Skip to main content
Top
Published in: Journal of Neural Transmission 3/2018

01-03-2018 | Translational Neurosciences - Review Article

The use of nonhuman primate models to understand processes in Parkinson’s disease

Authors: Javier Blesa, Inés Trigo-Damas, Natalia López-González del Rey, José A. Obeso

Published in: Journal of Neural Transmission | Issue 3/2018

Login to get access

Abstract

Research with animal models has led to critical health advances that have saved or improved the lives of millions of human beings. Specifically, nonhuman primate’s genetic and anatomo-physiological similarities to humans are especially important for understanding processes like Parkinson’s disease, which only occur in humans. Unambiguously, the unique contribution made by nonhuman primate research to our understanding of Parkinson’s disease is widely recognized. For example, monkeys with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) parkinsonisms are responsive to dopamine replacement therapies, mimicking what is seen in PD patients. Moreover, groundbreaking neuroanatomical and electrophysiological studies using this monkey model in the 1980s and 1990s enabled researchers to identify the neuronal circuits responsible for the cardinal motor features of PD. This led to the development of subthalamic surgical ablation and deep brain stimulation, the current therapeutic gold standard for neurosurgical treatment. More recently, the mechanisms of α-synuclein spreading testing the prion hypothesis for PD have yielded exciting results. In this review, we discuss and highlight how the findings from nonhuman primate research contribute to our understanding of idiopathic Parkinson’s disease.
Literature
go back to reference Adachi K, Kobayashi M, Kawasaki T et al (2012) Disruption of programmed masticatory movements in unilateral MPTP-treated monkeys as a model of jaw movement abnormality in Parkinson’s disease. J Neural Transm 119:933–941. doi:10.1007/s00702-012-0768-0 PubMedCrossRef Adachi K, Kobayashi M, Kawasaki T et al (2012) Disruption of programmed masticatory movements in unilateral MPTP-treated monkeys as a model of jaw movement abnormality in Parkinson’s disease. J Neural Transm 119:933–941. doi:10.​1007/​s00702-012-0768-0 PubMedCrossRef
go back to reference Akai T, Ozawa M, Yamaguchi M et al (1995) Behavioral involvement of central dopamine D1 and D2 receptors in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-lesioned parkinsonian cynomolgus monkeys. Jpn J Pharmacol 67:117–124PubMedCrossRef Akai T, Ozawa M, Yamaguchi M et al (1995) Behavioral involvement of central dopamine D1 and D2 receptors in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-lesioned parkinsonian cynomolgus monkeys. Jpn J Pharmacol 67:117–124PubMedCrossRef
go back to reference Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375PubMedCrossRef Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375PubMedCrossRef
go back to reference Aziz TZ, Peggs D, Sambrook MA, Crossman AR (1991) Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism in the primate. Mov Disord 6:288–292PubMedCrossRef Aziz TZ, Peggs D, Sambrook MA, Crossman AR (1991) Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism in the primate. Mov Disord 6:288–292PubMedCrossRef
go back to reference Ballard PA, Tetrud JW, Langston JW (1985) Permanent human parkinsonism due to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP): seven cases. Neurology 35:949–956PubMedCrossRef Ballard PA, Tetrud JW, Langston JW (1985) Permanent human parkinsonism due to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP): seven cases. Neurology 35:949–956PubMedCrossRef
go back to reference Bankiewicz KS, Eberling JL, Kohutnicka M et al (2000) Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using pro-drug approach. Exp Neurol 164:2–14. doi:10.1006/exnr.2000.7408 PubMedCrossRef Bankiewicz KS, Eberling JL, Kohutnicka M et al (2000) Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using pro-drug approach. Exp Neurol 164:2–14. doi:10.​1006/​exnr.​2000.​7408 PubMedCrossRef
go back to reference Benazzouz A, Gross C, Féger J et al (1993) Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur J Neurosci 5:382–389PubMedCrossRef Benazzouz A, Gross C, Féger J et al (1993) Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur J Neurosci 5:382–389PubMedCrossRef
