Differences between subacute and chronic MPTP mice models: Investigation of dopaminergic neuronal degeneration and α-synuclein inclusions

Journal of Neurochemistry

Volumn 109, Issue 5, 2009, Pages 1469-1482

  Gibrat, Claire ^a   Saint Pierre, Martine ^a   Bousquet, Mélanie ^a   Lévesque, Daniel ^b   Rouillard, Claude ^a,c   Cicchetti, Francesca ^a,c  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

Animal models; Dopamine; Neurodegeneration; Nurr1; Parkinson's disease; Tyrosine hydroxylase

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ALPHA SYNUCLEIN; NUCLEAR RECEPTOR RELATED FACTOR 1; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC TOXICITY; CONTROLLED STUDY; CYTOPLASM; DOPAMINERGIC NERVE CELL; IMMUNOREACTIVITY; MALE; MOUSE; NERVE CELL DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBSTANTIA NIGRA;

ANIMALIA; MUS; RODENTIA;

EID: 65549105080     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06072.x     Document Type: Article

References (67)

1. Allen P. (2008) Allen Brain Atlas. Allen Institute for Brain Science, Seattle, WA. http://www.brain-map.org.
2. Alvarez-Fischer D., Guerreiro S., Hunot S., Saurini F., Marien M., Sokoloff P., Hirsch E. C., Hartmann A. Michel P. P. (2008) Modelling Parkinson-like neurodegeneration via osmotic minipump delivery of MPTP and probenecid. J. Neurochem. 107, 701 711.
3. Anderson D. W., Bradbury K. A. Schneider J. S. (2006) Neuroprotection in Parkinson models varies with toxin administration protocol. Eur. J. Neurosci. 24, 3174 3182.
4. Aubin N., Curet O., Deffois A. Carter C. (1998) Aspirin and salicylate protect against MPTP-induced dopamine depletion in mice. J. Neurochem. 71, 1635 1642. (Pubitemid 28443036)
5. Baba M., Nakajo S., Tu P. H., Tomita T., Nakaya K., Lee V. M., Trojanowski J. Q. Iwatsubo T. (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 152, 879 884. (Pubitemid 28173348)
6. Beal M. F. (2003) Mitochondria, oxidative damage, and inflammation in Parkinson's disease. Ann. NY Acad. Sci. 991, 120 131. (Pubitemid 36793808)
7. Beaudry G., Langlois M. C., Weppe I., Rouillard C. Levesque D. (2000) Contrasting patterns and cellular specificity of transcriptional regulation of the nuclear receptor nerve growth factor-inducible B by haloperidol and clozapine in the rat forebrain. J. Neurochem. 75, 1694 1702.
8. Bezard E., Dovero S., Prunier C., Ravenscroft P., Chalon S., Guilloteau D., Crossman A. R., Bioulac B., Brotchie J. M. Gross C. E. (2001) Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson's disease. J. Neurosci. 21, 6853 6861. (Pubitemid 32781128)
9. Bezard E., Gross C. E. Brotchie J. M. (2003) Presymptomatic compensation in Parkinson's disease is not dopamine-mediated. Trends Neurosci. 26, 215 221. (Pubitemid 36412004)
10. Braak H. Del Tredici K. (2008) Invited article: nervous system pathology in sporadic Parkinson disease. Neurology 70, 1916 1925.
11. Cenci M. A., Whishaw I. Q. Schallert T. (2002) Animal models of neurological deficits: how relevant is the rat? Nat. Rev. Neurosci. 3, 574 579. (Pubitemid 135706667)
12. Chen L. Feany M. B. (2005) Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. Nat. Neurosci. 8, 657 663. (Pubitemid 40594208)
13. Chu Y., Le W., Kompoliti K., Jankovic J., Mufson E. J. Kordower J. H. (2006) Nurr1 in Parkinson's disease and related disorders. J. Comp. Neurol. 494, 495 514. (Pubitemid 41790998)
14. Cicchetti F., Lapointe N., Roberge-Tremblay A., Saint-Pierre M., Jimenez L., Ficke B. W. Gross R. E. (2005) Systemic exposure to paraquat and maneb models early Parkinson's disease in young adult rats. Neurobiol. Dis. 20, 360 371. (Pubitemid 41476262)
