A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression

Journal of Neuroscience

Volumn 19, Issue 7, 1999, Pages 2489-2499

  Calabresi, Paolo ^a   Gubellini, Paolo ^a,b   Centonze, Diego ^a   Sancesario, Giuseppe ^a   Morello, Maria ^a   Giorgi, Mauro ^c   Pisani, Antonio ^a   Bernardi, Giorgio ^a,d  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

^d IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Calmodulin dependent phosphodiesterases; Electron microscopy; Intracellular recordings; Nitric oxide synthase; Striatum; Zaprinast

Indexed keywords

CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; ZAPRINAST;

ANIMAL TISSUE; ARTICLE; CORPUS STRIATUM; DEPRESSION; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE CELL PLASTICITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

EID: 0033119685     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-07-02489.1999     Document Type: Article

References (70)

1. Ariano MA (1983) Distribution of components of the guanosine 3′-5′-phosphate system in rat caudate-putamen. Neuroscience 10:707-723.
2. Ariano MA, Lewicki JA, Brandwein HJ, Murad F (1982) Immunohis-tochemical localization of guanylate cyclase within neurons of rat brain. Proc Natl Acad Sci USA 79:1316-1320.
3. Beavo JA (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 75:725-748.
4. Beavo JA, Reifsnyder DH (1990) Primary sequence of cyclic nucleotide phosphodiesterase isozyme and the design of selective inhibitors. Trends Pharmacol Sci 11:150-155.
5. Berridge MJ (1993) A tale of two messengers. Nature 365:388-389.
6. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
7. Boegman RJ, Parent A (1988) Differential sensitivity of neuropeptide Y, somatostatin and NADPH-diaphorase containing neurons in rat cortex and striatum to quinolinic acid. Brain Res 445:358-362.
8. Bon C, Böhme GA, Doble A, Stutzmann J-M, Blanchard J-C (1992) A role for nitric oxide in long-term potentiation. Eur J Neurosci 4:420-424.
9. Boulton CL, Southam E, Garthwaite J (1995) Nitric oxide-dependent long-term potentiation is blocked by a specific inhibitor of soluble guanylyl cyclasc. Neuroscience 3:699-703.
10. Boxall RA, Garthwaite J (1996) Long-term depression in rat cerebellum requires both NO synthase and NO-sensitive guanylyl cyclase. Eur J Neurosci 8:2209-2212.
11. Broome MR, Collingridge GL, Irving AJ (1994) Activation of the NO-cGM P signalling pathway depresses hippocampal synaptic transmission through an adenosine receptor-dependent mechanism. Neuropharmacology 33:1511-1513.
12. Calabresi P, Mercuri NB, Bernardi G (1990) Synaptic and intrinsic control of membrane excitability of neostriatal neurons. II. An in vitro analysis. J Neurophysiol 63:663-675.
13. Calabresi P, Mercuri NB, De Murtas M, Bernardi G (1991) Involvement of GABA systems in the feed-back regulation of glutamate- and GABA-mediated synaptic potentials in the striatum. J Physiol (Lond) 440:581-599.
14. Calabresi P, Maj R, Mercuri NB, Bernardi G (1992a) Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci Lett 142:95-99.
15. Calabresi P, Maj R, Pisani A, Mercuri NB, Bernardi G (1992b) Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12:4224-4233.
16. Calabresi P, Pisani A, Mercuri NB, Bernardi G (1993) Lithium treatment blocks long-term synaptic depression in the striatum. Neuron 10:955-962.
17. Calabresi P, Pisani A, Mercuri NB, Bernardi G (1994) Post-receptor mechanisms underlying striatal long-term depression. J Neurosci 14:4871-4881.
18. 2+ in striatal LTD and LTP. Semin Neurosci 8:321-328.
19. Calabresi P, Pisani A, Mercuri NB, Bernardi G (1996b) The corticostriatal projection: from synaptic plasticity to basal ganglia disorders. Trends Neurosci 19:19-24.
20. Calabresi P, Centonze D, Pisani A, Bernardi G (1997a) Endogenous adenosine mediates the presynaptic inhibition induced by aglycemia at corticostriatal synapses. J Neurosci 17:4509-4516.
