Dysregulation of gene expression in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-lesioned mouse substantia nigra

Journal of Neuroscience

Volumn 24, Issue 34, 2004, Pages 7445-7454

  Miller, Renee M ^a   Callahan, Linda M ^a,c   Casaceli, Cindy ^a   Chen, Linlin ^a   Kiser, Gretchen L ^b   Chui, Buena ^b   Kaysser Kranich, Tamma M ^b   Sendera, Timothy J ^b   Palaniappan, Chockalingam ^b   Federoff, Howard J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b GE HEALTHCARE   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Cytoskeleton; Gene expression; Microarray; Mouse; MPTP; Parkinson's disease

Indexed keywords

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

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL DEATH; CONTROLLED STUDY; CYTOSKELETON; DOPAMINERGIC NERVE CELL; GENE EXPRESSION REGULATION; MALE; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIMATE; PRIORITY JOURNAL; SUBSTANTIA NIGRA;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; CELL CYCLE; CELL DEATH; CHRONIC DISEASE; CYTOSKELETON; DISEASE MODELS, ANIMAL; DOPAMINE; DOWN-REGULATION; GENE EXPRESSION PROFILING; MALE; MICE; MICE, INBRED C57BL; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARKINSON DISEASE, SECONDARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUBSTANTIA NIGRA;

EID: 4444368405     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4204-03.2004     Document Type: Article

References (69)

