Skip to main content
Download PDF

Modeling Parkinson’s disease in the common marmoset (Callithrix jacchus): overview of models, methods, and animal care

Laboratory Animal Research volume 31, pages 155–165 (2015)Cite this article

Abstract

The common marmoset (Callithrix jacchus) is a small-bodied, popular New World monkey and is used widely in reproductive biology, neuroscience, and drug development, due to its comparative ease of handling, high reproductive efficiency, and its unique behavioral characters. In this review, we discuss the marmoset models in Parkinson’s disease (PD), which is a neurological movement disorder primarily resulting from a degeneration of dopaminergic neurons with clinical features of tremor, rigidity, postural instability, and akinesia. The most common PD models involve the administration of 1-methyl-4-phenyl- 1,2,3,6-tetrahydropyridine (MPTP) or 6-hydroxydopamine to study the pathogenesis and to evaluate novel therapies. Following the systemic or local administration of these neurotoxins, the marmosets with very severe Parkinson’s symptoms are recommended to be placed in an intensive care unit with artificial feeding to increase survival rate. All procedures with MPTP should be conducted in a special room with enclosed cages under negative-pressure by trained researchers with personal protection. Behavioral tests are conducted to provide an external measure of the brain pathology. Along with several biomarkers, including α-synuclein and DJ-1, non-invasive neuroimaging techniques such as positron emission tomography and magnetic resonance imaging are used to evaluate the functional changes associated with PD. With the recent growing interest in potential and novel therapies such as stem cell and gene therapy for PD in Korea, the marmoset can be considered as a suitable non-human primate model in PD research to bridge the gap between rodent studies and clinical applications.

References

  1. Lang AE, Lozano AM. Parkinson’s disease. First of two parts. N Engl J Med 1998; 339(15): 1044–1053.

    CAS  PubMed  Google Scholar 

  2. Dauer W, Przedborski S. Parkinson’s disease: mechanisms and models. Neuron 2003; 39(6): 889–909.

    CAS  PubMed  Google Scholar 

  3. Yuan H, Zhang ZW, Liang LW, Shen Q, Wang XD, Ren SM, Ma HJ, Jiao SJ, Liu P. Treatment strategies for Parkinson’s disease. Neurosci Bull 2010; 26(1): 66–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Liu Y, Yue F, Tang R, Tao G, Pan X, Zhu L, Kung HF, Chan P. Progressive loss of striatal dopamine terminals in MPTP-induced acute parkinsonism in cynomolgus monkeys using vesicular monoamine transporter type 2 PET imaging ([(18)F]AV-133). Neurosci Bull 2014; 30(3): 409–416.

    CAS  PubMed  Google Scholar 

  5. Hirsch EC, Hunot S. Neuroinflammation in Parkinson’s disease: a target for neuroprotection? Lancet Neurol 2009; 8(4): 382–397.

    CAS  PubMed  Google Scholar 

  6. Hornykiewicz O, Kish SJ. Biochemical pathophysiology of Parkinson’s disease. In: Parkinson’s disease (Yahr M and Bergmann KJ, eds), Raven Press, New York, 1987; pp 19–34.

    Google Scholar 

  7. Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K. Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 2004; 318(1): 121–134.

    PubMed  Google Scholar 

  8. Le W, Sayana P, Jankovic J. Animal models of Parkinson’s disease: a gateway to therapeutics? Neurotherapeutics 2014; 11(1): 92–110.

    CAS  PubMed  Google Scholar 

  9. Blandini F, Armentero MT. Animal models of Parkinson’s disease. FEBS J 2012; 279(7): 1156–1166.

    CAS  PubMed  Google Scholar 

  10. Tieu K. A guide to neurotoxic animal models of Parkinson’s disease. Cold Spring Harb Perspect Med 2011; 1(1): a009316.

    PubMed  PubMed Central  Google Scholar 

  11. Okano H, Hikishima K, Iriki A, Sasaki E. The common marmoset as a novel animal model system for biomedical and neuroscience research applications. Semin Fetal Neonatal Med 2012; 17(6): 336–340.

