Evidence for involvement of the cGMP-protein kinase G signaling system in the induction of long-term depression, but not long-term potentiation, in the dentate gyrus in vitro

Journal of Neuroscience

Volumn 18, Issue 10, 1998, Pages 3589-3596

  Wu, Jianqun ^a   Wang, Yue ^a   Rowan, Michael J ^a   Anwyl, Roger ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

cGMP; EPSP; Hippocampus; Long term depression; Long term potentiation; Protein kinase G

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP PHOSPHODIESTERASE; GUANYLATE CYCLASE; GUANYLATE CYCLASE INHIBITOR; KT 5823; METABOTROPIC RECEPTOR; ZAPRINAST;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

EID: 0032525267     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-10-03589.1998     Document Type: Article

References (46)

1. Arancio O, Kandel ER, Hawkins RD (1995) Activity-dependent longterm enhancement of transmitter release by presynaptic 3′, 5′-cyclic GMP in cultured hippocampal neurons. Nature 376:74-80.
2. Arancio O, Kiebler M, Lee J, Lev-Ram V, Tsien RY, Kandel ER, Hawkins RD (1996) Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87:1025-1035.
3. Beavo JA, Reifsnyder DH (1990) Primary sequence of cyclic nucleotide phosphodiesterase isozymes and the design of selective inhibitors. Trends Pharmacol Sci 11:150-155.
4. Bohme GA. Bon C, Stutzmunn JM, Doble A, Blanchurd JC (1991) Possible involvement of nitric oxide in long-term potentiation. Eur J Pharmacol 199:379-381.
5. Bon C, Bohme A, Dohle A, Blanchard JC (1992) A role for nitric oxide in long-term potentiation. J Neurosci 4:420-424.
6. Boxall AR, Garthsvaite J (1996) Long-term depression in rat cerebellum requires both NO synthase and NO-sensitive guanylyl cyclase. Eur J Neurosci 8:2209-2212.
7. Boulton CL, Irving AJ, Southam E, Potier B, Garthwaite J, Collingridge GL (1994) The nitric oxide-cyclic GMP pathway and synaptie depression in rat hippocampal slices. Eur J Neurosci 6:1528-1535.
8. Boulton CL, Southam B, Garthwaite J (1995) Nitric oxide-dependent long-term potentiation is blocked by a specific inhibitor of soluble guanylyl cyclase. Neuroscience 69:699-703.
9. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia H, Peters MF, Froehner SC, Bredt DS (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α-syntrophin mediated by PDZ domains. Cell 84:757-767.
10. Chctkovitch DM, Klann E, Sweatt JD (1993) Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. NeuroReport 4:919-922.
11. Conquet F, Bashir ZA, Davies CH, Daniel H, Feraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F, Collingridge GL, Crepel F (1994) Motor deficit and impairment of synaptic plasticity in mice lacing mGluRI. Nature 372:237-243.
12. Cummings JA, Nicola SM, Mulenka RC (1994) Induction in the rat hippocampus of long-term potentiation and long-term depression in the presence of a nitric oxide synthase inhibitor. Neurosci Lett 176:110-114.
13. Dinnerman JL, Dawson TD, Scell MJ, Snowman A, Snyder SH (1994) Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implication for synaptic plasticity. Proc Natl Acad Sci USA 91:4214-4218.
14. Doyle CA, Slater P (1997) Localization of neuronal and endothelial nitric oxide synthase isoforms in human hippocampus. Neuroscience 76:387-395.
15. Doyle C, Holscher C, Rowan MJ, Anwyl R (1996) The selective neuronal NO synthase inhibitor 7-nitro-indazole blocks both long-term potentiation and depotentiation officiel EPSPs in rat hippocampal CA1 in vivo. J Neurosci 16:418-424.
16. Eliusson MJL, Blackshaw S, Schell MJ, Snyder SH (1997) Neuronal nitric oxide synthase alternatively spliced forms: prominent functional localization in the brain. Proc Natl Acad Sci USA 94:3396-3401.
17. Gage AT, Reyes M, Stanton PK (1997) Nitric oxide-guanylyl cyclase-dependent and independent components of multiple forms of long-term synaptie depression. Hippocampus 7:286-295.
18. Garthwaite J, Boulton CL (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683-706.
19. Garthwaite J, Sotham E, Boulton CL, Neilson EB, Schmidt K, Mayer B (1995) Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by (1H-[1,2,4] oxadiazolo[4,3,-a]quinoxalin-1-one). Mol Pharmacol 48:184-188.
20. Haley JE, Wilcox GL, Chapman PF (1992) The role of nitric oxide in hippocampal long-term potentiation. Neuron 8:211-216.
