Phosphorylation of proteins in chick ciliary ganglion under conditions that induce long-lasting changes in synaptic transmission: Phosphoprotein targets for nitric oxide action

Neuroscience

Volumn 90, Issue 2, 1999, Pages 607-619

  Lengyel, I ^a   Olesen, L E ^a   Nichol, K A ^b   Brain, K L ^b   Wang, X ^c   Robinson, P J ^c   Bennett, M R ^b   Rostas, J A P ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Ciliary ganglion; Long term potentiation; Nitric oxide; PKA; PKG; Protein phosphorylation

Indexed keywords

NITRIC OXIDE;

ANIMAL TISSUE; ARTICLE; CHICKEN; CILIARY GANGLION; ENZYME ACTIVATION; INFORMATION PROCESSING; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM; CHICKENS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC GMP-DEPENDENT PROTEIN KINASES; GANGLIA, PARASYMPATHETIC; LONG-TERM POTENTIATION; NERVE TISSUE PROTEINS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROPRUSSIDE; PEPTIDE MAPPING; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; SUBSTRATE SPECIFICITY; SYNAPTIC TRANSMISSION;

EID: 0032928625     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00452-7     Document Type: Article

References (60)

1. Abeliovich A., Chen C., Goda Y., Silva A.J., Stevens C.F., Tonegawa S. Modified hippocampal long-term potentiation in PKC gamma-mutant mice. Cell. 75:1993;1253-1262.
2. Ariano M.A. Distribution of components of the guanosine 3′,5′-phosphate system in rat caudate-putamen. Neuroscience. 10:1983;707-723.
3. Bliss T.V. P., Collingridge G.L. A synaptic model of memory: long-term potentiation in hippocampus. Nature. 359:1993;417-420.
4. Brain K.L., Bennett M.R. Calcium in the nerve terminals of chick ciliary ganglia during facilitation, augmentation and potentiation. J. Physiol. 489:1995;637-648.
5. Brain K.L., Bennett M.R. Calcium in sympathetic varicosities of mouse vas deferens during facilitation, augmentation and autoinhibition. J. Physiol., Lond. 502:1997;521-536.
6. Carrier G.O., Fuchs L.C., Winecoff A.P., Giulumian A.D., White R.E. Nitrovasodilators relax mesenteric microvessels by cGMP-induced stimulation of Ca-activated K channels. Am. J. Physiol. 273:1997;H76-H84.
7. Cetiner M., Bennett M.R. Nitric oxide modulation of calcium-activated potassium channels in postganglionic neurones of avian cultured ciliary ganglia. Br. J. Pharmac. 110:1993;995-1002.
8. Cummings J.A., Nicola S.M., Malenka R.C. Induction in the rat hippocampus of long-term potentiation (LTP) and long-term depression (LTD) in the presence of a nitric oxide synthase inhibitor. Neurosci. Lett. 176:1994;110-114.
9. Delaney K.R., Zucker R.S., Tank D.W. Calcium in motor nerve terminals associated with posttetanic potentiation. J. Neurosci. 9:1989;3558-3567.
10. Eberhard M., Erne P. Calcium binding to fluorescent calcium indicators: calcium green, calcium orange and calcium crimson. Biochem. biophys. Res. Commun. 180:1991;209-215.
11. Finn J.T., Grunwald M.E., Yau K.W. Cyclic nucleotide-gated ion channels: an extended family with diverse functions. A. Rev. Physiol. 58:1996;395-426.
12. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:1991;60-67.
13. Garthwaite J., Boulton C.L. Nitric oxide signaling in the central nervous system. A. Rev. Physiol. 57:1995;683-706.
14. Gatti A., Wang X., Robinson P.J. Protein kinase C-alpha is multiply phosphorylated in response to phorbol ester stimulation of PC12 cells. Biochim. biophys. Acta. 1313:1996;111-118.
15. Hampl V., Huang J.M., Weir E.K., Archer S.L. Activation of the cGMP-dependent protein kinase mimics the stimulatory effect of nitric oxide and cGMP on calcium-gated potassium channels. Physiol. Res. 44:1995;39-44.
