Nitric oxide synthase inhibition decreases l-DOPA-induced dyskinesia and the expression of striatal molecular markers in Pitx3-/- aphakia mice

Neurobiology of Disease

Volumn 73, Issue , 2015, Pages 49-59

  Solís, Oscar ^a,b   Espadas, Isabel ^a,b   Del Bel, Elaine A ^c   Moratalla, Rosario ^a,b  

^a INSTITUTO CAJAL   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Abnormal involuntary movements; FosB; Histone3; L DOPA; Molsidomine; Nitrergic system; NO cGMP; Parkinson disease; Pitx3 deficient aphakia mice; Striatum; Zaprinast

Indexed keywords

7 NITROINDAZOLE; GUANOSINE PHOSPHATE; HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE; MOLSIDOMINE; NITRIC OXIDE SYNTHASE; TRANSCRIPTION FACTOR FOSB; ZAPRINAST; 7-NITROINDAZOLE; ANTIPARKINSON AGENT; BENSERAZIDE; DOPAMINE RECEPTOR STIMULATING AGENT; ENZYME INHIBITOR; HOMEODOMAIN PROTEIN; INDAZOLE DERIVATIVE; LEVODOPA; NITRIC OXIDE DONOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PITX3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDYSKINETIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG ACTIVITY; DYSKINESIA; ENZYME ACTIVITY; HISTONE ACETYLATION; LOCOMOTION; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NITRERGIC NERVE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; ROTAROD TEST; SIGNAL TRANSDUCTION; STRIATE CORTEX; UPREGULATION; ANIMAL; CELL COUNT; CORPUS STRIATUM; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; DYSKINESIA, DRUG-INDUCED; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PARKINSON DISEASE; PATHOLOGY; TIME;

ANIMALS; ANTIPARKINSON AGENTS; BENSERAZIDE; CELL COUNT; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE AGENTS; DYSKINESIA, DRUG-INDUCED; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; INDAZOLES; LEVODOPA; MICE; MICE, KNOCKOUT; MOLSIDOMINE; NITRIC OXIDE DONORS; PARKINSON DISEASE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84908316828     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.09.010     Document Type: Article

References (77)