1. Ali RR, Reichel MB, de Alwis M, Kanuga N, Kinnon C, Levinsky RJ, Hunt DM, Bhattacharya SS, Thrasher AJ (1998) Adeno-associated virus gene transfer to mouse retina. Hum Gene Ther 9:81-86.
2. Beal F (2001) Experimental models of Parkinson's disease. Nat Rev Neurosci 2:325-332.
3. Bezard E, Jaber M, Gonon F, Boireau A, Bloch B, Gross CE (2000) 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 12:2892-2900.
4. Blalock EM, Chen K-C, Sharrow K, Herman JP, Porter NM, Foster TC, Landfield PW (2003) Gene microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci 23:3807-3819.
5. Bohm H, Brinkmann V, Drab M, Henske A, Kurzchalia TV (1997) Mammaliam homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity. Curr Biol 7:603-606.
6. Brill II LB, Bennett Jr JP (2003) Dependence on electron transport chain function and intracellular signaling of genomic responses in SH-SY5Y cells to the mitochondrial neurotoxin MPP+. Exp Neurol 181:25-38.
7. Brooks AI, Chadwick CA, Gelbard HA, Cory-Slechta DA, Federoff HJ (1999) Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res 823:1-10.
8. Callaban L, Vaules W, Coleman P (1999) Quantitative decrease in synaptophysin message expression and increase in cathepsin D message expression in Alzheimer disease neurons containing neurofibrillary tangles. J Neuropathol Exp Neurol 58:275-287.
9. Callahan LM, Vaules WA, Coleman PD (2002) Progressive reduction of synaptophysin message in single neurons in Alzheimer disease. J Neuropathol Exp Neurol 61:384-395.
10. Calon F, Lavertu N, Lemieux AM, Morissette M, Goulet M, Grondin R, Blanchet PJ, Bedard PJ, Di Paolo T (2001) Effect of MPTP-induced denervation on basal ganglia GABA(B) receptors: correlation with dopamine concentrations and dopamine transporter. Synapse 40:225-234.
11. Chassain C, Eschalier A, Durif F (2001) Assessment of motor behavior using a video system and a clinical rating scale in parkinsonian monkeys lesioned by MPTP. J Neurosci Methods 111:9-16.
12. Chiba K, Trevor A, Castagnoli Jr N (1985) Active uptake of MPP+, metabolite of MPTP, by brain synaptosomes. Biochem Biophys Res Commun 128:1228-1232.
13. Chow N, Cox C, Callahan L, Weimer J, Guo L, Coleman P (1998) Expression profiles of multiple genes in single neurons of Alzheimer's disease. Proc Natl Acad Sci USA 95:9620-9634.
14. Cruz-Sanchez FF, Cardozo A, Ambrosio S, Tolosa E, Mahy N (1993) Plasticity of the nigrostriatal system in MPTP-treated mice. Mol Chem Neuropathol 19:163-176.
15. Darbinian N, Gallia GL, King J, Del Valle L, Johnson EM, Khalili K (2001) Growth inhibition of glioblastoma cells by human pur(alpha). J Cell Physiol 189:334-340.
16. Davis GC, Williams AC, Markey SP, Ebert MH, Caine ED, Reichert CM, Kopin IJ (1979) Chronic parkinsonism secondary to intravenous injection of meperidine analogs. Psychiatry Res 1:249-254.
17. Dawson VL, Dawson TM (1998) Nitric oxide in neurodegeneration. Prog Brain Res 118:215-229.
18. Dipasquale B, Marini M, Youl RJ (1991) Apoptosis and DNA degradation by 1-methyl-4-phenylpyridinium ion (MPP+) in neurons. Biochem Biophys Res Commun 181:1442-1448.
19. Dranovsky A, Vincent I, Gregori L, Schwarzman A, Colflesh D, Enghild J, Strittmatter W, Davies P, Goldgaber D (2001) Cdc2 phosphorylation of nucleolin demarcates mitotic stages and Alzheimer's disease pathology. Neurobiol Aging 105:639-650.
20. Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89:297-308.
21. Furuya T, Hayakawa H, Yamada M, Yoshimi K, Hisahara S, Miura M, Mizuno Y, Mochizuki H (2004) Caspase-11 mediates inflammatory dopaminergic cell death in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease. J Neurosci 24:1865-1872.
22. Garrett WT, McBride RL, Williams JKJ, Feringa ER (1991) Fluor-Gold's toxicity makes it inferior to True Blue for long-term studies of dorsal root ganglion neurons and motoneurons. Neurosci Lett 128:137-139.
23. Hayley S, Crocker SJ, Smith PD, Shree T, Jackson-Lewis V, Przedborski S, Mount M, Slack R, Anisman H, Park DS (2004) Regulation of dopaminergic loss by Fas in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J Neurosci 24:2045-2053.
24. Hoppel CL, Greenblatt D, Kwok HC (1987) Inhibition of mitochondrial respiration by analogs of 4-phenylpyridine and 1-methyl-4-phenylpyridinium cation (MPP+), the neurotoxic metabolite of MPTP. Biochem Biophys Res Commun 148:684-693.
