Enhanced substantia nigra mitochondrial pathology in human α-synuclein transgenic mice after treatment with MPTP

Experimental Neurology

Volumn 186, Issue 2, 2004, Pages 158-172

  Song, David D ^a   Shults, Clifford W ^a,b   Sisk, Abbyann ^b   Rockenstein, Edward ^b   Masliah, Eliezer ^b,c  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Synuclein; 1 Methyl 4 phenyl 1,2,3,6 tetrahydropyridine; Electron microscopy; Inclusion bodies; Lewy bodies; Mitochondria; Oxidative stress; Parkinson's disease

Indexed keywords

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

ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CELL INCLUSION; CONTROLLED STUDY; DEGENERATIVE DISEASE; GENE OVEREXPRESSION; HIPPOCAMPUS; MITOCHONDRION SWELLING; MOUSE; NEOCORTEX; NERVE FIBER DEGENERATION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SPECIES COMPARISON; SUBSTANTIA NIGRA; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; WILD TYPE;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ALPHA-SYNUCLEIN; ANIMALS; ANTIGENS, THY-1; DOPAMINE AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; LEWY BODIES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MITOCHONDRIA; NERVE DEGENERATION; NERVE TISSUE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUBSTANTIA NIGRA; SYNUCLEINS;

EID: 1542617769     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00342-X     Document Type: Article

References (67)