21. Calabresi P, De Murtas M, Bernardi G (1997b) The neostriatum beyond the motor function. Neuroscience 78:39-60.
22. Calabresi P, Saiardi A, Pisani A, Baik J-H, Centonze D, Mercuri NB, Bernardi G (1997c) Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci 17:4536-4544.
23. Cherubini E, Herrling PL, Lanfumey L, Stanzione P (1988) Excitatory amino-acids in synaptic excitation of rat striatal neurons in vitro. J Physiol (Lond) 400:677-690.
24. Choi S, Lovinger DM (1997) Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci USA 94:2665-2670.
25. Crépel F, Jaillard D (1990) Protein kinases, nitric oxide and long-term depression of synapses in the cerebellum. NeuroReport 1:133-136.
26. Daniel H, Hemart N, Jaillard D, Crepel F (1993) Long-term depression requires nitric oxide and guanosine 3′,5′ cyclic monophosphate production in rat cerebellar Purkinje cells. Eur J Neurosci 5:1079-1082.
27. East SJ, Parry-Jones A, Brotchie JM (1996) Ionotropic glutamate receptors and nitric oxide synthesis in the rat striatum. NeuroReport 8:71-75.
28. Figueredo-Cardenas G, Morello M, Sancesario G, Bernardi G, Reiner A (1997) Colocalization of somatostatin, neuropeptide Y, neuronal nitric oxide synthase and NADPH-diaphorase in striatal interneurons in rats. Brain Res 735:317-324.
29. Furuyama T, Inagaki S, Takagi H (1993) Localizations of α-1 and β-1 subunits of soluble guanylate cyclase in the rat brain. Mol Brain Res 20:335-344.
30. Garthwaite J, Southam E, Boulton CL, Neilsen 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]quinoxalyn-1-one. Mol Pharmacol 48:184-188.
31. Glaum SR, Slater NT, Rossi DJ, Miller RJ (1992) Role of metabotropic glutamate (ACPD) receptors at the parallel fibre-Purkinje cell synapse. J Neurophysiol 68:1453-1462.
32. Graybiel AM (1990) Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13:244-254.
33. Graybiel AM (1995) Building action repertoires: memory and learning functions of the basal ganglia. Curr Opin Neurobiol 5:733-741.
34. Gribkoff VK, Lum-Ragan JT (1992) Evidence for nitric oxide synthase inhibitor-sensitive and insensitive hippocampal synaptic potentiation. J Neurophysiol 68:639-642.
35. Groves PM (1983) A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement. Brain Res Rev 5:109-132.
36. Haley JE, Malen PL, Chapman PF (1993) Nitric oxide inhibitors block long-term potentiation induced by weak hut not strong tetanic stimulation at physiological brain temperatures in rat hippocampal slices. Neurosci Lett 160:85-88.
37. Hartell NA (1996) Inhibition of cGMP breakdown promotes the induction of cerebellar long-term depression. J Neurosci 16:2881-2890.
38. Herrling PL (1985) Pharmacology of the corticocaudate excitatory postsynaptic potential in the cat: evidence for its mediation by quisqualate or kainate receptors. Neuroscience 14:417-426.
39. Hölscher C (1997) Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci 7:298-303.
40. Horikawa H, Armstrong WE (1988) A versatile means of intracellular labelling: injection of hiocytin and its detection with avidin conjugates. J Neurosci Methods 25:1-11.
41. Ichimura M, Eiki R, Osawa K, Nakanishi S, Kase H (1996) KS-505a, an isoform-selective inhibitor of calmodulin-dependent cyclic nucleotide phosphodicsterasc. Biochem J 316:311-316.
42. Jiang ZG, North RA (1991) Membrane properties and synaptic responses of rat striatal neurones in vitro. J Physiol (Lond) 443:533-553.
43. Kato K, Zorumski CF (1993) Nitric oxide inhihitors facilitate the induction of hippocampal long-term potentiation by modulating NMDA responses. J Neurophysiol 70:1260-1263.
44. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
45. Kitai ST, Kocsis JD, Preston RJ, Sugimori M (1976) Monosynaptic inputs to caudate neurons identified by intracellular injection of horseradish peroxidase. Brain Res 109:601-606.
