Animal models of l-DOPA-induced dyskinesia: An update on the current options

Neuroscience

Volumn 211, Issue , 2012, Pages 13-27

  Iderberg, H ^a   Francardo, V ^a   Pioli, E Y ^b  

^a LUND UNIVERSITY   (Sweden)

^b Williams House   (United Kingdom)

Author keywords

6 OHDA; Abnormal involuntary movements; Animal models; L DOPA induced dyskinesia; MPTP; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; AMANTADINE; ANTIPARKINSON AGENT; BROMOCRIPTINE; METABOTROPIC RECEPTOR; OXIDOPAMINE; ROPINIROLE;

ANIMAL MODEL; CALLITRICHINAE; CHOREA; DOPAMINE INDUCED DYSKINESIA; DYSKINESIA; DYSTONIA; GENETIC ENGINEERING; GENETIC MANIPULATION; HUMAN; INVOLUNTARY MOVEMENT; LOCOMOTION; MACACA; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; RELIABILITY; REVIEW; RISK FACTOR; SYNAPTIC TRANSMISSION; UNIFIED PARKINSON DISEASE RATING SCALE; VALIDITY;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; DYSKINESIA, DRUG-INDUCED; HUMANS; LEVODOPA; PARKINSON DISEASE; REPRODUCIBILITY OF RESULTS;

EID: 84860621650     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.03.023     Document Type: Review

References (178)

1. Ahlskog J.E., Muenter M.D. Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature. Mov Disord 2001, 16:448-458.
2. Ahmed M.R., Berthet A., Bychkov E., Porras G., Li Q., Bioulac B.H., Carl Y.T., Bloch B., Kook S., Aubert I., Dovero S., Doudnikoff E., Gurevich V.V., Gurevich E.V., Bezard E. Lentiviral overexpression of GRK6 alleviates l-dopa-induced dyskinesia in experimental Parkinson's disease. Sci Transl Med 2010, 2:28ra28.
3. Almirall H., Bautista V., Sánchez-Bahillo A., Trinidad-Herrero M. Ultradian and circadian body temperature and activity rhythms in chronic MPTP treated monkeys. Neurophysiol Clin 2001, 31:161-170.
4. Alvarez-Fischer D., Henze C., Strenzke C., Westrich J., Ferger B., Hoglinger G.U., Oertel W.H., Hartmann A. Characterization of the striatal 6-OHDA model of Parkinson's disease in wild type and alpha-synuclein-deleted mice. Exp Neurol 2008, 210:182-193.
5. 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.
6. Aubert I., Guigoni C., Li Q., Dovero S., Bioulac B.H., Gross C.E., Crossman A.R., Bloch B., Bezard E. Enhanced preproenkephalin-B-derived opioid transmission in striatum and subthalamic nucleus converges upon globus pallidus internalis in l-3,4-dihydroxyphenylalanine-induced dyskinesia. Biol Psychiatry 2007, 61:836-844.
7. Augood S.J., Emson P.C. Adenosine A2a receptor mRNA is expressed by enkephalin cells but not by somatostatin cells in rat striatum: a co-expression study. Brain Res Mol Brain Res 1994, 22:204-210.
8. Barraud Q., Lambrecq V., Forni C., McGuire S., Hill M., Bioulac B., Balzamo E., Bezard E., Tison F., Ghorayeb I. Sleep disorders in Parkinson's disease: the contribution of the MPTP non-human primate model. Exp Neurol 2009, 219:574-582.
9. Bélanger N., Grégoire L., Hadj Tahar A., Bedard P.J. Chronic treatment with small doses of cabergoline prevents dopa-induced dyskinesias in parkinsonian monkeys. Mov Disord 2003, 18:1436-1441.
10. Berg D., Godau J., Trenkwalder C., Eggert K., Csoti I., Storch A., Huber H., Morelli-Canelo M., Stamelou M., Ries V., Wolz M., Schneider C., Di Paolo T., Gasparini F., Hariry S., Vandemeulebroecke M., Abi-Saab W., Cooke K., Johns D., Gomez-Mancilla B. AFQ056 treatment of levodopa-induced dyskinesias: results of 2 randomized controlled trials. Mov Disord 2011, 26:1243-1250.
11. Berton O., Guigoni C., Li Q., Bioulac B.H., Aubert I., Gross C.E., Dileone R.J., Nestler E.J., Bezard E. Striatal overexpression of DeltaJunD resets l-DOPA-induced dyskinesia in a primate model of Parkinson disease. Biol Psychiatry 2009, 66:554-561.
12. Bezard E., Brotchie J.M., Gross C.E. Pathophysiology of levodopa-induced dyskinesia: potential for new therapies. Nat Rev Neurosci 2001, 2:577-588.
13. Bezard E., Dovero S., Prunier C., Ravenscroft P., Chalon S., Guilloteau D., Bioulac B., Brotchie J.M., Gross C.E. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease. J Neurosci 2001, 21:6853-6861.
14. Bézard E., Ferry S., Mach U., Stark H., Leriche L., Boraud T., Gross C.E., Sokoloff P. Attenuation of levodopa-induced dyskinesia by normalizing dopamine D3 receptor function. Nat Med 2003, 9:762-767.
15. Bezard E., Hill M.P., Crossman A.R., Brotchie J.M., Michel A., Grimee R., Klitgaard H. Levetiracetam improves choreic levodopa-induced dyskinesia in the MPTP-treated macaque. Eur J Pharmacol 2004, 485:159-164.
16. Bezard E., Imbert C., Deloire X., Bioulac B., Gross C. A chronic MPTP model reproducing the slow evolution of Parkinson's disease: evolution of motor symptoms in the monkey. Brain Res 1997, 766:107-112.