    PubMed  Google Scholar 

  12. Orsi A, Rees D, Andreini I, Venturella S, Cinelli S, Oberto G. Overview of the marmoset as a model in nonclinical development of pharmaceutical products. Regul Toxicol Pharmacol 2011; 59(1): 19–27.

    CAS  PubMed  Google Scholar 

  13. Tardif SD, Smucny DA, Abbott DH, Mansfield K, Schultz-Darken N, Yamamoto ME. Reproduction in captive common marmosets (Callithrix jacchus). Comp Med 2003; 53(4): 364–368.

    CAS  PubMed  Google Scholar 

  14. Abbott DH, Barnett DK, Colman RJ, Yamamoto ME, Schultz-Darken NJ. Aspects of common marmoset basic biology and life history important for biomedical research. Comp Med 2003; 53(4): 339–350.

    CAS  PubMed  Google Scholar 

  15. Mansfield K. Marmoset models commonly used in biomedical research. Comp Med 2003; 53(4): 383–392.

    CAS  PubMed  Google Scholar 

  16. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci USA 2003; 100(7): 4078–4083.

    CAS  PubMed  Google Scholar 

  17. Bezard E, Jaber M, Gonon F, Boireau A, Bloch B, Gross CE. Adaptive changes in the nigrostriatal pathway in response to increased 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurodegeneration in the mouse. Eur J Neurosci 2000; 12(8): 2892–2900.

    CAS  PubMed  Google Scholar 

  18. irik D, Rosenblad C, Björklund A. Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6- hydroxydopamine in the rat. Exp Neurol 1998; 152(2): 259–277.

    Google Scholar 

  19. Schneider JS, Schroeder JA, Rothblat DS. Differential recovery of sensorimotor function in GM1 ganglioside-treated vs. spontaneously recovered MPTP-treated cats: partial striatal dopaminergic reinnervation vs. neurochemical compensation. Brain Res 1998; 813(1): 82–87.

    CAS  PubMed  Google Scholar 

  20. Mikkelsen M, Møller A, Jensen LH, Pedersen A, Harajehi JB, Pakkenberg H. MPTP-induced Parkinsonism in minipigs: A behavioral, biochemical, and histological study. Neurotoxicol Teratol 1999; 21(2): 169–175.

    CAS  PubMed  Google Scholar 

  21. Baskin DS, Browning JL, Widmayer MA, Zhu ZQ, Grossman RG. Development of a model for Parkinson’s disease in sheep using unilateral intracarotid injection of MPTP via slow continuous infusion. Life Sci 1994; 54(7): 471–479.

    CAS  PubMed  Google Scholar 

  22. Jenner P, Rupniak NM, Rose S, Kelly E, Kilpatrick G, Lees A, Marsden CD. 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine- induced parkinsonism in the common marmoset. Neurosci Lett 1984; 50(1-3): 85–90.

    CAS  PubMed  Google Scholar 

  23. Fox SH, Visanji N, Reyes G, Huot P, Gomez-Ramirez J, Johnston T, Brotchie JM. Neuropsychiatric behaviors in the MPTP marmoset model of Parkinson’s disease. Can J Neurol Sci 2010; 37(1): 86–95.

    PubMed  Google Scholar 

  24. Philippens IH, Wubben JA, Finsen B, ’t Hart BA. Oral treatment with the NADPH oxidase antagonist apocynin mitigates clinical and pathological features of parkinsonism in the MPTP marmoset model. J Neuroimmune Pharmacol 2013; 8(3): 715–726.

    PubMed  Google Scholar 

  25. Kelava I, Reillo I, Murayama AY, Kalinka AT, Stenzel D, Tomancak P, Matsuzaki F, Lebrand C, Sasaki E, Schwamborn JC, Okano H, Huttner WB, Borrell V. Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb Cortex 2012; 22(2): 469–481.

    PubMed  Google Scholar 

  26. Smith D, Trennery P, Farningham D, Klapwijk J. The selection of marmoset monkeys (Callithrix jacchus) in pharmaceutical toxicology. Lab Anim 2001; 35(2): 117–130.

    CAS  PubMed  Google Scholar 

  27. Dell’Mour V, Range F, Huber L. Social learning and mother’s behavior in manipulative tasks in infant marmosets. Am J Primatol 2009; 71(6): 503–509.