15. Cossette M., Parent A. Levesque D. (2004) Tyrosine hydroxylase-positive neurons intrinsic to the human striatum express the transcription factor Nurr1. Eur. J. Neurosci. 20, 2089 2095. (Pubitemid 39331129)
16. Costantini L. C., Cole D., Chaturvedi P. Isacson O. (2001) Immunophilin ligands can prevent progressive dopaminergic degeneration in animal models of Parkinson's disease. Eur. J. Neurosci. 13, 1085 1092. (Pubitemid 32275745)
17. Dauer W., Kholodilov N., Vila M. et al. (2002) Resistance of alpha-synuclein null mice to the parkinsonian neurotoxin MPTP. Proc. Natl Acad. Sci. USA 99, 14524 14529. (Pubitemid 35257704)
18. Dawson T. M. (2000) New animal models for Parkinson's disease. Cell 101, 115 118. (Pubitemid 32004742)
19. Donnan G. A., Kaczmarczyk S. J., Solopotias T., Rowe P., Kalnins R. M., Vajda F. J. Mendelsohn F. A. (1986) The neurochemical and clinical effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in small animals. Clin. Exp. Neurol. 22, 155 164.
20. Eells J. B., Yeung S. K. Nikodem V. M. (2002) Dopamine neurons heterozygous for the Nurr1-null allele have reduced survival in vitro. Neurosci. Res. Commun. 30, 173 183.
21. Emborg H. D., Andersen J. S., Seyfarth A. M. Wegener H. C. (2004) Relations between the consumption of antimicrobial growth promoters and the occurrence of resistance among Enterococcus faecium isolated from broilers. Epidemiol. Infect. 132, 95 105. (Pubitemid 38240078)
22. Feany M. B. Bender W. W. (2000) A Drosophila model of Parkinson's disease. Nature 404, 394 398. (Pubitemid 30164341)
23. Fearnley J. M. Lees A. J. (1991) Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114, 2283 2301.
24. + kinetics and MPTP-induced nigrostriatal dopamine depletions. J. Pharmacol. Exp. Ther. 283, 100 107. (Pubitemid 27438951)
25. Fornai F., Soldani P., Lazzeri G., di Poggio A. B., Biagioni F., Fulceri F., Batini S., Ruggieri S. Paparelli A. (2005a) Neuronal inclusions in degenerative disorders. Do they represent static features or a key to understand the dynamics of the disease? Brain Res. Bull. 65, 275 290. (Pubitemid 41057796)
26. Fornai F., Schluter O. M., Lenzi P. et al. (2005b) Parkinson-like syndrome induced by continuous MPTP infusion: convergent roles of the ubiquitin-proteasome system and alpha-synuclein. Proc. Natl Acad. Sci. USA 102, 3413 3418. (Pubitemid 40328059)
27. Forno L. S., DeLanney L. E., Irwin I. Langston J. W. (1993) Similarities and differences between MPTP-induced parkinsonsim and Parkinson's disease. Neuropathologic considerations. Adv. Neurol. 60, 600 608.
28. Glaser J. R. Glaser E. M. (2000) Stereology, morphometry, and mapping: the whole is greater than the sum of its parts. J. Chem. Neuroanat. 20, 115 126.
29. Hashimoto M., Rockenstein E. Masliah E. (2003) Transgenic models of alpha-synuclein pathology: past, present, and future. Ann. NY Acad. Sci. 991, 171 188.
30. Heikkila R. E., Hess A. Duvoisin R. C. (1984) Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine in mice. Science 224, 1451 1453. (Pubitemid 14123348)
31. Hirsch E. (1999) Mechanism and consequences of nerve cell death in Parkinson's disease. J. Neural Transm. Suppl. 56, 127 137.
32. Jackson-Lewis V., Jakowec M., Burke R. E. Przedborski S. (1995) Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 4, 257 269.
33. Javitch J. A. Snyder S. H. (1984) Uptake of MPP(+) by dopamine neurons explains selectivity of parkinsonism-inducing neurotoxin, MPTP. Eur. J. Pharmacol. 106, 455 456. (Pubitemid 15210642)