17. Bezard E., Przedborski S. A tale on animal models of Parkinson's disease. Mov Disord 2011, 26:993-1002.
18. Bibbiani F., Oh J.D., Petzer J.P., Castagnoli N., Chen J.F., Schwarzschild M.A., Chase T.N. A2A antagonist prevents dopamine agonist-induced motor complications in animal models of Parkinson's disease. Exp Neurol 2003, 184:285-294.
19. 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.
20. Blanchet P.J., Konitsiotis S., Chase T.N. Amantadine reduces levodopa-induced dyskinesias in parkinsonian monkeys. Mov Disord 1998, 13:798-802.
21. Blandini F., Armentero M.T., Martignoni E. The 6-hydroxydopamine model: news from the past. Parkinsonism Relat Disord 2008, 14(Suppl 2):S124-S129.
22. Bonifati V., Fabrizio E., Cipriani R., Vanacore N., Meco G. Buspirone in levodopa-induced dyskinesias. Clin Neuropharmacol 1994, 17:73-82.
23. Bordia T., McIntosh J.M., Quik M. Nicotine reduces antipsychotic-induced orofacial dyskinesia in rats. J Pharmacol Exp Ther 2012, 340:612-619.
24. Boyce S., Clarke C.E., Luquin R., Peggs D., Robertson R.G., Mitchell I.J., Sambrook M.A., Crossman A.R. Induction of chorea and dystonia in parkinsonian primates. Mov Disord 1990, 5:3-7.
25. Burns R.S., Chiueh C.C., Markey S.P., Ebert M.H., Jacobowitz D.M., Kopin I.J. A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc Natl Acad Sci U S A 1983, 80:4546-4550.
26. Cao X., Yasuda T., Uthayathas S., Watts R.L., Mouradian M.M., Mochizuki H., Papa S.M. Striatal overexpression of DeltaFosB reproduces chronic levodopa-induced involuntary movements. J Neurosci 2010, 30:7335-7343.
27. Carta A.R., Frau L., Pinna A., Pontis S., Simola N., Schintu N., Morelli M. Behavioral and biochemical correlates of the dyskinetic potential of dopaminergic agonists in the 6-OHDA lesioned rat. Synapse 2008, 62:524-533.
28. Carta M., Bezard E. Contribution of pre-synaptic mechanisms to l-DOPA-induced dyskinesia. Neuroscience 2011, 198:245-251.
29. Carta M., Carlsson T., Kirik D., Bjorklund A. Dopamine released from 5-HT terminals is the cause of l-DOPA-induced dyskinesia in parkinsonian rats. Brain 2007, 130:1819-1833.
30. Carta M., Lindgren H.S., Lundblad M., Stancampiano R., Fadda F., Cenci M.A. Role of striatal l-DOPA in the production of dyskinesia in 6-hydroxydopamine lesioned rats. J Neurochem 2006, 96:1718-1727.
31. Cenci M.A., Konradi C. Maladaptive striatal plasticity in l-DOPA-induced dyskinesia. Recent advances in Parkinson's disease: translational and clinical research. Prog Brain Res 2010, 183:209-233.
32. Cenci M.A., Lee C.S., Bjorklund A. l-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur J Neurosci 1998, 10:2694-2706.
33. Cenci M.A., Lundblad M. Utility of 6-hydroxydopamine lesioned rats in the preclinical screening of novel treatments for Parkinson's disease. Animal models of movement disorders 2005, 193-208. Elsevier Academic Press, San Diego. M. LeDoux (Ed.).
34. Cenci M.A., Lundblad M. Ratings of l-DOPA-induced dyskinesia in the unilateral 6-OHDA lesion model of Parkinson's disease in rats and mice. Curr Protoc Neurosci 2007, Chapter 9:Unit 9 25.
35. Cenci M.A., Ohlin K.E., Odin P. Current options and future possibilities for the treatment of dyskinesia and motor fluctuations in Parkinson's disease. CNS Neurol Disord Drug Targets 2011, 10:670-684.
36. Cenci M.A., Whishaw I.Q., Schallert T. Animal models of neurological deficits: how relevant is the rat?. Nat Rev Neurosci 2002, 3:574-579.
37. Chaumette T., Lebouvier T., Aubert P., Lardeux B., Qin C., Li Q., Accary D., Bezard E., Bruley des Varannes S., Derkinderen P., Neunlist M. Neurochemical plasticity in the enteric nervous system of a primate animal model of experimental Parkinsonism. Neurogastroenterol Motil 2009, 21:215-222.
38. Chesselet M.F. In vivo alpha-synuclein overexpression in rodents: a useful model of Parkinson's disease?. Exp Neurol 2008, 209:22-27.
39. Chesselet M.F., Fleming S., Mortazavi F., Meurers B. Strengths and limitations of genetic mouse models of Parkinson's disease. Parkinsonism Relat Disord 2008, 14(Suppl 2):S84-S87.
40. Clarke C.E., Sambrook M.A., Mitchell I.J., Crossman A.R. Levodopa-induced dyskinesia and response fluctuations in primates rendered parkinsonian with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). J Neurol Sci 1987, 78:273-280.
41. da Silva-Júnior F.P., Braga-Neto P., Sueli Monte F., de Bruin V.M. Amantadine reduces the duration of levodopa-induced dyskinesia: a randomized, double-blind placebo-controlled study. Parkinsonism Relat Disord 2005, 11:449-452.
42. 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.
43. Date I., Felten D.L., Felten S.Y. Long-term effect of MPTP in the mouse brain in relation to aging: neurochemical and immunocytochemical analysis. Brain Res 1990, 519:266-276.
44. Dawson T.M., Ko H.S., Dawson V.L. Genetic animal models of Parkinson's disease. Neuron 2010, 66:646-661.
45. de la Fuente-Fernández R., Sossi V., Huang Z., Furtado S., Lu J.Q., Calne D.B., Ruth T.J., Stoessl A.J. Levodopa-induced changes in synaptic dopamine levels increase with progression of Parkinson's disease: implications for dyskinesias. Brain 2004, 127:2747-2754.
