7-Nitroindazole down-regulates dopamine/DARPP-32 signaling in neostriatal neurons in a rat model of Parkinson's disease

Neuropharmacology

Volumn 63, Issue 7, 2012, Pages 1258-1267

  Yuste, J E ^a   Echeverry, M B ^a   Ros Bernal, F ^a   Gomez, A ^a   Ros, C M ^a   Campuzano, C M ^a   Fernandez Villalba, E ^a   Herrero, M T ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

6 OHDA; 7 NI; DARPP 32; Dorsolateral; EBST; Neostriatum; nNOS; SNpc; TH

Indexed keywords

7 NITROINDAZOLE; DOPAMINE; NEURONAL NITRIC OXIDE SYNTHASE; NEUROTRANSMITTER; NITRIC OXIDE; OXIDOPAMINE; PHOSPHOPROTEIN DARPP 32;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE MODEL; DOPAMINERGIC NERVE CELL; DOWN REGULATION; HISTOPATHOLOGY; MALE; NEOSTRIATUM; NERVE CELL; NERVE CELL LESION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RAT; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA PARS COMPACTA;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; ENZYME INHIBITORS; INDAZOLES; MALE; NEOSTRIATUM; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84866052969     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.07.031     Document Type: Article

References (65)

1. T. Baluchnejadmojarad, and M. Roghani Evaluation of functional asymmetry in rats with dose-dependent lesions of dopaminergic nigrostriatal system using elevated body swing test Physiol. Behav. 82 2-3 2004 369 373
2. C. Barcia, A. Sánchez Bahillo, E. Fernández-Villalba, V. Bautista, M. Poza Y Poza, A. Fernández-Barreiro, E.C. Hirsch, and M.T. Herrero Evidence of active microglia in substantia nigra pars compacta of parkinsonian monkeys 1 year after MPTP exposure Glia 46 4 2004 402 409
3. F. Blandini, M.T. Armentero, R. Fancellu, E. Blaugrund, and G. Nappi Neuroprotective effect of rasagiline in a rodent model of Parkinson's disease Exp. Neurol. 187 2 2004 455 459
4. F. Blandini, G. Levandis, E. Bazzini, G. Nappi, and M.T. Armentero Time-course of nigrostriatal damage, basal ganglia metabolic changes and behavioural alterations following intrastriatal injection of 6-hydroxydopamine in the rat: new clues from an old model Eur. J. Neurosci. 25 2007 397 405
5. D. Blum, S. Torch, N. Lambeng, M. Nissou, A.L. Benabid, R. Sadoul, and J.M. Verna Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease Prog. Neurobiol. 65 2001 135 172
6. C.V. Borlongan, and P.R. Sanberg Elevated body swing test: a new behavioral parameter for rats with 6-hydroxydopamine-induced hemiparkinsonism J. Neurosci. 15 1995 5372 5378
7. D.S. Bredt, and S.H. Snyder Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme Proc. Nat. Acad. Sci. 87 1990 682 685
8. P. Calabresi, P. Gubellini, D. Centonze, B. Picconi, G. Bernardi, K. Chergui, P. Svenningsson, A.A. Fienberg, and P. Greengard 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 22 2000 8443 8451
9. P. Calabresi, B. Picconi, A. Tozzi, and M. Di Filippo Dopamine-mediated regulation of corticostriatal synaptic plasticity Trends Neurosci. 30 5 2007 211 219
10. B. Costall, and R.J. Naylor A comparison of circling models for the detection of antiparkinson activity Psychopharmacology (Berlin) 41 1975 57 64
11. B. Costall, C.D. Marsden, R.I. Naylor, and C.J. Pycock The relationship between striatal and mesolimbic dopamine dysfunction and the nature of circling responses following 6-OHDA and electrolytic lesions of the ascending dopamine systems of rats brain Brain Res. 118 1976 87 113