25. Irizarry RA, Bolstead BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:1-8.
26. Ishizawa T, Mattila P, Davies P, Wang D, Dickson DW (2003) Colocalization of tau and alpha-synuclein epitopes in Lewy bodies. J Neuropathol Exp Neurol 62:389-397.
27. Itoh H, Wortman MJ, Kanovsky M, Uson RR, Gordon RE, Alfano N, Johnson EM (1998) Alterations in Pur(alpha) levels and intracellular localization in the CV-1 cell cycle. Cell Growth Differ 9:651-665.
28. 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 82:2173-2177.
29. Kobayashi S, Agui K, Kamo S, Li Y, Anzai K (2000) Neural BC1 RNA associates with pur alpha, a single-stranded DNA and RNA binding protein, which is involved in teh transcription of the BC1 RNA gene. Biochem Biophys Res Commun 277:341-347.
30. Kondo S, Sato-Yoshitake R, Noda Y, Aizawa H, Nakata T, Matsuura Y, Hirokawa N (1994) KIF3A is a new microtubule-based anterograde motor in the nerve axon. J Cell Biol 125:1095-1107.
31. Kowall NW, Hantraye P, Brouillet E, Beal MF, McKee AC, Ferrante RJ (2000) MPTP induces alpha-synuclein aggregation in the substantia nigra of baboons. NeuroReport 11:211-213.
32. Langston JW, Ballard P, Tetrud JW, Irwin I (1983) Chronic parkinsonism in humans due a product of meperidine analog synthesis. Science 219:979-980.
33. Lee ES, Charlton CG (2001) 1-Methyl-4-phenyl-pyridinium increases S-adenosyl-L-methionine dependent phospholipid methylation. Pharmacol Biochem Behav 70:105-114.
34. Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E, Harta G, Brownstein MJ, Jonnalagada S, Chernova T, Dehejia A, Lavedan C, Gasser T, Steinbach PJ, Wilkinson KD, Polymeropoulos MH (1998) The ubiquitin pathway in Parkinson's disease. Nature 395:451-452.
35. Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31-36.
36. Maguire-Zeiss KA, Federoff HJ (2003) Convergent pathobiologic model of Parkinson's disease. Ann NY Acad Sci 991:152-166.
37. Mandir AS, Przedborski S, Jackson-Lewis V, Wang Z-Q, Simbulan-Rosenthal CM, Smulson ME, Hoffman BE, Guastella DB, Dawson VL, Dawson TM (1999) Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine (MPTP)-induced parkinsonism. Proc Natl Acad Sci USA 96:5774-5779.
38. Martin M, Iyadurai SJ, Gassman A, Gindhart Jr JG, Hays TS, Saxton WM (1999) Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell 10:3717-3728.
39. Mizuno Y, Saitoh T, Sone N (1987) Inhibition of mitochondrial alpha-ketoglutarate dehydrogenase by 1-methyl-4-phenylpyridinium ion. Biochem Biophys Res Commun 143:971-976.
40. Mochizuki H, Nakamura N, Nishi K, Mizuno Y (1994) Apoptosis is induced by 1-methyl-4-phenylpyridinium ion (MPP+) in a ventral mesencephalic-striatal co-culture. Neurosci Lett 170:191-194.
41. Mochizuki H, Hayakawa H, Migita M, Tanaka R, Suzuki A, Shimo-Nakanishi Y, Urabe T, Yamada M, Tamayose K, Shiumada T, Miura M, Mizuno Y (2001) An AAV-derived Apaf-1 dominant negative inhibitor prevents MPTP toxicity as antiapoptotic gene therapy for Parkinson's disease. Proc Natl Acad Sci USA 98:10918-10923.
42. Muramatsu Y, Kurosaki R, Watanabe H, Michimata M, Matsubara M, Imai Y, Araki T (2003) Expression of S-100 protein is related to neuronal damage in MPTP-treated mice. Glia 42:307-313.
43. Ohashi S, Kobayashi S, Omori A, Ohara S, Omae A, Muramatsu T, Li Y, Anzai K (2000) The single-stranded DNA- and RNA- binding proteins Pur alpha and pur beta link BC1 RNA to microtubules through binding to the dendrite targeting RNA motifs. J Neurochem 75:1781-1790.
44. Park SU, Ferrer JV, Javitch JA, Kuhn DM (2002) Peroxynitrite inactivates the human dopamine transporter by modification of cysteine 342: potential mechanism of neurotoxicity in dopamine neurons. J Neurosci 22:4399-4405.
45. Paxinou E, Chen Q, Weisse M, Giasson BI, Norris EH, Rueter SM, Trojanowski JQ, Lee VM-Y, Ishiropoulos H (2001) Induction of α-synuclein aggregation by intracellular nitrative insult. J Neurosci 21:8053-8061.
46. Pennathur S, Jackson-Lewis V, Przedborski S, Heinecke JW (1999) Mass spectrometic quantification of 3-nitrotyrosine, ortho-tyrosine and o,o′-dityrosine in brain tissue of 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-treated mice, a model of oxidative stress in Parkinson's disease. J Biol Chem 274:34621-34628.
47. Poulsen KT, Armanini MP, Klein RD, Hynes MA, Phillips HS, Rosenthal A (1994) TGF beta 2 and TGF beta 3 are potent survival factors for midbrain dopaminergic neurons. Neuron 13:1245-1252.
