Effects of UCH-L1 on α-synuclein over-expression mouse model of Parkinson's disease

Journal of Neurochemistry

Volumn 108, Issue 4, 2009, Pages 932-944

  Yasuda, Toru ^a   Nihira, Tomoko ^a   Ren, Yong Ri ^a   Cao, Xu Qing ^a   Wada, Keiichiro ^a   Setsuie, Rieko ^b   Kabuta, Tomohiro ^b   Wada, Keiji ^b   Hattori, Nobutaka ^a   Mizuno, Yoshikuni ^a   Mochizuki, Hideki ^a  

^a JUNTENDO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

synuclein; Adeno associated virus; Dopaminergic neurons; Parkinson's disease; Ubiquitin carboxy terminal hydrolase L1

Indexed keywords

ALPHA SYNUCLEIN; PARVOVIRUS VECTOR; UBIQUITIN CARBOXY TERMINAL HYDROLASE L1; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LEWY BODY; MALE; MOUSE; NERVE FIBER DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TRANSGENIC MOUSE;

AGED; ALPHA-SYNUCLEIN; ANIMALS; BRAIN CHEMISTRY; CELL DEATH; DISEASE MODELS, ANIMAL; DOPAMINE; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; NERVE DEGENERATION; NEURONS; PARKINSON DISEASE; SUBSTANTIA NIGRA; UBIQUITIN THIOLESTERASE;

ADENO-ASSOCIATED VIRUS; MUS;

EID: 58549119203     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05827.x     Document Type: Article

References (48)