go back to reference Berger B, Gaspar P, Verney C (1991) Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci 14:21–27PubMedCrossRef Berger B, Gaspar P, Verney C (1991) Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci 14:21–27PubMedCrossRef
go back to reference Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science (80) 249:1436–1438 Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science (80) 249:1436–1438
go back to reference Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507–520PubMedCrossRef Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507–520PubMedCrossRef
go back to reference Boyce S, Rupniak NM, Steventon MJ, Iversen SD (1990) Nigrostriatal damage is required for induction of dyskinesias by l-DOPA in squirrel monkeys. Clin Neuropharmacol 13:448–458PubMedCrossRef Boyce S, Rupniak NM, Steventon MJ, Iversen SD (1990) Nigrostriatal damage is required for induction of dyskinesias by l-DOPA in squirrel monkeys. Clin Neuropharmacol 13:448–458PubMedCrossRef
go back to reference Braak H, Del Tredici K, Rüb U et al (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMedCrossRef Braak H, Del Tredici K, Rüb U et al (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMedCrossRef
go back to reference Burns RS, Chiueh CC, Markey SP et al (1983) 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 USA 80:4546–4550PubMedPubMedCentralCrossRef Burns RS, Chiueh CC, Markey SP et al (1983) 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 USA 80:4546–4550PubMedPubMedCentralCrossRef
go back to reference Carpenter MB, Whittier JR, Mettler FA (1950) Analysis of choreoid hyperkinesia in the Rhesus monkey; surgical and pharmacological analysis of hyperkinesia resulting from lesions in the subthalamic nucleus of Luys. J Comp Neurol 92:293–331PubMedCrossRef Carpenter MB, Whittier JR, Mettler FA (1950) Analysis of choreoid hyperkinesia in the Rhesus monkey; surgical and pharmacological analysis of hyperkinesia resulting from lesions in the subthalamic nucleus of Luys. J Comp Neurol 92:293–331PubMedCrossRef
go back to reference Chaumette T, Lebouvier T, Aubert P et al (2009) Neurochemical plasticity in the enteric nervous system of a primate animal model of experimental Parkinsonism. Neurogastroenterol Motil 21:215–222PubMedCrossRef Chaumette T, Lebouvier T, Aubert P et al (2009) Neurochemical plasticity in the enteric nervous system of a primate animal model of experimental Parkinsonism. Neurogastroenterol Motil 21:215–222PubMedCrossRef
go back to reference Chen JJ (2010) Parkinson’s disease: health-related quality of life, economic cost, and implications of early treatment. Am J Manag Care 16:S87–S93 Chen JJ (2010) Parkinson’s disease: health-related quality of life, economic cost, and implications of early treatment. Am J Manag Care 16:S87–S93
go back to reference Chen M, Liu J, Lu Y et al (2016) Age-dependent alpha-synuclein accumulation is correlated with elevation of mitochondrial TRPC3 in the brains of monkeys and mice. J Neural Transm. doi:10.1007/s00702-016-1654-y Chen M, Liu J, Lu Y et al (2016) Age-dependent alpha-synuclein accumulation is correlated with elevation of mitochondrial TRPC3 in the brains of monkeys and mice. J Neural Transm. doi:10.​1007/​s00702-016-1654-y
go back to reference 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 24:587–591PubMedCrossRef 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 24:587–591PubMedCrossRef
go back to reference de Celis Alonso B, Hidalgo-Tobón SS, Menéndez-González M et al (2015) Magnetic resonance techniques applied to the diagnosis and treatment of Parkinson’s disease. Front Neurol 6:146. doi:10.3389/fneur.2015.00146 de Celis Alonso B, Hidalgo-Tobón SS, Menéndez-González M et al (2015) Magnetic resonance techniques applied to the diagnosis and treatment of Parkinson’s disease. Front Neurol 6:146. doi:10.​3389/​fneur.​2015.​00146
go back to reference DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–285PubMedCrossRef DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–285PubMedCrossRef
go back to reference DeLong MR, Crutcher MD, Georgopoulos AP (1985) Primate globus pallidus and subthalamic nucleus: functional organization. J Neurophysiol 53:530–543PubMedCrossRef DeLong MR, Crutcher MD, Georgopoulos AP (1985) Primate globus pallidus and subthalamic nucleus: functional organization. J Neurophysiol 53:530–543PubMedCrossRef