1. Andersson M., Hilbertson A., Cenci M.A. Striatal fosB expression is causally linked with l-DOPA-induced abnormal involuntary movements and the associated upregulation of striatal prodynorphin mRNA in a rat model of Parkinson's disease. Neurobiol. Dis. 1999, 6:461-474.
2. Ares-Santos S., Granado N., Espadas I., Martinez-Murillo R., Moratalla R. Methamphetamine causes degeneration of dopamine cell bodies and terminals of the nigrostriatal pathway evidenced by silver staining. Neuropsychopharmacology 2014, 39:1066-1080.
3. Bertran-Gonzalez J., Håkansson K., Borgkvist A., Irinopoulou T., Brami-Cherrier K., Usiello A., Greengard P., Hervé D., Girault J.A., Valjent E., Fisone G. Histone H3 phosphorylation is under the opposite tonic control of dopamine D2 and adenosine A2A receptors in striatopallidal neurons. Neuropsychopharmacology 2009, 34:1710-1720.
4. Bido S., Marti M., Morari M. Amantadine attenuates levodopa-induced dyskinesia in mice and rats preventing the accompanying rise in nigral GABA levels. J. Neurochem. 2011, 118:1043-1055.
5. Carta A.R., Giuffrida A., Fisone G. Dyskinesia in Parkinson's disease therapy. Park. Dis. 2012, 2012:639080.
6. Cenci M.A., Konradi C. Maladaptive striatal plasticity in L-DOPA-induced dyskinesia. Prog. Brain Res. 2010, 183:209-233.
7. Cenci M.A., Tranberg A., Andersson M., Hilbertson A. Changes in the regional and compartmental distribution of FosB- and JunB-like immunoreactivity induced in the dopamine-denervated rat striatum by acute or chronic L-dopa treatment. Neuroscience 1999, 94:515-527.
8. Chalimoniuk M., Langfort J. The effect of subchronic, intermittent L-DOPA treatment on neuronal nitric oxide synthase and soluble guanylyl cyclase expression and activity in the striatum and midbrain of normal and MPTP-treated mice. Neurochem. Int. 2007, 50:821-833.
9. Ciccarelli A., Calza A., Santoru F., Grasso F., Concas A., Sassoè-Pognetto M., Giustetto M. Morphine withdrawal produces ERK-dependent and ERK-independent epigenetic marks in neurons of the nucleus accumbens and lateral septum. Neuropharmacology 2013, 70:168-179.
10. Czarnecka A., Lenda T., Domin H., Konieczny J., Smiałowska M., Lorenc-Koci E. Alterations in the expression of nNOS in the substantia nigra and subthalamic nucleus of 6-OHDA-lesioned rats: the effects of chronic treatment with l-DOPA and the nitric oxide donor, molsidomine. Brain Res. 2013, 1541:92-105.
11. Darmopil S., Muñetón-Gómez V.C., de Ceballos M.L., Bernson M., Moratalla R. Tyrosine hydroxylase cells appearing in the mouse striatum after dopamine denervation are likely to be projection neurones regulated by L-DOPA. Eur. J. Neurosci. 2008, 27:580-592.
12. Darmopil S., Martín A.B., De Diego I.R., Ares S., Moratalla R. Genetic inactivation of dopamine D1 but not D2 receptors inhibits L-DOPA-induced dyskinesia and histone activation. Biol. Psychiatry 2009, 66:603-613.
13. Dauer W., Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003, 39:889-909.
14. Del Bel E.A., Souza A.S., Guimarães F.S., da-Silva C.A., Nucci-da-Silva L.P. Motor effects of acute and chronic inhibition of nitric oxide synthesis in mice. Psychopharmacology 2002, 161:32-37.
15. Del Bel E.A., Guimarães F.S., Bermúdez-Echeverry M., Gomes M.Z., Schiaveto-de-souza A., Padovan-Neto F.E., Tumas V., Barion-Cavalcanti A.P., Lazzarini M., Nucci-da-Silva L.P., de Paula-Souza D. Role of nitric oxide on motor behavior. Cell. Mol. Neurobiol. 2005, 25:371-392.
16. Del-Bel E., Padovan-Neto F.E., Szawka R.E., da-Silva C.A., Raisman-Vozari R., Anselmo-Franci J., Romano-Dutra A.C., Guimaraes F.S. Counteraction by nitric oxide synthase inhibitor of neurochemical alterations of dopaminergic system in 6-OHDA-lesioned rats under L-DOPA treatment. Neurotox. Res. 2014, 25:33-44.
17. Deutsch S.I., Rosse R.B., Paul S.M., Tomasino V., Koetzner L., Morn C.B., Mastropaolo J. 7-Nitroindazole and methylene blue, inhibitors of neuronal nitric oxide synthase and NO-stimulated guanylate cyclase, block MK-801-elicited behaviors in mice. Neuropsychopharmacology 1996, 15:37-43.
