A nitric oxide/cyclic GMP-dependent protein kinase pathway alters transmitter release and inhibition by somatostatin at a site downstream of calcium entry

Journal of Neurochemistry

Volumn 72, Issue 5, 1999, Pages 1981-1990

  Gray, D Bruce ^a   Polo Parada, Luis ^b   Pilar, Guillermo R ^b   Eang, Peau ^a   Metzger, Ryan R ^c,d   Klann, Eric ^c   Meriney, Stephen D ^c  

^a SIMMONS COLLEGE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

Acetylcholine; Calcium; Cyclic GMP dependent protein kinase; Nitric oxide

Indexed keywords

CALCIUM ION; CATECHOLAMINE; CYCLIC GMP DEPENDENT PROTEIN KINASE; NEUROTRANSMITTER; NITRIC OXIDE SYNTHASE; POTASSIUM ION; SOMATOSTATIN;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME BINDING; INHIBITION KINETICS; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ACETYLCHOLINE; ANIMALS; CALCIUM; CHICK EMBRYO; CHOROID; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; HORMONE ANTAGONISTS; INTRACELLULAR MEMBRANES; NERVE ENDINGS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROPRUSSIDE; SOMATOSTATIN;

ANIMALIA;

EID: 0033010061     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0721981.x     Document Type: Article

References (55)