go back to reference Di Paolo T, Grégoire L, Feuerbach D et al (2014) AQW051, a novel and selective nicotinic acetylcholine receptor α7 partial agonist, reduces l-Dopa-induced dyskinesias and extends the duration of l-Dopa effects in parkinsonian monkeys. Parkinsonism Relat Disord 20:1119–1123. doi:10.1016/j.parkreldis.2014.05.007 PubMedCrossRef Di Paolo T, Grégoire L, Feuerbach D et al (2014) AQW051, a novel and selective nicotinic acetylcholine receptor α7 partial agonist, reduces l-Dopa-induced dyskinesias and extends the duration of l-Dopa effects in parkinsonian monkeys. Parkinsonism Relat Disord 20:1119–1123. doi:10.​1016/​j.​parkreldis.​2014.​05.​007 PubMedCrossRef
go back to reference Everett GM, Blockus LE, Shepperd IM (1956) Tremor induced by tremorine and its antagonism by anti-Parkinson drugs. Science 124:79PubMedCrossRef Everett GM, Blockus LE, Shepperd IM (1956) Tremor induced by tremorine and its antagonism by anti-Parkinson drugs. Science 124:79PubMedCrossRef
go back to reference Fox SH, Visanji N, Reyes G et al (2010) Neuropsychiatric behaviors in the MPTP marmoset model of Parkinson’s disease. Can J Neurol Sci 37:86–95PubMedCrossRef Fox SH, Visanji N, Reyes G et al (2010) Neuropsychiatric behaviors in the MPTP marmoset model of Parkinson’s disease. Can J Neurol Sci 37:86–95PubMedCrossRef
go back to reference Grondin R, Zhang Z, Yi A et al (2002) Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 125:2191–2201PubMedCrossRef Grondin R, Zhang Z, Yi A et al (2002) Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 125:2191–2201PubMedCrossRef
go back to reference Grondin R, Cass WA, Zhang Z et al (2003) Glial cell line-derived neurotrophic factor increases stimulus-evoked dopamine release and motor speed in aged rhesus monkeys. J Neurosci 23:1974–1980PubMed Grondin R, Cass WA, Zhang Z et al (2003) Glial cell line-derived neurotrophic factor increases stimulus-evoked dopamine release and motor speed in aged rhesus monkeys. J Neurosci 23:1974–1980PubMed
go back to reference Guridi J, Rodriguez-Oroz MC, Lozano AM, Moro E, Albanese A, Nuttin B, Gybels J, Ramos E, Obeso JA (2000) Targeting the basal ganglia for deep brain stimulation in Parkinson's disease. Neurology 55(6):S21–S28 Guridi J, Rodriguez-Oroz MC, Lozano AM, Moro E, Albanese A, Nuttin B, Gybels J, Ramos E, Obeso JA (2000) Targeting the basal ganglia for deep brain stimulation in Parkinson's disease. Neurology 55(6):S21–S28
go back to reference Hikishima K, Ando K, Yano R et al (2015b) Parkinson disease: diffusion MR imaging to detect nigrostriatal pathway loss in a marmoset model treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Radiology 275:430–437. doi:10.1148/radiol.14140601 PubMedCrossRef Hikishima K, Ando K, Yano R et al (2015b) Parkinson disease: diffusion MR imaging to detect nigrostriatal pathway loss in a marmoset model treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Radiology 275:430–437. doi:10.​1148/​radiol.​14140601 PubMedCrossRef
go back to reference Hill MP, Ravenscroft P, Bezard E et al (2004) 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. doi:10.1124/jpet.104.066191 PubMedCrossRef Hill MP, Ravenscroft P, Bezard E et al (2004) 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. doi:10.​1124/​jpet.​104.​066191 PubMedCrossRef
go back to reference Jackson MJ, Swart T, Pearce RKB, Jenner P (2014) Cholinergic manipulation of motor disability and l-DOPA-induced dyskinesia in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated common marmosets. J Neural Transm 121:163–169. doi:10.1007/s00702-013-1082-1 PubMedCrossRef Jackson MJ, Swart T, Pearce RKB, Jenner P (2014) Cholinergic manipulation of motor disability and l-DOPA-induced dyskinesia in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated common marmosets. J Neural Transm 121:163–169. doi:10.​1007/​s00702-013-1082-1 PubMedCrossRef
go back to reference Jarraya B, Boulet S, Scott Ralph G et al (2009) Dopamine gene therapy for Parkinson’s disease in a nonhuman primate without associated dyskinesia. Sci Transl Med 1:2ra4–2ra4. doi:10.1126/scitranslmed.3000130 Jarraya B, Boulet S, Scott Ralph G et al (2009) Dopamine gene therapy for Parkinson’s disease in a nonhuman primate without associated dyskinesia. Sci Transl Med 1:2ra4–2ra4. doi:10.​1126/​scitranslmed.​3000130