46. Decamp E., Schneider J.S. Interaction between nicotinic and dopaminergic therapies on cognition in a chronic Parkinson model. Brain Res 2009, 1262:109-114.
47. Dekundy A., Lundblad M., Danysz W., Cenci M.A. Modulation of l-DOPA-induced abnormal involuntary movements by clinically tested compounds: further validation of the rat dyskinesia model. Behav Brain Res 2007, 179:76-89.
48. 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.
49. 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.
50. Dubach M., Schmidt R., Kunkel D., Bowden D.M., Martin R., German D.C. Primate neostriatal neurons containing tyrosine hydroxylase: immunohistochemical evidence. Neurosci Lett 1987, 75:205-210.
51. Dupre K.B., Ostock C.Y., Eskow Jaunarajs K.L., Button T., Savage L.M., Wolf W., Bishop C. Local modulation of striatal glutamate efflux by serotonin 1A receptor stimulation in dyskinetic, hemiparkinsonian rats. Exp Neurol 2011, 229:288-299.
52. Eskow K.L., Gupta V., Alam S., Park J.Y., Bishop C. The partial 5-HT(1A) agonist buspirone reduces the expression and development of l-DOPA-induced dyskinesia in rats and improves l-DOPA efficacy. Pharmacol Biochem Behav 2007, 87:306-314.
53. Fasano S., Bezard E., D'Antoni A., Francardo V., Indrigo M., Qin L., Dovero S., Cerovic M., Cenci M.A., Brambilla R. Inhibition of Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) signaling in the striatum reverts motor symptoms associated with l-dopa-induced dyskinesia. Proc Natl Acad Sci U S A 2010, 107:21824-21829.
54. Fleming S.M. Cardiovascular autonomic dysfunction in animal models of Parkinson's disease. J Parkinson's Dis 2011, 1:321-327.
55. Fox S., Silverdale M., Kellett M., Davies R., Steiger M., Fletcher N., Crossman A., Brotchie J. Non-subtype-selective opioid receptor antagonism in treatment of levodopa-induced motor complications in Parkinson's disease. Mov Disord 2004, 19:554-560.
56. Fox S.H., Brotchie J.M. The MPTP-lesioned non-human primate models of Parkinson's disease. Past, present, and future. Prog Brain Res 2010, 184:133-157.
57. Fox S.H., Visanji N.P., Johnston T.H., Gomez-Ramirez J., Voon V., Brotchie J.M. Dopamine receptor agonists and levodopa and inducing psychosis-like behavior in the MPTP primate model of Parkinson disease. Arch Neurol 2006, 63:1343-1344.
58. Francardo V., Recchia A., Popovic N., Andersson D., Nissbrandt H., Cenci M.A. Impact of the lesion procedure on the profiles of motor impairment and molecular responsiveness to l-DOPA in the 6-hydroxydopamine mouse model of Parkinson's disease. Neurobiol Dis 2011, 42:327-340.
59. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J.Q., Eidelberg D., Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 2001, 344:710-719.
60. Gautier C.A., Kitada T., Shen J. Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci U S A 2008, 105:11364-11369.
61. Gerlach M., Bartoszyk G.D., Riederer P., Dean O., van den Buuse M. Role of dopamine D3 and serotonin 5-HT 1A receptors in l: -DOPA-induced dyskinesias and effects of sarizotan in the 6-hydroxydopamine-lesioned rat model of Parkinson's disease. J Neural Transm 2011, 118:1733-1742.
62. Gispert S., Ricciardi F., Kurz A., Azizov M., Hoepken H.H., Becker D., Voos W., Leuner K., Muller W.E., Kudin A.P., Kunz W.S., Zimmermann A., Roeper J., Wenzel D., Jendrach M., Garcia-Arencibia M., Fernandez-Ruiz J., Huber L., Rohrer H., Barrera M., Reichert A.S., Rub U., Chen A., Nussbaum R.L., Auburger G. Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One 2009, 4:e5777.
63. Goetz C.G., Damier P., Hicking C., Laska E., Muller T., Olanow C.W., Rascol O., Russ H. Sarizotan as a treatment for dyskinesias in Parkinson's disease: a double-blind placebo-controlled trial. Mov Disord 2007, 22:179-186.
64. Goetz C.G., Laska E., Hicking C., Damier P., Muller T., Nutt J., Warren Olanow C., Rascol O., Russ H. Placebo influences on dyskinesia in Parkinson's disease. Mov Disord 2008, 23:700-707.
65. Gold S.J., Hoang C.V., Potts B.W., Porras G., Pioli E., Kim K.W., Nadjar A., Qin C., LaHoste G.J., Li Q., Bioulac B.H., Waugh J.L., Gurevich E., Neve R.L., Bezard E. RGS9-2 negatively modulates l-3,4-dihydroxyphenylalanine-induced dyskinesia in experimental Parkinson's disease. J Neurosci 2007, 27:14338-14348.
66. Goldberg M.S., Pisani A., Haburcak M., Vortherms T.A., Kitada T., Costa C., Tong Y., Martella G., Tscherter A., Martins A., Bernardi G., Roth B.L., Pothos E.N., Calabresi P., Shen J. Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron 2005, 45:489-496.
67. Grealish S., Mattsson B., Draxler P., Bjorklund A. Characterisation of behavioral and neurodegenerative changes induced by intranigral 6-hydroxydopamine lesions in a mouse model of Parkinson's disease. Eur J Neurosci 2010, 31:2266-2278.
