Pituitary adenylate cyclase-activating polypeptide activates a phospholipase C-dependent signal pathway in chick ciliary ganglion neurons that selectively inhibits α7-containing nicotinic receptors

Journal of Neuroscience

Volumn 19, Issue 15, 1999, Pages 6327-6337

  Pardi, Desiree ^a,b   Margiotta, Joseph F ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine; Ca2+ imaging; Fast perfusion; Ion channel; Modulation; Neuropeptide; Whole cell recording

Indexed keywords

ALPHA BUNGAROTOXIN; CALCIUM ION; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; INOSITOL PHOSPHATE; NICOTINIC RECEPTOR; PHOSPHOLIPASE C;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHICKEN; CILIARY GANGLION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0033179081     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-15-06327.1999     Document Type: Article

References (47)

1. Alkondon M, Albuquerque EX (1993) 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.
2. Amador M, Dani JA (1995) Mechanism for modulation of nicotinic acetylcholine receptors that can influence synaptic transmission. J Neurosci 15:4525-4532.
3. Barnhart DC, Sarosi GA, Mullholland MW (1997) PACAP-38 causes phospholipase C-dependent calcium signaling in rat acinar cell line. Surgery 122:465-475.
4. Basille M, Gonzalez BJ, Desrues L, Demas M, Fournier A, Vaudry H (1995) Pituitary adenylate cyclase-activating polypeptide (PACAP) stimulates adenylate cyclase and PLC activity in rat cerebellar neuroblasts. J Neurochem 65:1318-1324.
5. Berridge MJ (1993) Inositol triphosphate and calcium signaling. Nature 361:315-326.
6. Berridge MJ (1997) Elementary and global aspects of calcium signaling. J Physiol (Lond) 499:291-306.
7. Blumenthal EM, Shoop RD, Berg DK (1999) Developmental changes in the nicotinic responses of ciliary ganglion neurons. J Neurophysiol 81:111-120.
8. Conroy WG, Berg DK (1995) Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J Biol Chem 270:4424-4431.
9. Cornell-Bell A, Finkbeiner S, Cooper M, Smith S (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247:470-473.
10. Couturier S, Bertrand D, Matter J-M, Hernandez M-C, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-Btx. Neuron 5:847-496.
11. Cuevas J, Adams D (1996) VIP modulation of nAChR channels in rat intracardiac neurons. J Physiol (Lond) 493:503-515.
12. Deutsch PJ, Sun Y (1992) The 38-amino acid form of pituitary adenylate cyclase-activating polypeptide stimulates dual signaling cascades in PC12 cells and promotes neurite outgrowth. J Biol Chem 267:5108-5113.
13. Exton JH (1996) Regulation of phosphoinositide phospholipases by hormones, neurotransmitters, and other agonists linked to G-proteins. Annu Rev Pharmacol Toxicol 36:481-509.
14. Ghosh TK, Eis PS, Mullaney JM, Ebert CL, Gill DL (1988) Competitive, reversible and potent antagonism of inositol 1,4,5-triphosphate-activated calcium release by heparin. J Biol Chem 263:11075-11079.
15. Gurantz D, Harootunian AT, Tsien RY, Dionne VE, Margiotta JF (1994) VIP modulates neuronal nicotinic acetylcholine receptor function by a cyclic AMP-dependent mechanism. J Neurosci 14:3540-3547.
16. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
17. Hashimoto H, Ishihara T, Shigemoto R, Mori K, Nagata S (1993) Molecular cloning and tissue distribution of a receptor for pituitary adenylate cyclase-activating polypeptide. Neuron 11:333-342.
18. Hille B (1992) G protein-coupled mechanisms and nervous signaling. Neuron 9:187-195.
19. Jonas P (1995) Fast application of agonists to isolated membrane patches. In: Single channel recording (Sakmann B, Necher E, eds). New York: Plenum.
20. Kano M, Garaschuk O, Verkhratsky A, Konnerth A (1995) Ryanodine receptor-mediated intracellular calcium release in rat cerebellar Purkinje neurons. J Physiol (Lond) 487.1:1-16.
21. Kao JPY, Harootunian AT, Tsien RY (1989) Photochemically generated cytosolic calcium pulses and their detection by Fluo-3. J Biochem 264:8179-8184.
22. Kennedy M (1989) Regulation of neuronal function by calcium. Trends Neurosci 112:417-420.