1. Anglade P., Vyas S., Javoy-Agid F., Herrero M.T., Michel P.P., Marquez J., Mouatt-Prigent A., Ruberg M., Hirsch E.C., Agid Y. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol. 12:1997;25-31.
2. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3:2000;1301-1306.
3. Brooks A.I., Chadwick C.A., Gelbard H.A., Cory-Slechta D.A., Federoff H.J. Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res. 823:1999;1-10.
4. Cheramy A., Leviel V., Glowinski J. Dendritic release of dopamine in the substantia nigra. Nature. 289:1981;537-542.
5. Clarke P.G.H. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 181:1990;195-213.
6. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., Lansbury P.T. Jr. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. U. S. A. 97:2000;571-576.
7. D'Andrea M.R., Ilyin S., Plata-Salaman C.R. Abnormal patterns of microtubule-associated protein-2 (MAP-2) immunolabeling in neuronal nuclei and Lewy bodies in Parkinson's disease substantia nigra brain tissues. Neurosci. Lett. 306:2001;137-140.
8. Dauer W.T., Kholodilov N.G., Vila M., Trillat A.-C., Goodchild R.E., Larsen K.E., Staal R.G., Tieu K., Schmitz Y., Yuan C.A., Rocha M., Jackson-Lewis V., Hersch S., Sulzer D., Przedborski S., Burke R.E., Hen R. Resistance of α-synuclein null mice to the Parkinsonian neurotoxin MPTP. Proc. Natl. Acad. Sci. U. S. A. 99:2002;14524-14529.
9. Dexter D.T., Carter C.J., Wells F.R., Javoy-Agid F., Agid Y., Lees A., Jenner P., Marsden C.D. Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem. 52:1989;381-389.
10. Ding T.T., Lee S.J., Rochet J.C., Lansbury P.T. Jr. Annular alpha-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes. Biochemistry. 41:2002;10209-10217.
11. Duan W., Rangnekar V.M., Mattson M.P. Prostate apoptosis response-4 production in synaptic compartments following apoptotic and excitotoxic insults: evidence for a pivotal role in mitochondrial dysfunction and neuronal degeneration. J. Neurochem. 72:1999;2312-2322.
12. Duffy P.E., Tennyson V.M. Phase and electron microscopic observations of Lewy bodies and melanin granules in the substantia nigra and locus caeruleus in Parkinson's disease. J. Neuropathol. Exp. Neurol. 24:1965;398-414.
13. El-Agnaf O.M., Jakes R., Curran M.D., Middleton D., Ingenito R., Bianchi E., Pessi A., Neill D., Wallace A. Aggregates from mutant and wild-type α-synuclein proteins and NAC peptide induce apoptotic cell death in human neuroblastoma cells by formation of beta-sheet and amyloid-like filaments. FEBS Lett. 440:1998;71-75.
14. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature. 404:2000;394-398.
15. Forno L.S. Neuropathologic features of Parkinson's disease. Marsden C.D., Fahn S. Movement Disorders. 1982;25-40 Butterworth & Co. London.
16. Forno L.S. Neuropathologic features of Parkinson's, Huntington's, and Alzheimer's diseases. Ann. N.Y. Acad. Sci. 648:1992;6-16.
17. Forno L.S., Langston J.W., DeLanney L., Irwin I. An electron microscopic study of MPTP-induced inclusion bodies in an old monkey. Brain Res. 448:1988;150-157.
18. Gai W.P., Yuan H.X., Li X.Q., Power J.T., Blumbergs P.C., 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.
19. Gerlach M., Riederer P. Animal models of Parkinson's disease: an empirical comparison with the phenomenology of the disease in man. J. Neural Transm. 103:1996;987-1041.
20. Giasson B.I., Duda J.E., Murray I.V.J., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., Lee V.M.Y. Oxidative damage linked to neurodegeneration by selective α-synuclein nitration in synucleinopathy lesions. Science. 290:2000;985-989.
21. Goldberg M.S., Lansbury P.T. Jr. Is there a cause-and-effect relationship between α-synuclein fibrillization and Parkinson's disease? Nat. Cell Biol. 2:2000;E115-E119.
22. Gosavi N., Lee H.J., Lee J.S., Patel S., Lee S.J. Golgi fragmentation occurs in the cells with prefibrillar alpha-synuclein aggregates and precedes the formation of fibrillar inclusion. J. Biol. Chem. 277:2002;48984-48992.
23. Haas R.H., Nasirian F., Nakano K., Ward D., Pay M., Hill R., Shults C.W. Low platelet mitochondrial complex I and complex II/III activity in early untreated Parkinson's disease. Ann. Neurol. 37:1995;714-722.
24. Hashimoto M., Hsu L.J., Xia Y., Takeda A., Sisk A., Sundsmo M., Masliah E. Oxidative stress induces amyloid-like aggregate formation of NACP/α-S in vitro. NeuroReport. 10:1999;717-721.
25. Hashimoto M., Takeda A., Hsu L.J., Takenouchi T., Masliah E. Role of cytochrome c as a stimulator of α-S aggregation in Lewy body disease. J. Biol. Chem. 274:1999;28849-28852.
26. Hsu L.J., Sagara Y., Arroyo A., Rockenstein E., Sisk A., Mallory M., Wong J., Takenouchi T., Hashimoto M., Masliah E. Alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am. J. Pathol. 157:2000;401-410.
27. Irwin I., Finnegan K.T., Delanney L.E., Di Monte D.A., Langston J.W. The relationship between aging, monoamine oxidase, striatal dopamine and the effects of MPTP in C57BL/6 mice: a critical reassessment. Brain Res. 572:1992;224-231.
28. Iwai A., Masliah E., Yoshimoto M., Ge N., Flanagan L., de Silva H.A., Kittel A., Saitoh T. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron. 14:1995;467-475.
29. Jackson-Lewis V., Jakowec M., Burke R.E., Przedborski S. Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration. 4:1995;257-269.
30. Jensen P.H., Nielsen M.S., Jakes R., Dott C.G., Goeder M. Binding of α-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J. Biol. Chem. 273:1998;26292-26294.
31. Kowall N.W., Hantraye P., Brouillet E., Beal F.M., McKee A.C., Ferrante R.J. MPTP induces alpha-synuclein aggregation in the substantia nigra of baboons. NeuroReport. 11:1999;211-213.
32. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J.T., Schols L., Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18:1998;106-108.
33. Lee H.J., Lee S.J. Characterization of cytoplasmic alpha-synuclein aggregates. Fibril formation is tightly linked to the inclusion-forming process in cells. J. Biol. Chem. 277:2002;48976-48983.