go back to reference Javitch JA, D’Amato RJ, Strittmatter SM, Snyder SH (1985) Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. Proc Natl Acad Sci USA 82:2173–2177PubMedPubMedCentralCrossRef Javitch JA, D’Amato RJ, Strittmatter SM, Snyder SH (1985) Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. Proc Natl Acad Sci USA 82:2173–2177PubMedPubMedCentralCrossRef
go back to reference Jenner P, Rupniak NM, Rose S et al (1984) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism in the common marmoset. Neurosci Lett 50:85–90PubMedCrossRef Jenner P, Rupniak NM, Rose S et al (1984) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism in the common marmoset. Neurosci Lett 50:85–90PubMedCrossRef
go back to reference Joel D, Weiner I (2000) The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96:451–474PubMedCrossRef Joel D, Weiner I (2000) The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96:451–474PubMedCrossRef
go back to reference Johnston TM, Fox SH (2014) Symptomatic models of Parkinson’s disease and l-DOPA-induced dyskinesia in non-human primates. In: Current topics in behavioral neurosciences, pp 221–235 Johnston TM, Fox SH (2014) Symptomatic models of Parkinson’s disease and l-DOPA-induced dyskinesia in non-human primates. In: Current topics in behavioral neurosciences, pp 221–235
go back to reference Ko WKD, Pioli E, Li Q et al (2014) Combined fenobam and amantadine treatment promotes robust antidyskinetic effects in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-lesioned primate model of Parkinson’s disease. Mov Disord 29:772–779. doi:10.1002/mds.25859 PubMedCrossRef Ko WKD, Pioli E, Li Q et al (2014) Combined fenobam and amantadine treatment promotes robust antidyskinetic effects in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-lesioned primate model of Parkinson’s disease. Mov Disord 29:772–779. doi:10.​1002/​mds.​25859 PubMedCrossRef
go back to reference Kobylecki C, Hill MP, Crossman AR, Ravenscroft P (2011) Synergistic antidyskinetic effects of topiramate and amantadine in animal models of Parkinson’s disease. Mov Disord 26:2354–2363. doi:10.1002/mds.23867 PubMedCrossRef Kobylecki C, Hill MP, Crossman AR, Ravenscroft P (2011) Synergistic antidyskinetic effects of topiramate and amantadine in animal models of Parkinson’s disease. Mov Disord 26:2354–2363. doi:10.​1002/​mds.​23867 PubMedCrossRef
go back to reference Koprich JB, Fox SH, Johnston TH et al (2011) 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 26:1225–1233. doi:10.1002/mds.23631 PubMedCrossRef Koprich JB, Fox SH, Johnston TH et al (2011) 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 26:1225–1233. doi:10.​1002/​mds.​23631 PubMedCrossRef
go back to reference Koprich JB, Johnston TH, Reyes G et al (2016) Towards a non-human primate model of alpha-synucleinopathy for development of therapeutics for Parkinson’s disease: optimization of AAV1/2 delivery parameters to drive sustained expression of alpha synuclein and dopaminergic degeneration in macaque. PLoS One 11:e0167235. doi:10.1371/journal.pone.0167235 PubMedPubMedCentralCrossRef Koprich JB, Johnston TH, Reyes G et al (2016) Towards a non-human primate model of alpha-synucleinopathy for development of therapeutics for Parkinson’s disease: optimization of AAV1/2 delivery parameters to drive sustained expression of alpha synuclein and dopaminergic degeneration in macaque. PLoS One 11:e0167235. doi:10.​1371/​journal.​pone.​0167235 PubMedPubMedCentralCrossRef
go back to reference Kordower JH, Palfi S, Chen EY et al (1999) Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson’s disease. Ann Neurol 46:419–424PubMedCrossRef Kordower JH, Palfi S, Chen EY et al (1999) Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson’s disease. Ann Neurol 46:419–424PubMedCrossRef
go back to reference Kordower JH, Emborg ME, Bloch J et al (2000) Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson’s disease. Science 290:767–773PubMedCrossRef Kordower JH, Emborg ME, Bloch J et al (2000) Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson’s disease. Science 290:767–773PubMedCrossRef