68. Grégoire L., Morin N., Ouattara B., Gasparini F., Bilbe G., Johns D., Vranesic I., Sahasranaman S., Gomez-Mancilla B., Di Paolo T. The acute antiparkinsonian and antidyskinetic effect of AFQ056, a novel metabotropic glutamate receptor type 5 antagonist, in l-Dopa-treated parkinsonian monkeys. Parkinsonism Relat Disord 2011, 17:270-276.
69. Grégoire L., Samadi P., Graham J., Bedard P.J., Bartoszyk G.D., Di Paolo T. Low doses of sarizotan reduce dyskinesias and maintain antiparkinsonian efficacy of l-Dopa in parkinsonian monkeys. Parkinsonism Relat Disord 2009, 15:445-452.
70. Grondin R., Bédard P.J., Hadj Tahar A., Gregoire L., Mori A., Kase H. Antiparkinsonian effect of a new selective adenosine A2A receptor antagonist in MPTP-treated monkeys. Neurology 1999, 52:1673-1677.
71. Guigoni C., Li Q., Aubert I., Dovero S., Bioulac B.H., Bloch B., Crossman A.R., Gross C.E., Bezard E. Involvement of sensorimotor, limbic, and associative basal ganglia domains in l-3,4-dihydroxyphenylalanine-induced dyskinesia. J Neurosci 2005, 25:2102-2107.
72. Hadj Tahar A., Grégoire L., Darré A., Belanger N., Meltzer L., Bedard P.J. Effect of a selective glutamate antagonist on l-dopa-induced dyskinesias in drug-naive parkinsonian monkeys. Neurobiol Dis 2004, 15:171-176.
73. Hagell P., Cenci M.A. Dyskinesias and dopamine cell replacement in Parkinson's disease: a clinical perspective. Brain Res Bull 2005, 68:4-15.
74. Hauber W., Neuscheler P., Nagel J., Muller C.E. Catalepsy induced by a blockade of dopamine D1 or D2 receptors was reversed by a concomitant blockade of adenosine A(2A) receptors in the caudate-putamen of rats. Eur J Neurosci 2001, 14:1287-1293.
75. Hauser R.A., Cantillon M., Pourcher E., Micheli F., Mok V., Onofrj M., Huyck S., Wolski K. Preladenant in patients with Parkinson's disease and motor fluctuations: a phase 2, double-blind, randomised trial. Lancet Neurol 2011, 10:221-229.
76. Henry B., Crossman A.R., Brotchie J.M. Characterization of enhanced behavioral responses to l-DOPA following repeated administration in the 6-hydroxydopamine-lesioned rat model of Parkinson's disease. Exp Neurol 1998, 151:334-342.
77. Henry B., Duty S., Fox S.H., Crossman A.R., Brotchie J.M. Increased striatal pre-proenkephalin B expression is associated with dyskinesia in Parkinson's disease. Exp Neurol 2003, 183:458-468.
78. Henry B., Fox S.H., Crossman A.R., Brotchie J.M. Mu- and delta-opioid receptor antagonists reduce levodopa-induced dyskinesia in the MPTP-lesioned primate model of Parkinson's disease. Exp Neurol 2001, 171:139-146.
79. Hill M.P., Ravenscroft P., Bezard E., Crossman A.R., Brotchie J.M., Michel A., Grimee R., Klitgaard H. Levetiracetam potentiates the antidyskinetic action of amantadine in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-lesioned primate model of Parkinson's disease. J Pharmacol Exp Ther 2004, 310:386-394.
80. Hope B.T., Nye H.E., Kelz M.B., Self D.W., Iadarola M.J., Nakabeppu Y., Duman R.S., Nestler E.J. Induction of a long-lasting AP-1 complex composed of altered Fos-like proteins in brain by chronic cocaine and other chronic treatments. Neuron 1994, 13:1235-1244.
81. Hsu A., Togasaki D.M., Bezard E., Sokoloff P., Langston J.W., Di Monte D.A., Quik M. Effect of the D3 dopamine receptor partial agonist BP897 [N-[4-(4-(2-methoxyphenyl)piperazinyl)butyl]-2-naphthamide] on l-3,4-dihydroxyphenylalanine-induced dyskinesias and parkinsonism in squirrel monkeys. J Pharmacol Exp Ther 2004, 311:770-777.
82. Huot P., Johnston T.H., Lewis K.D., Koprich J.B., Reyes M.G., Fox S.H., Piggott M.J., Brotchie J.M. Characterization of 3,4-methylenedioxymethamphetamine (MDMA) enantiomers in vitro and in the MPTP-lesioned primate: R-MDMA reduces severity of dyskinesia, whereas S-MDMA extends duration of ON-time. J Neurosci 2010, 31:7190-7198.
83. Huot P., Parent A. Dopaminergic neurons intrinsic to the striatum. J Neurochem 2007, 101:1441-1447.
84. Imbert C., Bezard E., Guitraud S., Boraud T., Gross C.E. Comparison between eight clinical rating scales used for the assessment of MPTP-induced parkinsonism in the macaque monkey. J Neurosci Methods 2000, 96:71-76.
85. Itier J.M., Ibanez P., Mena M.A., Abbas N., Cohen-Salmon C., Bohme G.A., Laville M., Pratt J., Corti O., Pradier L., Ret G., Joubert C., Periquet M., Araujo F., Negroni J., Casarejos M.J., Canals S., Solano R., Serrano A., Gallego E., Sanchez M., Denefle P., Benavides J., Tremp G., Rooney T.A., Brice A., Garcia de Yebenes J. Parkin gene inactivation alters behavior and dopamine neurotransmission in the mouse. Hum Mol Genet 2003, 12:2277-2291.
86. Jackson-Lewis V., Przedborski S. Protocol for the MPTP mouse model of Parkinson's disease. Nat Protoc 2007, 2:141-151.
