Modeling Parkinson's disease in primates: The MPTP model

Cold Spring Harbor Perspectives in Medicine

Volumn 2, Issue 3, 2012, Pages

  Porras, Gregory ^a,b   Li, Qin ^c   Bezard, Erwan ^a,b,c  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

^c INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; BIOLOGICAL MARKER; DOPAMINE; NEUROTOXIN;

ARTICLE; BEHAVIOR; BODY MOVEMENT; CALLITHRIX; CHLOROCEBUS SABAEUS; CHRONOBIOLOGICAL DISTURBANCE; CLINICAL GLOBAL IMPRESSION SCALE; COGNITIVE DEFECT; DENERVATION; DOPAMINERGIC NERVE CELL; DYSKINESIA; ELECTROMYOGRAPHY; LEWY BODY; MACACA FASCICULARIS; MONOAMINERGIC SYSTEM; MOTOR PERFORMANCE; MPTP-INDUCED PARKINSONISM; NONHUMAN; PARKINSON DISEASE; PHENOMENOLOGY; PRIMATE; RHESUS MONKEY; SAIMIRI SCIUREUS; SLEEP AROUSAL DISORDER; SLEEP DISORDER; ANIMAL; CERCOPITHECUS; DISEASE COURSE; DISEASE MODEL; HAPLORHINI; INTOXICATION; MOVEMENT (PHYSIOLOGY); PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSLATIONAL RESEARCH;

PRIMATES;

ANIMALS; CERCOPITHECINAE; CHRONOBIOLOGY DISORDERS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HAPLORHINI; LEWY BODIES; MOVEMENT; MPTP POISONING; PARKINSON DISEASE; SLEEP DISORDERS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84886692989     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a009308     Document Type: Article

References (72)