18. Ding Y., Restrepo J., Won L., Hwang D.Y., Kim K.S., Kang U.J. Chronic 3,4-dihydroxyphenylalanine treatment induces dyskinesia in aphakia mice, a novel genetic model of Parkinson's disease. Neurobiol. Dis. 2007, 27:11-23.
19. Ding Y., Won L., Britt J.P., Lim S.A., McGehee D.S., Kang U.J. Enhanced striatal cholinergic neuronal activity mediates L-DOPA-induced dyskinesia in parkinsonian mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:840-845.
20. Ebihara K., Ishida Y., Takeda R., Abe H., Matsuo H., Kawai K., Magata Y., Nishimori T. Differential expression of FosB, c-Fos, and Zif268 in forebrain regions after acute or chronic L-DOPA treatment in a rat model of Parkinson's disease. Neurosci. Lett. 2011, 496:90-94.
21. Espadas I., Darmopil S., Vergaño-Vera E., Ortiz O., Oliva I., Vicario-Abejón C., Martín E.D., Moratalla R. L-DOPA-induced increase in TH-immunoreactive striatal neurons in parkinsonian mice: insights into regulation and function. Neurobiol. Dis. 2012, 48:271-281.
22. Eve D.J., Nisbet A.P., Kingsbury A.E., Hewson E.L., Daniel S.E., Lees A.J., Marsden C.D., Foster O.J. Basal ganglia neuronal nitric oxide synthase mRNA expression in Parkinson's disease. Brain Res. Mol. Brain Res. 1998, 63:62-71.
23. Feelisch M. The use of nitric oxide donors in pharmacological studies. Naunyn Schmiedeberg's Arch. Pharmacol. 1998, 358:113-122.
24. Feyder M., Södersten E., Santini E., Vialou V., LaPlant Q.C., Watts E.L., Spigolon G., Hansen K., Caboche J., Nestler E., Fisone G. A role for mitogen- and stress-activated kinase 1 in L-DOPA-induced dyskinesia and δFosB expression. Biol. Psychiatry 2014, 10.1016/j.biopsych.2014.07.019.
25. Fisone G., Bezard E. Molecular mechanisms of l-DOPA-induced dyskinesia. Int. Rev. Neurobiol. 2011, 98:95-122.
26. Fuchs J., Mueller J.C., Lichtner P., Schulte C., Munz M., Berg D., Wüllner U., Illig T., Sharma M., Gasser T. The transcription factor PITX3 is associated with sporadic Parkinson's disease. Neurobiol. Aging 2009, 30:731-738.
27. Garthwaite J. Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 2008, 27:2783-2802.
28. Gerlach M., Riederer P., Scheller D. Mechanisms underlying and medical management of L-Dopa-associated motor complications. J. Neural Transm. 2011, 118:1659-1660.
29. Giorgi M., D'Angelo V., Esposito Z., Nuccetelli V., Sorge R., Martorana A., Stefani A., Bernardi G., Sancesario G. Lowered cAMP and cGMP signalling in the brain during levodopa-induced dyskinesias in hemiparkinsonian rats: new aspects in the pathogenetic mechanisms. Eur. J. Neurosci. 2008, 28:941-950.
30. González-Aparicio R., Moratalla R. Oleoylethanolamide reduces L-DOPA-induced dyskinesia via TRPV1 receptor in a mouse model of Parkinson's disease. Neurobiol. Dis. 2014, 62:416-425.
31. Granado N., O'Shea E., Bove J., Vila M., Colado M.I., Moratalla R. Persistent MDMA-induced dopaminergic neurotoxicity in the striatum and substantia nigra of mice. J. Neurochem. 2008, 107:1102-1112.
32. Granado N., Ares-Santos S., Oliva I., O'Shea E., Martin E.D., Colado M.I., Moratalla R. Dopamine D2-receptor knockout mice are protected against dopaminergic neurotoxicity induced by methamphetamine or MDMA. Neurobiol Dis. 2011, 42:391-403.
33. Huot P., Johnston T.H., Koprich J.B., Fox S.H., Brotchie J.M. The pharmacology of L-DOPA-induced dyskinesia in Parkinson's disease. Pharmacol. Rev. 2013, 65:171-222.
34. Hwang D.Y., Ardayfio P., Kang U.J., Semina E.V., Kim K.S. Selective loss of dopaminergic neurons in the substantia nigra of Pitx3-deficient aphakia mice. Brain Res. Mol. Brain Res. 2003, 114:123-131.
35. Hwang D.Y., Fleming S.M., Ardayfio P., Moran-Gates T., Kim H., Tarazi F.I., Chesselet M.F., Kim K.S. 3,4-dihydroxyphenylalanine reverses the motor deficits in Pitx3-deficient aphakia mice: behavioral characterization of a novel genetic model of Parkinson's disease. J. Neurosci. 2005, 25:2132-2137.
36. Iderberg H., Francardo V., Pioli E.Y. Animal models of L-DOPA-induced dyskinesia: an update on the current options. Neuroscience 2012, 211:13-27.
37. Iravani M.M., Jenner P. Mechanisms underlying the onset and expression of levodopa-induced dyskinesia and their pharmacological manipulation. J. Neural Transm. 2011, 118:1661-1690.