12. T.M. Dawson, D.S. Bredt, M. Fotuhi, P.M. Hwang, and S.H. Snyder Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues Proc. Natl. Acad. Sci. USA. 88 17 1991 7797 7801
13. T.M. Dawson, and S.H. Snyder Gases as biological messengers: nitric oxide and carbon monoxide in the brain J. Neurosci. 14 9 1994 5147 5159
14. T. Debeir, L. Ginestet, C. Francois, S. Laurens, J.C. Martel, P. Chopin, M. Marien, F. Colpaert, and R. Raisman-Vozari Effect of intrastriatal 6-OHDA lesion on dopaminergic innervation of the rat cortex and globus pallidus Exp. Neurol. 193 2005 444 454
15. A. Denicola, and R. Radi Peroxynitrite and drug-dependent toxicity Toxicology 208 2 2005 273 288
16. V. Di Matteo, M. Pierucci, A. Benigno, G. Crescimanno, E. Esposito, and G. Di Giovanni Involvement of nitric oxide in nigrostriatal dopaminergic system degeneration: a neurochemical study Ann. NY Acad. Sci. 1155 2009 309 315
17. D.A. Di Monte, J.E. Royland, A. Anderson, K. Castagnoli, N. Castagnoli Jr. , and J.W. Langston Inhibition of monoamine oxidase contributes to the protective effect of 7-nitroindazole against MPTP neurotoxicity J. Neurochem. 69 4 1997 1771 1773
18. A. Di Stefano, P. Sozio, I. Cacciatore, A. Cocco, G. Giorgioni, B. Costa, M. Montali, A. Lucacchini, C. Martini, G. Spoto, F. Di Pietrantonio, E. Di Matteo, and F. Pinnen Preparation and pharmacological characterization of trans-2-amino5(6)-fluoro-6(5)-hydroxy-1-phenyl-2,3-dihydro-1H-indenes as D2-like dopamine receptor agonists J. Med. Chem. 48 2005 2646 2654
19. M.B. Echeverry, F.S. Guimarães, and E.A. Del Bel Acute and delayed restraint stress-induced changes in nitric oxide producing neurons in limbic regions Neuroscience 125 4 2004 981 993
20. R.J. Ferrante, P. Hantraye, E. Brouillet, and M.F. Beal Increased nitrotyrosine immunoreactivity in Substantia Nigra neurons in MPTP treated baboons is blocked by inhibition of neuronal nitric oxide synthase Brain Res. 823 1-2 1999 177 182
21. M.Z. Gomes, R. Raisman-Vozari, and E.A. Del Bel A nitric oxide synthase inhibitor decreases 6-hydroxydopamine effects on tyrosine hydroxylase and neuronal nitric oxide synthase in the rat nigrostriatal pathway Brain Res. 1203 2008 160 169
22. S.M. Gomez-Urquijo, T. Hökfelt, R. Ubink, G. Lubec, and M. Herrera-Marschitz Neurocircuitries of the basal ganglia studied in organotypic cultures: focus on tyrosine hydroxylase, nitric oxide synthase and neuropeptide immunocytochemistry Neuroscience 94 4 1999 1133 1151
23. P. Greengard, P.B. Allen, and A.C. Nairn Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade Neuron 23 3 1999 435 447
24. B.H. Guevara, G.C. Cespedes, and L.X. Cubeddu Treatment with 7-nitroindazole enhances kainic acid induced cholinergic neurotoxicity in the rat striatum: a neuroprotective role for neuronal nitric oxide Cell. Mol. Neurobiol. 22 5-6 2002 827 834
25. P. Hantraye, E. Brouillet, R. Ferrante, S. Palfi, R. Dolan, R.T. Matthews, and M.F. Beal Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons Nat. Med. 2 1996 1017 1021
26. H.C. Hemmings Jr. , K.R. Williams, W.H. Konigsberg, and P. Greengard DARPP-32, a dopamine- and adenosine 3′:5′-monophosphate-regulated neuronal phosphoprotein. I. Amino acid sequence around the phosphorylated threonine J. Biol. Chem. 259 1984 14486 14490
27. M. Herrera-Marschitz, and U. Ungerstedt Evidence that striatal efferents relate to different dopamine receptors Brain Res. 323 2 1984 269 278
28. K.E. Hoque, R.P. Indorkar, S. Sammut, and A.R. West Impact of dopamine-glutamate interactions on striatal neuronal nitric oxide synthase activity Psychopharmacology (Berlin) 207 2010 571 581