21. Haley JE, Malen P, Chapman PF (1993) Nitric oxide synthase inhibitors block long-term potentiation induced by weak but not strong tetanic stimulation at physiological brain temperatures in rat hippocampal slices. Neurosci Lett 160:85-88.
22. Hara H, Waeber PL, Huang PL, Fuji M, Fishman MC, Moskowitz MA (1996) Brain distribution of nitric oxide synthase in neuronal or endothelial nitric oxide synthase mutant mice using [H]L-N-nitro-arginine autoradiography. Neuroscience 75:881-890.
23. Hartell NA (1994) Induction of cerebellar long-term depression requires activation of glutamate metabotropic receptors. NeuroReport 5:913-916.
24. Hartell NA (1996) Inhibition of cGMP breakdown promotes the induction of cerebellar long-term depression. J Neurosci 16:2881-2890.
25. Huang LQ, Rowan MJ, Anwyl R (1997) mGluRII agonist inhibition of LTP induction, and mGluRII antagonist inhibition of LTD induction, in the dentate gyrus in vitro. NeuroReport 8:687-693.
26. Ito M, Karochet L (1990) Receptor subtypes involved in, and time course of, the long-term depression of glutamate receptors in cerebellar Purkinje cells. Neurosci Res 14:27-38.
27. Izumi Y, Zorumski CFX (1995) Nitric oxide and long-term synaptic depression in the rat hippocampus. NeuroReport 4:1131-1134.
28. Kantor DB, Lanzrein M, Stary SJ, Sandoval GM, Smith WB, Sullivan BM, Davidson N, Schuman EM (1996) A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science 274:1744-1748.
29. Kase H (1988) New inhibitors of protein kinases from microbial source. In: Biology of actinomycetes. Proceedings of Seventh International Symposium on Biology of Actinomycetes (Okami Y, Beppu T, Ogawara H, eds), pp 159-164. Tokyo: Japan Scientific Societies.
30. Lev-Ram V, Makings LR, Keitz PF, Kao JP, Tsien RY (1995) Long-term depression in cerebellar Purkinje neurons results from coincidence of nitric oxide and depolarization-induced Ca transients. Neuron 15:408-414.
31. Lev-Ram V, Jiang T, Wood J, Lawrence DS, Tsien RY (1997) Synergies and coincidence requirements between NO, cGMP and Ca in the induction of cerebellar long-term depression. Neuron 18:1025-1038.
32. Malen PL, Chapman PF (1997) Nitric oxide facilitates long-term potentiation, but not long-term depression. J Neurosci 17:2645-2651.
33. Nakanishi S (1989) K-252-derivatives K252a, K252b, KT5720, KT5962, KT5823. Seitaino-Kagaku 40:364-365.
34. O'Connor JJ, Rowan MJ, Anwyl R (1995) Tetanically induced LTP involves a similar increase in the AMPA and NMDA receptor components of the excitatory postsynaptic current: investigations of the involvement of mGlu receptors. J Neurosci 15:2013-2020.
35. O'Dell TJ, Hawkins RD, Kundel ER, Arancio O (1991) Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible retrograde messenger. Proc Natl Acad Sci USA 88:11285-11289.
36. O'Dell TJ, Huang PL, Danwson TM, Dinerman JL, Snyder SH, Kandel ER, Fishman MC (1994) Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 265:542-546.
37. O'Mara SM, Rowan MJ, Anwyl R (1995) Metabotropic glutamate receptor-induced long-term depression and depotentiation in the dentate gyrus of the rat hippocampus in vitro. Neuropharmaeology 34:983-989.
38. Schumann EM, Madison DV (1991) A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254:1503-1506.
39. Schumann EM, Madison DV (1994) Nitric oxide and synaptic function. Annu Rev Neurosci 17:153-183.
40. Schumann EM, Meffert MK, Schulman H, Madison DV (1994) An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation. Proc Natl Acad Sci USA 91:11958-11962.
41. Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015-1023.
42. Wang Y, Rowan MJ, Anwyl R (1997) Induction of LTD is NMDAR-independent, but dependent on Ca influx via low voltage activated Ca channels and release of Ca from intracellular stores in the dentate gyrus in vitro. J Neurophysiol 77:812-825.
43. Wu J, Wang Y, Rowan MJ, Anwyl R (1997) Evidence for involvement of the neuronal isoform of nitric oxide synthase during induction of long-term potentiation and long-term depression in the rat dentate gyrus in vitro. Neuroscience 78:393-398.
44. Zhuo M, Small SA, Kandel ER, Hawkins RD (1993) Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science 260:1946-1950.
45. Zhou M, Kandel ER, Hawkins RD (1994a) Nitric oxide and cGMP can produce either synaptic depression or potentiation depending on the frequency of presynaptic stimulation in the hippocampus. NeuroReport 5:1033-1036.
46. Zhuo M, Hu Y, Schultz C, Kandel ER, Hawkins RD (1994b) Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368:635-639.