    PubMed  Google Scholar 

  28. Eslamboli A, Georgievska B, Ridley RM, Baker HF, Muzyczka N, Burger C, Mandel RJ, Annett L, Kirik D. Continuous low-level glial cell line-derived neurotrophic factor delivery using recombinant adeno-associated viral vectors provides neuroprotection and induces behavioral recovery in a primate model of Parkinson’s disease. J Neurosci 2005; 25(4): 769–777.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Hansard MJ, Smith LA, Jackson MJ, Cheetham SC, Jenner P. Dopamine, but not norepinephrine or serotonin, reuptake inhibition reverses motor deficits in 1-methyl-4-phenyl-1,2,3,6-tetrahydro- pyridine-treated primates. J Pharmacol Exp Ther 2002; 303(3): 952–958.

    CAS  PubMed  Google Scholar 

  30. Annett LE, Torres EM, Clarke DJ, Ishida Y, Barker RA, Ridley RM, Baker HF, Dunnett SB. Survival of nigral grafts within the striatum of marmosets with 6-OHDA lesions depends critically on donor embryo age. Cell Transplant 1997; 6(6): 557–569.

    CAS  PubMed  Google Scholar 

  31. Bezard E, Przedborski S. A tale on animal models of Parkinson’s disease. Mov Disord 2011; 26(6): 993–1002.

    PubMed  Google Scholar 

  32. Eslamboli A, Romero-Ramos M, Burger C, Bjorklund T, Muzyczka N, Mandel RJ, Baker H, Ridley RM, Kirik D. Longterm consequences of human alpha-synuclein overexpression in the primate ventral midbrain. Brain 2007; 130(Pt 3): 799–815.

    PubMed  Google Scholar 

  33. Sasaki E. Prospects for genetically modified non-human primate models, including the common marmoset. Neurosci Res 2015; 93: 110–115.

    CAS  PubMed  Google Scholar 

  34. Sasaki E, Suemizu H, Shimada A, Hanazawa K, Oiwa R, Kamioka M, Tomioka I, Sotomaru Y, Hirakawa R, Eto T, Shiozawa S, Maeda T, Ito M, Ito R, Kito C, Yagihashi C, Kawai K, Miyoshi H, Tanioka Y, Tamaoki N, Habu S, Okano H, Nomura T. Generation of transgenic non-human primates with germline transmission. Nature 2009; 459(7246): 523–527.

    CAS  PubMed  Google Scholar 

  35. Dawson TM, Ko HS, Dawson VL. Genetic animal models of Parkinson’s disease. Neuron 2010; 66(5): 646–661.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Santana M, Palmér T, Simplício H, Fuentes R, Petersson P. Characterization of long-term motor deficits in the 6-OHDA model of Parkinson’s disease in the common marmoset. Behav Brain Res 2015; 290: 90–101.

    CAS  PubMed  Google Scholar 

  37. Ando K, Obayashi S, Nagai Y, Oh-Nishi A, Minamimoto T, Higuchi M, Inoue T, Itoh T, Suhara T. PET analysis of dopaminergic neurodegeneration in relation to immobility in the MPTP-treated common marmoset, a model for Parkinson’s disease. PLoS One 2012; 7(10): e46371.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Langston JW, Ballard P, Tetrud JW, Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 1983; 219(4587): 979–980.

    CAS  PubMed  Google Scholar 

  39. Davis GC, Williams AC, Markey SP, Ebert MH, Caine ED, Reichert CM, Kopin IJ. Chronic Parkinsonism secondary to intravenous injection of meperidine analogues. Psychiatry Res 1979; 1(3): 249–254.

    CAS  PubMed  Google Scholar 

  40. Bezard E, Imbert C, Gross CE. Experimental models of Parkinson’s disease: from the static to the dynamic. Rev Neurosci 1998; 9(2): 71–90.

    CAS  PubMed  Google Scholar 

  41. Przedborski S, Jackson-Lewis V, Naini AB, Jakowec M, Petzinger G, Miller R, Akram M. The parkinsonian toxin 1-methyl-4- phenyl-1,2,3,6-tetrahydropyridine (MPTP): a technical review of its utility and safety. J Neurochem 2001; 76(5): 1265–1274.