29. O. Hornykiewicz, and S.J. Kish Biochemical pathophysiology of Parkinson's disease Adv. Neurol. 45 1987 19 34
30. L.J. Ignarro Nitric oxide. A novel signal transduction mechanism for transcellular communication Hypertension 16 5 1990 477 483
31. S.D. Iversen, and G.F. Koob Behavioral implications of dopaminergic neurons in the mesolimbic system Adv. Biochem. Psychopharmacol. 16 1977 209 214
32. D. Kirik, C. Rosenblad, and A. Bjorklund Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat Exp. Neurol. 152 1998 259 277
33. G.F. Koob, H. Simon, J.P. Herman, and M. Le Moal Neuroleptic-like disruption of the avoidance response requires destruction of both the mesolimbic and nigrostriatal dopamine systems Brain Res. 303 2 1984 319 329
34. M. Lindskog, P. Svenningsson, L. Pozzi, Y. Kim, A.A. Fienberg, J.A. Bibb, B.B. Fredholm, A.C. Nairn, P. Greengard, and G. Fisone Involvement of DARPP-32 phosphorylation in the stimulant action of caffeine Nature 418 2002 774 778
35. M.A. Marletta Nitric oxide synthase: aspects concerning structure and catalysis Cell 78 6 1994 927 930
36. S. Moncada, R.M.J. Palmer, and E.A. Higgs Nitric oxide: physiology, pathophysiology, and pharmacology Pharmacol. Rev. 43 1991 109 142
37. S. Murphy, M.L. Simmons, L. Agullo, A. Garcia, D.L. Feinstein, E. Galea, D.J. Reis, D. Minc-Golomb, and J.P. Schwartz Synthesis of nitric oxide in CNS glial cells Trends Neurosci. 16 8 1993 323 328
38. A.C. Nairn, P. Svenningsson, A. Nishi, G. Fisone, J.A. Girault, and P. Greengard The role of DARPP-32 in the actions of drugs of abuse Neuropharmacology 47 2004 14 23
39. A. Nishi, Y. Watanabe, H. Higashi, M. Tanaka, A.C. Nairn, and P. Greengard Glutamate regulation of DARPP-32 phosphorylation in neostriatal neurons involves activation of multiple signaling cascades PNAS 102 4 2005 1199 1204
40. M.E. Old, D.B. Jacques, and O. Kopyov Subthalamic responses to amphetamine and apomorphine in the behaving rat with a unilateral 6-OHDA lesion in the Substantia Nigra Synapse 34 1999 228 240
41. C.C. Ouimet, P.E. Miller, H.C. Hemmings Jr. , S.I. Walaas, and P. Greengard DARPP-32, a dopamine- and adenosine 3′:5′-monophosphate- regulated phosphoprotein enriched in dopamine-innervated brain regions. III. Immunocytochemical localization J. Neurosci. 4 1 1984 111 124
42. C.C. Ouimet, K.C. Langley-Gullion, and P. Greengard Quantitative immunocytochemistry of DARPP-32-expressing neurons in the rat caudatoputamen Brain Res. 808 1998 8 12
43. F.E. Padovan-Neto, M.B. Echeverry, V. Tumas, and E.A. Del-Bel Nitric oxide synthase inhibition attenuates L-DOPA-induced dyskinesias in a rodent model of Parkinson's disease Neuroscience 159 3 2009 927 935
44. D.J. Park, and A.R. West Regulation of striatal nitric oxide synthesis by local dopamine and glutamate interactions J. Neurochem. 111 2009 1457 1465
45. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates fourth ed. 1998 Academic Press New York
46. M. Pierucci, S. Galati, M. Valentino, V. Di Matteo, A. Benigno, R. Muscat, A. Pitruzzella, and G. Di Giovanni Nitric oxide modulation of the basal ganglia circuitry: therapeutic implication for Parkinson's disease and other motor disorders CNS Neurol. Disord. Drug Targets 10 2011 777 791
47. S. Przedborski, M. Levivier, H. Jiang, M. Ferreira, V. Jackson-Lewis, D. Donaldson, and D.M. Togasaki Dose-dependent lesions of the dopaminergic nigrostriatal pathway induced by intrastriatal injection of 6-hydroxydopamine Neuroscience 67 1995 631 647
