Rat model of Parkinson's disease: Chronic central delivery of 1-methyl-4-phenylpyridinium (MPP+)

Experimental Neurology

Volumn 200, Issue 1, 2006, Pages 172-183

  Yazdani, U ^a   German, D C ^a   Liang, C L ^a   Manzino, L ^b   Sonsalla, P K ^b   Zeevalk, G D ^b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Chronic model; Dopamine; Inclusion bodies; Neurodegeneration; Stereology; Substantia nigra

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; ALPHA SYNUCLEIN; DOPAMINE; TYROSINE 3 MONOOXYGENASE; UBIQUITIN;

ADIPSIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APHAGIA; ARTICLE; BRAIN VENTRICLE; CELL INCLUSION; CONTROLLED STUDY; ELECTRON MICROSCOPE; IMMUNOREACTIVITY; LEWY BODY; MALE; MITOCHONDRION; MORTALITY; NERVE DEGENERATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OSMOTIC MINIPUMP; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; STRESS;

1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; INJECTIONS, INTRAVENTRICULAR; MALE; PARKINSON DISEASE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY; SURVIVAL RATE;

EID: 33746089104     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2006.02.002     Document Type: Article

References (59)

1. Altar A., Neve K.A., Loughlin S.E., Marshall J.F., and Fallon J.H. The crossed mesostriatal projection: neurochemistry and developmental response to lesion. Brain Res. 279 (1983) 1-8
2. Berger K., Przedborski S., and Cadet J.L. Retrograde degeneration of nigrostriatal neurons induced by intrastriatal injection in rats. Brain Res. Bull. 26 (1991) 301-307
3. Bernardini G., Speciale S.G., and German D.C. Increased midbrain dopaminergic cell activity following 2′CH3-MPTP-induced dopaminergic cell loss: an in vitro electrophysiological study. Brain Res. 527 (1990) 123-129
4. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., and Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3 (2000) 1301-1306
5. Bizat N., Hermel J.-M., Boyer F., Jacquard C., Creminon C., Quary S., Escartin C., Hantraye P., Krajewski S., and Brouillet E. Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: implications for Huntington's disease. J. Neurosci. 23 (2003) 5020-5030
6. Boveris A., and Chance B. The mitochondrial generation of hydrogen peroxide. Biochem. J. 134 (1973) 707-716
7. Braak E., Sandmann-Keil D., Rub U., Gai WP., deVos RA., Steur E.N., Arai K., and Braak H. Alpha-synuclein immunopositive Parkinson's disease-related inclusion bodies in lower brain stem nuclei. Acta Neuropathol. 101 (2001) 195-201
8. Fornai F., Lenzi P., Gesi M., Ferrucci M., Lazzeri G., Busceti C., Ruffoli R., Soldani P., Ruggieri S., Alessandri M.G., and Paparelli A. Fine structure and biochemical mechanisms underlying nigrostriatal inclusions and cell death after proteasome inhibition. J. Neurosci. 23 (2003) 8955-8966
9. Fornai F., Schluter O.M., Lenzi P., Gesi M., Ruffoli R., Ferrucci M., Lazzeri G., Busceti C.L., Pontarelli F., Battaglia G., Pellegrini A., Nicoletti F., Ruggieri S., Paperelli A., and Sudhof T.C. Parkinson-like syndrome induced by continuous MPTP infusion: convergent roles of the ubiquitin-proteasome system and alpha-synuclein. Proc. Natl. Acad. Sci. 102 (2005) 3413-3418
10. Forno L.S. The Lewy body in Parkinson's disease. Adv. Neurol. 45 (1986) 35-43
11. Forno L.S. Neuropathology of Parkinson's disease. J. Neuropathol. Exp. Neurol. 55 (1996) 259-272
12. Forno L.S., Langston J.W., DeLanney L., and Irwin I. An electron microscopic study of MPTP-induced inclusions bodies in an old monkey. Brain Res. 448 (1988) 150-157
13. Gai W.P., Yuan H.X., Li X.Q., Power J.T.H., Blumbergs P.C., and Jensen P.H. In situ and in vitro study of colocalization and segregation of alpha-synuclein, ubiquitin and lipids in Lewy bodies. Exp. Neurol. 166 (2000) 324-333
14. Ganguly A., Oo T.F., Rzhetskaya M., Pratt R., Yarygina O., Momoi T., Kholodilov N., and Burke R.E. CEP11004, a novel inhibitor of the mixed lineage kinases, suppresses apoptotic death in dopamine neurons of the substantia nigra induced by 6-hydroxydopamine. J. Neurochem. 88 (2004) 469-480
