Disruption of protein quality control in Parkinson's disease

Cold Spring Harbor Perspectives in Medicine

Volumn 2, Issue 5, 2012, Pages

  Cook, Casey ^a   Stetler, Caroline ^a   Petrucelli, Leonard ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; UBIQUITIN PROTEIN LIGASE E3; ADENOSINE TRIPHOSPHATASE; PROTEASOME; PROTEIN; UBIQUITIN;

ARTICLE; GENE MUTATION; HUMAN; MACROAUTOPHAGY; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN QUALITY; PROTEIN SYNTHESIS; QUALITY CONTROL; SIGNAL TRANSDUCTION; AGING; ANIMAL; AUTOPHAGY; DRUG EFFECT; GENETICS; LYSOSOME; METABOLISM; MOUSE; MUTATION; PHYSIOLOGY; POLLUTANT; PROTEIN FOLDING; PROTEOSTASIS DEFICIENCY; RAT; REVIEW; RISK FACTOR;

ADENOSINE TRIPHOSPHATASES; AGING; ANIMALS; AUTOPHAGY; ENVIRONMENTAL POLLUTANTS; HUMANS; LYSOSOMES; MICE; MUTATION; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEINS; PROTEOLYSIS; PROTEOSTASIS DEFICIENCIES; RATS; RISK FACTORS; SIGNAL TRANSDUCTION; UBIQUITIN;

EID: 84869014351     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a009423     Document Type: Article

References (136)

