Role for the ubiquitin-proteasome system in Parkinson’s disease and other neurodegenerative brain amyloidoses

Abeliovich, A., Schmitz, Y., Farinas, I., et al. (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25, 239–252. Alam Z. I., Daniel S. E., Lees A. J., et al. (1997) A generalised increase in protein carbonyls in the brain in Parkinson’s but not incidental Lewy body disease. J. Neurochem. 69, 1326–1329. Auluck P. K. and Bonini N. M. (2002) Pharmacological prevention of Parkinson disease in Drosophila. Nat. Med. 8, 1185–1186. Auluck P. K., Chan H. Y., Trojanowski J. Q., Lee V. M., and Bonini N. M. (2002) Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson’s disease. Science 295, 865–868. Bence N. F., Sampat R. M., and Kopito R. R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552–1555. Bennett M. C., Bishop J. F., Leng Y., et al. (1999) Degradation of alpha-synuclein by proteasome. J. Biol. Chem. 274, 33855–33858. Bonifati V., Rizzu P., van Baren M. J., et al. (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299, 256–259. Bonifati V., De Michele G., Lucking C. B., et al. (2001) The parkin gene and its phenotype. Italian PD Genetics Study Group, French PD Genetics Study Group and the European Consortium on Genetic Susceptibility in Parkinson’s Disease. Neurol. Sci. 22, 51–52. Chung K. K., Dawson V. L., and Dawson T. M. (2001a) The role of the ubiquitin-proteasomal pathway in Parkinson’s disease and other neurodegenerative disorders. Trends Neurosci. 24, S7-S14. Chung K. K., Zhang Y., Lim K. L., et al. (2001b) Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: implications for Lewy-body formation in Parkinson disease. Nat. Med. 7, 1144–1150. Ciechanover A., Orian A., and Schwartz A. L. (2000) Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays 22, 442–451. Conway K. A., Rochet J. C., Bieganski R. M., and Lansbury, Jr., P. T. (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294, 1346–1349. Conway K. A., Harper J. D., and Lansbury P. T. (1998) Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med. 4, 1318–1320. Corti O., Hampe C., Koutnikova H., et al. (2003) The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration. Hum. Mol. Genet. 12, 1427–1437. Cummings C. J., Reinstein E., Sun Y., et al. (1999) Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron 24, 879–92. Dawson T. M. and Dawson V. L. (2003) Rare genetic mutations shed light on the pathogenesis of Parkinson disease. J. Clin. Invest. 111, 145–151. Feany M. B. and Bender W. W. (2000) A Drosophila model of Parkinson’s disease. Nature 404, 394–398. Forno L. S. (1996) Neuropathology of Parkinson’s disease. J. Neuropathol. Exp. Neurol. 55, 259–272. Gasser T. (2003) Overview of the genetics of parkinsonism. Adv. Neurol. 91, 143–152. Ghee M., Fournier A., and Mallet J. (2000) Rat alpha-synuclein interacts with Tat binding protein 1, a component of the 26S proteasomal complex. J. Neurochem. 75, 2221–2224. Giasson B. I., Duda J. E., Quinn S. M., Zhang B., Trojanowski J. Q., and Lee V. M. (2002) Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. Neuron 34, 521–533. Glickman M. H. and Ciechanover A. (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82, 373–428. Goedert M. (2001) Alpha-synuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2, 492–501. Golbe L. I., Di Iorio G., Bonavita V., Miller D. C., and Duvoisin R. C. (1990) A large kindred with autosomal dominant Parkinson’s disease. Ann. Neurol. 27, 276–282. Gomez-Isla T., Irizarry M. C., Mariash A., et al. (2003) Motor dysfunction and gliosis with preserved dopaminergic markers in human alpha-synuclein A30P transgenic mice. Neurobiol. Aging 24, 245–258. Greene J. C., Whitworth A. J., Kuo I., et al. (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. USA 100, 4078–4083. Grune T., Merker K., Sandig G., and Davies K. J. (2003) Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem. Biophys. Res. Commun. 