Parkin gene therapy for α-synucleinopathy: A rat model of Parkinson's disease

Human Gene Therapy

Volumn 16, Issue 2, 2005, Pages 262-270

  Yamada, Masanori ^a   Mizuno, Yoshikuni ^a,b   Mochizuki, Hideki ^a,b  

^a JUNTENDO UNIVERSITY   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ALPHA SYNUCLEIN; PARKIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG EFFECT; EMBRYO; GENE OVEREXPRESSION; GENE THERAPY; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOTOR DYSFUNCTION; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PROTEIN FUNCTION; RAT; SUBSTANTIA NIGRA; VIRUS RECOMBINANT;

ALPHA-SYNUCLEIN; ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; GENE TARGETING; GENE THERAPY; GENETIC VECTORS; HUMANS; LENTIVIRUS; NERVE TISSUE PROTEINS; NEURONS; PARKINSON DISEASE; RATS; SUBSTANTIA NIGRA; SYNUCLEINS; UBIQUITIN-PROTEIN LIGASES;

ADENOVIRIDAE; ANIMALIA;

EID: 14844303486     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2005.16.262     Document Type: Article

References (51)

1. CHOI, P., GOLTS, N., SNYDER, H., CHONG, M., PETRUCELLI, L., HARDY, J., SPARKMAN, D., COCHRAN, E., LEE, J.M., and WOLOZIN, B. (2001). Co-association of parkin and alpha-synuclein. Neuroreport 12, 2839-2843.
2. CHUNG, K.K., ZHANG, Y., LIM, K.L., TANAKA, Y., HUANG, H., GAO, J., ROSS, C.A., DAWSON, V.L., and DAWSON, T.M. (2001). Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: Implications for Lewy-body formation in Parkinson disease. Nat. Med. 7, 1144-1150.
3. CONWAY, K.A., HARPER, J.D., and LANSBURY, P.T. Jr. (1998). Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med. 4, 1318-1320.
4. CONWAY, K.A., LEE, S.J., ROCHET, J.C., DING, T.T., WILLIAMSON, R.E., and LANSBURY, P.T., Jr. (2000). 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, 571-576.
5. DARIOS, F., CORTI, O., LUCKING, C.B., HAMPE, C., MURIEL, M.P., ABBAS, N., GU, W.J., HIRSCH, E.G., ROONEY, T., RUBERG, M., and BRICE, A. (2003). Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria- dependent cell death. Hum. Mol. Genet. 12, 517-526.
6. DAUER, W., and PRZEDBORSKI, S. (2003). Parkinson's disease: Mechanisms and models. Neuron 39, 889-909.
7. DAVIDSON, W.S., JONAS, A., CLAYTON, D.F., and GEORGE, J.M. (1998). Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273, 9443-9449.
8. DAWSON, T.M., and DAWSON, V.L. (2003). Molecular pathways of neurodegeneration in Parkinson's disease. Science 302, 819-822.
9. DONG, Z., FERGER, B., PATERNA, J.C., VOGEL, D., FURLER, S., OSINDE, M., FELDON, J., and BUELER, H. (2003). Dopamine-dependent neurodegeneration in rats induced by viral vector-mediated overexpression of the parkin target protein, CDCrel-1. Proc. Natl. Acad. Sci. U.S.A. 100, 12438-12443.
10. FAHN, S., and PRZEDBORSKI, S. (2000). Parkinsonism. In Merritt's Neurology L.P. Rowland, ed. (Lippincott Williams and Wilkins, New York) pp. 679-693.
11. FURLER, S., PATERNA, J.C., WEIBEL, M., and BUELER, H. (2001). Recombinant AAV vectors containing the foot and mouth disease virus 2A sequence confer efficient bicistronic gene expression in cultured cells and rat substantia nigra neurons. Gene Ther. 8, 864-873.
12. HASEGAWA, M., FUJIWARA, H., NONAKA, T., WAKABAYASHI, K., TAKAHASHI, H., LEE, V.M., TROJANOWSKI, J.Q., MANN, D., and IWATSUBO, T. (2002). Phosphorylated alpha-synuclein is ubiquitinated in alpha-synucleinopathy lesions. J. Biol. Chem. 277, 49071-49076.
13. HASHIMOTO, M., ROCKENSTEIN, E., and MASLIAH, E. (2003). Transgenic models of alpha-synuclein pathology: Past, present, and future. Ann. N.Y. Acad. Sci. 991, 171-188.
14. HIGASHI, Y., ASANUMA, M., MIYAZAKI, I., HATTORI, N., MIZUNO, Y., and OGAWA, N. (2004). Parkin attenuates manganese-induced dopaminergic cell death. J. Neurochem. 89, 1490-1497.
15. HSU, L.J., SAGARA, Y., ARROYO, A., ROCKENSTEIN, E., SISK, A., MALLORY, M., WONG, J., TAKENOUCHI, T., HASHIMOTO, M., and MASLIAH, E. (2000). Alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am. J. Pathol. 157, 401-410.