38. Itokawa K., Ohkuma A., Araki N., Tamura N., Shimazu K. Effect of L-DOPA on nitric oxide production in striatum of freely mobile mice. Neurosci. Lett. 2006, 402:142-144.
39. Itzhak Y. Modulation of cocaine- and methamphetamine-induced behavioral sensitization by inhibition of brain nitric oxide synthase. J. Pharmacol. Exp. Ther. 1997, 282:521-527.
40. Jankovic J. Motor fluctuations and dyskinesias in Parkinson's disease: clinical manifestations. Mov. Disord. 2005, 20(Suppl. 11):S11-S16.
41. Johnston T.H., Lee J., Gomez-Ramirez J., Fox S.H., Brotchie J.M. A simple rodent assay for the in vivo identification of agents with potential to reduce levodopa-induced dyskinesia in Parkinson's disease. Exp. Neurol. 2005, 191:243-250.
42. Kiss J.P., Vizi E.S. Nitric oxide: a novel link between synaptic and nonsynaptic transmission. Trends Neurosci. 2001, 24:211-215.
43. Li L., Zhou F.M. Parallel dopamine D1 receptor activity dependence of l-Dopa-induced normal movement and dyskinesia in mice. Neuroscience 2013, 236:66-76.
44. Lorenc-Koci E., Czarnecka A., Lenda T., Kamińska K., Konieczny J. Molsidomine, a nitric oxide donor, modulates rotational behavior and monoamine metabolism in 6-OHDA lesioned rats treated chronically with L-DOPA. Neurochem. Int. 2013, 63:790-804.
45. Lundblad M., Usiello A., Carta M., Håkansson K., Fisone G., Cenci M.A. Pharmacological validation of a mouse model of l-DOPA-induced dyskinesia. Exp. Neurol. 2005, 194:66-75.
46. Muñoz A., Li Q., Gardoni F., Marcello E., Qin C., Carlsson T., Kirik D., Di Luca M., Björklund A., Bezard E., Carta M. Combined 5-HT1A and 5-HT1B receptor agonists for the treatment of L-DOPA-induced dyskinesia. Brain 2008, 131:3380-3394.
47. Murer M.G., Moratalla R. Striatal signaling in L-DOPA-induced dyskinesia: common mechanisms with drug abuse and long term memory involving D1 dopamine receptor stimulation. Front. Neuroanat. 2011, 5:51.
48. Nishi A., Watanabe Y., Higashi H., Tanaka M., Nairn A.C., Greengard P. Glutamate regulation of DARPP-32 phosphorylation in neostriatal neurons involves activation of multiple signaling cascades. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1199-1204.
49. Novaretti N., Padovan-Neto F.E., Tumas V., da-Silva C.A., Del Bel E.A. Lack of tolerance for the anti-dyskinetic effects of 7-nitroindazole, a neuronal nitric oxide synthase inhibitor, in rats. Braz. J. Med. Biol. Res. 2010, 43:1047-1053.
50. Nunes I., Tovmasian L., Silva R.M., Burke R.E., Goff S.P. Pitx3 is required for development of substantia nigra dopaminergic neurons. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:4245-4250.
51. Ohno M., Watanabe S. Nitric oxide synthase inhibitors block behavioral sensitization to methamphetamine in mice. Eur. J. Pharmacol. 1995, 275:39-44.
52. Padovan-Neto F.E., Echeverry M.B., Tumas V., Del-Bel E.A. Nitric oxide synthase inhibition attenuates L-DOPA-induced dyskinesias in a rodent model of Parkinson's disease. Neuroscience 2009, 159:927-935.
53. Padovan-Neto F.E., Echeverry M.B., Chiavegatto S., Del-Bel E. Nitric oxide synthase inhibitor improves de novo and long-term l-DOPA-induced dyskinesia in hemiparkinsonian rats. Front. Syst. Neurosci. 2011, 5:40.
54. Padovan-Neto F.E., Ferreira N.R., de Oliveira-Tavares D., de Aguiar D., da Silva C.A., Raisman-Vozari R., Del Bel E. Anti-dyskinetic effect of the neuronal nitric oxide synthase inhibitor is linked to decrease of FosB/deltaFosB expression. Neurosci. Lett. 2013, 541:126-131.
55. Park D.J., West A.R. Regulation of striatal nitric oxide synthesis by local dopamine and glutamate interactions. J. Neurochem. 2009, 111:1457-1465.
56. Pavón N., Martín A.B., Mendialdua A., Moratalla R. ERK phosphorylation and FosB expression are associated with L-DOPA-induced dyskinesia in hemiparkinsonian mice. Biol. Psychiatry 2006, 59:64-74.
57. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego.
58. Picconi B., Bagetta V., Ghiglieri V., Paillè V., Di Filippo M., Pendolino V., Tozzi A., Giampà C., Fusco F.R., Sgobio C., Calabresi P. Inhibition of phosphodiesterases rescues striatal long-term depression and reduces levodopa-induced dyskinesia. Brain 2011, 134:375-387.