46. Kleschevnikov AM, Sokolov MV, Kuhnt U, Dawc GS, Stephenson JD, Voronin LL (1997) Changes in paired-pulse facilitation correlate with induction of long-term potentiation in area CA1 of rat hippocampal slices. Neurosciencc 76:829-843.
47. 2+ transients. Neuron 15:407-415.
48. 2+ in the induction of cerebellar long-term depression. Neuron 18:1025-1038.
49. Linden DJ, Connor JA (1992) Long-term depression of glutamate currents in cultured cerebellar Purkinje neurons does not require nitric oxide signaling. Eur J Neurosci 4:10-15.
50. Loughney K, Martins TJ, Harris EAS, Sadhu K, Hicks JB, Sonnenburg WK, Beavo JA, Ferguson K (1996) Isolation and characterization of cDNAs corresponding to two human calcium, calmodulin-regulated, 3′,5′-cydic nuclcotide phosphodiesterases. J Biol Chem 271:796-806.
51. Lovinger DM, Tyler EC, Merritt A (1993) Short-and long-term synaptic depression in rat neostriatum. J Neurophysiol 70:1937-1949.
52. Malen PL, Chapman PF (1997) Nitric oxide facilitates long-term potentiation, but not long-term depression. J Neurosci 17:2645-2651.
53. Matsuoka I, Giuili G, Poyard M, Stengel D, Parma J, Guellaen G, Hanoune J (1992) Localization of adenylyl and guanylyl cyclase in rat brain by in situ hybridization: comparison with calmodulin mRNA distribution. J Neurosci 12:3350-3360.
54. Moore PK, Handy RLC (1997) Selective inhibitors of neuronal nitric oxide synthase: is no NOS really good NOS for the nervous system? Trends Pharmacol Sci 18:204-211.
55. Morello M, Reiner A, Sancesario G, Karle EJ, Bernardi G (1997) Ultrastructural study of nitric oxide synthase-containing striatal neurons and their relationship with parvalbumin-containing neurons in rats. Brain Res 776:30-39.
56. Polli JW, Kincaid RL (1994) Expression of a calmodulin-dependent phosphodiesterase isoform (PDE1B1) correlates with brain regions having extensive dopaminergic innervation. J Neurosci 14:1251-1261.
57. Schuman EM, Madison DV (1991) A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254:1503-1506.
58. Shibuki K, Okada D (1991) Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349:326-328.
59. Smith AD, Bolam JP (1990) The neuronal network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci 13:259-265.
60. Son H, Hawkins RD, Martin K, Kichler 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.
61. Southam E, Garthwaite J (1991) Comparative effects of some nitric oxide donors on cyclic GMP levels in rat cerebellar slices. Neurosci Lett 130:107-111.
62. Thompson WJ, Appleman MM (1971) Multiple cyclic nucleotide phosphodiesterase activities from rat brain. Biochemistry 10:311-316.
63. Vincent SR, Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-784.
64. Walsh JP (1993) Depression of excitatory synaptic input in rat striatal neurons. Brain Res 608:123-128.
65. Wang X, Robinson PJ (1997) Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J Neurochem 68:443-456.
66. Williams JH, Li Y-G, Nayak A, Errington ML, Murphy KPSJ, Bliss TVP (1993) The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent. Neuron 11:877-884.
67. Wu Z, Sharma RK, Wang JH (1992) Catalytic and regulatory properties of calmodulin-stimulated phosphodiesterase isozymes. In: Advances in second messenger and phosphoprotcin research (Strada SJ, Hidaka H, eds), pp 29-43. New York: Raven.
68. Van C, Bentley JK, Sonnenburg WK, Beavo JA (1994) Differential expression of the 61 kDa and 63 kDa calmodulin-dependent phosphodiesterases in the mouse brain. J Neurosci 14:973-984.
69. Yu J, Wolda SL, Frazier AL, Florio VA, Martins TJ, Snyder PB, Harris EA, McCaw KN, Farrell CA, Steiner B, Bentley JK, Beavo JA, Ferguson K, Geinas R (1997) Identification and characterisation of a human calmodulin-stimulated phosphodiesterase PDE1B1. Cell Signal 9:519-529.
70. 2+/CaM-activated phosphodiesterases. In: Advances in second messenger and phosphoprotein research, Vol 31 (Corbin JD, Francis SH. eds), pp 237-251. Philadelphia: Lippincott-Raven.