87. Jan C., Pessiglione M., Tremblay L., Tande D., Hirsch E.C., Francois C. Quantitative analysis of dopaminergic loss in relation to functional territories in MPTP-treated monkeys. Eur J Neurosci 2003, 18:2082-2086.
88. Jankovic J., Stacy M. Medical management of levodopa-associated motor complications in patients with Parkinson's disease. CNS Drugs 2007, 21:677-692.
89. Jenner P. Molecular mechanisms of l-DOPA-induced dyskinesia. Nat Rev Neurosci 2008, 9:665-677.
90. Jenner P., Rupniak N.M., Rose S., Kelly E., Kilpatrick G., Lees A., Marsden C.D. 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism in the common marmoset. Neurosci Lett 1984, 50:85-90.
91. Johansson P.A., Andersson M., Andersson K.E., Cenci M.A. Alterations in cortical and basal ganglia levels of opioid receptor binding in a rat model of l-dopa-induced dyskinesia. Neurobiol Dis 2001, 8:220-239.
92. Johansson P.A., Andersson M., Andersson K.E., Cenci M.A. Alterations in cortical and basal ganglia levels of opioid receptor binding in a rat model of l-DOPA-induced dyskinesia. Neurobiol Dis 2001, 8:220-239.
93. Jollivet C., Montero-Menei C.N., Venier-Julienne M.C., Sapin A., Benoit J.P., Menei P. Striatal tyrosine hydroxylase immunoreactive neurons are induced by l-dihydroxyphenylalanine and nerve growth factor treatment in 6-hydroxydopamine lesioned rats. Neurosci Lett 2004, 362:79-82.
94. Kitada T., Pisani A., Porter D.R., Yamaguchi H., Tscherter A., Martella G., Bonsi P., Zhang C., Pothos E.N., Shen J. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A 2007, 104:11441-11446.
95. Kobylecki C., Cenci M.A., Crossman A.R., Ravenscroft P. Calcium-permeable AMPA receptors are involved in the induction and expression of l-DOPA-induced dyskinesia in Parkinson's disease. J Neurochem 2010, 114:499-511.
96. Kobylecki C., Hill M.P., Crossman A.R., Ravenscroft P. Synergistic antidyskinetic effects of topiramate and amantadine in animal models of Parkinson's disease. Mov Disord 2011, 26:2354-2363.
97. Koprich J.B., Fox S.H., Johnston T.H., Goodman A., Le Bourdonnec B., Dolle R.E., DeHaven R.N., DeHaven-Hudkins D.L., Little P.J., Brotchie J.M. The selective mu-opioid receptor antagonist ADL5510 reduces levodopa-induced dyskinesia without affecting antiparkinsonian action in MPTP-lesioned macaque model of Parkinson's disease. Mov Disord 2011, 26:1225-1233.
98. Lane E.L., Bjorklund A., Dunnett S.B., Winkler C. Neural grafting in Parkinson's disease unraveling the mechanisms underlying graft-induced dyskinesia. Recent advances in Parkinson's disease: translational and clinical research 2010, 184:295-309.
99. Langston J.W., Ballard P.A., Tetrud J.W., Irwin I. Chronic parkinsonism in human due to a product of meperidine analog synthesis. Science 1983, 219:979-980.
100. Langston J.W., Quik M., Petzinger G., Jakowec M., Di Monte D.A. Investigating levodopa-induced dyskinesias in the parkinsonian primate. Ann Neurol 2000, 47:S79-S89.
101. Lee C.S., Cenci M.A., Schulzer M., Bjorklund A. Embryonic ventral mesencephalic grafts improve levodopa-induced dyskinesia in a rat model of Parkinson's disease. Brain 2000, 123(Pt 7):1365-1379.
102. Lelos M.J., Dunnett S.B. Aberrant dopamine transmission and cognitive dysfunction in animal models of Parkinson's disease. Journal of Parkinson's Disease 2011, 1:151-165.
103. Levandis G., Bazzini E., Armentero M.T., Nappi G., Blandini F. Systemic administration of an mGluR5 antagonist, but not unilateral subthalamic lesion, counteracts l-DOPA-induced dyskinesias in a rodent model of Parkinson's disease. Neurobiol Dis 2008, 29:161-168.
104. Li X., Patel J.C., Wang J., Avshalumov M.V., Nicholson C., Buxbaum J.D., Elder G.A., Rice M.E., Yue Z. Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson's disease mutation G2019S. J Neurosci 2010, 30:1788-1797.
105. Li Y., Liu W., Oo T.F., Wang L., Tang Y., Jackson-Lewis V., Zhou C., Geghman K., Bogdanov M., Przedborski S., Beal M.F., Burke R.E., Li C. Mutant LRRK2(R1441G) BAC transgenic mice recapitulate cardinal features of Parkinson's disease. Nat Neurosci 2009, 12:826-828.
106. Lindgren H.S., Andersson D.R., Lagerkvist S., Nissbrandt H., Cenci M.A. l-DOPA-induced dopamine efflux in the striatum and the substantia nigra in a rat model of Parkinson's disease: temporal and quantitative relationship to the expression of dyskinesia. J Neurochem 2010, 112:1465-1476.
107. Lindgren H.S., Ohlin K.E., Cenci M.A. Differential involvement of D1 and D2 dopamine receptors in l-DOPA-induced angiogenic activity in a rat model of Parkinson's disease. Neuropsychopharmacology 2009, 34:2477-2488.
108. Lindgren H.S., Rylander D., Iderberg H., Andersson M., O'Sullivan S.S., Williams D.R., Lees A.J., Cenci M.A. Putaminal upregulation of FosB/FosB-like immunoreactivity in Parkinson's disease patients with dyskinesia. J Parkinson's Dis 2011, 1:347-357.
