Development of a stable, early stage unilateral model of Parkinson's disease in middle-aged rhesus monkeys

Experimental Neurology

Volumn 212, Issue 2, 2008, Pages 431-439

  Ding, Feng ^a,b   Luan, Liming ^a,b   Ai, Yi ^b   Walton, Ashley ^b   Gerhardt, Greg A ^b   Gash, Don M ^b   Grondin, Richard ^b   Zhang, Zhiming ^b  

^a SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BEHAVIOR; COMPARATIVE STUDY; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FEMALE; METABOLITE; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PATHOLOGY; PRIORITY JOURNAL; RHESUS MONKEY; SUBSTANTIA NIGRA;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; AGE FACTORS; ANIMALS; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION ROUTES; FEMALE; FUNCTIONAL LATERALITY; MACACA MULATTA; PARKINSONIAN DISORDERS; SUBSTANTIA NIGRA;

EID: 47349086425     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.04.027     Document Type: Article

References (56)

1. Albanese A., Granata R., Gregori B., Piccardi M.P., Colosimo C., and Tonali P. Chronic administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine to monkeys: behavioural, morphological and biochemical correlates. Neuroscience 55 3 (1993) 823-832
2. Alexander G.M., Schwartzman R.J., Brainard L., Gordon S.W., and Grothusen J.R. Changes in brain catecholamines and dopamine uptake sites at different stages of MPTP parkinsonism in monkeys. Brain Res. 588 2 (1992) 261-269
3. Andersen A.H., Zhang Z., Zhang M., Gash D.M., and Avison M.J. Age-associated changes in rhesus CNS composition identified by MRI. Brain Res. 829 1-2 (1999) 90-98
4. Araki T., Sasaki Y., and Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305 5686 (2004) 1010-1013
5. Ballard P.A., Tetrud J.W., and Langston J.W. Permanent human parkinsonism due to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP): seven cases. Neurology 35 7 (1985) 949-956
6. Bankiewicz K.S., Oldfield E.H., Chiueh C.C., Doppman J.L., Jacobowitz D.M., and Kopin I.J. Hemiparkinsonism in monkeys after unilateral internal carotid artery infusion of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Life Sci 39 (1986) 7-16
7. Bender K., Newsholme P., Brennan L., and Maechler P. The importance of redox shuttles to pancreatic beta-cell energy metabolism and function. Biochem. Soc. Trans. 34 pt 5 (2006) 811-814
8. Bohnen N.I., Albin R.L., Koeppe R.A., Wernette K.A., Kilbourn M.R., Minoshima S., and Frey K.A. Positron emission tomography of monoaminergic vesicular binding in aging and Parkinson disease. J. Cereb. Blood Flow Metab. 26 9 (2006) 1198-1212
9. Brooks D.J., Salmon E.P., Mathias C.J., Quinn N., Leenders K.L., Bannister R., Marsden C.D., and Frackowiak R.S. The relationship between locomotor disability, autonomic dysfunction, and the integrity of the striatal dopaminergic system in patients with multiple system atrophy, pure autonomic failure, and Parkinson's disease, studied with PET. Brain 113 Pt 5 (1990) 1539-1552
10. Collier T.J., Lipton J., Daley B.F., Palfi S., Chu Y., Sortwell C., Bakay R.A., Sladek Jr. J.R., and Kordower J.H. Aging-related changes in the nigrostriatal dopamine system and the response to MPTP in nonhuman primates: diminished compensatory mechanisms as a prelude to parkinsonism. Neurobiol. Dis. 26 1 (2007) 56-65
11. Crossman A.R., Clarke C.E., Boyce S., Robertson R.G., and Sambrook M.A. "MPTP-induced parkinsonism in the monkey: neurochemical pathology, complications of treatment and pathophysiological mechanisms.". Can. J. Neurol. Sci. 14 3 Suppl (1987) 428-435
12. Davis G.C., Williams A.C., Markey S.P., Ebert M.H., Caine E.D., Reichert C.M., and Kopin I.J. Chronic Parkinsonism secondary to intravenous injection of meperidine analogues. Psychiatry Res. 1 3 (1979) 249-254
13. Degryse A.D., and Colpaert F.C. Symptoms and behavioral features induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in an old Java monkey [Macaca cynomolgus fascicularis (Raffles)]. Brain Res. Bull. 16 5 (1986) 561-571