1. Ahmed MR, Berthet A, Bychkov E, Porras G, Li Q, Bioulac BH, Carl YT, Bloch B, Kook S, Aubert I, et al. 2010. Lentiviral overexpression of GRK6 alleviates L-dopa-induced dyskinesia in experimental Parkinson's disease. Sci Transl Med 2: 28ra28.
2. Arnulf I, Konofal E, Merino-Andreu M, Houeto JL, Mesnage V, Welter ML, Lacomblez L, Golmard JL, Derenne JP, Agid Y. 2002. Parkinson's disease and sleepiness: An integral part of PD. Neurology 58: 1019-1024.
3. Barraud Q, Lambrecq V, Forni C, McGuire S, Hill M, Bioulac B, Balzamo E, Bezard E, Tison F, Ghorayeb I. 2009. Sleep disorders in Parkinson's disease: The contribution of the MPTP non-human primate model. Exp Neurol 219: 574-582.
4. Barraud Q, Obeid I, Aubert I, Barriere G, Contamin H, McGuire S, Ravenscroft P, Porras G, Tison F, Bezard E, et al. 2010. Neuroanatomical study of the a11 diencephalospinal pathway in the non-human primate. PLoS One 5: e13306.
5. Belanger N, Gregoire L, Hadj Tahar A, Bedard PJ. 2003. Chronic treatment with small doses of cabergoline prevents dopa-induced dyskinesias in parkinsonian monkeys. Mov Disord 18: 1436-1441.
6. Benazzouz A, Gross C, Bioulac B. 1992. MPTP-induced hemiparkinsonism in monkeys: Behavioral, mechanographic, electromyographic and immunohistochemical studies. Exp Brain Res 90: 116-120.
7. Benazzouz A, Gross C, Feger J, Boraud T, Bioulac B. 1993. Reversal of rigidity and improvement in motor performance by subthalamic high frequency stimulation in MPTP-treated monkeys. Eur J Neurosci 5: 382-389.
8. Berton O, Guigoni C, Li Q, Bioulac BH, Aubert I, Gross CE, Dileone RJ, NestlerEJ, Bezard E. 2009. Striatal overexpression of DeltaJunD resets L-DOPA-induced dyskinesia in a primate model of Parkinson disease. Biol Psychiatry 66: 554-561.
9. Bezard E, Imbert C, Deloire X, Bioulac B, Gross C. 1997. A chronic MPTP model reproducing the slow evolution of Parkinson's disease: Evolution of motor symptoms in the monkey. Brain Res 766: 107-112.
10. Bezard E, Imbert C, Gross CE. 1998. Experimental models of Parkinson's disease: From the static to the dynamic. Rev Neurosci 9: 71-90.
11. Bezard E, Brotchie JM, Gross CE. 2001a. Pathophysiology of levodopa-induced dyskinesia: Potential for new therapies. Nature Rev Neurosci 2: 577-588.
12. Bezard E, Crossman AR, Gross CE, Brotchie JM. 2001b. Structures outside the basal ganglia may compensate for dopamine loss in the pre-symptomatic stages of Parkinson's disease. FASEB J 15: 1092-1094.
13. Bezard E, Dovero S, Prunier C, Ravenscroft P, Chalon S, Guilloteau D, Bioulac B, Brotchie JM, Gross CE. 2001c. 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 21: 6853-6861.
14. Bezard E, Ferry S, Mach U, Stark H, Leriche L, Boraud T, Gross CE, Sokoloff P. 2003. Attenuation of levodopa-induced dyskinesia by normalizing dopamine D3 receptor function. Nature Med 9: 762-767.
15. Bezard E, Hill MP, McGuire SG, Crossman AR, Brotchie JM, Michel A, Grimée R., Klitgaard H. 2004. Levetiracetam improves choreic levodopa-induced dyskinesia in the MPTP-treated macaque. Eur J Pharmacol 485: 159-164.
16. Bezard E, Przedborski S. 2011. A tale on animal models of Parkinson's Disease. Mov Disord 26: 993-1002.
17. Chaumette T, Lebouvier T, Aubert P, Lardeux B, Qin C, Li Q, Accary D, BézardE, Varannes SBd, Derkinderen P, et al. 2009. Neurochemical plasticity in the enteric nervous system of a primate animal model of experimental Parkinsonism. Neurogastroenterol Motil 21: 215-222.
18. Chiueh CC, Markey SD, Burns RS, Johannessen JN, Jacobowitz DM, Kopin IJ. 1984. Neurochemical and behavioral effects of MPTP in rat, guinea pig and monkey. Psychopharmacol Bull 20: 548-553.