    CAS  PubMed  Google Scholar 

  42. Chen MK, Kuwabara H, Zhou Y, Adams RJ, Brasiæ JR, McGlothan JL, Verina T, Burton NC, Alexander M, Kumar A, Wong DF, Guilarte TR. VMAT2 and dopamine neuron loss in a primate model of Parkinson’s disease. J Neurochem 2008; 105(1): 78–90.

    CAS  PubMed  Google Scholar 

  43. Bergman H, Raz A, Feingold A, Nini A, Nelken I, Hansel D, Ben-Pazi H, Reches A. Physiology of MPTP tremor. Mov Disord 1998; 13 Suppl 3: 29–34.

    PubMed  Google Scholar 

  44. Forno LS, DeLanney LE, Irwin I, Langston JW. Similarities and differences between MPTP-induced parkinsonsim and Parkinson’s disease. Neuropathologic considerations. Adv Neurol 1993; 60: 600–608.

    CAS  PubMed  Google Scholar 

  45. Serra PA, Pluchino S, Marchetti B, Desole MS, Miele E. The MPTP mouse model: cues on DA release and neural stem cell restorative role. Parkinsonism Relat Disord 2008; 14 Suppl 2: S189–S193.

    PubMed  Google Scholar 

  46. Mizuno Y, Sone N, Saitoh T. Effects of 1-methyl-4-phenyl- 1,2,3,6-tetrahydropyridine and 1-methyl-4-phenylpyridinium ion on activities of the enzymes in the electron transport system in mouse brain. J Neurochem 1987; 48(6): 1787–1793.

    CAS  PubMed  Google Scholar 

  47. Nicklas WJ, Vyas I, Heikkila RE. Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetra- hydropyridine. Life Sci 1985; 36(26): 2503–2508.

    CAS  PubMed  Google Scholar 

  48. Forno LS, Langston JW, DeLanney LE, Irwin I, Ricaurte GA. Locus ceruleus lesions and eosinophilic inclusions in MPTP- treated monkeys. Ann Neurol 1986; 20(4): 449–455.

    CAS  PubMed  Google Scholar 

  49. Eslamboli A. Marmoset monkey models of Parkinson’s disease: which model, when and why? Brain Res Bull 2005; 68(3): 140–149.

    PubMed  Google Scholar 

  50. Fox SH, Henry B, Hill M, Crossman A, Brotchie J. Stimulation of cannabinoid receptors reduces levodopa-induced dyskinesia in the MPTP-lesioned nonhuman primate model of Parkinson’s disease. Mov Disord 2002; 17(6): 1180–1187.

    PubMed  Google Scholar 

  51. Hansard MJ, Smith LA, Jackson MJ, Cheetham SC, Jenner P. Dopamine reuptake inhibition and failure to evoke dyskinesia in MPTP-treated primates. Eur J Pharmacol 2002; 451(2): 157–160.

    CAS  PubMed  Google Scholar 

  52. van der Stelt M, Fox SH, Hill M, Crossman AR, Petrosino S, Di Marzo V, Brotchie JM. A role for endocannabinoids in the generation of parkinsonism and levodopa-induced dyskinesia in MPTP-lesioned non-human primate models of Parkinson’s disease. FASEB J 2005; 19(9): 1140–1142.

    PubMed  Google Scholar 

  53. Rose S, Nomoto M, Jackson EA, Gibb WR, Jaehnig P, Jenner P, Marsden CD. Age-related effects of 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine treatment of common marmosets. Eur J Pharmacol 1993; 230(2): 177–185.

    CAS  PubMed  Google Scholar 

  54. Jackson-Lewis V, Przedborski S. Protocol for the MPTP mouse model of Parkinson’s disease. Nat Protoc 2007; 2(1): 141–151.

    CAS  PubMed  Google Scholar 

  55. Yang SC, Markey SP, Bankiewicz KS, London WT, Lunn G. Recommended safe practices for using the neurotoxin MPTP in animal experiments. Lab Anim Sci 1988; 38(5): 563–567.