305, 709–718. Harhangi B. S., Farrer M. J., Lincoln S., et al. (1999) The Ile93Met mutation in the ubiquitin carboxy-terminal-hydrolase-L1 gene is not observed in European cases with familial Parkinson’s disease. Neurosci. Lett. 270, 1–4. Hartmann-Petersen R., Seeger M., and Gordon C. (2003) Transferring substrates to the 26S proteasome. Trends Biochem. Sci. 28, 26–31. Hasegawa M., Fujiwara H., Nonaka T., et al. (2002) Phosphorylated alpha-synuclein is ubiquitinated in alpha-synucleinopathy lesions. J. Biol. Chem. 277, 49071–49076. Ii K., Ito H., Tanaka K., and Hirano A. (1997) Immunocytochemical co-localization of the proteasome in ubiquitinated structures in neurodegenerative diseases and the elderly. J. Neuropathol. Exp. Neurol. 56, 125–131. Imai Y., Soda M., Hatakeyama S., et al. (2002) CHIP is associated with Parkin, a gene responsible for familial Parkinson’s disease, and enhances its ubiquitin ligase activity. Mol. Cell 10, 55–67. Imai Y., Soda M., Inoue H., et al. (2001) An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105, 891–902. 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. Kirik D., Rosenblad C., Burger C., et al. (2002) Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. J. Neurosci. 22, 2780–2791. Kitada T., Asakawa S., Hattori N., et al. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605–608. 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. Kruger R., Kuhn W., Muller T., et al. (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson’s disease. Nat. Genet. 18, 106–108. Lakso M., Vartiainen S., Moilanen A. M., et al. (2003) Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J. Neurochem. 86, 165–172. Lang A. E. and Lozano A. M. (1998a) Parkinson’s disease. First of two parts. N. Engl. J. Med. 339, 1044–1053. Lang A. E. and Lozano A. M. (1998b) Parkinson’s disease. Second of two parts. N. Engl. J. Med. 339, 1130–1143. Larsen C. N., Krantz B. A., and Wilkinson K. D. (1998) Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry 37, 3358–3368. Lee M., Hyun D., Halliwell B., and Jenner P. (2001) Effect of the overexpression of wild-type or mutant alpha-synuclein on cell susceptibility to insult. J. Neurochem. 76, 998–1009. Lee M. K., Stirling W., Xu Y., et al. (2002) Human alpha-synuclein-harboring familial Parkinson’s disease-linked Ala-53 → Thr mutation causes neurodegenerative disease with alpha-synuclein aggregation in transgenic mice. Proc. Natl. Acad. Sci. USA 99, 8968–8973. Leroy E., Boyer R., Auburger G., et al. (1998) The ubiquitin pathway in Parkinson’s disease. Nature 395, 451–452. Lim K. L., Tanaka Y., Zhang Y., et al. (2002) Parkin mediates lysine-63 (K-63)-linked ubiquitination of synphilin-1: implications for Lewy body formation. Abstr. Soc. Neurosci. 32, 484.13. Liu Y., Fallon L., Lashuel H. A., Liu Z., and Lansbury, Jr., P. T. (2002) The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson’s disease susceptibility. Cell 111, 209–218. Lo Bianco C., Ridet J. 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. USA 99, 10813–10818. Lopiano L., Fasano M., Giraudo S., et al. (2000) Nuclear magnetic relaxation dispersion profiles of substantia nigra pars compacta in Parkinson’s disease patients are consistent with protein aggregation. Neurochem. Int 37, 331–336. Lowe J., McDermott H., Landon M., Mayer R. J., and 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. Maraganore D. M., Farrer M. J., Hardy J. A., et al (1999) Case-control study of the ubiquitin carboxy-terminal hydrolase L1 gene in Parkinson’s