1. 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.
2. Castegna A., Thongboonkerd V., Klein J., Lynn B. C., Wang Y. L., Osaka H., Wada K. Butterfield D. A. (2004) Proteomic analysis of brain proteins in the gracile axonal dystrophy (gad) mouse, a syndrome that emanates from dysfunctional ubiquitin carboxyl-terminal hydrolase L-1, reveals oxidation of key proteins. J. Neurochem. 88, 1540 1546.
3. Chandra S., Gallardo G., Fernandez-Chacon R., Schluter O. M. Sudhof T. C. (2005) Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123, 383 396.
4. Choi J., Levey A. I., Weintraub S. T., Rees H. D., Gearing M., Chin L. S. Li L. (2004) Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J. Biol. Chem. 279, 13256 13264.
5. Chu Y. Kordower J. H. (2007) Age-associated increases of alpha-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: is this the target for Parkinson's disease? Neurobiol. Dis. 25, 134 149.
6. Conway K. A., Rochet J. C., Bieganski R. M. Lansbury P. T. Jr. (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294, 1346 1349.
7. da Costa C. A., Ancolio K. Checler F. (2000) Wild-type but not Parkinson's disease-related ala-53 - > Thr mutant alpha-synuclein protects neuronal cells from apoptotic stimuli. J. Biol. Chem. 275, 24065 24069.
8. Farrer M. J. (2006) Genetics of Parkinson disease: paradigm shifts and future prospects. Nat. Rev. Genet. 7, 306 318.
9. 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.
10. Gong B., Cao Z., Zheng P., Vitolo O. V., Liu S., Staniszewski A., Moolman D., Zhang H., Shelanski M. Arancio O. (2006) Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 126, 775 788.
11. Gorbatyuk O. S., Li S., Sullivan L. F., Chen W., Kondrikova G., Manfredsson F. P., Mandel R. J. Muzyczka N. (2008) The phosphorylation state of Ser-129 in human alpha-synuclein determines neurodegeneration in a rat model of Parkinson disease. Proc. Natl Acad. Sci. USA 105, 763 768.
12. Harada T., Harada C., Wang Y. L. et al. (2004) Role of ubiquitin carboxy terminal hydrolase-L1 in neural cell apoptosis induced by ischemic retinal injury in vivo. Am. J. Pathol. 164, 59 64.
13. Kabuta T. Wada K. (2008) Insights into links between familial and sporadic Parkinson's disease: physical relationship between UCH-L1 variants and chaperone-mediated autophagy. Autophagy 4, 827 829.
14. Kabuta T., Furuta A., Aoki S., Furuta K. Wada K. (2008a) Aberrant interaction between Parkinson's disease-associated mutant UCH-L1 and the lysosomal receptor for chaperone-mediated autophagy. J. Biol. Chem. 283, 23731 23738.
15. Kabuta T., Setsuie R., Mitsui T., Kinugawa A., Sakurai M., Aoki S., Uchida K. Wada K. (2008b) Aberrant molecular properties shared by familial Parkinson's disease-associated mutant UCH-L1 and carbonyl-modified UCH-L1. Hum. Mol. Genet. 17, 1482 1496.
16. Kirik D., Rosenblad C., Burger C., Lundberg C., Johansen T. E., Muzyczka N., Mandel R. J. Bjorklund A. (2002) Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. J. Neurosci. 22, 2780 2791.
17. Kirik D., Annett L. E., Burger C., Muzyczka N., Mandel R. J. 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. USA 100, 2884 2889.
18. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J. T., Schols L. Riess O. (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18, 106 108.
19. Kurihara L. J., Kikuchi T., Wada K. Tilghman S. M. (2001) Loss of Uch-L1 and Uch-L3 leads to neurodegeneration, posterior paralysis and dysphagia. Hum. Mol. Genet. 10, 1963 1970.
20. Larsen C. N., Price J. S. Wilkinson K. D. (1996) Substrate binding and catalysis by ubiquitin C-terminal hydrolases: identification of two active site residues. Biochemistry 35, 6735 6744.
21. Larsen C. N., Krantz B. A. Wilkinson K. D. (1998) Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry 37, 3358 3368.
22. Leroy E., Boyer R., Auburger G. et al. (1998) The ubiquitin pathway in Parkinson's disease. Nature 395, 451 452.
23. Li W., Lesuisse C., Xu Y., Troncoso J. C., Price D. L. Lee M. K. (2004) Stabilization of alpha-synuclein protein with aging and familial Parkinson's disease-linked A53T mutation. J. Neurosci. 24, 7400 7409.
24. Liu Y., Fallon L., Lashuel H. A., Liu Z. Lansbury P. T. Jr. (2002) The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 111, 209 218.
25. Lo Bianco C., Ridet J. L., Schneider B. L., Deglon N. Aebischer P. (2002) Alpha-synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc. Natl Acad. Sci. USA 99, 10813 10818.
26. Lombardino A. J., Li X. C., Hertel M. Nottebohm F. (2005) Replaceable neurons and neurodegenerative disease share depressed UCHL1 levels. Proc. Natl Acad. Sci. USA 102, 8036 8041.
27. Lowe J., McDermott H., Landon M., Mayer R. J. Wilkinson K. D. (1990) Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases. J. Pathol. 161, 153 160.
28. Mandir A. S., Przedborski S., Jackson-Lewis V., Wang Z. Q., Simbulan-Rosental C. M., Smulson M. E., Hoffman B. E., Guastella D. B., Dawson V. L. Dawson T. M. (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.
29. Miura H., Oda K., Endo C., Yamazaki K., Shibasaki H. Kikuchi T. (1993) Progressive degeneration of motor nerve terminals in GAD mutant mouse with hereditary sensory axonopathy. Neuropathol. Appl. Neurobiol. 19, 41 51.
30. Mosharov E. V., Staal R. G., Bove J. et al. (2006) Alpha-synuclein overexpression increases cytosolic catecholamine concentration. J. Neurosci. 26, 9304 9311.
31. Nishikawa K., Li H., Kawamura R. et al. (2003) Alterations of structure and hydrolase activity of parkinsonism-associated human ubiquitin carboxyl-terminal hydrolase L1 variants. Biochem. Biophys. Res. Commun. 304, 176 183.
32. Nishioka K., Hayashi S., Farrer M. J. et al. (2006) Clinical heterogeneity of alpha-synuclein gene duplication in Parkinson's disease. Ann. Neurol. 59, 298 309.
33. Norris E. H., Giasson B. I., Hodara R., Xu S., Trojanowski J. Q., Ischiropoulos H. Lee V. M. (2005) Reversible inhibition of alpha-synuclein fibrillization by dopaminochrome-mediated conformational alterations. J. Biol. Chem. 280, 21212 21219.
34. Oda K., Yamazaki K., Miura H., Shibasaki H. Kikuchi T. (1992) Dying back type axonal degeneration of sensory nerve terminals in muscle spindles of the gracile axonal dystrophy (GAD) mutant mouse. Neuropathol. Appl. Neurobiol. 18, 265 281.
35. Osaka H., Wang Y. L., Takada K. et al. (2003) Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. Hum. Mol. Genet. 12, 1945 1958.
36. Polymeropoulos M. H., Lavedan C., Leroy E. et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276, 2045 2047.
37. Ramirez A., Heimbach A., Grundemann J. et al. (2006) Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat. Genet. 38, 1184 1191.
38. Saigoh K., Wang Y. L., Suh J. G. et al. (1999) Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat. Genet. 23, 47 51.
39. Sambrook J. Russell D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Setsuie R., Wang Y. L., Mochizuki H. et al. (2007) Dopaminergic neuronal loss in transgenic mice expressing the Parkinson's disease-associated UCH-L1 I93M mutant. Neurochem. Int. 50, 119 129.
41. Singleton A. B., Farrer M., Johnson J. et al. (2003) Alpha-synuclein locus triplication causes Parkinson's disease. Science 302, 841.
42. Spillantini M. G., Schmidt M. L., Lee V. M., Trojanowski J. Q., Jakes R. Goedert M. (1997) Alpha-synuclein in Lewy bodies. Nature 388, 839 840.
43. Wilkinson K. D., Lee K. M., Deshpande S., Duerksen-Hughes P., Boss J. M. Pohl J. (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246, 670 673.
44. Xu J., Kao S. Y., Lee F. J., Song W., Jin L. W. Yankner B. A. (2002) Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat. Med. 8, 600 606.
45. Yamada M., Iwatsubo T., Mizuno Y. Mochizuki H. (2004) Overexpression of alpha-synuclein in rat substantia nigra results in loss of dopaminergic neurons, phosphorylation of alpha-synuclein and activation of caspase-9: resemblance to pathogenetic changes in Parkinson's disease. J. Neurochem. 91, 451 461.
46. Yasuda T., Miyachi S., Kitagawa R. et al. (2007) Neuronal specificity of alpha-synuclein toxicity and effect of Parkin co-expression in primates. Neuroscience 144, 743 753.
47. Zarranz J. J., Alegre J., Gomez-Esteban J. C. et al. (2004) The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 55, 164 173.
48. Zhou Y., Gu G., Goodlett D. R., Zhang T., Pan C., Montine T. J., Montine K. S., Aebersold R. H. Zhang J. (2004) Analysis of alpha-synuclein-associated proteins by quantitative proteomics. J. Biol. Chem. 279, 39155 39164.