48. Y. Sagi, S. Mandel, T. Amit, and M.B. Youdim Activation of tyrosine kinase receptor signaling pathway by rasagiline facilitates neurorescue and restoration of nigrostriatal dopamine neurons in post-MPTP-induced parkinsonism Neurobiol. Dis. 25 1 2007 35 44
49. C. Salum, R. Raisman-Vozari, P.P. Michel, M.Z. Gomes, M. Mitkovski, J.E. Ferrario, L. Ginestet, and E.A. Del Bel Modulation of dopamine uptake by nitric oxide in cultured mesencephalic neurons Brain Res. 1198 2008 27 33
50. S. Sammut, A. Dec, D. Mitchell, J. Linardakis, M. Ortiguela, and A.R. West Phasic dopaminergic transmission increases NO efflux in the rat dorsal striatum via a neuronal NOS and a dopamine D(1/5) receptor-dependent mechanism Neuropsychopharmacology 31 2006 493 505
51. R.K. Schwarting, and J.P. Huston The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments Prog. Neurobiol. 50 1996 275 331
52. J.A. Siuciak, S.A. McCarthy, D.S. Chapin, R.A. Fujiwara, L.C. James, R.D. Williams, J.L. Stock, J.D. McNeish, C.A. Strick, F.S. Menniti, and C.J. Schmidt Genetic deletion of the striatum-enriched phosphodiesterase PDE10A: evidence for altered striatal function Neuropharmacology 51 2006 374 385
53. M.P. Smith, and W.A. Cass Oxidative stress and dopamine depletion in an intrastriatal 6-hydroxydopamine model of Parkinson's disease Neuroscience 144 3 2007 1057 1066
54. G.J. Southan, and C. Szabó Selective pharmacological inhibition of distinct nitric oxide synthase isoforms Biochem. Pharmacol. 51 4 1996 383 394
55. P. Svenningsson, A. Nishi, G. Fisone, J.A. Girault, A.C. Nairn, and P. Greengard DARPP-32: an integrator of neurotransmission Ann. Rev. Pharmacol. Toxicol. 44 2004 269 296
56. K. Tsou, G.L. Snyder, and P. Greengard Nitric oxide/cGMP pathway stimulates phosphorylation of DARPP-32, a dopamine- and cAMP-regulated phosphoprotein, in the Substantia Nigra Proc. Natl. Acad. Sci. 90 1993 3462 3465
57. U. Ungerstedt, and G.W. Arbuthnott Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system Brain Res. 24 3 1970 485 493
58. U. Ungerstedt Postsynaptic supersensitivity after 6-hydroxy-dopamine induced degeneration of the nigro-striatal dopamine system Acta Physiol. Scand. Suppl. 367 1971 69 93
59. S.R. Vincent, and H. Kimura Histochemical mapping of nitric oxide synthase in the rat brain Neuroscience 46 1992 755 784
60. T.J. Volz, and J.O. Schenk L-arginine increases dopamine transporter activity in rat striatum via a nitric oxide synthase-dependent mechanism Synapse 54 2004 173 182
61. Von Bohlen Und Halbach Synucleins and their relationship to Parkinson's disease Cell. Tissue Res. 318 1 2004 163 174
62. A.R. West, and A.A. Grace The nitric oxide-guanylyl cyclase signaling pathway modulates membrane activity states and electrophysiological properties of striatal medium spiny neurons recorded in vivo J. Neurosci. 24 8 2004 1924 1935
63. A.R. West, and K.Y. Tseng Nitric oxide-soluble guanylyl cyclase-cyclic GMP signaling in the striatum: new targets for the treatment of Parkinson's disease? Front. Syst. Neurosci. 5 2011 55 59
64. K.J. Wiechelman, R.D. Braund, and J.D. Fitzpatrick Investigation of the bicinchoninic acid protein assay: identification of the groups responsible for colour formation Anal. Biochem. 175 1988 231 237
65. H. Yuan, S. Sarre, G. Ebinger, and Y. Michotte Histological, behavioural and neurochemical evaluation of medial forebrain bundle and striatal 6-OHDA lesions as rat models of Parkinson's disease J. Neurosci. Methods 144 2005 35 45