14. Elsworth J.D., Deutch A.Y., Redmond Jr. D.E., Taylor J.R., Sladek Jr. J.R., and Roth R.H. Symptomatic and asymptomatic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primates: biochemical changes in striatal regions. Neuroscience 33 2 (1989) 323-331
15. Fearnley J.M., and Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114 Pt 5 (1991) 2283-2301
16. Finkel E. The mitochondrion: is it central to apoptosis?. Science 292 5517 (2001) 624-626
17. Gash D.M., Zhang Z., Cass W.A., Ovadia A., Simmerman L., Martin D., Russell D., Collins F., Hoffer B.J., and Gerhardt G.A. Morphological and functional effects of intranigrally administered GDNF in normal rhesus monkeys. J. Comp. Neurol. 363 3 (1995) 345-358
18. Gash D.M., Zhang Z., Ovadia A., Cass W.A., Yi A., Simmerman L., Russell D., Martin D., Lapchak P.A., Collins F., Hoffer B.J., and Gerhardt G.A. Functional recovery in parkinsonian monkeys treated with GDNF. Nature 380 6571 (1996) 252-255
19. Gerhardt G.A., Cass W.A., Yi A., Zhang Z., and Gash D.M. Changes in somatodendritic but not terminal dopamine regulation in aged rhesus monkeys. J. Neurochem. 80 1 (2002) 168-177
20. Grondin R., Zhang Z., Yi A., Cass W.A., Maswood N., Andersen A.H., Elsberry D.D., Klein M.C., Gerhardt G.A., and Gash D.M. Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 125 Pt 10 (2002) 2191-2201
21. Hantraye P., Varastet M., Peschanski M., Riche D., Cesaro P., Willer J.C., and Maziere M. Stable parkinsonian syndrome and uneven loss of striatal dopamine fibres following chronic MPTP administration in baboons. Neuroscience 53 1 (1993) 169-178
22. Irwin I., Delanney L., Chan P., Sandy M.S., Di Monte D.A., and Langston J.W. Nigrostriatal monoamine oxidase A and B in aging squirrel monkeys and C57BL/6 mice. Neurobiol. Aging 18 2 (1997) 235-241
23. Jellinger K.A. Recent developments in the pathology of Parkinson's disease. J. Neural Transm., Suppl. 62 (2002) 347-376
24. Jakowec M.W., and Petzinger G.M. 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned model of parkinson's disease, with emphasis on mice and nonhuman primates. Comp. Med 54 (2004) 497-513
25. Kirik D., Rosenblad C., and Bjorklund A. Preservation of a functional nigrostriatal dopamine pathway by GDNF in the intrastriatal 6-OHDA lesion model depends on the site of administration of the trophic factor. Eur. J. Neurosci. 12 11 (2000) 3871-3882
26. Kish S.J., Shannak K., and Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N. Engl. J. Med. 318 14 (1988) 876-880
27. Kish S.J., Tong J., Hornykiewicz O., Rajput A., Chang L.J., Guttman M., and Furukawa Y. Preferential loss of serotonin markers in caudate versus putamen in Parkinson's disease. Brain 131 (2008) 120-131
28. Kraytsberg Y., Kudryavtseva E., McKee A.C., Geula C., Kowall N.W., and Khrapko K. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet. 38 5 (2006) 518-520
29. Kurlan R., Kim M., and Gash D.M. Time course and magnitude of spontaneous recovery of parkinsonism produced by intracarotid administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine to monkeys. Ann. Neurol. 29 6 (1991) 677-679
30. Lang A.E., and Lozano A.M. Parkinson's disease. First of two parts. N. Engl. J. Med. 339 15 (1998) 1044-1053
31. Lang A.E., and Lozano A.M. Parkinson's disease. Second of two parts. N. Engl. J. Med. 339 16 (1998) 1130-1143
32. Langston J.W., and Ballard Jr. P.A. Parkinson's disease in a chemist working with 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. N. Engl. J. Med. 309 5 (1983) 310
33. Lee C.S., Schulzer M., de la Fuente-Fernandez R., Mak E., Kuramoto L., Sossi V., Ruth T.J., Calne D.B., and Stoessl A.J. Lack of regional selectivity during the progression of Parkinson disease: implications for pathogenesis. Arch. Neurol. 61 12 (2004) 1920-1925
34. Mayeux R., Marder K., Cote L.J., Denaro J., Hemenegildo N., Mejia H., Tang M.X., Lantigua R., Wilder D., and Gurland B. The frequency of idiopathic Parkinson's disease by age, ethnic group, and sex in northern Manhattan, 1988-1993. Am. J. Epidemiol. 142 8 (1995) 820-827