16. Harris R.A., McQuilkin S.J., Paylor R., Abeliovich A.X., Tonegawa S., Wehner J.M. Mutant mice lacking the gamma isoform of protein kinase C show decreased behavioral actions of ethanol and altered function of gamma-aminobutyrate type A receptors. Proc. natn. Acad. Sci. U.S.A. 92:1995;3658-3662.
17. Hawkins R.D., Zhuo M., Arancio O. Nitric oxide and carbon monoxide as possible retrograde messengers in hippocampal long-term potentiation. J. Neurobiol. 25:1994;652-665.
18. Hess A. Developmental changes in the structure of the synapse on the myelinated cell bodies of the chicken ciliary ganglion. J. Cell Biol. 25:1965;1-19.
19. Homayoun P., Lust W.D., Harik S.I. Effect of several vasoactive agents on guanylate cyclase activity in isolated rat brain microvessels. Neurosci. Lett. 107:1991;273-278.
20. Huang Y.Y., Kandel E.R., Varshavsky L., Brandon E.P., Qi M., Idzerda R.L., McKnight G.S., Bourtchouladze R. A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell. 83:1995;1211-1222.
21. Jiang H., Shabb J.B., Corbin J.D. Cross-activation: overriding cAMP/cGMP selectivities of protein kinases in tissues. Biochem. Cell Biol. 70:1992;1283-1289.
22. Kantor D.B., Lanzrein M., Stary S.J., Sandoval G.M., Smith W.B., Sullivan B.M., Davidson N., Schuman E.M. A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science. 274:1996;1744-1748.
23. Khurana G., Bennett M.R. Nitric oxide and arachidonic acid modulation of calcium currents in postganglionic neurones of avian cultured ciliary ganglia. Br. J. Pharmac. 109:1993;480-485.
24. Klann E., Chen S.J., Sweatt J.D. Mechanism of protein kinase C activation during the induction and maintenance of long-term potentiation probed using a selective peptide substrate. Proc. natn. Acad. Sci. U.S.A. 90:1993;8337-8341.
25. A receptors. Molec. Brain Res. 42:1996;131-134.
26. 2+/calmodulin-dependent protein kinase II are localised in different neurons in chick ciliary ganglion. NeuroReport (in press).
27. Lengyel I., Nichol K.A., Sim A.T., Bennett M.R., Dunkley P.R., Rostas J.A. P. Characterization of protein kinase and phosphatase systems in chick ciliary ganglion. Neuroscience. 70:1996;577-588.
28. Lin Y.Q., Bennett M.R. Nitric oxide modulation of quantal secretion in chick ciliary ganglia. J. Physiol. 481:1994;385-394.
29. Luo Y., Vallano M.L. Arachidonic acid, but not sodium nitroprusside, stimulates presynaptic protein kinase C and phosphorylation of GAP-43 in rat hippocampal slices and synaptosomes. J. Neurochem. 64:1995;1808-1818.
30. Malenka R.C., Kauer J.A., Perkel D.J., Mauk M.D., Kelly P.T., Nicoll R.A., Waxham M.N. An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature. 340:1989;554-557.
31. Malinow R., Schulman H., Tsien R.W. Inhibition of postsynaptic PKC or CAMK-II blocks induction but not expression of LTP. Science. 245:1989;862-866.
32. Marley P.D., Thomson K.A. Inhibition of nicotinic responses of bovine adrenal chromaffin cells by the protein kinase C inhibitor, Ro 31-8220. Br. J. Pharmac. 119:1996;416-422.
33. Martin A.R., Pilar G. Dual mode of synaptic transmission in the avian ciliary ganglion. J. Physiol. 168:1963;443-463.
34. Marwitt R., Pilar G., Weakley J.N. Characteristics of two ganglion cell populations in avian ciliary ganglia. Brain Res. 25:1971;317-334.
35. Maurice D.H., Haslam R.J. Molecular basis of the synergistic inhibition of platelet function by nitrovasodilators and activators of adenylate cyclase: inhibition of cyclic AMP breakdown by cyclic GMP. Molec. Pharmac. 37:1990;671-681.
36. Meffert M.K., Premack B.A., Schulman H. Nitric oxide stimulates Ca(2+)-independent synaptic vesicle release. Neuron. 12:1994;1235-1244.
37. Moncada S., Palmer R.J., Higgs E.A. Biosynthesis of nitric oxide from L-arginine: a pathway for the regulation of cell function and communication. Biochem. Pharmac. 38:1989;1709-1715.
38. Nguyen P.V., Kandel E.R. A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J. Neurosci. 16:1996;3189-3198.