1. Augustine G. J. and Charlton M. P. (1986) Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J. Physiol. (Lond.) 381, 619-640.
2. Borst J. G. G. and Sakmann B. (1996) Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431-434.
3. Bourne H. R. and Nicoll R. (1993) Molecular machines integrate coincident synaptic signals. Cell 72, 65-75.
4. 2+ homeostasis. J. Neurochem. 66, 403-411.
5. 2+ channel kinetics by receptor agonists in IMR32 cells. Biophys. J. 70, 2144-2154.
6. Chetkovich D. M., Klann E., and Sweatt J. D. (1993) Nitric oxide synthase-independent long-term potentiation in area CA 1 of hippocampus. Neuroreport 4, 919-922.
7. Crean G., Pilar G., Tuttle J. B., and Vaca K. (1982) Enhanced chemosensitivity of chick parasympathetic neurones in co-culture with myotubes. J. Physiol. (Lond). 331, 97-104.
8. Dale N. and Kandel E. R. (1990) Facilitatory and inhibitory transmitters modulate spontaneous transmitter release at cultured Aplysia sensorimotor synapses. J. Physiol. (Lond.) 421, 203-229.
9. De Stefano M. E., Luzzato A., and Mugnaini E. (1993) Neuronal ultrastructure and somatostatin immunolocalization in the ciliary ganglion of chicken and quail. J. Neurocytol. 22, 868-892.
10. Dodge F. A. and Ranamimoff R. (1967) Co-operative action of calcium ions in transmitter release at the neuromuscular junction, J. Physiol. (Lond.) 193, 419-432.
11. Dolphin A. C. (1998) Mechanisms of modulation of voltage-dependent calcium channels by G proteins. J. Physiol. (Lond.) 506, 3-11.
12. 2+ currents in acutely dissociated neurons of the chick ciliary ganglion: inhibition by somatostatin-14 and somatostatin-28. Neuroscience 44, 663-672.
13. Epstein M. L., Davis J. P., Gellman L. E., Lamb J. R., and Dahl J. L. (1988) Cholinergic neurons of the chicken ciliary ganglion contain somatostatin. Neuroscience 25, 1053-1060.
14. i oscillations in bullfrog sympathetic neurons. Neuron 8, 1109-1125.
15. Garthwaite J. and Boulton C. L. (1995) Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 57, 683-706.
16. Golard A. and Siegelbaum S. A. (1993) Kinetic basis for the voltage-dependent inhibition of N-type calcium current by somatostatin and norepinephrine in chick sympathetic neurons. J. Neurosci. 13, 3884-3894.
17. Gray D. B. and Tuttle J. B. (1987) ACh synthesis in cultured ciliary ganglion neurons: effects of myotube membranes. Dev. Biol. 119, 290-298.
18. Gray D. B., Pilar G. R., and Ford M. J. (1989) Opiate and peptide inhibition of transmitter release in parasympathetic nerve terminals. J. Neurosci. 9, 1683-1692.
19. Gray D. B., Zelazny D., Manthay N., and Pilar G. (1990) Endogenous modulation of ACh release by somatostatin and the differential roles of calcium channels. J. Neurosci. 10, 2687-2698.
20. 2+ channels coupled to acetylcholine release. Neuron 8, 715-724.
21. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
22. Hamburger V. and Hamilton H. L. (1951) A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
23. Hille B. (1992) G protein-coupled mechanisms and nervous signaling. Neuron 9, 187-195.
24. Hille B. (1994) Modulation of ion channels by G-protein coupled receptors. Trends Neurosci. 17, 531-535.
25. Hokfelt T. (1991) Neuropeptides in perspective: the last ten years. Neuron 7, 867-879.
26. Ikeda S. R. and Schofield G. G. (1989) Somatostatin blocks a calcium current in rat sympathetic ganglion neurons. J. Physiol. (Lond.) 409, 221-240.
27. Johnson D. A. and Pilar G. (1980) The release of acetylcholine from postganglionic cell bodies in response to depolarization. J. Physiol. (Lond.) 299, 605-619.
28. Kilbinger H. (1996) Modulation of acetylcholine release by nitric oxide. Prog. Brain Res. 109, 219-224.
29. Man-Son-Hing H., Zoran M. J., Lukowiak K., and Haydon P. G. (1989) A neuromodulator of synaptic transmission acts on the secretory apparatus as well as on ion channels. Nature 341, 237-239.
30. Meng W., Ma J., Ayata C., Hara H., Huang P. L., Fishman M. C., and Moskowitz M. A. (1996) ACh dilates pial arterioles in endothelial and neuronal NOS knockout mice by NO-dependent mechanisms. Am. J. Physiol. 271, H1145-H1150.
31. 2+ current modulated by cGMP-dependent protein kinase. Nature 369, 336-339.
32. Meulemans A., Mothet J. P., Schirar A., Fossier P., Tauc L., and Baux G. (1995) A nitric oxide synthase activity is involved in the modulation of acetylcholine release in Aplysia ganglion neurons: a histological, voltammetric and electrophysiological study. Neuroscience 69, 985-995.
33. Momiyama A. and Takahashi T. (1994) Calcium channels responsible for potassium-induced transmitter release at rat cerebellar synapses. J. Physiol. (Lond.) 476, 197-202.
34. Nestler E. J. and Greengard P. (1984) Neuron-specific phosphoproteins in mammalian brain. Adv. Cyclic Nucleotide Protein Phosphorylation Res. 17, 483-488.
35. Nichol K. A., Chan N., Davey D. F., and Bennett M. R. (1995) Location of nitric oxide synthase in developing avian ciliary ganglion. J. Auton. Nerv. Syst. 51, 91-102.
36. Patil P. G., de Leon M., Reed R. R., Dubel S., Snutch T. P., and Yue D. T. (1996) Elementary events underlying voltage-dependent G protein inhibition of N-type calcium channels. Biophys. J. 71, 2509-2521.
37. Pilar G., Gray D. B., and Meriney S. D. (1996) Membrane delimited and intracellular soluble pathways in the somatostatin modulation of ACh release. Life Sci. 58, 1979-1996.
38. 3H]noradrenaline release in chick sympathetic neurons. J. Physiol (Lond.) 437, 201-220.
39. 2+ channel/ syntaxin interaction. J. Neurosci. 17, 6647-6656.
40. Sah D. W. (1990) Neurotransmitter modulation of calcium current in rat spinal cord neurons. J. Neurosci. 10, 136-141.
41. + current in identified Aplysia neurons. J. Neurosci. Res. 44, 21-26.
42. Stanley E. F. and Goping G. (1991) Characterization of a calcium current in a vertebrate cholinergic presynaptic nerve terminal. J. Neurosci. 11, 985-993.
43. Surprenant A., Shen K. Z., North R. A., and Tatsumi H. (1990) Inhibition of calcium currents by noradrenaline, somatostatin and opioids in guinea-pig submucosal neurones. J. Physiol. (Lond.) 431, 585-608.
44. Suzuki T., Nakajima K., Fujimoto K., Fujii T., and Kawashima K. (1997) Nitric oxide increases stimulation-evoked acetylcholine release from rat hippocampal slices by a cyclic GMP-independent mechanism. Brain Res. 760, 158-162.
45. Takahashi T., Forsythe I. A., Tsujimoto T., Barnes-Davis M., and Onodera K. (1996) Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274, 594-597.
46. Trudeau L.-E., Emery D. G., and Haydon P. G. (1996) Direct modulation of the secretory machinery underlies PKA-dependent synpatic facilitation in hippocampal neurons. Neuron 17, 789-797.
47. Trudeau L.-E., Fang Y., and Haydon P. G. (1998) Modulation of an early step in the secretory machinery in hippocampal nerve terminals. Proc. Natl. Acad. Sci. USA 95, 7163-7168.
48. Vaca K. and Pilar G. (1979) Mechanisms controlling choline transport and acetylcholine synthesis in motor nerve terminals during electrical stimulation. J. Gen. Physiol. 73, 605-628.
49. Viana F. and Hille B. (1996) Modulation of high voltage-activated calcium channels by somatostatin in acutely isolated rat amygdaloid neurons. J. Neurosci. 16, 6000-6011.
50. Wang H. L., Reisine T., and Dichter M. (1990) Somatostatin-14 and somatostatin-28 inhibit calcium currents in rat neocortical neurons. Neuroscience 38, 335-342.
51. White M. G., Crumling M. A., and Meriney S. D. (1997) Developmental changes in calcium current pharmacology and somatostatin inhibition in chick parasympathetic neurons. J. Neurosci. 17, 6302-6313.
52. Wu L. G. and Saggau P. (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci. 20, 204-212.
53. Wu S. Y., Dun S. L., Forstermann U., and Dun N. J. (1997) Nitric oxide and excitatory postsynaptic currents in immature rat sympathetic preganglionic neurons in vitro. Neuroscience 79, 237-245.
54. Yazejian B., DiGregorio D. A., Vergara J. L., Poage R. E., Meriney S. D., and Grinnell A. D. (1997) Direct measurements of presynaptic calcium and calcium-activated potassium currents regulating neurotransmitter release at cultured Xenopus nerve - muscle synapses. J. Neurosci. 17, 2990-3001.
55. Yokoyama C. T., Sheng Z. H., and Catterall W. A. (1997) Phosphorylation of the synaptic protein interaction site on N-type calcium channels inhibits interactions with SNARE proteins. J. Neurosci. 17, 6929-6938.