go back to reference Kordower JH, Herzog CD, Dass B et al (2006) Delivery of neurturin by AAV2 (CERE-120)-mediated gene transfer provides structural and functional neuroprotection and neurorestoration in MPTP-treated monkeys. Ann Neurol 60:706–715. doi:10.1002/ana.21032 PubMedCrossRef Kordower JH, Herzog CD, Dass B et al (2006) Delivery of neurturin by AAV2 (CERE-120)-mediated gene transfer provides structural and functional neuroprotection and neurorestoration in MPTP-treated monkeys. Ann Neurol 60:706–715. doi:10.​1002/​ana.​21032 PubMedCrossRef
go back to reference Kupsch A, Sautter J, Götz ME et al (2001) Monoamine oxidase-inhibition and MPTP-induced neurotoxicity in the non-human primate: comparison of rasagiline (TVP 1012) with selegiline. J Neural Transm 108:985–1009. doi:10.1007/s007020170018 PubMedCrossRef Kupsch A, Sautter J, Götz ME et al (2001) Monoamine oxidase-inhibition and MPTP-induced neurotoxicity in the non-human primate: comparison of rasagiline (TVP 1012) with selegiline. J Neural Transm 108:985–1009. doi:10.​1007/​s007020170018 PubMedCrossRef
go back to reference Laitinen LV, Bergenheim AT, Hariz MI (1992) Ventroposterolateral pallidotomy can abolish all parkinsonian symptoms. Stereotact Funct Neurosurg 58:14–21PubMedCrossRef Laitinen LV, Bergenheim AT, Hariz MI (1992) Ventroposterolateral pallidotomy can abolish all parkinsonian symptoms. Stereotact Funct Neurosurg 58:14–21PubMedCrossRef
go back to reference Langston JW, Forno LS, Rebert CS, Irwin I (1984) Selective nigral toxicity after systemic administration of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyrine (MPTP) in the squirrel monkey. Brain Res 292:390–394PubMedCrossRef Langston JW, Forno LS, Rebert CS, Irwin I (1984) Selective nigral toxicity after systemic administration of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyrine (MPTP) in the squirrel monkey. Brain Res 292:390–394PubMedCrossRef
go back to reference Lee JM, Derkinderen P, Kordower JH et al (2017) The search for a peripheral biopsy indicator of α-synuclein pathology for Parkinson disease. J Neuropathol Exp Neurol nlw103. doi:10.1093/jnen/nlw103 Lee JM, Derkinderen P, Kordower JH et al (2017) The search for a peripheral biopsy indicator of α-synuclein pathology for Parkinson disease. J Neuropathol Exp Neurol nlw103. doi:10.​1093/​jnen/​nlw103
go back to reference Limousin P, Pollak P, Benazzouz A et al (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet (London, England) 345:91–95 Limousin P, Pollak P, Benazzouz A et al (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet (London, England) 345:91–95
go back to reference Marks WJ Jr, Ostrem JL, Verhagen L et al (2008) Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson’s disease: an open-label, phase I trial. Lancet Neurol 7:400–408PubMedCrossRef Marks WJ Jr, Ostrem JL, Verhagen L et al (2008) Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson’s disease: an open-label, phase I trial. Lancet Neurol 7:400–408PubMedCrossRef
go back to reference Martínez-Fernández R, Schmitt E, Martinez-Martin P, Krack P (2016) The hidden sister of motor fluctuations in Parkinson’s disease: a review on nonmotor fluctuations. Mov Disord 31:1080–1094. doi:10.1002/mds.26731 PubMedCrossRef Martínez-Fernández R, Schmitt E, Martinez-Martin P, Krack P (2016) The hidden sister of motor fluctuations in Parkinson’s disease: a review on nonmotor fluctuations. Mov Disord 31:1080–1094. doi:10.​1002/​mds.​26731 PubMedCrossRef
go back to reference Miller WC, De Long MR (1987) Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism. In: Carpenter MB, Jayaraman A (eds) The basal ganglia II. Plenum Press, New York, pp 415–427CrossRef Miller WC, De Long MR (1987) Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism. In: Carpenter MB, Jayaraman A (eds) The basal ganglia II. Plenum Press, New York, pp 415–427CrossRef
go back to reference Miller GM, Yatin SM, De La Garza R et al (2001) Cloning of dopamine, norepinephrine and serotonin transporters from monkey brain: relevance to cocaine sensitivity. Brain Res Mol Brain Res 87:124–143PubMedCrossRef Miller GM, Yatin SM, De La Garza R et al (2001) Cloning of dopamine, norepinephrine and serotonin transporters from monkey brain: relevance to cocaine sensitivity. Brain Res Mol Brain Res 87:124–143PubMedCrossRef
go back to reference Mitchell IJ, Clarke CE, Boyce S et al (1989) Neural mechanisms underlying parkinsonian symptoms based upon regional uptake of 2-deoxyglucose in monkeys exposed to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neuroscience 32:213–226PubMedCrossRef Mitchell IJ, Clarke CE, Boyce S et al (1989) Neural mechanisms underlying parkinsonian symptoms based upon regional uptake of 2-deoxyglucose in monkeys exposed to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neuroscience 32:213–226PubMedCrossRef