    CAS  PubMed  Google Scholar 

  56. Tranzer JP, Thoenen H. Selective destruction of adrenergic nerve terminals by chemical analogues of 6-hydroxydopamine. Experientia 1973; 29(3): 314–315.

    CAS  PubMed  Google Scholar 

  57. Glinka Y, Gassen M, Youdim MB. Mechanism of 6-hydroxy-dopamine neurotoxicity. J Neural Transm Suppl 1997; 50: 55–66.

    CAS  PubMed  Google Scholar 

  58. Eslamboli A, Baker HF, Ridley RM, Annett LE. Sensorimotor deficits in a unilateral intrastriatal 6-OHDA partial lesion model of Parkinson’s disease in marmoset monkeys. Exp Neurol 2003; 183(2): 418–429.

    CAS  PubMed  Google Scholar 

  59. Annett LE, Torres EM, Ridley RM, Baker HF, Dunnett SB. A comparison of the behavioural effects of embryonic nigral grafts in the caudate nucleus and in the putamen of marmosets with unilateral 6-OHDA lesions. Exp Brain Res 1995; 103(3): 355–371.

    CAS  PubMed  Google Scholar 

  60. Henderson JM, Stanic D, Tomas D, Patch J, Horne MK, Bourke D, Finkelstein DI. Postural changes after lesions of the substantia nigra pars reticulata in hemiparkinsonian monkeys. Behav Brain Res 2005; 160(2): 267–276.

    PubMed  Google Scholar 

  61. Svenningsson P, Arts J, Gunne L, Andren PE. Acute and repeated treatment with L-DOPA increase c-jun expression in the 6- hydroxydopamine-lesioned forebrain of rats and common marmosets. Brain Res 2002; 955(1-2): 8–15.

    CAS  PubMed  Google Scholar 

  62. Garea-Rodríguez E, Schlumbohm C, Czéh B, König J, Helms G, Heckmann C, Meller B, Meller J, Fuchs E. Visualizing dopamine transporter integrity with iodine-123-FP-CIT SPECT in combination with high resolution MRI in the brain of the common marmoset monkey. J Neurosci Methods 2012; 210(2): 195–201.

    PubMed  Google Scholar 

  63. Duty S, Jenner P. Animal models of Parkinson’s disease: a source of novel treatments and clues to the cause of the disease. Br J Pharmacol 2011; 164(4): 1357–1391.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Annett LE, Rogers DC, Hernandez TD, Dunnett SB. Behavioural analysis of unilateral monoamine depletion in the marmoset. Brain 1992; 115 (Pt 3): 825–856.

    PubMed  Google Scholar 

  65. Mitchell IJ, Hughes N, Carroll CB, Brotchie JM. Reversal of parkinsonian symptoms by intrastriatal and systemic manipulations of excitatory amino acid and dopamine transmission in the bilateral 6-OHDA lesioned marmoset. Behav Pharmacol 1995; 6(5-6): 492–507.

    CAS  PubMed  Google Scholar 

  66. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT. Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci 2000; 3(12): 1301–1306.

    CAS  PubMed  Google Scholar 

  67. Cannon JR, Tapias V, Na HM, Honick AS, Drolet RE, Greenamyre JT. A highly reproducible rotenone model of Parkinson’s disease. Neurobiol Dis 2009; 34(2): 279–290.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Alam M, Schmidt WJ. Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats. Behav Brain Res 2002; 136(1): 317–324.

    CAS  PubMed  Google Scholar 

  69. Alam M, Schmidt WJ. L-DOPA reverses the hypokinetic behaviour and rigidity in rotenone-treated rats. Behav Brain Res 2004; 153(2): 439–446.

    CAS  PubMed  Google Scholar 

  70. Betarbet R, Canet-Aviles RM, Sherer TB, Mastroberardino PG, McLendon C, Kim JH, Lund S, Na HM, Taylor G, Bence NF, Kopito R, Seo BB, Yagi T, Yagi A, Klinefelter G, Cookson MR, Greenamyre JT. Intersecting pathways to neurodegeneration in Parkinson’s disease: effects of the pesticide rotenone on DJ-1, alpha-synuclein, and the ubiquitin-proteasome system. Neurobiol Dis 2006; 22(2): 404–420.