23. Khiroug L, Sokolova E, Giniatullin R, Afzalov R, Nistri A (1998) Recovery from desensitization of neuronal nicotinic acetylcholine receptors of rat chromaffin cells is modulated by intracellular calcium through distinct second messengers. J Neurosci 18:2458-2466.
24. Kurosawa M (1994) Phosphorylation and dephosphorylation of proteins in regulating cellular function. J Pharmacol Toxicol Methods 31:135-139.
25. Levitan IB (1994) Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu Rev Physiol 56:193-212.
26. Margiotta JF, Gurantz D (1989) Changes in the number, function and regulation of nicotinic acetylcholine receptors during neuronal development. Dev Biol 135:326-399.
27. Margiotta JF, Pardi D (1995) Pituitary adenylate cyclase-activating polypeptide type I receptors mediate cyclic AMP-dependent enhancement of neuronal acetylcholine sensitivity. Mol Pharmacol 48:63-71.
28. Margiotta JF, Berg DK, Dionne VE (1987) Cyclic AMP regulates the proportion of functional acetylcholine receptors on chick ciliary ganglion neurons. Proc Natl Acad Sci USA 84:8155-8159.
29. Mayer RJ, Marshall LA (1993) New insights on mammalian phospholipase A2: comparison of arachidonoyl-selective and nonselective enzymes. FASEB J 7:339-348.
30. Moss SJ, McDonald BJ, Rudhard Y, Schoepfer R (1996) Phosphorylation of the predicted major intracellular domains of the rat and chick nicotinic a7 subunit by cAMP-dependent protein kinase. Neuropharmacology 35:1023-1028.
31. Motulsky H (1995) Intuitive Biostatistics. New York: Oxford.
32. Pardi D, Margiotta JF (1996) PACAP receptor activation inhibits α7-containing neuronal acetylcholine receptors. Soc Neurosci Abstr 22:1522.
33. Pisegna JR, Wank SA (1993) Molecular cloning and functional expression of the pituitary adenylate cyclase-activating polypeptide type I receptor. Proc Natl Acad Sci USA 90:6345-6349.
34. Rathouz MM, Vijayaraghavan S, Berg DK (1995) Acetylcholine differentially affects intracellular calcium via nicotinic and muscarinic receptors on the same population of neurons. J Biol Chem 270:14366-14375.
35. Rawlings SR (1994) At the cutting edge: PACAP, PACAP receptors and intracellular signaling. Mol Cell Endocrinol 101:C5-C9.
36. 2+]i in rat gonadotrophs through an inositol triphosphate-dependent mechanism. J Biol Chem 269:5680-5686.
37. Ross EM (1989) Signal sorting and amplification through G-protein coupled receptors. Neuron 3:141-152.
38. Selyanko AA, Brown DA (1996) Intracellular calcium directly inhibits potassium M channels in excised membrane patches from rat sympathetic neurons. Neuron 16:151-162.
39. Spengler D, Waeber C, Pantaloni C, Holsboer F, Bockaert J, Seeburg P, Journot L (1993) Differential signal transduction by five splice variants of the PACAP receptor. Nature 365:170-175.
40. Stella N, Magistretti PJ (1996) Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activating polypeptide (PACAP) potentiate the glutamate-evoked release of arachidonic acid from mouse cortical neurons. J Biol Chem 271:23705-23710.
41. Swope SL, Moss SJ, Blackstone CD, Huganir RL (1993) Phosphorylation of ligand-gated ion channels: a possible mode of synaptic plasticity. FASEB J 6:2514-2523.
42. Vernallis AB, Conroy WG, Berg DK (1993) Neurons assemble AChRs with as many as 3 kinds of subunits while maintaining subunit segregation among subtypes. Neuron 10:451-464.
43. Vijayaraghavan D, Schmid HA, Halvorsen SW, Berg DK (1990) Cyclic AMP-dependent phosphorylation of a neuronal acetylcholine receptor α-type subunit. J Neurosci 10:3255-3262.
44. 2+. Neuron 8:353-362.
45. Vijayaraghavan S, Huang B, Blumenthal EM, Berg DK (1995) Arachidonic acid as a possible negative feedback inhibitor of nicotinic acetylcholine receptors on neurons. J Neurosci 15:3679-3687.
46. Yakel JL (1997) Calcineurin regulation of synaptic function: from ion channels to transmitter release and gene expression. Trends Pharmacol Sci 18:124-134.
47. Zhang Z-W, Vijayaraghavan S, Berg DK (1994) Neuronal acetylcholine receptors that bind a-bungarotoxin with high affinity function as ligand-gated ion channels. Neuron 12:167-177.