go back to reference Morin N, Morissette M, Grégoire L, Di Paolo T (2015b) Effect of a chronic treatment with an mGlu5 receptor antagonist on brain serotonin markers in parkinsonian monkeys. Prog Neuro-Psychopharmacol Biol Psychiatry 56:27–38. doi:10.1016/j.pnpbp.2014.07.006 CrossRef Morin N, Morissette M, Grégoire L, Di Paolo T (2015b) Effect of a chronic treatment with an mGlu5 receptor antagonist on brain serotonin markers in parkinsonian monkeys. Prog Neuro-Psychopharmacol Biol Psychiatry 56:27–38. doi:10.​1016/​j.​pnpbp.​2014.​07.​006 CrossRef
go back to reference Morin N, Morissette M, Grégoire L, Di Paolo T (2016) mGlu5, dopamine D2 and adenosine A2A receptors in l-DOPA-induced dyskinesias. Curr Neuropharmacol 14:481–493PubMedPubMedCentralCrossRef Morin N, Morissette M, Grégoire L, Di Paolo T (2016) mGlu5, dopamine D2 and adenosine A2A receptors in l-DOPA-induced dyskinesias. Curr Neuropharmacol 14:481–493PubMedPubMedCentralCrossRef
go back to reference Muramatsu S-I, Fujimoto K-I, Ikeguchi K et al (2002) Behavioral recovery in a primate model of Parkinson’s disease by triple transduction of striatal cells with adeno-associated viral vectors expressing dopamine-synthesizing enzymes. Hum Gene Ther 13:345–354. doi:10.1089/10430340252792486 PubMedCrossRef Muramatsu S-I, Fujimoto K-I, Ikeguchi K et al (2002) Behavioral recovery in a primate model of Parkinson’s disease by triple transduction of striatal cells with adeno-associated viral vectors expressing dopamine-synthesizing enzymes. Hum Gene Ther 13:345–354. doi:10.​1089/​1043034025279248​6 PubMedCrossRef
go back to reference Nader MA, Czoty PW (2008) Brain imaging in nonhuman primates: insights into drug addiction. ILAR J 49:89–102PubMedCrossRef Nader MA, Czoty PW (2008) Brain imaging in nonhuman primates: insights into drug addiction. ILAR J 49:89–102PubMedCrossRef
go back to reference Nutt JG, Burchiel KJ, Comella CL et al (2003) Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 60:69–73PubMedCrossRef Nutt JG, Burchiel KJ, Comella CL et al (2003) Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 60:69–73PubMedCrossRef
go back to reference Obeso JA, Rodriguez MC, Guridi J et al (2001) Lesion of the basal ganglia and surgery for Parkinson disease. Arch Neurol 58:1165–1166PubMedCrossRef Obeso JA, Rodriguez MC, Guridi J et al (2001) Lesion of the basal ganglia and surgery for Parkinson disease. Arch Neurol 58:1165–1166PubMedCrossRef
go back to reference Oertel W, Schulz JB (2016) Current and experimental treatments of Parkinson disease: a guide for neuroscientists. J Neurochem. doi:10.1111/jnc.13750 Oertel W, Schulz JB (2016) Current and experimental treatments of Parkinson disease: a guide for neuroscientists. J Neurochem. doi:10.​1111/​jnc.​13750
go back to reference Palfi S, Leventhal L, Chu Y et al (2002) Lentivirally delivered glial cell line-derived neurotrophic factor increases the number of striatal dopaminergic neurons in primate models of nigrostriatal degeneration. J Neurosci 22:4942–4954PubMed Palfi S, Leventhal L, Chu Y et al (2002) Lentivirally delivered glial cell line-derived neurotrophic factor increases the number of striatal dopaminergic neurons in primate models of nigrostriatal degeneration. J Neurosci 22:4942–4954PubMed
go back to reference Parkinson J (1817) An essay on the shaking palsy. J Neuropsychiatry Clin Neurosci 14:223–236CrossRef Parkinson J (1817) An essay on the shaking palsy. J Neuropsychiatry Clin Neurosci 14:223–236CrossRef
go back to reference Pearce RK, Jackson M, Smith L et al (1995) Chronic l-DOPA administration induces dyskinesias in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated common marmoset (Callithrix jacchus). Mov Disord 10:731–740. doi:10.1002/mds.870100606 PubMedCrossRef Pearce RK, Jackson M, Smith L et al (1995) Chronic l-DOPA administration induces dyskinesias in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated common marmoset (Callithrix jacchus). Mov Disord 10:731–740. doi:10.​1002/​mds.​870100606 PubMedCrossRef