    CAS  PubMed  Google Scholar 

  71. Emborg ME. Nonhuman primate models of Parkinson’s disease. ILAR J 2007; 48(4): 339–355.

    CAS  PubMed  Google Scholar 

  72. Ando K, Maeda J, Inaji M, Okauchi T, Obayashi S, Higuchi M, Suhara T, Tanioka Y. Neurobehavioral protection by single dose l- deprenyl against MPTP-induced parkinsonism in common marmosets. Psychopharmacology (Berl) 2008; 195(4): 509–516.

    CAS  Google Scholar 

  73. Pearce RK, Jackson M, Britton DR, Shiosaki K, Jenner P, Marsden CD. Actions of the D1 agonists A-77636 and A-86929 on locomotion and dyskinesia in MPTP-treated L-dopa-primed common marmosets. Psychopharmacology (Berl) 1999; 142(1): 51–60.

    CAS  Google Scholar 

  74. Roberts AC, De Salvia MA, Wilkinson LS, Collins P, Muir JL, Everitt BJ, Robbins TW. 6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine. J Neurosci 1994; 14(5 Pt 1): 2531–2544.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Verhave PS, Vanwersch RA, van Helden HP, Smit AB, Philippens IH. Two new test methods to quantify motor deficits in a marmoset model for Parkinson’s disease. Behav Brain Res 2009; 200(1): 214–219.

    PubMed  Google Scholar 

  76. Przybyszewski AW, Sosale S, Chaudhuri A. Quantification of three-dimensional exploration in the cylinder test by the common marmoset (Callithrix jacchus). Behav Brain Res 2006; 170(1): 62–70.

    PubMed  Google Scholar 

  77. Palmér T, Tamtè M, Halje P, Enqvist O, Petersson P. A system for automated tracking of motor components in neurophysiological research. J Neurosci Methods 2012; 205(2): 334–344.

    PubMed  Google Scholar 

  78. Philippens IH, Melchers BP, Roeling TA, Bruijnzeel PL. Behavioral test systems in marmoset monkeys. Behav Res Methods Instrum Comput 2000; 32(1): 173–179.

    CAS  PubMed  Google Scholar 

  79. Annett LE, Martel FL, Rogers DC, Ridley RM, Baker HF, Dunnett SB. Behavioral assessment of the effects of embryonic nigral grafts in marmosets with unilateral 6-OHDA lesions of the nigrostriatal pathway. Exp Neurol 1994; 125(2): 228–246.

    CAS  PubMed  Google Scholar 

  80. Henderson JM, Annett LE, Torres EM, Dunnett SB. Behavioural effects of subthalamic nucleus lesions in the hemiparkinsonian marmoset (Callithrix jacchus). Eur J Neurosci 1998; 10(2): 689–698.

    CAS  PubMed  Google Scholar 

  81. Yamane J, Nakamura M, Iwanami A, Sakaguchi M, Katoh H, Yamada M, Momoshima S, Miyao S, Ishii K, Tamaoki N, Nomura T, Okano HJ, Kanemura Y, Toyama Y, Okano H. Transplantation of galectin-1-expressing human neural stem cells into the injured spinal cord of adult common marmosets. J Neurosci Res 2010; 88(7): 1394–1405.

    CAS  PubMed  Google Scholar 

  82. Montoya CP, Astell S, Dunnett SB. Effects of nigral and striatal grafts on skilled forelimb use in the rat. Prog Brain Res 1990; 82: 459–466.

    CAS  PubMed  Google Scholar 

  83. Montoya CP, Campbell-Hope LJ, Pemberton KD, Dunnett SB. The “staircase test”: a measure of independent forelimb reaching and grasping abilities in rats. J Neurosci Methods 1991; 36(2-3): 219–228.

    CAS  PubMed  Google Scholar 

  84. Blesa J, Juri C, Collantes M, Peñuelas I, Prieto E, Iglesias E, Martí-Climent J, Arbizu J, Zubieta JL, Rodríguez-Oroz MC, García-García D, Richter JA, Cavada C, Obeso JA. Progression of dopaminergic depletion in a model of MPTP-induced Parkinsonism in non-human primates. An (18)F-DOPA and (11)C-DTBZ PET study. Neurobiol Dis 2010; 38(3): 456–463.