19. Courtine G, Roy RR, Hodgson J, McKay H, Raven J, Zhong H, Yang H, TuszynskiMH, Edgerton VR. 2005a. Kinematic and EMG determinants in quadrupedal locomotion of a non-human primate (Rhesus). J Neurophysiol 93: 3127-3145.
20. Courtine G, Roy RR, Raven J, Hodgson J, McKay H, Yang H, Zhong H, TuszynskiMH, Edgerton VR. 2005b. Performance of locomotion and foot grasping following a unilateral thoracic corticospinal tract lesion in monkeys (Macaca mulatta). brain 128: 2338-2358.
21. Crossman AR, Mitchell IJ, Sambrook MA. 1985. Regional brain uptake of 2-deoxyglucose in N-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP)-induced parkinsonism in the macaque monkey. Neuropharmacology 24: 587-591.
22. Decamp E, Schneider JS. 2004. Attention and executive function deficits in chronic low-dose MPTP-treated non-human primates. Eur J Neurosci 20: 1371-1378.
23. Decamp E, Schneider JS. 2006. Effects of nicotinic therapies on attention and executive functions in chronic low-dose MPTP-treated monkeys. Eur J Neurosci 24: 2098-2104.
24. Decamp E, Tinker JP, Schneider JS. 2004. Attentional cueing reverses deficits in spatial working memory task performance in chronic low dose MPTP-treated monkeys. Behav Brain Res 152: 259-262.
25. Di Monte DA, McCormack A, Petzinger G, Janson AM, Quik M, Langston WJ. 2000. Relationship among nigrostriatal denervation, parkinsonism, and dyskinesias in the MPTP primate model. Mov Disord 15: 459-466.
26. Doudet D, Gross C, Lebrun-Grandie P, Bioulac B. 1985. MPTP primate model of Parkinson's disease: A mechanographic and electromyographic study. Brain Res 335: 194-199.
27. Doudet D, Gross C, Lebrun-Grandié P, Bioulac B. 1986. Mechanographic and kinematic studies of a voluntary elbow movement in MPTP-treated monkeys. Effects of L-Dopa therapies. In MPTP: A neurotoxin producing a parkinsonian syndrome (ed. Sanford P, Markey P), pp. 651-666. Academic Press, Orlando, FL.
28. Doudet DJ, Gross C, Arluison M, Bioulac B. 1990. Modifications of precentral cortex discharges and EMG activity in monkey with MPTP-induced lesions of DA nigral neurons. Exp Brain Res 80: 177-188.
29. Ekstrand MI, Terzioglu M, Galter D, Zhu S, Hofstetter C, Lindqvist E, Thams S, Bergstrand A, Hansson FS, Trifunovic A, et al. 2007. Progressive parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc Natl Acad Sci 104: 1325-1330.
30. Fasano S, Bezard E, D'Antoni A, Francardo V, Indrigo M, Qin L, Dovero S, Cerovic M, Cenci MA, Brambilla R. 2010. 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 107: 21824-21829.
31. Fernagut PO, Li Q, Dovero S, Chan P, Wu T, Ravenscroft P, Hill M, Chen Z, Bezard E. 2010. Dopamine transporter binding is unaffected by L-DOPA administration in normal and MPTP-treated monkeys. Plos One 5: e14053.
32. Ghorayeb I, Loundou A, Auquier P, Dauvilliers Y, Bioulac B, Tison F. 2007. A nationwide survey of excessive daytime sleepiness in Parkinson's disease in France. Mov Disord 22: 1567-1572.
33. Gold SJ, Hoang CV, Potts BW, Porras G, Pioli E, Kim KW, Nadjar A, Qin C, LaHoste GJ, Li Q, et al. 2007. RGS9-2 negatively modulates L-3, 4-dihydroxyphenylalanine-induced dyskinesia in experimental Parkinson's disease. J Neurosci 27: 14338-14348.
34. Guehl D, Pessiglione M, Francois C, Yelnik J, Hirsch EC, Feger J, Tremblay L. 2003. Tremor-related activity of neurons in the 'motor' thalamus: Changes in firing rate and pattern in the MPTP vervet model of parkinsonism. Eur J Neurosci 17: 2388-2400.
35. Guigoni C, Dovero S, Aubert I, Qin L, Bioulac BH, Bloch B, Gurevich EV, GrossCE, Bezard E. 2005. Levodopa-induced dyskinesia in MPTP-treated macaque is not dependent of the extent and pattern of the nigrostrial lesion. Eur J Neurosci 22: 283-287.
