The Nitric Oxide-Guanylyl Cyclase Signaling Pathway Modulates Membrane Activity States and Electrophysiological Properties of Striatal Medium Spiny Neurons Recorded In Vivo

Journal of Neuroscience

Volumn 24, Issue 8, 2004, Pages 1924-1935

  West, Anthony R ^a   Grace, Anthony A ^b  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

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

Author keywords

cGMP; Guanylyl cyclase; Medium spiny neuron; Nitric oxide; Reverse microdialysis; Striatum

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 7 NITROINDAZOLE; 8 BROMO CYCLIC GMP; CYCLIC GMP; GUANYLATE CYCLASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; ZAPRINAST;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME INHIBITION; MALE; MEDIUM SPINY NEURON; MEMBRANE POTENTIAL; MICRODIALYSIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STEADY STATE;

ANIMALS; CELL MEMBRANE; CORPUS STRIATUM; CYCLIC GMP; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; FREE RADICAL SCAVENGERS; GUANYLATE CYCLASE; MALE; MICRODIALYSIS; MICROELECTRODES; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 1442300196     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4470-03.2004     Document Type: Article

References (47)

1. Ariano MA (1983) Distribution of the components of the guanosine 3′,5′-phosphate system in rat caudate-putamen. Neuroscience 10:707-723.
2. Bockelmann R, Wolf G, Ransmayr G, Riederer P (1994) NADPH-diaphorase/nitric oxide synthase containing in normal and Parkinson's disease putamen. J Neural Transm Park Dis Dement Sect 7:115-121.
3. Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M, Pisani A, Bernardi G (1999a) A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci 19:2489-2499.
4. Calabresi P, Centonze D, Gubellini P, Marfia GA, Bernardi G (1999b) Glutamate-triggered events inducing corticostriatal long-term depression. J Neurosci 19:6102-6110.
5. Calabresi P, Centonze D, Gubellini P, Marfia GA, Pisani A, Sancesario G, Bernardi G (2000a) Synaptic transmission in the striatum: from plasticity to neurodegeneration. Prog Neurobiol 61:231-265.
6. Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K, Svenningsson P, Fienberg A, Greengard P (2000b) Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci 20:8443-8451.
7. Cavas M, Navarro JF (2002) Coadministration of L-NOARG and tiapride: effects on catalepsy in male mice. Prog Neuropsychopharmacol Biol Psychiatry 26:69-73.
8. Charpier S, Deniau JM (1997) In vivo activity-dependent plasticity at cortico-striatal connections: evidence for physiological long-term potentiation. Proc Natl Acad Sci USA 94:7036-7040.
9. Deniau JM, Menetrey A, Charpier S (1996) The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections. Neuroscience 73:761-781.
10. Deutsch SI, Rosse RB, Paul SM, Tomasino V, Koetzner L, Morn CB, Mastropaolo J (1996) 7-Nitroindazole and methylene blue, inhibitors of neuronal nitric oxide synthase and NO-stimulated guanylyl cyclase, block MK-801 elicited behaviors in mice. Neuropsychopharmacology 15:37-43.
11. de Vente J, Markerink-van Ittersum M, Van Abeelen J, Emson PC, Axer H, Steinbusch HWM (2000) NO-mediated cGMP synthesis in cholinergic neurons in the rat forebrain: effects of lesioning dopaminergic or serotonergic pathways on nNOS and cGMP synthesis. Eur J Neurosci 12:507-519.
12. Di Giovanni G, Ferraro G, Sardo P, Galati S, Esposito E, La Grutta V (2003) Nitric oxide modulates striatal neuronal activity via soluble guanylyl cyclase: an in vivo microiontophoretic study in rats. Synapse 48:100-107.
13. East JS, Parry-Jone A, Brotchie JM (1996) Ionotropic glutamate receptors and nitric oxide in the rat striatum. NeuroReport 8:71-75.
14. Eve DJ, Nisbet AP, Kingsbury AE, Hewson EL, Daniel SE, Lees AJ, Marsden CD, Foster OJ (1998) Basal ganglia neuronal nitric oxide synthase mRNA expression in Parkinson's disease. Mol Brain Res 63:62-71.
15. Garthwaite J, Boulton CL (1995) (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683-706.
16. Globus MY, Prado R, Busto R (1995) Ischemia-induced changes in extracellular levels of striatal cyclic GMP: role of nitric oxide. NeuroReport 6:1909-1912.
17. Gomez-Urquijo SM, Hokfelt T, Ubink R, Lubec G, Herrera-Marschitz M (1999) Neurocircuitries of the basal ganglia studied in organotypic cultures: focus on tyrosine hydroxylase, nitric oxide synthase, and neuropeptide immunocytochemistry. Neuroscience 94:1133-1151.
18. Greengard P, Allen PB, Nairn AC (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23:435-447.
19. Guevara-Guzman R, Emson PC, Kendrick KM (1994) Modulation of in vivo striatal transmitter release by nitric oxide and cyclic-GMP. J Neurochem 62:807-810.