disease. Neurology 53, 1858–1860. Masliah E., Rockenstein E., Veinbergs I., et al. (2000) Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287, 1265–1269. Matsuoka Y., Vila M., Lincoln S., et al. (2001) Lack of nigral pathology in transgenic mice expressing human alpha-synuclein driven by the tyrosine hydroxylase promoter. Neurobiol. Dis. 8 535–539. McLean P. J., Kawamata H., and Hyman B. T. (2001) Alpha-synuclein-enhanced green fluorescent protein fusion proteins form proteasome sensitive inclusions in primary neurons. Neuroscience 104, 901–912. McNaught K. S., Belizaire R., Isacson O., Jenner P., and Olanow C. W. (2003) Altered proteasomal function in sporadic Parkinson’s disease. Exp. Neurol. 179, 38–46. McNaught K. S. and Olanow C. W. (2003) Proteolytic stress: a unifying concept for the etiopathogenesis of Parkinson’s disease. Ann. Neurol. 53, S73-S84. McNaught K. S., Shashidharan P., Perl D. P., Jenner P., and Olanow C. W. (2002a) Aggresome-related biogenesis of Lewy bodies. Eur. J. Neurosci. 16, 2136–2148. McNaught K. S., Mytilineou C., Jnobaptiste R., Yabut J., Shashidharan P., Jenner P., et al. (2002b) Impairment of the ubiquitin-proteasome system causes dopaminergic cell death and inclusion body formation in ventral mesencephalic cultures. J. Neurochem. 81, 301–306. McNaught K. S., Belizaire R., Jenner P., Olanow C. W., and Isacson O. (2002c) Selective loss of 20S proteasome alpha-subunits in the substantia nigra pars compacta in Parkinson’s disease. Neurosci. Lett. 326, 155–158. McNaught K. S., Bjorklund L. M., Belizaire R., et al. (2002d) Proteasome inhibition causes nigral degeneration with inclusion bodies in rats. Neuroreport 13, 1437–1441. McNaught K. S. and Jenner P. (2001) Proteasomal function is impaired in substantia nigra in Parkinson’s disease. Neurosci. Lett. 297, 191–194. Mizuno Y., Hattori N., Mori H., Suzuki T., and Tanaka K. (2001) Parkin and Parkinson’s disease. Curr. Opin. Neurol. 14, 477–482. Mori H., Kondo T., Yokochi M., et al. (1998) Pathologic and biochemical studies of juvenile parkinsonism linked to chromosome 6q. Neurology 51, 890–892. Nam S., Smith D. M., and Dou Q. P. (2001) Ester bond-containing tea polyphenols potently inhibit proteasome activity in vitro and in vivo. J. Biol. Chem. 276, 13322–13330. Perez R. G., Waymire J. C., Lin E., et al. (2002) A role for alpha-synuclein in the regulation of dopamine biosynthesis. J. Neurosci. 22, 3090–3099. Petrucelli L., O’Farrell C., Lockhart P. J., et al. (2002) Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36, 1007–1019. Pickart C. M. (2001) Mechanisms underlying ubiquitination. Ann. Rev. Biochem. 70, 503–533. 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. Ren Y., Zhao J., and Feng J. (2003) Parkin binds to alpha/beta tubulin and increases their ubiquitination and degradation. J. Neurosci. 23, 3316–3324. Rideout H. J., Larsen K. E., Sulzer D., and Stefanis L. (2001) Proteasomal inhibition leads to formation of ubiquitin/alpha-synuclein-immunoreactive inclusions in PC12 cells. J. Neurochem. 78, 899–908. 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. Sakata E., Yamaguchi Y., Kurimoto E., et al. (2003) Parkin binds the Rpn10 subunit of 26S proteasomes through its ubiquitin-like domain. EMBO Rep. 4, 301–306. Sampathu D. M., Giasson B. I., Pawlyk A. C., Trojanowski J. Q., and Lee V. M. (2003) Ubiquitination of alpha-synuclein is not required for formation of pathological inclusions in alpha-synucleinopathies. Am. J. Pathol. 