15. German D.C., and Manaye K.F. Midbrain dopaminergic neurons (nuclei A8, A9 and A10): 3-dimensional reconstruction in the rat. J. Comp. Neurol. 331 (1993) 297-309
16. German D.C., Dubach M., Askari S., Special S.G., and Bowden D.M. 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine-induced parkinsonian syndrome in Macaca fascicularis. Which midbrain dopaminergic neurons are lost?. Neuroscience 24 (1988) 161-174
17. German D.C., Manaye K., Smith W.K., Woodward D.J., and Saper C.B. Midbrain dopaminergic cell loss in Parkinson's disease: computer visualization. Ann. Neurol. 26 (1989) 507-514
18. Giovanni A., Sieber B.A., Heikkila R.E., and Sonsalla P.K. Studies on species sensitivity to the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Part I: Systemic administration. J. Pharmacol. Exp. Ther. 270 (1994) 1000-1008
19. Hald A., and Lotharius J. Oxidative stress and inflammation in Parkinson's disease: is there a causal link?. Exp. Neurol. 193 (2005) 279-290
20. Hassler R. Zur pathologischen anatomie des senilen und des parkinsonistichen tremor. J. Psychol. Neurol. 49 (1939) 13-55
21. Heikkila R.E., Hess A., and Duvoisin R.C. Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6 tetrahydropyridine in mice. Science 224 (1984) 1451-1453
22. Heikkila R.E., Sieber B.A., Manzino L., and Sonsalla P.K. Some features of the nigrostriatal dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in the mouse. Mol. Chem. Neuropathol. 10 (1989) 171-183
23. Hoglinger G.U., Feger J., Prigent A., Michel P.P., Parain K., Champy P., Ruberg M., Oertel W.H., and Hirsch E.C. Chronic systemic complex I inhibition induces a hypokinetic multisystem degeneration in rats. J. Neurochem. 84 (2003) 491-502
24. Hornykiewicz O., and Kish S.J. Biochemical pathophysiology of Parkinson's disease. Adv. Neurol. 45 (1986) 19-34
25. Jenner P. Oxidative stress in Parkinson's disease. Ann. Neurol. 53 (2003) S26-S36
26. Korf J., and Venema K. Amino acids in the substantia nigra of rats with striatal lesions produced by kainic acid. J. Neurochem. 40 (1983) 1171-1173
27. Lapointe N., St.-Hilaire M., Martinoli M.G., Blanchet J., Gould P., Rouillard C., and Cicchetti F. Rotenone induces non-specific central nervous system and systemic toxicity. FASEB J. 18 (2004) 717-719
28. Liang C.-L., Kozlowski G.P., and German D.C. Leucine-enkephalin afferents to midbrain dopaminergic neurons: light and electron microscopic examination. J. Comp. Neurol. 332 (1993) 269-281
29. Lin W.-L., Delucia M.W., and Dickson D.W. Alpha-synuclein immunoreactivity in neuronal nuclear inclusions and neuritis in multiple system atrophy. Neurosci. Lett. 354 (2004) 99-102
30. Liu Y.B., Fiskum G., and Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80 (2002) 780-787
31. McNaught K.St.P., and Jenner P. Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci. Lett. 297 (2001) 191-194
32. McNaught K.St.P., Perl D.P., Brownell A.-L., and Olanow C.W. Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's disease. Ann. Neurol. 56 (2004) 149-162
33. Meredith G.E., Totterdell S., Petroske E., Santa Cruz K., Callison R.C., and Lau Y.-S. Lysosomal malfunction accompanies alpha-synuclein aggregation in a progressive mouse model of Parkinson's disease. Brain Res. 956 (2002) 156-165
34. Meredith G.E., Halliday G.M., and Totterdell S. A critical review of the development and importance of proteinaceous aggregates in animal models of Parkinson's disease: new insights into Lewy body formation. Parkinsonism Relat. Disord. 10 (2004) 191-202
35. Mithofer K., Sandy M.S., Smith M.T., and DiMonte D. Mitochondrial poisons cause depletion of reduced glutathione in isolated hepatocytes. Arch. Biochem. Biophys. 295 (1992) 132-136
36. Mizukawa K., Sora Y.H., and Ogawa N. Ultrastructural changes of the substantia nigra, ventral tegmental area and striatum in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice. Res. Commun. Chem. Pathol. Pharmacol. 67 (1990) 307-320