36. Hadj Tahar A, Gregoire L, Darre A, Belanger N, Meltzer L, Bedard PJ. 2004. Effect of a selective glutamate antagonist on L-dopa-induced dyskinesias in drug-naive parkinsonian monkeys. Neurobiol Dis 15: 171-176.
37. Heikkila RE, Hess A, Duvoisin RC. 1984. Dopaminergic neurotoxicity of MPTP in mice. Science 224: 1451-1453.
38. Henry B, Fox SH, Crossman AR, Brotchie JM. 2001. mu-and δ-Opioid receptor antagonists reduce levodopa-induced dyskinesia in the MPTP-lesioned primate model of Parkinson's Disease. Exp Neurol 171: 139-146.
39. Henry B, Duty S, Fox SH, Crossman AR, Brotchie JM. 2003. Increased striatal pre-proenkephalin B expression is associated with dyskinesia in Parkinson's disease. Exp Neurol 183: 458-468.
40. Hill MP, Brotchie JM, McGuire S, Crossman AR, Bezard E, Grimée R, Klitgaard H. 2004a. Levetiracetam interferes with L-dopa priming process in the MPTP-lesioned drug naïve marmoset. Clin Neuropharmacol 27: 171-177.
41. Hill MP, Ravenscroft P, Bezard E, Crossman AR, Brotchie JM, Michel A, GrimeeR, Klitgaard H. 2004b. 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 310: 386-394.
42. Hsu A, Togasaki DM, Bezard E, Sokoloff P, Langston JW, Di Monte DA, Quik M. 2004. 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 311: 770-777.
43. Imbert C, Bezard E, Guitraud S, Boraud T, Gross CE. 2000. Comparison between eight clinical rating scales used for the assessment of MPTP-induced parkinsonism in the macaque monkey. J Neurosci Meth 96: 71-76.
44. Iravani MM, Jackson MJ, Kuoppamaki M, Smith LA, Jenner P. 2003. 3, 4-methylenedioxymethamphetamine (ecstasy) inhibits dyskinesia expression and normalizes motor activity in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated primates. J Neurosci 23: 9107-9115.
45. Iravani MM, Syed E, Jackson MJ, Johnston LC, Smith LA, Jenner P. 2005. A modified MPTP treatment regime produces reproducible partial nigrostriatal lesions in common marmosets. Eur J Neurosci 21: 841-854.
46. Jan C, Pessiglione M, Tremblay L, Tandé D, Hirsch EC, François C. 2003. Quantitative analysis of dopaminergic loss in relation to functional territories in MPTP-treated monkeys. Eur J Neurosci 18: 2082-2086.
47. Jenner P. 2008. Molecular mechanisms of L-DOPA-induced dyskinesia. Nat Rev Neurosci 9: 665-677.
48. Kordower JH, Liu Y-T, Winn SR, Emerich DF. 1995. Encapsulated PC12 cell transplants into hemiparkinsonian monkeys: A behavioral, neuroanatomical and neurochemical analysis. Cell Trans 4: 55-171.
49. Langston JW, Forno LS, Rebert CS, Irwin I. 1984. Selective nigral toxicity after systemic administration of 1-methyl-4-phenyl 1-1, 2, 3, 6, tetrahydropyridine (MPTP) in the squirrel monkey. Brain Res 292: 390-394.
50. Langston JW, Quik M, Petzinger G, Jakowec M, Di Monte DA. 2000. Investigating levodopa-induced dyskinesias in the Parkinsonian primate. Ann Neurol 47: S79-S89.
51. Meissner W, Prunier C, Guilloteau D, Chalon S, Gross CE, Bezard E. 2003. Time course of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease. Mol Neurobiol 28: 87-96.
52. Moratalla R, Quinn B, DeLanney LE, Irwin I, Langston JW, Graybiel AM. 1992. Differential vulnerability of primate caudate-putamen and striosome-matrix dopamine systems to the neurotoxic effects of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. Proc Natl Acad Sci 89: 3859-3863.
53. Morissette M, Grondin R, Goulet M, Bedard PJ, Di Paolo T. 1999. Differential regulation of striatal preproenkephalin and preprotachykinin mRNA levels in MPTP-lesioned monkeys chronically treated with dopamine D-1 or D-2 receptor agonists. J Neurochem 72: 682-692.
54. Ouattara B, Belkhir S, Morissette M, Dridi M, Samadi P, Gregoire L, Meltzer LT, Di Paolo T. 2009. 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 38: 128-142.