109. Lindgren H.S., Rylander D., Ohlin K.E., Lundblad M., Cenci M.A. The "motor complication syndrome" in rats with 6-OHDA lesions treated chronically with l-DOPA: relation to dose and route of administration. Behav Brain Res 2007, 177:150-159.
110. Luginger E., Wenning G.K., Bösch S., Poewe W. Beneficial effects of amantadine on l-dopa-induced dyskinesias in Parkinson's disease. Mov Disord 2000, 15:873-878.
111. Lundblad M., Andersson M., Winkler C., Kirik D., Wierup N., Cenci M.A. Pharmacological validation of behavioral measures of akinesia and dyskinesia in a rat model of Parkinson's disease. Eur J Neurosci 2002, 15:120-132.
112. Lundblad M., Picconi B., Lindgren H., Cenci M.A. A model of l-DOPA-induced dyskinesia in 6-hydroxydopamine lesioned mice: relation to motor and cellular parameters of nigrostriatal function. Neurobiol Dis 2004, 16:110-123.
113. Lundblad M., Usiello A., Carta M., Hakansson K., Fisone G., Cenci M.A. Pharmacological validation of a mouse model of l-dopa-induced dyskinesia. Exp Neurol 2005, 194:66-75.
114. Lundblad M., Vaudano E., Cenci M.A. Cellular and behavioral effects of the adenosine A2a receptor antagonist KW-6002 in a rat model of l-DOPA-induced dyskinesia. J Neurochem 2003, 84:1398-1410.
115. Luquin M.R., Scipioni O., Vaamonde J., Gershanik O., Obeso J.A. Levodopa-induced dyskinesias in Parkinson's disease: clinical and pharmacological classification. Mov Disord 1992, 7:117-124.
116. Maratos E.C., Jackson M.J., Pearce R.K., Jenner P. Antiparkinsonian activity and dyskinesia risk of ropinirole and l-DOPA combination therapy in drug naive MPTP-lesioned common marmosets (Callithrix jacchus). Mov Disord 2001, 16:631-641.
117. Marin C., Bonastre M., Aguilar E., Jimenez A. The metabotropic glutamate receptor antagonist 2-methyl-6-(phenylethynyl) pyridine decreases striatal VGlut2 expression in association with an attenuation of l-dopa-induced dyskinesias. Synapse 2011, 65:1080-1086.
118. Marsden C.D., Parkes J.D., Quinn N. Fluctuations of disability in Parkinson's disease-clinical aspects. Movement disorders 1982, 96-122. Butterworths, London. C.D. Marsden, S. Fahn (Eds.).
119. Masuda M., Miura M., Inoue R., Imanishi M., Saino-Saito S., Takada M., Kobayashi K., Aosaki T. Postnatal development of tyrosine hydroxylase mRNA-expressing neurons in mouse neostriatum. Eur J Neurosci 2011, 34:1355-1367.
120. Meissner W., Ravenscroft P., Reese R., Harnack D., Morgenstern R., Kupsch A., Klitgaard H., Bioulac B., Gross C.E., Bezard E., Boraud T. Increased slow oscillatory activity in substantia nigra pars reticulata triggers abnormal involuntary movements in the 6-OHDA-lesioned rat in the presence of excessive extracellular striatal dopamine. Neurobiol Dis 2006, 22:586-598.
121. Meissner W.G., Frasier M., Gasser T., Goetz C.G., Lozano A., Piccini P., Obeso J.A., Rascol O., Schapira A., Voon V., Weiner D.M., Tison F., Bezard E. Priorities in Parkinson's disease research. Nat Rev Drug Discov 2011, 10(5):377-393.
122. Mela F., Marti M., Bido S., Cenci M.A., Morari M. In vivo evidence for a differential contribution of striatal and nigral D1 and D2 receptors to l-DOPA induced dyskinesia and the accompanying surge of nigral amino acid levels. Neurobiol Dis 2012, 45:573-582.
123. Mela F., Marti M., Dekundy A., Danysz W., Morari M., Cenci M.A. Antagonism of metabotropic glutamate receptor type 5 attenuates l-DOPA-induced dyskinesia and its molecular and neurochemical correlates in a rat model of Parkinson's disease. J Neurochem 2007, 101:483-497.
124. Melamed E. Early-morning dystonia. A late side effect of long-term levodopa therapy in Parkinson's disease. Arch Neurol 1979, 36:308-310.
125. Meredith G.E., Farrell T., Kellaghan P., Tan Y., Zahm D.S., Totterdell S. Immunocytochemical characterization of catecholaminergic neurons in the rat striatum following dopamine-depleting lesions. Eur J Neurosci 1999, 11:3585-3596.
126. Miguelez C., Aristieta A., Cenci M.A., Ugedo L. The locus coeruleus is directly implicated in l-DOPA-induced dyskinesia in parkinsonian rats: an electrophysiological and behavioral study. PLoS One 2011, 6:e24679.
127. Mitsumoto Y., Watanabe A., Mori A., et al. Spontaneous regeneration of nigrostriatal dopaminergic neurons in MPTP-treated C57BL/6 mice. Biochem Biophys Res Commun 1998, 248:660-663.
128. Muñoz A., Li Q., Gardoni F., Marcello E., Qin C., Carlsson T., Kirik D., Di Luca M., Bjorklund 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.
129. Nadjar A., Gerfen C.R., Bezard E. Priming for l-dopa-induced dyskinesia in Parkinson's disease: a feature inherent to the treatment or the disease?. Prog Neurobiol 2009, 87:1-9.
130. Nahimi A., Høltzermann M., Landau A.M., Simonsen M., Jakobsen S., Alstrup A.K., Vang K., Moller A., Wegener G., Gjedde A., Doudet D.J. Serotonergic modulation of receptor occupancy in rats treated with l-DOPA after unilateral 6-OHDA lesioning. J Neurochem 2012, 120:806-817.