    CAS  PubMed  Google Scholar 

  85. Nagai Y, Minamimoto T, Ando K, Obayashi S, Ito H, Ito N, Suhara T. Correlation between decreased motor activity and dopaminergic degeneration in the ventrolateral putamen in monkeys receiving repeated MPTP administrations: a positron emission tomography study. Neurosci Res 2012; 73(1): 61–67.

    CAS  PubMed  Google Scholar 

  86. Alexoff DL, Vaska P, Marsteller D, Gerasimov T, Li J, Logan J, Fowler JS, Taintor NB, Thanos PK, Volkow ND. Reproducibility of 11C-raclopride binding in the rat brain measured with the microPET R4: effects of scatter correction and tracer specific activity. J Nucl Med 2003; 44(5): 815–822.

    CAS  PubMed  Google Scholar 

  87. Collantes M, Prieto E, Peñuelas I, Blesa J, Juri C, Martí-Climent JM, Quincoces G, Arbizu J, Riverol M, Zubieta JL, Rodriguez-Oroz MC, Luquin MR, Richter JA, Obeso JA. New MRI, 18F- DOPA and 11C-(+)-alpha-dihydrotetrabenazine templates for Macaca fascicularis neuroimaging: advantages to improve PET quantification. Neuroimage 2009; 47(2): 533–539.

    CAS  PubMed  Google Scholar 

  88. Brown CA, Campbell MC, Karimi M, Tabbal SD, Loftin SK, Tian LL, Moerlein SM, Perlmutter JS. Dopamine pathway loss in nucleus accumbens and ventral tegmental area predicts apathetic behavior in MPTP-lesioned monkeys. Exp Neurol 2012; 236(1): 190–197.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Doudet DJ, Chan GL, Holden JE, McGeer EG, Aigner TA, Wyatt RJ, Ruth TJ. 6-[18F]Fluoro-L-DOPA PET studies of the turnover of dopamine in MPTP-induced parkinsonism in monkeys. Synapse 1998; 29(3): 225–232.

    CAS  PubMed  Google Scholar 

  90. Lundkvist C, Halldin C, Ginovart N, Swahn CG, Farde L. [18F] beta-CIT-FP is superior to [11C] beta-CIT-FP for quantitation of the dopamine transporter. Nucl Med Biol 1997; 24(7): 621–627.

    CAS  PubMed  Google Scholar 

  91. Saiki H, Hayashi T, Takahashi R, Takahashi J. Objective and quantitative evaluation of motor function in a monkey model of Parkinson’s disease. J Neurosci Methods 2010; 190(2): 198–204.

    CAS  PubMed  Google Scholar 

  92. Schultz-Darken NJ. Sample collection and restraint techniques used for common marmosets (Callithrix jacchus). Comp Med 2003; 53(4): 360–363.

    CAS  PubMed  Google Scholar 

  93. Pavese N, Brooks DJ. Imaging neurodegeneration in Parkinson’s disease. Biochim Biophys Acta 2009; 1792(7): 722–729.

    CAS  PubMed  Google Scholar 

  94. Miletich RS, Bankiewicz KS, Quarantelli M, Plunkett RJ, Frank J, Kopin IJ, Di Chiro G. MRI detects acute degeneration of the nigrostriatal dopamine system after MPTP exposure in hemi-parkinsonian monkeys. Ann Neurol 1994; 35(6): 689–697.

    CAS  PubMed  Google Scholar 

  95. Stephan H, Baron G, Schwerdtfeger WK. The brain of the common marmoset (Callithrix jacchus): a Stereotaxic Atlas, Springer-Verlag, Berlin, 1980.

    Google Scholar 

  96. Brownell AL, Jenkins BG, Elmaleh DR, Deacon TW, Spealman RD, Isacson O. Combined PET/MRS brain studies show dynamic and long-term physiological changes in a primate model of Parkinson disease. Nat Med 1998; 4(11): 1308–1312.