163, 91–100. Shashidharan P., Good P. F., Hsu A., et al. (2000) Torsin A accumulation in Lewy bodies in sporadic Parkinson’s disease. Brain Res. 877, 379–381. Sherman M. Y. and Goldberg A. L. (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29, 15–32. Shimura H., Schlossmacher M. G., Hattori N., et al. (2001) Ubiquitination of a new form of alpha-synuclein by parkin from human brain: implications for Parkinson’s disease. Science 293, 263–269. Shimura H., Hattori N., Kubo S., et al. (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet. 25, 302–5. Shimura H., Hattori N., Kubo S., et al. (1999) Immunohistochemical and subcellular localization of Parkin protein: absence of protein in autosomal recessive juvenile parkinsonism patients. Ann. Neurol. 45, 668–672. Snyder H., Mensah K., Theisler C., et al. (2003) Aggregated and monomeric alpha-synuclein bind to the S6′ proteasomal protein and inhibit proteasomal function. J. Biol. Chem. 278, 11753–11759. Solano S. M., Miller D. W., Augood S. J., Young A. B., and Penney, Jr., J. B. (2000) Expression of alpha-synuclein, parkin, and ubiquitin carboxy-terminal hydrolase L1 mRNA in human brain: genes associated with familial Parkinson’s disease. Ann. Neurol. 47, 201–210. Souza J. M., Giasson B. I., Lee V. M., and Ischiropoulos H. (2000) Chaperone-like activity of synucleins. FEBS Lett. 474, 116–119. Spillantini M. G., Crowther R. A., Jakes R., Hasegawa M., and Goedert M. (1998) alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson’s disease and dementia with lewy bodies. Proc. Natl. Acad. Sci. USA 95, 6469–6473. Spira P. J., Sharpe D. M., Halliday G., Cavanagh J., and Nicholson G. A. (2001) Clinical and pathological features of a Parkinsonian syndrome in a family with an Ala53Thr alpha-synuclein mutation. Ann. Neurol. 49, 313–319. Staropoli J. F., McDermott C., Martinat C., et al. (2003) Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron 37, 735–749. Stefanis L., Larsen K. E., Rideout H. J., Sulzer D., and Greene L. A. (2001) Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci. 21, 9549–9560. Tanaka Y., Engelender S., Igarashi S., et al. (2001) Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum. Mol. Genet. 10, 919–926. Tofaris G. K., Layfield R., and Spillantini M. G. (2001) alpha-synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett. 509, 22–26. Tsai Y. C., Fishman P. S., Thakor N. V., and Oyler G. A. (2003) Parkin facilitates the elimination of expanded polyglutamine proteins and leads to preservation of proteasome function. J. Biol. Chem. 278, 22044–22055. Voges D., Zwickl P., and Baumeister W. (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Ann. Rev. Biochem. 68, 1015–1068. Wakabayashi K., Engelender S., Yoshimoto M., et al. (2000) Synphilin-1 is present in Lewy bodies in Parkinson’s disease. Ann. Neurol. 47, 521–523. Warner T. T. and Schapira A. H. (2003) Genetic and environmental factors in the cause of Parkinson’s disease. Ann. Neurol. 53, S16-S23. Weinreb P. H., Zhen W., Poon A. W., Conway K. A., and Lansbury, Jr., P. T. (1996) NACP, a protein implicated in Alzheimer’s disease and learning, is natively unfolded. Biochemistry 35, 13709–13715. Wilkinson K. D., Lee K. M., Deshpande S., et al. (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246, 670–673. Wintermeyer P., Kruger R., Kuhn W., et al. (2000) Mutation analysis and association studies of the UCHL1 gene in German Parkinson’s disease patients. Neuroreport 11, 2079–2082. Xu J., Kao S. Y., Lee F. J., et al. (2002) Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat. Med. 8, 600–606. 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. Zhang Y., Gao J., Chung K. K., et al. (2000a) 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. USA 97, 13354–13359. Zhang J., Hattori N., Leroy E., et al. (2000b) Association between a polymorphism of ubiquitin carboxy-terminal hydrolase L1 (UCH-L1) gene and sporadic Parkinson’s disease. Parkinsonism Relat. Disord. 6, 195–197.