131. Nicholas A.P. Levodopa-induced hyperactivity in mice treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Mov Disord 2007, 22:99-104.
132. Ohlin K.E., Francardo V., Lindgren H.S., Sillivan S.E., O'Sullivan S.S., Luksik A.S., Vassoler F.M., Lees A.J., Konradi C., Cenci M.A. Vascular endothelial growth factor is upregulated by l-dopa in the parkinsonian brain: implications for the development of dyskinesia. Brain 2011, 134:2339-2357.
133. Ostock C.Y., Dupre K.B., Jaunarajs K.L., Walters H., George J., Krolewski D., Walker P.D., Bishop C. Role of the primary motor cortex in l-DOPA-induced dyskinesia and its modulation by 5-HT1A receptor stimulation. Neuropharmacology 2011, 61:753-760.
134. Ouattara B., Belkhir S., Morissette M., Dridi M., Samadi P., Gregoire L., Meltzer L.T., Di Paolo T. Implication of NMDA receptors in the antidyskinetic activity of cabergoline, CI-1041, and Ro 61-8048 in MPTP monkeys with levodopa-induced dyskinesias. J Mol Neurosci 2009, 38:128-142.
135. Paillé V., Henry V Lescaudron L., Brachet P., Damier P. Rat model of Parkinson's disease with bilateral motor abnormalities, reversible with levodopa, and dyskinesias. Mov Disord 2007, 22:533-539.
136. Palfi S., Leventhal L., Chu Y., Ma S.Y., Emborg M., Bakay R., Deglon N., Hantraye P., Aebischer P., Kordower J.H. Lentivirally delivered glial cell line-derived neurotrophic factor increases the number of striatal dopaminergic neurons in primate models of nigrostriatal degeneration. J Neurosci 2002, 22:4942-4954.
137. Papa S.M., Engber T.M., Kask A.M., Chase T.N. Motor fluctuations in levodopa treated parkinsonian rats: relation to lesion extent and treatment duration. Brain Res 1994, 662:69-74.
138. 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.
139. Pearce R.K., Banerji T., Jenner P., Marsden C.D. De novo administration of ropinirole and bromocriptine induces less dyskinesia than l-dopa in the MPTP-treated marmoset. Mov Disord 1998, 13:234-241.
140. Pearce R.K., Jackson M., Smith L., Jenner P., Marsden C.D. Chronic l-dopa administration induces dyskinesias in the MPTP-treated common marmoset (Callithrix Jacchus). Mov Disord 1995, 10:731-740.
141. Perez F.A., Palmiter R.D. Parkin-deficient mice are not a robust model of parkinsonism. Proc Natl Acad Sci U S A 2005, 102:2174-2179.
142. Piccini P., Morrish P.K., Turjanski N., Sawle G.V., Burn D.J., Weeks R.A., Mark M.H., Maraganore D.M., Lees A.J., Brooks D.J. Dopaminergic function in familial Parkinson's disease: a clinical and 18F-dopa positron emission tomography study. Ann Neurol 1997, 41:222-229.
143. Piccini P., Weeks R.A., Brooks D.J. Alterations in opioid receptor binding in Parkinson's disease patients with levodopa-induced dyskinesias. Ann Neurol 1997, 42:720-726.
144. Picconi B., Centonze D., Håkansson K., Bernardi G., Greengard P., Fisone G., Cenci M.A., Calabresi P. Loss of bidirectional striatal synaptic plasticity in l-DOPA-induced dyskinesia. Nat Neurosci 2003, 6:501-506.
145. Pifl C., Schingnitz G., Hornykiewicz O. Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on the regional distribution of brain monoamines in the rhesus monkey. Neuroscience 1991, 44:591-605.
146. Porras G., Qin L., Bezard E. Modeling Parkinson's disease in primates: the MPTP model. Cold Spring Harb Perspect Med 2012, 2:a009308.
147. Prashanth L.K., Fox S., Meissner W.G. l-Dopa-induced dyskinesia-clinical presentation, genetics, and treatment. Int Rev Neurobiol 2011, 98:31-54.
148. Quik M., Cox H., Parameswaran N., O'Leary K., Langston J.W., Di Monte D. Nicotine reduces levodopa-induced dyskinesias in lesioned monkeys. Ann Neurol 2007, 62:588-596.
149. Rascol O., Brooks D.J., Korczyn A.D., De Deyn P.P., Clarke C.E., Lang A.E. A five-year study of the incidence of dyskinesia in patients with early Parkinson's disease who were treated with ropinirole or levodopa. 056 Study Group. N Engl J Med 2000, 342:1484-1491.
150. Rascol O., Fabre N., Blin O., Poulik J., Sabatini U., Senard J.M., Ane M., Montastruc J.L., Rascol A. Naltrexone, an opiate antagonist, fails to modify motor symptoms in patients with Parkinson's disease. Mov Disord 1994, 9:437-440.
151. Ravenscroft P., Chalon S., Brotchie J.M., Crossman A.R. Ropinirole versus l-DOPA effects on striatal opioid peptide precursors in a rodent model of Parkinson's disease: implications for dyskinesia. Exp Neurol 2004, 185:36-46.
152. Reiner A., Medina L., Veenman C.L. Structural and functional evolution of the basal ganglia in vertebrates. Brain Res Brain Res Rev 1998, 28:235-285.
153. Rylander D. The serotonin system: a potential target for anti-dyskinetic treatments and biomarker discovery. Parkinsonism Relat Disord 2012, 18(Suppl 1):S126-S128.
154. Rylander D., Iderberg H., Li Q., Dekundy A., Zhang J., Li H., Baishen R., Danysz W., Bezard E., Cenci M.A. A mGluR5 antagonist under clinical development improves l-DOPA-induced dyskinesia in parkinsonian rats and monkeys. Neurobiol Dis 2010, 39:352-361.