    CAS  PubMed  Google Scholar 

  97. Gröger A, Kolb R, Schäfer R, Klose U. Dopamine reduction in the substantia nigra of Parkinson’s disease patients confirmed by in vivo magnetic resonance spectroscopic imaging. PLoS One 2014; 9(1): e84081.

    PubMed  PubMed Central  Google Scholar 

  98. Hong Z, Shi M, Chung KA, Quinn JF, Peskind ER, Galasko D, Jankovic J, Zabetian CP, Leverenz JB, Baird G, Montine TJ, Hancock AM, Hwang H, Pan C, Bradner J, Kang UJ, Jensen PH, Zhang J. DJ-1 and alpha-synuclein in human cerebrospinal fluid as biomarkers of Parkinson’s disease. Brain 2010; 133(Pt 3): 713–726.

    PubMed  PubMed Central  Google Scholar 

  99. Shi M, Zabetian CP, Hancock AM, Ginghina C, Hong Z, Yearout D, Chung KA, Quinn JF, Peskind ER, Galasko D, Jankovic J, Leverenz JB, Zhang J. Significance and confounders of peripheral DJ-1 and alpha-synuclein in Parkinson’s disease. Neurosci Lett 2010; 480(1): 78–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Haavik J, Toska K. Tyrosine hydroxylase and Parkinson’s disease. Mol Neurobiol 1998; 16(3): 285–309.

    CAS  PubMed  Google Scholar 

  101. Barcia C, Ros CM, Annese V, Gómez A, Ros-Bernal F, Aguado-Yera D, Martínez-Pagán ME, de Pablos V, Fernandez-Villalba E, Herrero MT. IFN-γ signaling, with the synergistic contribution of TNF-α, mediates cell specific microglial and astroglial activation in experimental models of Parkinson’s disease. Cell Death Dis 2011; 2: e142.

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Takagi Y, Takahashi J, Saiki H, Morizane A, Hayashi T, Kishi Y, Fukuda H, Okamoto Y, Koyanagi M, Ideguchi M, Hayashi H, Imazato T, Kawasaki H, Suemori H, Omachi S, Iida H, Itoh N, Nakatsuji N, Sasai Y, Hashimoto N. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 2005; 115(1): 102–109.

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Kikuchi T, Morizane A, Doi D, Onoe H, Hayashi T, Kawasaki T, Saiki H, Miyamoto S, Takahashi J. Survival of human induced pluripotent stem cell-derived midbrain dopaminergic neurons in the brain of a primate model of Parkinson’s disease. J Parkinsons Dis 2011; 1(4): 395–412.

    CAS  PubMed  Google Scholar 

  104. Kordower JH, Emborg ME, Bloch J, Ma SY, Chu Y, Leventhal L, McBride J, Chen EY, Palfi S, Roitberg BZ, Brown WD, Holden JE, Pyzalski R, Taylor MD, Carvey P, Ling Z, Trono D, Hantraye P, Déglon N, Aebischer P. Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson’s disease. Science 2000; 290(5492): 767–773.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Experimental Animal Research, Biomedical Research Institute, Seoul National University Hospital, Seoul, Korea

    Jun-Won Yun, Jae-Bum Ahn & Byeong-Cheol Kang

  2. Graduate School of Translational Medicine, Seoul National University College of Medicine, 101 Daehakro, Jongno-gu, Seoul, 110-744, Korea

    Jae-Bum Ahn & Byeong-Cheol Kang

  3. Designed Animal Research Center, Institute of GreenBio Science Technology, Seoul National University, Pyeongchang-gun, Gangwon, Korea

    Byeong-Cheol Kang

Authors
  1. Jun-Won Yun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jae-Bum Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Byeong-Cheol Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Byeong-Cheol Kang.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yun, JW., Ahn, JB. & Kang, BC. Modeling Parkinson’s disease in the common marmoset (Callithrix jacchus): overview of models, methods, and animal care. Lab Anim Res 31, 155–165 (2015). https://doi.org/10.5625/lar.2015.31.4.155

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.5625/lar.2015.31.4.155

Keywords

Laboratory Animal Research

ISSN: 2233-7660