34. Jiang C., Wan X., He Y., Pan T., Jankovic J. Le W. (2005) Age-dependent dopaminergic dysfunction in Nurr1 knockout mice. Exp. Neurol. 191, 154 162. (Pubitemid 39612401)
35. Jimenez-Jimenez F. J., Tabernero C., Mena M. A. et al. (1991) Acute effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in a model of rat designated a poor metabolizer of debrisoquine. J. Neurochem. 57, 81 87.
36. Jourdain S., Morissette M., Morin N. Di Paolo T. (2005) Oestrogens prevent loss of dopamine transporter (DAT) and vesicular monoamine transporter (VMAT2) in substantia nigra of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mice. J. Neuroendocrinol. 17, 509 517. (Pubitemid 40990692)
37. Joyce J. N., Smutzer G., Whitty C. J., Myers A. Bannon M. J. (1997) Differential modification of dopamine transporter and tyrosine hydroxylase mRNAs in midbrain of subjects with Parkinson's, Alzheimer's with parkinsonism, and Alzheimer's disease. Mov. Disord. 12, 885 897. (Pubitemid 27496764)
38. Kitamura Y., Kakimura J. Taniguchi T. (1998) Protective effect of talipexole on MPTP-treated planarian, a unique parkinsonian worm model. Jpn. J. Pharmacol. 78, 23 29. (Pubitemid 28464209)
39. Kolata G. (1983) Monkey model of Parkinson's disease. Science 220, 705.
40. Kopin I. J. Markey S. P. (1988) MPTP toxicity: implications for research in Parkinson's disease. Annu. Rev. Neurosci. 11, 81 96. (Pubitemid 18081034)
41. Langston J. W. Ballard P. A. Jr. (1983) Parkinson's disease in a chemist working with 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. N. Engl. J. Med. 309, 310.
42. Lapointe N., St-Hilaire M., Martinoli M. G., Blanchet J., Gould P., Rouillard C. Cicchetti F. (2004) Rotenone induces non-specific central nervous system and systemic toxicity. FASEB J. 18, 717 719.
43. Lau Y. S., Trobough K. L., Crampton J. M. Wilson J. A. (1990) Effects of probenecid on striatal dopamine depletion in acute and long-term 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice. Gen. Pharmacol. 21, 181 187. (Pubitemid 20097400)
44. Le W., Conneely O. M., He Y., Jankovic J. Appel S. H. (1999) Reduced Nurr1 expression increases the vulnerability of mesencephalic dopamine neurons to MPTP-induced injury. J. Neurochem. 73, 2218 2221. (Pubitemid 29491838)
45. Le W. D., Xu P., Jankovic J., Jiang H., Appel S. H., Smith R. G. Vassilatis D. K. (2003) Mutations in NR4A2 associated with familial Parkinson disease. Nat. Genet. 33, 85 89. (Pubitemid 36068688)
46. Lein E. S., Hawrylycz M. J., Ao N. et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168 176. (Pubitemid 46095716)
47. Liu Y., Roghani A. Edwards R. H. (1992) Gene transfer of a reserpine-sensitive mechanism of resistance to N-methyl-4-phenylpyridinium. Proc. Natl Acad. Sci. USA 89, 9074 9078.
48. Liu L. X., Chen W. F., Xie J. X. Wong M. S. (2008) Neuroprotective effects of genistein on dopaminergic neurons in the mice model of Parkinson's disease. Neurosci. Res. 60, 156 161. (Pubitemid 350181668)
49. Masliah E., Rockenstein E., Veinbergs I., Mallory M., Hashimoto M., Takeda A., Sagara Y., Sisk A. Mucke L. (2000) Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287, 1265 1269. (Pubitemid 30112148)
50. McCormack A. L., Thiruchelvam M., Manning-Bog A. B., Thiffault C., Langston J. W., Cory-Slechta D. A. Di Monte D. A. (2002) Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol. Dis. 10, 119 127.