16. HUNOT, S., and HIRSCH, E.G. (2003). Neuroinflammatory processes in Parkinson's disease. Ann. Neurol. 53, S49-S60.
17. IMAI, Y., SODA, M., and TAKAHASHI, R. (2000). Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J. Biol. Chem. 275, 35661-35664.
18. IMAI, Y., SODA, M., INOUE, H., HATTORI, N., MIZUNO, Y., and TAKAHASHI, R. (2001). An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of parkin. Cell 105, 891-902.
19. JIANG, H., REN, Y., ZHAO, J., and FENG, J. (2004). Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Hum. Mol. Genet. 13, 1745-1754.
20. KIM, S.J., SUNG, J.Y., UM, J.W., HATTORI, N., MIZUNO, Y., TANAKA, K., PAIK, S.R., KIM, J., and CHUNG, K.C. (2003). Parkin cleaves intracellular alpha-synuclein inclusions via the activation of calpain. J. Biol. Chem. 278, 41890-41899.
21. KIRIK, D., ROSENBLAD, C., BURGER, C., LUNDBERG, C., JOHANSEN, T.E., MUZYCZKA, N., MANDEL, R.J., and BJORKLUND, A. (2002). Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. J. Neurosci. 22, 2780-2791.
22. KIRIK, D., ANNETT, L.E., BURGER, C., MUZYCZKA, N., MANDEL, R.J. and BJORKLUND, A. (2003). Nigrostriatal alpha-synucleinopathy induced by viral vector-mediated overexpression of human alpha-synuclein: A new primate model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 100, 2884-2889.
23. KITADA, T., ASAKAWA, S., HATTORI, N., MATSUMINE, H., YAMAMURA, Y., MINOSHIMA, S., YOKOCHI, M., MIZUNO, Y., and SHIMIZU, N. (1998). Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608.
24. KLEIN, R.L., KING, M.A., HAMBY, M.E., and MEYER, E.M. (2002). Dopaminergic cell loss induced by human A30P alpha-synuclein gene transfer to the rat substantia nigra. Hum. Gene Ther. 13, 605-612.
25. LEWY, F.H. (1912). In Handbuch der Neurologie Band III. M. Lewandowski, ed. (Springer, Berlin) pp. 920-933.
26. LO BIANCO, C., RIDET, I.L., SCHNEIDER, B.L., DEGLON, N., and AEBISCHER, P. (2002). Alpha-synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 99, 10813-10818.
27. LO BIANCO, C., SCHNEIDER, B.L., BAUER, M., SAJADI, A., BRICE, A., IWATSUBO, T., and AEBISCHER, P. (2004). Lentiviral vector delivery of parkin prevents dopaminergic degeneration in an alpha-synuclein rat model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 101, 17510-17515.
28. LUCKING, C.B., and BRICE, A. (2000). Alpha-synuclein and Parkinson's disease. Cell. Mol. Life. Sci. 57, 1894-1908.
29. McLEAN, P.J., KAWAMATA, H., RIBICH, S., and HYMAN, B.T. (2000). Membrane association and protein conformation of alpha-synuclein in intact neurons. Effect of Parkinson's disease-linked mutations. J. Biol. Chem. 275, 8812-8816.
30. MIZUGUCHI, H., XU, Z., ISHII-WATABE, A., UCHIDA, E., and HAYAKAWA, T. (2000). IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol. Ther. 1, 376-382.
31. OLUWATOSIN-CHIGBU, Y., ROBBINS, A., SCOTT, C.W., ARRIZA, I.L., REID, I.D., and ZYSK, J.R. (2003). Parkin suppresses wild-type alpha-synuclein-induced toxicity in SHSY-5Y cells. Biochem. Biophys. Res. Commun. 309, 679-684.
32. PAXINOS, G., and WATSON, C. (1998). The Rat Brain in Stereotaxic Coordinates, 4th ed. (Academic Press, New York).
33. PETRUCELLI, L., O'FARRELL, C., LOCKHART, P.J., BAPTISTA, M., KEHOE, K., VINK, L., CHOI, P., WOLOZIN, B., FARRER, M., HARDY, I., and COOKSON, M.R. (2002). Parkin protects against the toxicity associated with mutant alpha-synuclein: Proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36, 1007-1019.
34. POLYMEROPOULOS, M.H., LAVEDAN, C., LEROY, E., IDE, S.E., DEHEIIA, A., DUTRA, A., PIKE, B., ROOT, H., RUBENSTEIN, I., 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., and NUSSBAUM, R.L. (1997). Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047.