59. Prashanth L.K., Fox S., Meissner W.G. l-Dopa-induced dyskinesia-clinical presentation, genetics, and treatment. Int. Rev. Neurobiol. 2011, 98:31-54.
60. Ruiz-DeDiego I., Mellstrom B., Vallejo M., Naranjo J.R., Moratalla R. Activation of DREAM (downstream regulatory element antagonistic modulator), a calcium-binding protein, reduces L-DOPA-induced dyskinesias in mice. Biol. Psychiatry 2014, 10.1016/j.biopsych.2014.03.023.
61. Sammut S., Dec A., Mitchell D., Linardakis J., Ortiguela M., West A.R. 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 2006, 31:493-505.
62. Sancesario G., Giorgi M., D'Angelo V., Modica A., Martorana A., Morello M., Bengtson C.P., Bernardi G. Down-regulation of nitrergic transmission in the rat striatum after chronic nigrostriatal deafferentation. Eur. J. Neurosci. 2004, 20:989-1000.
63. Sanchez J.J., Abreu P., Gonzalez M.C. Sodium nitroprusside stimulates L-DOPA release from striatal tissue through nitric oxide and cGMP. Eur. J. Pharmacol. 2002, 438:79-83.
64. Santini E., Valjent E., Usiello A., Carta M., Borgkvist A., Girault J.A., Hervé D., Greengard P., Fisone G. Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPA-induced dyskinesia. J. Neurosci. 2007, 27:6995-7005.
65. Santini E., Alcacer C., Cacciatore S., Heiman M., Hervé D., Greengard P., Girault J.A., Valjent E., Fisone G. L-DOPA activates ERK signaling and phosphorylates histone H3 in the striatonigral medium spiny neurons of hemiparkinsonian mice. J. Neurochem. 2009, 108:621-633.
66. Santini E., Sgambato-Faure V., Li Q., Savasta M., Dovero S., Fisone G., Bezard E. Distinct changes in cAMP and extracellular signal-regulated protein kinase signalling in L-DOPA-induced dyskinesia. PLoS One 2010, 5:e12322.
67. Schapira A.H. Neurobiology and treatment of Parkinson's disease. Trends Pharmacol. Sci. 2009, 30:41-47.
68. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25years of image analysis. Nat. Methods 2012, 9:671-675.
69. Smidt M.P., Smits S.M., Bouwmeester H., Hamers F.P., van der Linden A.J., Hellemons A.J., Graw J., Burbach J.P. Early developmental failure of substantia nigra dopamine neurons in mice lacking the homeodomain gene Pitx3. Development 2004, 131:1145-1155.
70. Stipanovich A., Valjent E., Matamales M., Nishi A., Ahn J.H., Maroteaux M., Bertran-Gonzalez J., Brami-Cherrier K., Enslen H., Corbillé A.G., Filhol O., Nairn A.C., Greengard P., Hervé D., Girault J.A. A phosphatase cascade by which rewarding stimuli control nucleosomal response. Nature 2008, 453:879-884.
71. Suárez L.M., Solís O., Caramés J.M., Taravini I.R., Solís J.M., Murer M.G., Moratalla R. L-DOPA treatment selectively restores spine density in dopamine receptor D2-expressing projection neurons in dyskinetic mice. Biol. Psychiatry 2014, 75:711-722.
72. Takuma K., Tanaka T., Takahashi T., Hiramatsu N., Ota Y., Ago Y., Matsuda T. Neuronal nitric oxide synthase inhibition attenuates the development of L-DOPA-induced dyskinesia in hemi-Parkinsonian rats. Eur. J. Pharmacol. 2012, 683:166-173.
73. Tsankova N., Renthal W., Kumar A., Nestler E.J. Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 2007, 8:355-367.
74. van den Munckhof P., Luk K.C., Ste-Marie L., Montgomery J., Blanchet P.J., Sadikot A.F., Drouin J. Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons. Development 2003, 130:2535-2542.
75. van den Munckhof P., Gilbert F., Chamberland M., Lévesque D., Drouin J. Striatal neuroadaptation and rescue of locomotor deficit by L-dopa in aphakia mice, a model of Parkinson's disease. J. Neurochem. 2006, 96:160-170.
76. West A.R., Tseng K.Y. Nitric oxide-soluble guanylyl cyclase-cyclic GMP signaling in the striatum: new targets for the treatment of Parkinson's disease?. Front. Syst. Neurosci. 2011, 5:55.
77. Westin J.E., Vercammen L., Strome E.M., Konradi C., Cenci M.A. Spatiotemporal pattern of striatal ERK1/2 phosphorylation in a rat model of L-DOPA-induced dyskinesia and the role of dopamine D1 receptors. Biol. Psychiatry 2007, 62:800-810.