51. Meredith G. E., Totterdell S., Potashkin J. A. Surmeier D. J. (2008) Modeling PD pathogenesis in mice: advantages of a chronic MPTP protocol. Parkinsonism Relat. Disord. 14 (Suppl. 2 S112 S115.
52. Murray A. M., Weihmueller F. B., Marshall J. F., Hurtig H. I., Gottleib G. L. Joyce J. N. (1995) Damage to dopamine systems differs between Parkinson's disease and Alzheimer's disease with parkinsonism. Ann. Neurol. 37, 300 312.
53. Nicklas W. J., Vyas I. Heikkila R. E. (1985) 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, 2503 2508. (Pubitemid 15072756)
54. + and mitochondrial function. Life Sci. 40, 721 729. (Pubitemid 17012446)
55. Perier C., Bove J., Vila M. Przedborski S. (2003) The rotenone model of Parkinson's disease. Trends Neurosci. 26, 345 346. (Pubitemid 36794549)
56. Przedborski S., Jackson-Lewis V., Naini A. B., Jakowec M., Petzinger G., Miller R. Akram M. (2001) The parkinsonian toxin 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine (MPTP): a technical review of its utility and safety. J. Neurochem. 76, 1265 1274. (Pubitemid 32198231)
57. Saint-Pierre M., Tremblay M. E., Sik A., Gross R. E. Cicchetti F. (2006) Temporal effects of paraquat/maneb on microglial activation and dopamine neuronal loss in older rats. J. Neurochem. 98, 760 772. (Pubitemid 44051277)
58. Samadi P., Gregoire L., Morissette M., Calon F., Hadj Tahar A., Belanger N., Dridi M., Bedard P. J. Di Paolo T. (2008) Basal ganglia group II metabotropic glutamate receptors specific binding in non-human primate model of L-Dopa-induced dyskinesias. Neuropharmacology 54, 258 268. (Pubitemid 350265053)
59. Sedelis M., Schwarting R. K. Huston J. P. (2001) Behavioral phenotyping of the MPTP mouse model of Parkinson's disease. Behav. Brain Res. 125, 109 125. (Pubitemid 33000449)
60. Steece-Collier K., Maries E. Kordower J. H. (2002) Etiology of Parkinson's disease: genetics and environment revisited. Proc. Natl Acad. Sci. USA 99, 13972 13974. (Pubitemid 35257609)
61. Sundstrom E., Stromberg I., Tsutsumi T., Olson L. Jonsson G. (1987) Studies on the effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on central catecholamine neurons in C57BL/6 mice. Comparison with three other strains of mice. Brain Res. 405, 26 38. (Pubitemid 17034929)
62. Tanner C. M. Goldman S. M. (1996) Epidemiology of Parkinson's disease. Neurol. Clin. 14, 317 335. (Pubitemid 26157425)
63. Tatton N. A. Kish S. J. (1997) In situ detection of apoptotic nuclei in the substantia nigra compacta of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- treated mice using terminal deoxynucleotidyl transferase labelling and acridine orange staining. Neuroscience 77, 1037 1048. (Pubitemid 27128779)
64. Thiruchelvam M., McCormack A., Richfield E. K., Baggs R. B., Tank A. W., Di Monte D. A. Cory-Slechta D. A. (2003) Age-related irreversible progressive nigrostriatal dopaminergic neurotoxicity in the paraquat and maneb model of the Parkinson's disease phenotype. Eur. J. Neurosci. 18, 589 600. (Pubitemid 37045378)
65. Tremblay M. E., Saint-Pierre M., Bourhis E., Levesque D., Rouillard C. Cicchetti F. (2006) Neuroprotective effects of cystamine in aged parkinsonian mice. Neurobiol. Aging 27, 862 870.
66. Wider C. Wszolek Z. K. (2008) Etiology and pathophysiology of frontotemporal dementia, Parkinson disease and Alzheimer disease: lessons from genetic studies. Neurodegener. Dis. 5, 122 125.
67. Zetterstrom R. H., Solomin L., Jansson L., Hoffer B. J., Olson L. Perlmann T. (1997) Dopamine neuron agenesis in Nurr1-deficient mice. Science 276, 248 250. (Pubitemid 27172681)