go back to reference Péchadre JC, Larochelle L, Poirier LJ (1976) Parkinsonian akinesia, rigidity and tremor in the monkey. Histopathological and neuropharmacological study. J Neurol Sci 28:147–157PubMedCrossRef Péchadre JC, Larochelle L, Poirier LJ (1976) Parkinsonian akinesia, rigidity and tremor in the monkey. Histopathological and neuropharmacological study. J Neurol Sci 28:147–157PubMedCrossRef
go back to reference Pessiglione M, Guehl D, Hirsch EC et al (2004) Disruption of self-organized actions in monkeys with progressive MPTP-induced parkinsonism. I. Effects of task complexity. Eur J Neurosci 19:426–436PubMedCrossRef Pessiglione M, Guehl D, Hirsch EC et al (2004) Disruption of self-organized actions in monkeys with progressive MPTP-induced parkinsonism. I. Effects of task complexity. Eur J Neurosci 19:426–436PubMedCrossRef
go back to reference Phillips KA, Ross CN, Spross J et al (2017) Behavioral phenotypes associated with MPTP induction of partial lesions in common marmosets (Callithrix jacchus). Behav Brain Res. doi:10.1016/j.bbr.2017.02.010 Phillips KA, Ross CN, Spross J et al (2017) Behavioral phenotypes associated with MPTP induction of partial lesions in common marmosets (Callithrix jacchus). Behav Brain Res. doi:10.​1016/​j.​bbr.​2017.​02.​010
go back to reference Poirier LJ (1960) Experimental and histological study of midbrain dyskinesias. J Neurophysiol 23:534–551PubMedCrossRef Poirier LJ (1960) Experimental and histological study of midbrain dyskinesias. J Neurophysiol 23:534–551PubMedCrossRef
go back to reference Poirier LJ, Lafleur J, de Lean J et al (1974) Physiopathology of the cerebellum in the monkey. 2. Motor disturbances associated with partial and complete destruction of cerebellar structures. J Neurol Sci 22:491–509PubMedCrossRef Poirier LJ, Lafleur J, de Lean J et al (1974) Physiopathology of the cerebellum in the monkey. 2. Motor disturbances associated with partial and complete destruction of cerebellar structures. J Neurol Sci 22:491–509PubMedCrossRef
go back to reference Pollak P, Benabid AL, Gross C et al (1993) Effects of the stimulation of the subthalamic nucleus in Parkinson disease. Rev Neurol (Paris) 149:175–176 Pollak P, Benabid AL, Gross C et al (1993) Effects of the stimulation of the subthalamic nucleus in Parkinson disease. Rev Neurol (Paris) 149:175–176
go back to reference Potts LF, Park ES, Woo J-M et al (2015) Dual κ-agonist/μ-antagonist opioid receptor modulation reduces levodopa-induced dyskinesia and corrects dysregulated striatal changes in the nonhuman primate model of Parkinson disease. Ann Neurol 77:930–941. doi:10.1002/ana.24375 PubMedCrossRef Potts LF, Park ES, Woo J-M et al (2015) Dual κ-agonist/μ-antagonist opioid receptor modulation reduces levodopa-induced dyskinesia and corrects dysregulated striatal changes in the nonhuman primate model of Parkinson disease. Ann Neurol 77:930–941. doi:10.​1002/​ana.​24375 PubMedCrossRef
go back to reference Recasens A, Dehay B, Bové J et al (2014a) Lewy body extracts from Parkinson disease brains trigger α-synuclein pathology and neurodegeneration in mice and monkeys. Ann Neurol 75:351–362. doi:10.1002/ana.24066 PubMedCrossRef Recasens A, Dehay B, Bové J et al (2014a) Lewy body extracts from Parkinson disease brains trigger α-synuclein pathology and neurodegeneration in mice and monkeys. Ann Neurol 75:351–362. doi:10.​1002/​ana.​24066 PubMedCrossRef
go back to reference Recasens A, Dehay B, Carballo-Carbajal I et al (2014) Lewy body extracts from Parkinson’s disease brain trigger alfa-synuclein pathology and neurodegeneration in mice and monkeys. Ann Neurol 351–362 Recasens A, Dehay B, Carballo-Carbajal I et al (2014) Lewy body extracts from Parkinson’s disease brain trigger alfa-synuclein pathology and neurodegeneration in mice and monkeys. Ann Neurol 351–362
go back to reference Schneider JS (1990) Chronic exposure to low doses of MPTP. II. Neurochemical and pathological consequences in cognitively-impaired, motor asymptomatic monkeys. Brain Res 534:25–36PubMedCrossRef Schneider JS (1990) Chronic exposure to low doses of MPTP. II. Neurochemical and pathological consequences in cognitively-impaired, motor asymptomatic monkeys. Brain Res 534:25–36PubMedCrossRef
go back to reference Schneider JS, Kovelowski CJ 2nd (1990) Chronic exposure to low doses of MPTP. I. Cognitive deficits in motor asymptomatic monkeys. Brain Res 519:122–128PubMedCrossRef Schneider JS, Kovelowski CJ 2nd (1990) Chronic exposure to low doses of MPTP. I. Cognitive deficits in motor asymptomatic monkeys. Brain Res 519:122–128PubMedCrossRef