20. Hidaka S, Totterdell S (2001) Ultrastructural features of the nitric oxide synthase-containing interneurons in the nucleus accumbens and their relationship with tyrosine hydroxylase containing terminals. J Comp Neurol 431:139-154.
21. + current expressed in Xenopus oocytes. FEBS Lett 402:12-16.
22. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923.
23. Kawaguchi Y (1997) Neostriatal cell subtypes and their functional roles. Neurosci Res 27:1-8.
24. Kharazia VN, Schmidt HHW, Weinberg RJ (1994) Type 1 nitric oxide synthase fully accounts for NADPH-diaphorase in rat striatum but not cortex. Neuroscience 62:983-987.
25. Kubota Y, Mikawa S, Kawaguchi Y (1993) Neostriatal GABAergic interneurons contain NOS, calretinin or parvalbumin. NeuroReport 5:205-208.
26. Mancuso F, Calignano A, Sorrentino L (1994) Endogenous nitric oxide modulates the behavioral effects elicited by substance P in rat. Eur J Pharmacol 271:329-333.
27. Marin P, Lafon-Cazal M, Bockaert J (1992) A nitric oxide activity selectively stimulated by NMDA receptors depends on protein kinase C activation in mouse striatal neurons. Eur J Neurosci 4:425-432.
28. O'Donnell P, Grace AA (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 15:3622-3639.
29. O'Donnell P, Grace AA (1997) Cortical afferents modulate striatal gap junction permeability via nitric oxide. Neuroscience 76:1-5.
30. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. New York: Academic.
31. Reed TM, Repaske DR, Snyder GL, Greengard P, Vorhees CV (2002) Phosphodiesterase 1B knock-out mice exhibit exaggerated locomotor hyperactivity and DARPP-32 phosphorylation in response to dopamine agonists and display impaired spatial learning. J Neurosci 22:5188-5197.
32. Sahach VF, Baziliuk OV, Oleshko MM, Kotsiuruba OV, Bukhanevych OM, Appenzeller O (2000) The nitric oxide system in a chronic deficiency of mesostriatal dopamine: the action of nitroglycerin. Fiziol Zh 46:55-63.
33. Sancesario G, Morello M, Reiner A, Giacomini P, Massa R, Schoen S, Bernardi G (2000) Nitrergic neurons make synapses on dual-input dendritic spines of neurons in the cerebral cortex and the striatum of the rat: implications for a postsynaptic action of nitric oxide. Neuroscience 99:627-642.
34. Sanchez JJ, Abreu P, Gonzalez C (2002) Sodium nitroprusside stimulates L-DOPA release from striatal tissue through nitric oxide and cGMP. Eur J Pharmacol 438:79-83.
35. Starr MS, Starr BS (1995) Do NMDA receptor-mediated changes in motor behavior involve nitric oxide? Eur J Pharmacol 272:211-217.
36. Stewart J, Deschamps S-E, Amir S (1994) Inhibition of nitric oxide synthase does not block the development of sensitization to the behavioral activating effects of amphetamine. Brain Res 641:141-144.
37. Tsou K, Snyder G, Greengard P (1993) Nitric oxide/cGMP pathway stimulates phosphorylation of DARPP-32, a dopamine and cAMP-regulated phosphoprotein in the substantia nigra. Proc Natl Acad Sci USA 90:3462-3465.
38. West AR, Galloway MP (1997) Endogenous nitric oxide facilitates striatal dopamine and glutamate efflux in vivo: role of ionotropic glutamate receptor-dependent mechanisms. Neuropharmacology 36:1571-1581.
39. West AR, Grace AA (2000) Striatal nitric oxide signaling regulates the neuronal activity of midbrain dopamine neurons in vivo. J Neurophysiol 83:1796-1808.
40. West AR, Grace AA (2001) Endogenous nitric oxide modulates the excitability of striatal neurons exhibiting bistable membrane potentials: studies using combined in vivo intracellular recordings and microdialysis in vivo. Soc Neurosci Abstr 27:31.5.
41. 2 receptor activation on activity states and electrophysiological properties of striatal neurons: studies combining in vivo intracellular recordings and reverse microdialysis. J Neurosci 22:294-304.
42. West AR, Grace AA (2002b) Guanylyl cyclase modulates the excitability of striatal neurons exhibiting bistable membrane potentials in vivo. Soc Neurosci Abstr 28:249.17.
43. West AR, Galloway MP, Grace AA (2002a) Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms. Synapse 44:227-245.
44. West AR, Moore HM, Grace AA (2002b) Direct examination of local regulation of membrane activity in striatal and prefrontal cortical neurons in vivo using simultaneous intracellular recording and microdialysis. J Pharmacol Exp Ther 301:867-877.
45. A receptor function via coactivation of cGMP-dependent kinase and phosphodiesterase. J Neurosci 18:2342-2349.
46. Wilson CJ (1993) The generation of natural firing patterns in neostriatal neurons. In: Chemical signaling in the basal ganglia: progress in brain research (Arbuthnott GW and Emson PC, eds), pp 277-297. Amsterdam: Elsevier.
47. Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397-2410.