55. Pearce RK, Banerji T, Jenner P, Marsden CD. 1998. De novo administration of ropinirole and bromocriptine induces less dyskinesia than L-dopa in the MPTP-treated marmoset. Mov Disord 13: 234-241.
56. Pifl C, Schingnitz G, Hornykiewicz O. 1991. Effect of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine on the regional distribution of brain monoamines in the rhesus monkey. Neuroscience 44: 591-605.
57. Prunier C, Bezard E, Mantzarides M, Besnard JC, Baulieu JL, Gross CE, GuilloteauD, Chalon S. 2003. Presymptomatic diagnosis of experimental parkinsonism with 123I-PE2I SPECT. Neuroimage 19: 810-816.
58. Purisai MG, McCormack AL, Langston WJ, Johnston LC, Di Monte DA. 2005. α-synuclein expression in the substantia nigra of MPTP-lesioned non-human primates. Neurobiol Dis 20: 898-906.
59. Raz A, Vaadia E, Bergman H. 2000. Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine vervet model of parkinsonism. J Neurosci 20: 8559-8571.
60. Roeltgen DP, Schneider JS. 1991. Chronic low-dose MPTP in nonhuman primates: a possible model for attention deficit disorder. J Child Neurol 6 (Suppl): S82-S89.
61. Roeltgen DP, Schneider JS. 1994. Task persistence and learning ability in normal and chronic low dose MPTP-treated monkeys. Behav Brain Res 60: 115-124.
62. Rose S, Nomoto M, Jackson EA, Gibb WRG, Jaehnig P, Jenner P, Marsden CD. 1993. Age-related effects of MPTP treatment of common marmosets. Eur J Pharmacol 230: 177-185.
63. Rylander D, Iderberg H, Li Q, Dekundy A, Zhang J, Li H, Baishen R, Danysz W, Bezard E, Cenci MA. 2010. A mGluR5 antagonist under clinical development improves L-DOPA-induced dyskinesia in parkinsonian rats and monkeys. Neurobiol Dis 39: 352-361.
64. Savola JM, Hill M, Engstrom M, Merivuori H, Wurster S, McGuire SG, Fox SH, Crossman AR, Brotchie JM. 2003. Fipamezole (JP-1730) is a potent α2 adrenergic receptor antagonist that reduces levodopa-induced dyskinesia in the MPTP-lesioned primate model of Parkinson's disease. Mov Disord 18: 872-883.
65. Schneider JS. 1990. Chronic exposure to low doses of MPTP. II. Neurochemical and pathological consequences in cognitively-impaired, motor asymptomatic monkeys. Brain Res 534: 25-36.
66. Schneider JS, Kovelowski CJ. 1990. Chronic exposure to low doses of MPTP. I. Cognitive deficits in motor asymptomatic monkeys. Brain Res 519: 122-128.
67. Schneider JS, Roeltgen DP. 1993. Delayed matching-to-sample, object retrieval, and discrimination reversal deficits in chronic low dose MPTP-treated monkeys. Brain Res 615: 351-354.
68. Schneider JS, McLaughlin WW, Roeltgen DP. 1992. Motor and non-motor behavioral deficits in monkeys made hemiparkinsonian by intracarotid MPTP infusion. Neurology 42: 1565-1572.
69. Schneider JS, Van Velson M, Menzaghi F, Lloyd GK. 1998. Effects of the nicotinic acetylcholine receptor agonist SIB-1508Y on object retrieval performance in MPTP-treated monkeys: comparison with levodopa treatment. Ann Neurol 43: 311-317.
70. Smith LA, Tel BC, Jackson MJ, Hansard MJ, Braceras R, Bonhomme C, Chezaubernard C, Del Signore S, Rose S, Jenner P. 2002. Repeated administration of piribedil induces less dyskinesia than L-dopa in MPTP-treated common marmosets: A behavioural and biochemical investigation. Mov Disord 17: 887-901.
71. Tieu K. 2011. A guide to neurotoxic animal models in Parkinson's disease. Cold Spring Harb Perspect Med doi: 10. 1101/cshperspect. a009316.
72. Vital A, Li Q, Canron MH, Ravenscroft P, Hill M, Bezard E. 2010. Comprehensive pathological analysis in MPTP-treated macaques reveal widespread synucleopathy and tauopathy. Mov Disord 25: S203-S203.