go back to reference Spillantini MG, Schmidt ML, Lee VM et al (1997) Alpha-synuclein in Lewy bodies. Nature 388:839–840PubMedCrossRef Spillantini MG, Schmidt ML, Lee VM et al (1997) Alpha-synuclein in Lewy bodies. Nature 388:839–840PubMedCrossRef
go back to reference Taylor JR, Elsworth JD, Roth RH et al (1990) Cognitive and motor deficits in the acquisition of an object retrieval/detour task in MPTP-treated monkeys. Brain 617–37 Taylor JR, Elsworth JD, Roth RH et al (1990) Cognitive and motor deficits in the acquisition of an object retrieval/detour task in MPTP-treated monkeys. Brain 617–37
go back to reference Taylor JR, Roth RH, Sladek JR, Redmond DE (1990b) Cognitive and motor deficits in the performance of an object retrieval task with a barrier-detour in monkeys (Cercopithecus aethiops sabaeus) treated with MPTP: long-term performance and effect of transparency of the barrier. Behav Neurosci 104:564–576PubMedCrossRef Taylor JR, Roth RH, Sladek JR, Redmond DE (1990b) Cognitive and motor deficits in the performance of an object retrieval task with a barrier-detour in monkeys (Cercopithecus aethiops sabaeus) treated with MPTP: long-term performance and effect of transparency of the barrier. Behav Neurosci 104:564–576PubMedCrossRef
go back to reference Uchida S, Soshiroda K, Okita E et al (2015) The adenosine A2A receptor antagonist, istradefylline enhances anti-parkinsonian activity induced by combined treatment with low doses of l-DOPA and dopamine agonists in MPTP-treated common marmosets. Eur J Pharmacol 766:25–30. doi:10.1016/j.ejphar.2015.09.028 PubMedCrossRef Uchida S, Soshiroda K, Okita E et al (2015) The adenosine A2A receptor antagonist, istradefylline enhances anti-parkinsonian activity induced by combined treatment with low doses of l-DOPA and dopamine agonists in MPTP-treated common marmosets. Eur J Pharmacol 766:25–30. doi:10.​1016/​j.​ejphar.​2015.​09.​028 PubMedCrossRef
go back to reference Visanji NP, Gomez-Ramirez J, Johnston TH et al (2006) Pharmacological characterization of psychosis-like behavior in the MPTP-lesioned nonhuman primate model of Parkinson’s disease. Mov Disord 21:1879–1891. doi:10.1002/mds.21073 PubMedCrossRef Visanji NP, Gomez-Ramirez J, Johnston TH et al (2006) Pharmacological characterization of psychosis-like behavior in the MPTP-lesioned nonhuman primate model of Parkinson’s disease. Mov Disord 21:1879–1891. doi:10.​1002/​mds.​21073 PubMedCrossRef
go back to reference Weed MR, Woolverton WL, Paul IA (1998) Dopamine D1 and D2 receptor selectivities of phenyl-benzazepines in rhesus monkey striata. Eur J Pharmacol 361:129–142PubMedCrossRef Weed MR, Woolverton WL, Paul IA (1998) Dopamine D1 and D2 receptor selectivities of phenyl-benzazepines in rhesus monkey striata. Eur J Pharmacol 361:129–142PubMedCrossRef
go back to reference Whittier JR (1948) Rhesus hyperkinesia by subthalamic lesion. Fed Proc 7:133PubMed Whittier JR (1948) Rhesus hyperkinesia by subthalamic lesion. Fed Proc 7:133PubMed
go back to reference Whittier JR, Mettler FA (1947) Subthalamic lesion in the primate. Fed Proc 6:226PubMed Whittier JR, Mettler FA (1947) Subthalamic lesion in the primate. Fed Proc 6:226PubMed
go back to reference Wichmann T, Bergman H, DeLong MR (1994) The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 72(2):521–530 Wichmann T, Bergman H, DeLong MR (1994) The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 72(2):521–530
Metadata
Title
The use of nonhuman primate models to understand processes in Parkinson’s disease
Authors
Javier Blesa
Inés Trigo-Damas
Natalia López-González del Rey
José A. Obeso
Publication date
01-03-2018
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 3/2018
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-017-1715-x

Other articles of this Issue 3/2018

Journal of Neural Transmission 3/2018 Go to the issue

Neurology and Preclinical Neurological Studies - Review Article

Reward and value coding by dopamine neurons in non-human primates

Neurology and Preclinical Neurological Studies - Review Article

Dysregulation of striatal projection neurons in Parkinson’s disease

Neurology and Preclinical Neurological Studies - Review Article

Gene therapy approaches in the non-human primate model of Parkinson’s disease