48. Przedborski S, Vila M (2003) The 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model: a tool to explore the pathogenesis of Parkinson's disease. Ann NY Acad Sci 991:189-198.
49. Przedborski S, Jackson-Lewis V, Naini AB, Jakowec M, Petzinger G, Miller R, Akram M (2001) The Parkinsonian toxin 1-methyl-4-phenyl-1,2,3,6- tetrahydopyridine (MPTP): a technical review of its utility and safety. J Neurochem 76:1265-1274.
50. Ramsay RR, Dadgar J, Trevor A, Singer TP (1986) Energy-driven uptake of N-methyl-4-phenylpyridine by brain mitochondria mediates the neurotoxicity of MPTP. Life Sci 39:2503-2508.
51. Ren Y, Zhao J, Feng J (2003) Parkin binds to α/β tubulin and increases their ubiquitination and degradation. J Neurosci 23:3316-3324.
52. Ryu JK, Shin WH, Kim J, Joe EH, Lee YB, Cho KG, Oh YJ, Kim SU, Jin BK (2002) Trisialoganglioside GT1b induces in vivo degeneration of nigral dopaminergic neurons: role of microglia. Glia 38:15-23.
53. Shirvan A, Ziv I, Barzilai A, Djaldeti R, Zilkh-Falb R, Michlin T, Melamed E (1997) Induction of mitosis-related genes during dopamine-triggered apoptosis in sympathetic neurons. J Neural Transm 50:67-78.
54. Souza JM, Giasson BI, Chen Q, Lee VMY, Ishiropoulos H (2000) Dityrosine crosslinking promotes formation of stable alpha-synuclein polymers. J Biol Chem 275:18344-18349.
55. Stacey DW, Hitomi M, Kanovsky M, Gan L, Johnson EM (1999) Cell cycle arrest and morphological alterations following microinjection of NIH3T3 cells with Pur alpha. Oncogene 18:4254-4261.
56. Su QN, Namikawa K, Toki H, Kiyama H (1997) Differential display reveals transcriptional up-regulation of the motor molecules for both anterograde and retrograde axonal transport during nerve regeneration. Eur J Neurosci 9:1542-1547.
57. Suzuki H, Kumagai T, Goto A, Sugiura T (1998) Increase in intracellular hydrogen peroxide and upregulation of a nuclear respiratory gene evoked by impairment of mitochondrial electron transfer in human cells. Biochem Biophys Res Commun 249:542-545.
58. Takai Y, Irie K, Shimizu K, Sakisaka T, Ikeda W (2003) Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization. Cancer Sci 94:655-667.
59. Takemura R, Nakata T, Okada Y, Yamazaki H, Zhang Z, Hirokawa N (1996) mRNA expression of KIF1A, KIF1B, KIF2, KIF3A, KIF3B, KIF4, KIF5, and cytoplasmic dynein during axonal regeneration. J Neurosci 16:31-35.
60. Thatikunta P, Sawaya BE, Denisova L, Cole C, Yusibova G, Johnson EM, Khalili K, Amini S (1997) Identification of a cellular protein that binds to Tat-responsive element of TGF-beta promoter in glial cells. J Cell Biochem 67:466-477.
61. Tillerson JL, Caudle WM, Reveron ME, Miller GW (2002) Detection of behavioral impairments correlated to neurochemical deficits in mice treated with moderate doses of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Exp Neurol 178:80-90.
62. Tomashevski A, Hussman J, Jin LW, Nochlin D, Vincent I (2001) Constitutive Weel activity in adult brain neurons with M phase-type alterations in Alzheimer neurodegeneration. J Alzheimers Dis 3:195-207.
63. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121.
64. Ubl A, Berg D, Holzmann C, Kruger R, Berger K, Arzberger T, Bornemann A, Riess O (2002) 14-3-3 Protein is a component of Lewy bodies in Parkinson's disease-mutation analysis and association studies of 14-3-3 eta. Brain Res Mol Brain Res 108:33-39.
65. Vincent I, Jicha G, Rosado M, Dickson DW (1997) Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J Neurosci 17:3588-3598.
66. Vincent I, Zheng JH, Dickson DW, Kress Y, Davies P (1998) Mitotic phosphoepitopes precede paired helical filaments in Alzheimer's disease. Neurobiol Aging 19:287-296.
67. Viswanath V, Wu T, Boonplueang R, Chen S, Stevenson FF, Yantiri F, Yang L, Beal MF, Andersen JK (2001) Caspase-9 activation results in downstream caspase-8 activation and bid cleavage in 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-induced Parkinson's disease. J Neurosci 21:9519-9528.
68. Wesemann W, Grote C, Clement HW, Block F, Sontag KH (1993) Functional studies on monoaminergic transmitter release in parkinsonism. Prog Neuropsychopharmacol Biol Psychiatry 17:487-499.
69. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulos H, Przedborski S (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22:1763-1771.