35. SCHLOSSMACHER, M.G., FROSCH, M.P., GAI, W.P., MEDINA, M., SHARMA, N., FORNO, L., OCHIISHI, T., SHIMURA, H., SHARON, R., HATTORI, N., LANGSTON, J.W., MIZUNO, Y., HYMAN, B.T., SELKOE, D.I., and KOSIK, K.S. (2002). Parkin localizes to the Lewy bodies of Parkinson disease and dementia with Lewy bodies. Am. J. Pathol. 160, 1655-1667.
36. SCHWARTING, R.K., and HUSTON, J.P. (1996). The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments. Prog. Neurobiol. 50, 275-331.
37. SHIMURA, H., HATTORI, N., KUBO, S., YOSHIKAWA, M., KITADA, T., MATSUMINE, H., ASAKAWA, S., MINOSHIMA, S., YAMAMURA, Y., SHIMIZU, N., and MIZUNO, Y. (1999). Immunohistochemical and subcellular localization of parkin protein: Absence of protein in autosomal recessive juvenile parkinsonism patients. Ann. Neurol. 45, 668-672.
38. SHIMURA, H., HATTORI, N., KUBO, S., MIZUNO, Y., ASAKAWA, S., MINOSHIMA, S., SHIMIZU, N., IWAI, K., CHIBA, T., TANAKA, K., and SUZUKI, T. (2000). Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet. 25, 302-305.
39. SHIMURA, H., SCHLOSSMACHER, M.G., HATTORI, N., FROSCH, M.P., TROCKENBACHER, A., SCHNEIDER, R., MIZUNO, Y., KOSIK, K.S., and SELKOE, D.J. (2001). Ubiquitination of a new form of alpha-synuclein by parkin from human brain: Implications for Parkinson's disease. Science 293, 263-269.
40. SPILLANTINI, M.G., SCHMIDT, M.L., LEE, V.M., TROJANOWSKI, J.Q., JAKES, R., and GOEDERT, M. (1997). Alpha-synuclein in Lewy bodies. Nature 388, 839-840.
41. STAROPOLI, J.F., McDERMOTT, C., MARTINAT, C., SCHULMAN, B., DEMIREVA, E., and ABELIOVICH, A. (2003). Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron 37, 735-749.
42. TAKAHASHI, H., OHAMA, E., SUZUKI, S., HORIKAWA, Y., ISHIKAWA, A., MORITA, T., TSUJI, S., and IKUTA, F. (1994). Familial juvenile parkinsonism: Clinical and pathologic study in a family. Neurology 44, 437-441.
43. TANAKA, Y., ENGELENDER, S., IGARASHI, S., RAO, R.K., WANNER, T., TANZI, R.E., SAWA, A., V, L.D., DAWSON, T. M., and ROSS, C. A. (2001). Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum. Mol. Genet. 10, 919-926.
44. TOFARIS, G.K., RAZZAQ, A., GHETTI, B., LILLEY, K.S., and SPILLANTINI, M.G. (2003). Ubiquitination of alpha-synuclein in Lewy bodies is a pathological event not associated with impairment of proteasome function. J. Biol. Chem. 278, 44405-44411.
45. UNGERSTEDT, U., and ARBUTHNOTT, G. (1970). Quantitative recording of rotational behavior in rats after 6-hydroxydopamine lesions of the nigrostriatal dopamine system. Brain Res. 24, 485-493
46. WARNER, T.T., and SCHAPIRA, A.H. (2003). Genetic and environmental factors in the cause of Parkinson's disease. Ann. Neurol. 53, S16-S25.
47. YAMADA, M., IWATSUBO, T., MIZUNO, Y., and MOCHIZUKI, H. (2004). Overexpression of α-synuclein in rat substantia nigra results in loss of dopaminergic neurons, phosphorylation of α-synuclein and activation of caspase-9. Resemblance to pathogenetic changes in Parkinson's disease. J. Neurochem. 91, 451-461.
48. YANG, Y., NISHIMURA, I., IMAI, Y., TAKAHASHI, R., and LU, B. (2003). Parkin suppresses dopaminergic neuron-selective neurotoxicity induced by Pael-R in Drosophila. Neuron 37, 911-924.
49. ZARATE-LAGUNES, M., GU, W.J., BLANCHARD, V., FRANCOIS, C., MURIEL, M.P., MOUATT-PRIGENT, A., BONICI, B., PARENT, A., HARTMANN, A., YELNIK, J., BOEHME, G.A., PRADIER, L., MOUSSAOUI, S., FAUCHEUX, B., RAISMANVOZARI, R., AGID, Y., BRICE, A., and HIRSCH, E.C. (2001). Parkin immunoreactivity in the brain of human and non-human primates: An immunohistochemical analysis in normal conditions and in Parkinsonian syndromes. J. Comp. Neurol. 432, 184-196.
50. ZHANG, Y., GAO, J., CHUNG, K.K., HUANG, H., DAWSON, V.L., and DAWSON, T.M. (2000). Parkin functions as an E2-dependent ubiquitin-protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc. Natl. Acad. Sci. U.S.A. 97, 13354-13359.
51. ZHOU, Y., ARAN, J., GOTTESMAN, M.M., and PASTAN, I. (1998). Co-expression of human adenosine deaminase and multidrug resistance using a bicistronic retroviral vector. Hum. Gene Ther. 9, 287-293.