39. Nichol K.A., Chan N., Davey D.F., Bennett M.R. Location of nitric oxide synthase in the developing avian ciliary ganglion. J. auton. nerv. Syst. 51:1995;91-102.
40. O'Dell T.J., Huang P.L., Dawson T.M., Dinerman J.L., Snyder S.H., Kandel E.R., Fishman R.C. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science. 265:1994;542-546.
41. Ramakers G.M., Pasinelli P., Hens J.J., Gispen W.H., De Graan P.N. E. Protein kinase C in synaptic plasticity: changes in the in situ phosphorylation state of identified pre- and postsynaptic substrates. Prog. Neuropsychopharmac. biol. Psychiat. 21:1997;455-486.
42. A receptor function in the rat cerebral cortex and cerebellar granule cells. Neuroscience. 74:1996;99-105.
43. Robinson P.J., Dunkley P.R. Depolarisation-dependent protein phosphorylation in rat cortical synaptosomes: factors determining the magnitude of the response. J. Neurochem. 41:1983;909-918.
44. Robinson P.J., Dunkley P.R. Depolarisation-dependent protein phosphorylation and dephosphorylation in rat cortical synaptosomes is modulated by calcium. J. Neurochem. 44:1985;338-348.
45. Robinson P.J., Sontag J.M., Liu J.P., Fykse E.M., Slaughter C.X., McMahon H., Sudhof T.C. Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature. 365:1993;163-166.
46. Salter M., Strijbos P.J., Neale S., Duffy C., Follenfant R.L., Garthwaite J. The nitric oxide-cyclic GMP pathway is required for nociceptive signalling at specific loci within the somatosensory pathway. Neuroscience. 73:1996;649-655.
47. Scott T.R., Bennett M.R. The effect of ions and second messengers on long-term potentiation of chemical transmission in avian ciliary ganglia. Br. J. Pharmac. 110:1993;461-469.
48. Scott T.R., Bennett M.R. The effect of nitric oxide on the efficacy of synaptic transmission through the chick ciliary ganglion. Br. J. Pharmac. 110:1993;627-632.
49. Sessoms J.S., Chen S.J., Chetkovich D.M., Powell C.M., Roberson E.D., Sweatt J.D., Klann E. Ca(2+)-induced persistent protein kinase C activation in rat hippocampal homogenates. Sec. Mess. Phosphoprot. 14:1992;109-126.
50. Silva A.J., Stevens C.F., Tonegawa S.T., Wang Y. Deficient hippocampal long-term potentiation in α-calmodulin kinase II mutant mice. Science. 257:1992;201-206.
51. 2+ channels. J. Neurosci. Res. 45:1996;216-225.
52. Stanley E.F. Single calcium channels in the cholinergic presynaptic nerve terminal. Neuron. 7:1992;585-591.
53. Stralfors P., Hemmings H.C., Greengard P. Inhibitors of protein phosphatase-1: inhibitor-1 of bovine adipose tissue and dopamine- and cAMP-regulated phosphoprotein of bovine brain are identical. Eur. J. Biochem. 180:1989;143-148.
54. Swandulla D., Hans M., Zipser K., Augustine G.J. Role of residual calcium in synaptic depression and posttetanic potentiation: fast and slow calcium signalling in nerve terminals. Neuron. 7:1991;915-926.
55. Tsou K., Snyder G.L., Greengard P. Nitric oxide/cGMP pathway stimulates phosphorylation of DARPP-32, a dopamine- and cAMP-regulated phosphoprotein, in the substantia nigra. Proc. natn. Acad. Sci. U.S.A. 90:1993;3462-3465.
56. Vaandrager A.B., de Jonge H.R. Signalling by cGMP-dependent protein kinases. Molec. cell. Biochem. 157:1996;23-30.
57. Wang X., Robinson P.J. Cyclic GMP-dependent protein kinase substrates in rat brain. J. Neurochem. 65:1995;595-604.
58. Wang X., Robinson P.J. Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J. Neurochem. 68:1997;443-456.
59. A receptor function via coactivation of cGMP-dependent kinase and phosphodiesterase. J. Neurosci. 18:1998;2342-2349.
60. Wooten M.W., Seibenhener M.L., Matthews L.H., Zhou G., Coleman E.S. Modulation of zeta-protein kinase C by cyclic AMP in PC12 cells occurs through phosphorylation by protein kinase A. J. Neurochem. 67:1996;1023-1031.