35. McCormack A.L., Di Monte D.A., Delfani K., Irwin I., DeLanney L.E., Langston W.J., and Janson A.M. Aging of the nigrostriatal system in the squirrel monkey. J. Comp. Neurol. 471 4 (2004) 387-395
36. Moratalla R., Quinn B., DeLanney L.E., Irwin I., Langston J.W., and Graybiel A.M. 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. U. S. A. 89 9 (1992) 3859-3863
37. Mounayar S., Boulet S., Tande D., Jan C., Pessiglione M., Hirsch E.C., Feger J., Savasta M., Francois C., and Tremblay L. A new model to study compensatory mechanisms in MPTP-treated monkeys exhibiting recovery. Brain 130 (2007) 2898-2914
38. Narabayashi H. Similarity and dissimilarity of MPTP models to Parkinson's disease: importance of juvenile parkinsonism. Eur. Neurol. 26 Suppl 1 (1987) 24-29
39. Nicklas W.J., Vyas I., and Heikkila R.E. 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-tetrahydropyridine. Life Sci. 36 26 (1985) 2503-2508
40. Ovadia A., Zhang Z., and Gash D.M. Increased susceptibility to MPTP toxicity in middle-aged rhesus monkeys. Neurobiol. Aging 16 6 (1995) 931-937
41. Parkinson J. An essay on the shaking palsy. J. Neuropsychiatry Clin. Neurosci. 14 (2002) 223-236
42. Perez-Otano I., Oset C., Luquin M.R., Herrero M.T., Obeso J.A., and Del Rio J. MPTP-induced parkinsonism in primates: pattern of striatal dopamine loss following acute and chronic administration. Neurosci. Lett. 175 1-2 (1994) 121-125
43. Petzinger G.M., and Langston J.W. Advances in neurodegenerative disorders. Parkinson's Disease. Chapter 4. The MPTP-Lesioned Non-Human Primate: A Model for Parkinson's Disease 1 (1998), Prominent Press, Scottsdale
44. Pifl C., and Hornykiewicz O. Dopamine turnover is upregulated in the caudate/putamen of asymptomatic MPTP-treated rhesus monkeys. Neurochem. Int. 49 5 (2006) 519-524
45. Pifl C., Schingnitz G., and Hornykiewicz O. The neurotoxin MPTP does not reproduce in the rhesus monkey the interregional pattern of striatal dopamine loss typical of human idiopathic Parkinson's disease. Neurosci. Lett. 92 2 (1988) 228-233
46. Pifl C., Schingnitz G., and 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 44 3 (1991) 591-605
47. Przedborski S., Tieu K., Perier C., and Vila M. MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J. Bioenerg. Biomembranes 36 4 (2004) 375-379
48. Ramsay R.R., Salach J.I., and Singer T.P. Uptake of the neurotoxin 1-methyl-4-phenylpyridine (MPP+) by mitochondria and its relation to the inhibition of the mitochondrial oxidation of NAD+-linked substrates by MPP+. Biochem. Biophys. Res. Commun. 134 2 (1986) 743-748
49. Rose S., Nomoto M., Jackson E.A., Gibb W.R., Jaehnig P., Jenner P., and Marsden C.D. Age-related effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine treatment of common marmosets. Eur. J. Pharmacol. 230 2 (1993) 177-185
50. Sasaki Y., Araki T., and Milbrandt J. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J. Neurosci. 26 33 (2006) 8484-8491
51. Schneider J.S., Yuwiler A., and Markham C.H. "Selective loss of subpopulations of ventral mesencephalic dopaminergic neurons in the monkey following exposure to MPTP.". Brain Res. 411 1 (1987) 144-150
52. Smigrodzki R., Parks J., and Parker W.D. High frequency of mitochondrial complex I mutations in Parkinson's disease and aging. Neurobiol. Aging 25 10 (2004) 1273-1281
53. Soderstrom K., O'Malley J., Steece-Collier K., and Kordower J.H. Neural repair strategies for Parkinson's disease: insights from primate models. Cell Transplant 15 (2006) 251-265
54. Trimmer P.A., Swerdlow R.H., Parks J.K., Keeney P., Bennett Jr. J.P., Miller S.W., Davis R.E., and Parker Jr. W.D. Abnormal mitochondrial morphology in sporadic Parkinson's and Alzheimer's disease cybrid cell lines. Exp. Neurol. 162 1 (2000) 37-50
55. Walton A., Branham A., Gash D.M., and Grondin R. Automated video analysis of age-related motor deficits in monkeys using EthoVision. Neurobiol. Aging 27 10 (2006) 1477-1483
56. Zhang Z., Andersen A.H., Ai Y., Loveland A., Hardy P.A., Gerhardt G.A., and Gash D.M. Assessing nigrostriatal dysfunctions by pharmacological MRI in parkinsonian rhesus macaques. Neuroimage 33 (2006) 636-643