, J. S. AND ROGAWSKI, M. A. Acetylcholine. In: Neurotransmitter Actions in the Vertebrate Nervous System, edited by M. A. Rogawski and J. L. Barker. New York: Plenum Press, 1985, p. 143-197.
36. KUBO, T., FUKUDA, K., MIKAMI, A., MAEDA, A., TAKAHASHI, H., MISHINA, M., HAGA, T., HAGA, K., ICHIYAMA, A., KANGAWA, K., KOJIMA, M., MATSUO, H., HIROSE, T., AND NUMA, S. Cloning, sequencing and expression of complementary DNA encoding the muscarinic acetylcholine receptor. Nature Lond. 323: 411-416, 1986.
37. 1 muscarinic receptor is associated with the hydrolysis of phosphatidylinositols in transfected murine B82 cells. Life Sci. 42: 2489-2502, 1988.
38. LAI, J., WAITE, S. L., BLOOM, J. W. YAMAMURA, H. I., AND ROESKE, W. R. The M2 muscarinic acetylcholine receptors are coupled to multiple signaling pathways via pertussis toxin-sensitive guanine nucleotide regulatory proteins. J. Pharmacol. Exp. Ther. 258: 938-944, 1991.
39. LAMBRECHT, G., MOSER, U., GRIMM, U., PFAFF, O., HERMANNI, U., HILDEBRANDT, C., WAELBROECK, M., CHRISTOPHE, J., AND MUTSCHLER, E. New functionally selective muscarinic agonists. Life Sci. 52: 481-488, 1993.
40. LANCASTER, B. AND ADAMS, P. R. Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J. Neurophysiol. 55: 1268-1282, 1986.
41. 4 binding sites in rabbit lung, chicken heart, and NG108-15 cells. Mol. Pharmacol. 38: 805-815, 1990.
42. LAZARENO, S. AND ROBERTS, F. F. Functional and binding studies with muscarinic M2-subtype selective antagonists. Br. J. Pharmacol. 98: 309-317, 1989.
43. LEWIS, P. R. AND SHUTE, C. C. D. The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. Brain 90: 521-540, 1967.
44. MADISON, D. V., LANCASTER, B., AND NICOLL, R. A. Voltage clamp analysis of cholinergic action in the hippocampus. J. Neurosci. 7: 733-741, 1987.
45. MAEDA, A., KUBO, T., MISHINA, M., AND NUMA, S. Tissue distribution of mRNAs encoding muscarinic acetylcholine receptor subtypes. FEBS Lett. 239: 339-342, 1988.
46. MCCORMIC, D. A. AND PRINCE, D. A. Actions of acetylcholine in the guinea-pig and cat medial and lateral geniculate nuclei, in vitro. J. Physiol. Lond. 392: 147-165, 1987.
47. 1 muscarinic receptors expressed in murine fibroblast B82 cells. J. Pharmacol. Exp. Ther. 248: 661-670, 1988.
48. MICHELETTI, R., MONTAGNA, E., AND GIACHETTI, A. AF-DX 116, a cardioselective muscarinic antagonist. J. Pharmacol. Exp. Ther. 241: 628-634, 1987.
49. NISHIKAWA, M., MUNAKATA, M., AND AKAIKE, N. Muscarinic acetylcholine response in pyramidal neurones of rat cerebral cortex. Br. J. Pharmacol. 112: 1160-1166, 1994.
50. NEHER, E. Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol. 207: 123-131, 1992.
51. NORTH, R. A. Muscarinic cholinergic receptor regulation of ion channels. In: The Muscarinic Receptors, edited by J. H. Brown. Clifton, NJ: Humana, 1989, p. 341-373.
52. 2 muscarinic receptor in rat nucleus raphe magnus in vitro. J. Neurosci. 14: 1332-1338, 1994.
53. PARTRIDGE, L. D. AND SWANDULLA, D. Calcium-activated non-specific cation channels. Trends Neurosci. 11: 69-72, 1988.
54. PERALTA, E. G., ASHKENAZI, A., WINSLOW, J. W., RAMACHANDRAN, J., AND CAPON, D. J. Differential regulation of PI hydrolysis and adenylyl cyclase by muscarinic receptor subtypes. Nature Lond. 334: 434-437, 1988.
55. RUDY, B. Diversity and ubiquity of K channels. Neuroscience 25: 729-749, 1988.
56. SHEN, K.-Z. AND NORTH, R. A. Muscarine increases cation conductance and decreases potassium conductance in rat locus coeruleus neurones. J. Physiol. Lond. 455: 471-485, 1992.
57. SHUTE, C. C. D. AND LEWIS, P. R. The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. Brain 90: 497-520, 1967.
58. STEVENS, D. R., GALLAGHER, J. P., AND SHINNICK-GALLAGHER, P. Intracellular recordings from rat dorsolateral septal neurons, in vitro. Brain Res. 305: 353-356, 1984.
59. 3 neurons. Neurosci. Lett. 82: 41-46, 1987.
60. TWERY, M. J., WONG, L. A., AND GALLAGHER, J. P. Somatostatin induced hyperpolarization of septal neurons is not blocked by pertussis toxin. Eur. J. Pharmacol. 192: 287-291, 1991.
61. UCHIMURA, N. AND NORTH, R. A. Muscarine reduces inwardly rectifying potassium conductance in rat nucleus accumbens neurones. J. Physiol. Lond. 422: 369-380, 1990.
62. 2 receptor mRNA expression and receptor binding in cholinergic and non-cholinergic cells in the rat brain: a correlative study using in situ hybridization histochemistry and receptor autoradiography. Neuroscience 47: 367-393, 1992.
63. WAKAMORI, M., HIDAKA, H., AND AKAIKE, N. Hyperpolarizing muscarinic responses of freshly dissociated rat hippocampal CA1 neurones. J. Physiol. Lond. 463: 585-604, 1993.
64. WATSON, S. AND GIRDLESTONE, D. Trends in Pharmacological Sciences Receptor and Ion Channel Nomenclature Suppl. 7, 1996.
65. WESS, J., BONNER, T. I., AND BRANN, M. R. Chimeric m2/m3 muscarinic receptors: role of carboxyl terminal receptor domains in selectivity of ligand binding and coupling to phosphoinositide hydrolysis. Mol. Pharmacol. 38: 872-877, 1990.
66. WOMBLE, M. D. AND MOISES, H. C. Muscarinic inhibition of M-current and a potassium leak conductance in neurones of the rat basolateral amygdala. J. Physiol. Lond. 457: 93-114, 1992.