34. Lee F.J.S., Liu F., Pristupa Z.B., Niznik H.B. Direct binding and functional coupling of α-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. FASEB J. 15:2001;916-926.
35. Lee H., Choi C., Lee S. Membrane-bound α-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form. J. Biol. Chem. 277:2002;671-678.
36. Lee H., Shin S.Y., Choi C., Lee Y.H., Lee S. Formation and removal of α-synuclein aggregates in cells exposed to mitochondrial inhibitors. J. Biol. Chem. 277:2002;5411-5417.
37. Levi A.C., Ravazzani R., de Mattei M. Mitochondrial abnormalities in nigral neurons of the marmoset and Macaca fascicularis treated with MPTP. Panminerva Med. 36:1994;53-56.
38. Manning-Borg A.B., McCormack A.L., Li J., Uversky V.N., Fink A.L., Di Monte D.A. The herbicide paraquat causes up-regulation of α-synuclein in mice. J. Biol. Chem. 277:2002;1641-1644.
39. Maroteaux L., Scheller R.H. The rat brain synucleins: family of proteins transiently associated with neuronal membrane. Mol. Brain Res. 11:1991;335-343.
40. Masliah E., Rockenstein E., Veinbergs I., Mallory M., Hashimoto M., Takeda A., Sagara Y., Sisk A., Mucke L. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science. 287:2000;1265-1269.
41. Mattson M.P., Duan W. "Apoptotic" biochemical cascades in synaptic compartments: roles in adaptive plasticity and neurodegenerative disorders. J. Neurosci. Res. 58:1999;152-166.
42. McCormack A.L., Thiruchelvam M., Manning-Borg A.B., Thiffault C., Langston J.W., Cory-Slechta D.A., Di Monte D.A. Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol. Dis. 10:2002;119-127.
43. Mizukawa K., Sora Y.H., 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.
44. Nirenberg M.J., Vaughan R.A., Uhl G.R., Kuhar M.J., Pickel V.M. The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 16:1996;436-447.
45. Olanow C.W., Tatton W.G. Etiology and pathogenesis of Parkinson's disease. Annu. Rev. Neurosci. 22:1999;123-144.
46. Ostrerova-Golts N., Petrucelli L., Hardy J., Lee J.M., Farer M., Wolozin B. The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. J. Neurosci. 20:2000;6048-6054.
47. Pennathur S., Jackson-Lewis V., Przedborski S., Heinecke J.W. Mass spectrometric 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. 274:1999;34621-34628.
48. Pifl C., Giros B., Caron M.G. Dopamine transporter expression confers cytotoxicity to low doses of the parkinsonism-inducing neurotoxin 1-methyl-4-phenylpyridinium. J. Neurosci. 13:1993;4246-4253.
49. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., Nussbaum R.L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science. 276:1997;2045-2047.
50. Prensa L., Parent A. The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J. Neurosci. 21:2001;7247-7260.
51. Przedborski S., Jackson-Lewis V. Mechanisms of MPTP toxicity. Mov. Disord. 13(S1):1998;35-38.
52. Przedborski S., Chen Q., Vila M., Giasson B.I., Djaldatti R., Vukosavic S., Souza J.M., Jackson-Lewis V., Lee V.M.Y., Ischiropoulos H. Oxidative post-translational modifications of α-synuclein in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease. J. Neurochem. 76:2001;637-640.
53. Richfield E.K., Thiruchelvam M.-J., Cory-Slechta D.A., Wuertzer C., Gainetdinov R., Caron M., Di Monte D.A., Federoff H.J. Behavioral and neurochemical effects of wild-type and mutated human α-synuclein in transgenic mice. Exp. Neurol. 175:2002;35-48.
54. Rockenstein E., Mallory M., Hashimoto M., Song D.D., Shults C.W., Lang I., Masliah E. Differential neuropathological alterations in transgenic mice expressing α-synuclein from the PDGF-b and Thy-1 promoters. J. Neurosci. Res. 68:2002;568-578.
55. Roy S., Wolman L. Ultrastructural observations in parkinsonism. J. Pathol. 99:1969;39-44.
56. Schapira A.H., Cooper J.M., Dexter D., Clark J.B., Jenner P., Marsden C.D. Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 54:1990;823-827.
57. Sharon R., Goldberg M.S., Bar-Josef I., Betensky R.A., Shen J., Selkoe D.J. α-Synuclein occurs in lipid-rich high molecular weight complexes, binds fatty acids, and shows homology to the fatty acid-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 98:2001;9110-9115.
58. Sonsalla P.K., Heikkila R.E. The influence of dose and dosing interval on MPTP-induced dopaminergic neurotoxicity in mice. Eur. J. Pharmacol. 129:1986;339-345.
59. Spillantini M.G., Schmidt M.L., Lee V.Y., Trojanowski J.Q., Jakes R., Goedert M. α-Synuclein in Lewy bodies. Nature. 388:1997;839-840.
60. Sundstrom E., Luthman J., Goldstein M., Jonsson G. Time course of MPTP-induced degeneration of the nigrostriatal dopamine system in c57 Bl/6 mice. Brain Res. Bull. 21:1988;257-263.
61. Takeda A., Hashimoto M., Mallory M., Sundsmo M., Hansen L., Sisk A., Masliah E. Abnormal distribution of the non-Aβ component of Alzheimer's disease amyloid precursor/α-synuclein in Lewy body disease as revealed by proteinase K and formic acid pretreatment. Lab. Invest. 78:1998;1169-1177.
62. Tanaka J., Nakamura H., Honda S., Takada K., 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.
63. Tanner C.M., Hubble J.P., Chan P. Epidemiology and genetics of Parkinson's disease. Watts R.L., Koller W.C. Movement Disorders Neurologic Principles and Practice. 1997;137-152 McGraw-Hill, New York.
64. Trimmer P.A., Swerdlow R.H., Parks J.K., Keeney P., Bennett J.P. Jr., Miller S.W., Davis R.E., Parker W.D. Jr. Abnormal mitochondrial morphology in sporadic Parkinson's and Alzheimer's disease cybrid cell lines. Exp. Neurol. 162:2000;37-50.
65. Van Der Putten H., Weiderhold K.H., Probst A., Barbieri S., Mistl C., Danner S., Kauffmann S., Hofele K., Spooren W.P.J.M., Ruegg M.A., Lin S., Caroni P., Sommer B., Tolnay M., Bilbe G. Neuropathology in mice expressing human alpha-synuclein. J. Neurosci. 20:2000;6021-6029.
66. Wakabayashi K., Matsumoto K., Takayama K., Yoshimoto M., Takahashi H. NACP, a presynaptic protein, immunoreactivity in Lewy bodies in Parkinson's disease. Neurosci. Lett. 239:1997;45-48.
67. Wullner U., Brouillet E., Isacson O., Young A.B., Penney J.B. Glutamate receptor binding sites in MPTP-treated mice. Exp. Neurol. 121:1993;284-287.