155. Rylander D., Parent M., O'Sullivan S.S., Dovero S., Lees A.J., Bezard E., Descarries L., Cenci M.A. Maladaptive plasticity of serotonin axon terminals in levodopa-induced dyskinesia. Ann Neurol 2010, 68:619-628.
156. Rylander D., Recchia A., Mela F., Dekundy A., Danysz W., Cenci M.A. Pharmacological modulation of glutamate transmission in a rat model of l-DOPA-induced dyskinesia: effects on motor behavior and striatal nuclear signaling. J Pharmacol Exp Ther 2009, 330:227-235.
157. Santini E., Valjent E., Usiello A., Carta M., Borgkvist A., Girault J.A., Herve 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.
158. Schiffmann S.N., Libert F., Vassart G., Vanderhaeghen J.J. Distribution of adenosine A2 receptor mRNA in the human brain. Neurosci Lett 1991, 130:177-181.
159. Schneider J.S. Chronic exposure to low doses of MPTP. II. Neurochemical and pathological consequences in cognitively-impaired, motor asymptomatic monkeys. Brain Res 1990, 534:25-36.
160. Schneider J.S., Kovelowski C.J. Chronic exposure to low doses of MPTP. I. Cognitive deficits in motor asymptomatic monkeys. Brain Res 1990, 519:122-128.
161. Schneider J.S., Pope-Coleman A. Cognitive deficits precede motor deficits in a slowly progressing model of parkinsonism in the monkey. Neurodegeneration 1995, 4:245-255.
162. Sedelis M., Hofele K., Auburger G.W., Morgan S., Huston J.P., Schwarting R.K. MPTP susceptibility in the mouse: behavioral, neurochemical, and histological analysis of gender and strain differences. Behav Genet 2000, 30:171-182.
163. Sgambato-Faure V., Buggia V., Gilbert F., Levesque D., Benabid A.L., Berger F. Coordinated and spatial upregulation of arc in striatonigral neurons correlates with l-dopa-induced behavioral sensitization in dyskinetic rats. J Neuropathol Exp Neurol 2005, 64:936-947.
164. Sgambato-Faure V., Cenci M.A. Glutamatergic mechanisms in the dyskinesias induced by pharmacological dopamine replacement and deep brain stimulation for the treatment of Parkinson's disease. Prog Neurobiol 2012, 96:69-86.
165. Sharma J.C., Bachmann C.G., Linazasoro G. Classifying risk factors for dyskinesia in Parkinson's disease. Parkinsonism Relat Disord 2010, 16:490-497.
166. Smith G.A., Heuer A., Dunnett S.B., Lane E.L. Unilateral nigrostriatal 6-hydroxydopamine lesions in mice II: predicting l-DOPA-induced dyskinesia. Behav Brain Res 2012, 226:281-292.
167. Stocchi F. Dopamine receptor agonists in the treatment of advanced Parkinson's disease. Parkinsonism Relat Disord 2009, 15(Suppl 4):S54-S57.
168. Tashiro Y., Sugimoto T., Hattori T., Uemura Y., Nagatsu I., Kikuchi H., Mizuno N. Tyrosine hydroxylase-like immunoreactive neurons in the striatum of the rat. Neurosci Lett 1989, 97:6-10.
169. Thiele S.L., Warre R., Khademullah C.S., Fahana N., Lo C., Lam D., Talwar S., Johnston T.H., Brotchie J.M., Nash J.E. Generation of a model of l-DOPA-induced dyskinesia in two different mouse strains. J Neurosci Methods 2011, 197:193-208.
170. Ungerstedt U. 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur J Pharmacol 1968, 5:107-110.
171. Verhagen Metman L., Del Dotto P., van den Munckhof P., Fang J., Mouradian M.M., Chase T.N. Amantadine as treatment for dyskinesias and motor fluctuations in Parkinson's disease. Neurology 1998, 50:1323-1326.
172. Visanji N.P., Gomez-Ramirez J., Johnston T.H., Pires D., Voon V., Brotchie J.M., Fox S.H. Pharmacological characterization of psychosis-like behavior in the MPTP-lesioned nonhuman primate model of Parkinson's disease. Mov Disord 2006, 21:1879-1891.
173. Westin J.E., Lindgren H.S., Gardi J., Nyengaard J.R., Brundin P., Mohapel P., Cenci M.A. Endothelial proliferation and increased blood-brain barrier permeability in the basal ganglia in a rat model of 3,4-dihydroxyphenyl-l-alanine-induced dyskinesia. J Neurosci 2006, 26:9448-9461.
174. 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.
175. Winkler C., Kirik D., Björklund A., Cenci M.A. l-DOPA-induced dyskinesia in the intrastriatal 6-hydroxydopamine model of Parkinson's disease: relation to motor and cellular parameters of nigrostriatal function. Neurobiol Dis 2002, 10:165-186.
176. Wolf E., Seppi K., Katzenschlager R., Hochschorner G., Ransmayr G., Schwingenschuh P., Ott E., Kloiber I., Haubenberger D., Auff E., Poewe W. Long-term antidyskinetic efficacy of amantadine in Parkinson's disease. Mov Disord 2010, 25:1357-1363.
177. Xiao D., Bastia E., Xu Y.H., Benn C.L., Cha J.H., Peterson T.S., Chen J.F., Schwarzschild M.A. Forebrain adenosine A2A receptors contribute to l-3,4-dihydroxyphenylalanine-induced dyskinesia in hemiparkinsonian mice. J Neurosci 2006, 26:13548-13555.
178. Zeng B.Y., Iravani M.M., Jackson M.J., Rose S., Parent A., Jenner P. Morphological changes in serotoninergic neurites in the striatum and globus pallidus in levodopa primed MPTP treated common marmosets with dyskinesia. Neurobiol Dis 2010, 40:599-607.