37. Nomoto M., Iwata S.I., Kaseda S., Fukuda T., and Nakagawa S. Increased dopamine turnover in the putamen after MPTP treatment in common marmosets. Brain Res. 767 (1997) 235-238
38. Parker W.D., Boyson S.J., and Parks J.K. Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann. Neurol. 26 (1989) 719-733
39. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, Orlando
40. Petroske E., Meredith G.E., Callen S., Totterdell S., and Lau Y.S. Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience 106 (2001) 589-601
41. Ricaurte G.A., Langston J.W., DeLanney L.E., Irwin I., Peroutka S.J., and Forno L.S. Fate of nigrostriatal neurons in young mature mice given 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: a neurochemical and morphological reassessment. Brain Res. 376 (1986) 117-124
42. Rodriguez-Enriquez S., He L., and LeMasters J.J. Role of mitochondrial permeability transition pores in mitochondrial autophagy. Int. J. Biochem. Cell Biol. 36 (2004) 2463-2472
43. Roy S., and Wolman L. Ultrastructural observations in Parkinsonism. J. Pathol. 99 (1969) 39-44
44. Sapolsky R.M. Stress, the Aging Brain, and the Mechanisms of Neuron Death (1992), MIT Press, Cambridge, MA
45. Sauer H., and Oertel W.H. Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine; a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience 59 (1994) 401-415
46. Schapira A.H., Cooper J.M., Dexter D., Clark J.B., Jenner P., and Marsden C.D. Complex I deficiency in Parkinson's disease. J. Neurochem. 54 (1990) 823-827
47. Smith A.D., Castro S.L., and Zigmond M.J. Stress-induced Parkinson's disease: a working hypothesis. Physiol. Behav. 77 (2002) 527-531
48. Song D.D., Shults C.W., Sisk A., Rockenstein E., and Masliah E. Enhanced substantia nigra mitochondrial pathology in human alpha-synuclein transgenic mice after treatment with MPTP. Exp. Neurol. 186 (2004) 158-172
49. Takahashi H., Iwanaga K., Egawa S., and Ikuta F. Ultrastructural relationship between Lewy bodies and pale bodies studied in locus ceruleus neurons of a non-Parkinsonian patient. Neuropathology 14 (1994) 73-80
50. Tanaka J., Nakamura H., Honda S., Takada K., and Kato S. Neuropathological study on 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine of the crab-eating monkey. Acta Neuropathol. 75 (1988) 370-376
51. Thiffault C., Langston J.W., and DiMonte D.A. Increased striatal dopamine turnover following acute administration of rotenone to mice. Brain Res. 885 (2000) 283-288
52. Thiruchelvam M., McCormack A., Richfield E.K., Baggs R.B., Tank A.W., DiMonte D.A., and Cory-Slechta D.A. Age-related irreversible progressive nigrostriatal dopaminergic neurotoxicity in the paraquat and maneb model of the Parkinson's disease phenotype. Eur. J. Neurosci. 18 (2003) 589-600
53. 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 (2000) 37-50
54. Urakami K., Masaki N., Shimoda K., Nishikawa S., and Takahashi K. Increase of striatal dopamine turnover by stress in MPTP-treated mice. Clin. Neuropharmacol. 11 (1988) 360-368
55. Yong V.W., Perry T.L., and Krisman A.A. Depletion of glutathione in brainstem of mice caused by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine is prevented by antioxidant pretreatment. Neurosci. Lett. 63 (1986) 56-60
56. Zeevalk G.D., and Bernard L.P. Energy status, oxidative stress and ubiquitin proteasomal function during chronic and acute complex I inhibition with rotenone in mesencephalic cultures. Antioxid. Redox Signal. 7 (2005) 662-672
57. Zeevalk G.D., and Nicklas W.J. Mechanisms underlying initiation of excitotoxicity associated with metabolic inhibition. J. Pharmacol. Exp. Ther. 257 (1991) 870-878
58. Zeevalk G.D., Manzino L., and Sonsalla P.K. Protection of malonate-induced GABA but not dopamine loss by GABA transporter blockade in rat striatum. Exp. Neurol. 176 (2002) 193-202
59. Zigmond M.J., Hastings T.G., and Abercrombie E.D. Neurochemical responses to 6-hydroxydopamine and l-dopa therapy: implications for Parkinson's disease. Ann. N. Y. Acad. Sci. 648 (1992) 71-86