1. Alvarez-Erviti L, Rodriguez-Oroz MC, Cooper JM, Caballero C, Ferrer I, ObesoJA, Schapira AH. 2010. Chaperone-mediated autophagy markers in Parkinson disease brains. Arch Neurol 67: 1464-1472.
2. Anderson JP, Walker DE, Goldstein JM, de Laat R, Banducci K, Caccavello RJ, Barbour R, Huang J, Kling K, Lee M, et al. 2006. Phosphorylation of Ser-129 is the dominant pathological modification of α-synuclein in familial and sporadic Lewy body disease. J Biol Chem 281: 29739-29752.
3. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM. 2002. Chaperone suppression of α-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295: 865-868.
4. Balch WE, Morimoto RI, Dillin A, Kelly JW. 2008. Adapting proteostasis for disease intervention. Science 319: 916-919.
5. Bandyopadhyay U, Cuervo AM. 2007. Chaperone-mediated autophagy in aging and neurodegeneration: Lessons from α-synuclein. Exp Gerontol 42: 120-128.
6. Bence NF, Sampat RM, Kopito RR. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292: 1552-1555.
7. Bennett EJ, Bence NF, Jayakumar R, Kopito RR. 2005. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol Cell 17: 351-365.
8. Berman SB, Hastings TG. 1999. Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: Implications for Parkinson's disease. J Neurochem 73: 1127-1137.
9. Betarbet R, Canet-Aviles RM, Sherer TB, Mastroberardino PG, McLendon C, KimJH, Lund S, Na HM, Taylor G, Bence NF, et al. 2006. Intersecting pathways to neurodegeneration in Parkinson's disease: Effects of the pesticide rotenone on DJ-1, α-synuclein, and the ubiquitin-proteasome system. Neurobiol Dis 22: 404-420.
10. Bisaglia M, Mammi S, Bubacco L. 2007. Kinetic and structural analysis of the early oxidation products of dopamine: Analysis of the interactions with α-synuclein. J Biol Chem 282: 15597-15605.
11. Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E, DekkerMC, Squitieri F, Ibanez P, Joosse M, et al. 2003. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299: 256-259.
12. Bulteau AL, Lundberg KC, Humphries KM, Sadek HA, Szweda PA, Friguet B, Szweda LI. 2001. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J Biol Chem 276: 30057-30063.
13. Bussell R Jr., Eliezer D. 2001. Residual structure and dynamics in Parkinson's disease-associated mutants of α-synuclein. J Biol Chem 276: 45996-46003.
14. Chen L, Periquet M, Wang X, Negro A, McLean PJ, Hyman BT, Feany MB. 2009. Tyrosine and serine phosphorylation of α-synuclein have opposing effects on neurotoxicity and soluble oligomer formation. J Clin Invest 119: 3257-3265.
15. Ciechanover A, Brundin P. 2003. The ubiquitin proteasome system in neurodegenerative diseases: Sometimes the chicken, sometimes the egg. Neuron 40: 427-446.
16. Ciechanover A, Orian A, Schwartz AL. 2000. Ubiquitin-mediated proteolysis: Biological regulation via destruction. Bioessays 22: 442-451.
17. Corti O, Hampe C, Koutnikova H, Darios F, Jacquier S, Prigent A, Robinson JC, Pradier L, Ruberg M, Mirande M, 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.
18. Cuervo AM. 2004. Autophagy: In sickness and in health. Trends Cell Biol 14: 70-77.
19. Cuervo AM, Dice JF. 1996. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273: 501-503.
20. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D. 2004. Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science 305: 1292-1295.
21. Cuervo AM, Bergamini E, Brunk UT, Droge W, Ffrench M, Terman A. 2005. Autophagy and aging: The importance of maintaining "clean" cells. Autophagy 1: 131-140.
22. Cummings CJ, Reinstein E, Sun Y, Antalffy B, Jiang Y, Ciechanover A, Orr HT, Beaudet AL, Zoghbi HY. 1999. Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron 24: 879-892.
23. Cummings CJ, Sun Y, Opal P, Antalffy B, Mestril R, Orr HT, Dillmann WH, Zoghbi HY. 2001. Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum Mol Genet 10: 1511-1518.
24. Dauer W, Przedborski S. 2003. Parkinson's disease: Mechanisms and models. Neuron 39: 889-909.
25. Dick TP, Nussbaum AK, Deeg M, Heinemeyer W, Groll M, Schirle M, Keilholz W, Stevanovic S, Wolf DH, Huber R, et al. 1998. Contribution of proteasomal β-subunits to the cleavage of peptide substrates analyzed with yeast mutants. J Biol Chem 273: 25637-25646.
26. Emmanouilidou E, Stefanis L, Vekrellis K. 2010. Cell-produced α-synuclein oligomers are targeted to, and impair, the 26S proteasome. Neurobiol Aging 31: 953-968.
27. Erlich S, Shohami E, Pinkas-Kramarski R. 2006. Neurodegeneration induces upregulation of Beclin 1. Autophagy 2: 49-51.
28. Fornai F, Lenzi P, Gesi M, Ferrucci M, Lazzeri G, Busceti CL, Ruffoli R, Soldani P, Ruggieri S, Alessandri MG, et al. 2003. Fine structure and biochemical mechanisms underlying nigrostriatal inclusions and cell death after proteasome inhibition. J Neurosci 23: 8955-8966.
29. Fornai F, Schluter OM, Lenzi P, Gesi M, Ruffoli R, Ferrucci M, Lazzeri G, BuscetiCL, Pontarelli F, Battaglia G, et al. 2005. Parkinson-like syndrome induced by continuous MPTP infusion: Convergent roles of the ubiquitin-proteasome system and α-synuclein. Proc Natl Acad Sci 102: 3413-3418.
30. Friguet B, Stadtman ER, Szweda LI. 1994. Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Formation of cross-linked protein that inhibits the multicatalytic protease. J Biol Chem 269: 21639-21643.
31. Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, Goldberg MS, Shen J, Takio K, Iwatsubo T. 2002. α-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4: 160-164.
32. Giasson BI, Duda JE, Murray IV, Chen Q, Souza JM, Hurtig HI, Ischiropoulos H, Trojanowski JQ, Lee VM. 2000. Oxidative damage linked to neurodegeneration by selective α-synuclein nitration in synucleinopathy lesions. Science 290: 985-989.
33. Grune T, Reinheckel T, Joshi M, Davies KJ. 1995. Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome. J Biol Chem 270: 2344-2351.
34. Grune T, Reinheckel T, Davies KJ. 1996. Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J Biol Chem 271: 15504-15509.
35. Grune T, Blasig IE, Sitte N, Roloff B, Haseloff R, Davies KJ. 1998. Peroxynitrite increases the degradation of aconitase and other cellular proteins by proteasome. J Biol Chem 273: 10857-10862.
36. Hamacher-Brady A, Brady NR, Gottlieb RA. 2006. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 281: 29776-29787.
37. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-MigishimaR, Yokoyama M, Mishima K, Saito I, Okano H, et al. 2006. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441: 885-889.
38. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu Rev Biochem 67: 425-479.
39. Ii K, Ito H, Tanaka K, 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.
40. Ikeda F, Dikic I. 2008. Atypical ubiquitin chains: New molecular signals. "Protein Modifications: Beyond the Usual Suspects" review series. EMBO Rep 9: 536-542.
41. Iwata A, Christianson JC, Bucci M, Ellerby LM, Nukina N, Forno LS, Kopito RR. 2005a. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc Natl Acad Sci 102: 13135-13140.
42. Iwata A, Riley BE, Johnston JA, Kopito RR. 2005b. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280: 40282-40292.
43. Jana NR, Zemskov EA, Wang G, Nukina N. 2001. Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum Mol Genet 10: 1049-1059.
44. Kamimoto T, Shoji S, Hidvegi T, Mizushima N, Umebayashi K, Perlmutter DH, Yoshimori T. 2006. Intracellular inclusions containing mutant α1-antitrypsin Z are propagated in the absence of autophagic activity. J Biol Chem 281: 4467-4476.
45. Kegel KB, Kim M, Sapp E, McIntyre C, Castano JG, Aronin N, DiFiglia M. 2000. Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J Neurosci 20: 7268-7278.
46. Keller JN, Huang FF, Dimayuga ER, Maragos WF. 2000a. Dopamine induces proteasome inhibition in neural PC12 cell line. Free Radic Biol Med 29: 1037-1042.
47. Keller JN, Huang FF, Markesbery WR. 2000b. Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neuroscience 98: 149-156.
48. Kiffin R, Christian C, Knecht E, Cuervo AM. 2004. Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell 15: 4829-4840.
49. Kim J, Scott SV, Oda MN, Klionsky DJ. 1997. Transport of a large oligomeric protein by the cytoplasm to vacuole protein targeting pathway. J Cell Biol 137: 609-618.
50. Kim HT, Kim KP, Lledias F, Kisselev AF, Scaglione KM, Skowyra D, Gygi SP, Goldberg AL. 2007. Certain pairs of ubiquitin-conjugating enzymes (E2s) and ubiquitin-protein ligases (E3s) synthesize nondegradable forked ubiquitin chains containing all possible isopeptide linkages. J Biol Chem 282: 17375-17386.
51. Kirkin V, McEwan DG, Novak I, Dikic I. 2009b. A role for ubiquitin in selective autophagy. Mol Cell 34: 259-269.
52. Kisselev AF, Akopian TN, Castillo V, Goldberg AL. 1999. Proteasome active sites allosterically regulate each other, suggesting a cyclical bite-chew mechanism for protein breakdown. Mol Cell 4: 395-402.
53. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N. 1998. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608.
54. Klionsky DJ. 2005. Autophagy. Curr Biol 15: R282-R283.
55. Klionsky DJ. 2007. Autophagy: From phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8: 931-937.
56. Ko HS, Kim SW, Sriram SR, Dawson VL, Dawson TM. 2006. Identification of far upstream element-binding protein-1 as an authentic Parkin substrate. J Biol Chem 281: 16193-16196.
57. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, MizushimaN, Ohsumi Y, Uchiyama Y, et al. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169: 425-434.
58. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, et al. 2006. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441: 880-884.
59. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, Mizushima N, Iwata J, Ezaki J, Murata S, et al. 2007. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131: 1149-1163.
60. Kopito RR. 2000. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10: 524-530.
61. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, EpplenJT, Schols L, Riess O. 1998. Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease. Nat Genet 18: 106-108.
62. Larsen KE, Fon EA, Hastings TG, Edwards RH, Sulzer D. 2002. Methamphetamine-induced degeneration of dopaminergic neurons involves autophagy and upregulation of dopamine synthesis. J Neurosci 22: 8951-8960.
63. Lee HJ, Shin SY, Choi C, Lee YH, Lee SJ. 2002. Formation and removal of α-synuclein aggregates in cells exposed to mitochondrial inhibitors. J Biol Chem 277: 5411-5417.
64. Lee HJ, Khoshaghideh F, Patel S, Lee SJ. 2004. Clearance of α-synuclein oligomeric intermediates via the lysosomal degradation pathway. J Neurosci 24: 1888-1896.
65. Lennox G, Lowe J, Morrell K, Landon M, Mayer RJ. 1989. Anti-ubiquitin immunocytochemistry is more sensitive than conventional techniques in the detection of diffuse Lewy body disease. J Neurol Neurosurg Psychiatry 52: 67-71.
66. Levine B, Klionsky DJ. 2004. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev Cell 6: 463-477.
67. Liu CW, Corboy MJ, DeMartino GN, Thomas PJ. 2003. Endoproteolytic activity of the proteasome. Science 299: 408-411.
68. Lowe J, McDermott H, Landon M, Mayer RJ, Wilkinson KD. 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.
69. Machiya Y, Hara S, Arawaka S, Fukushima S, Sato H, Sakamoto M, Koyama S, Kato T. 2010. Phosphorylated α-synuclein at Ser-129 is targeted to the proteasome pathway in a ubiquitin-independent manner. J Biol Chem 285: 40732-40744.
70. Manning-Bog AB, McCormack AL, Li J, Uversky VN, Fink AL, Di Monte DA. 2002. The herbicide paraquat causes up-regulation and aggregation of α-synuclein in mice: Paraquat and α-synuclein. J Biol Chem 277: 1641-1644.
71. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, MosharovEV, Hodara R, Fredenburg R, Wu DC, Follenzi A, et al. 2008. Dopamine-modified α-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118: 777-788.
72. Masliah E, Rockenstein E, Adame A, Alford M, Crews L, Hashimoto M, SeubertP, Lee M, Goldstein J, Chilcote T, et al. 2005. Effects of α-synuclein immunization in a mouse model of Parkinson's disease. Neuron 46: 857-868.
73. Massey A, Kiffin R, Cuervo AM. 2004. Pathophysiology of chaperone-mediated autophagy. Int J Biochem Cell Biol 36: 2420-2434.
74. Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. 2006. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci 103: 5805-5810.
75. McNaught KS, Belizaire R, Jenner P, Olanow CW, Isacson O. 2002. Selective loss of 20S proteasome α-subunits in the substantia nigra pars compacta in Parkinson's disease. Neurosci Lett 326: 155-158.
76. Mizuno Y, Hattori N, Mori H, Suzuki T, Tanaka K. 2001. Parkin and Parkinson's disease. Curr Opin Neurol 14: 477-482.
77. Mizushima N. 2005. The pleiotropic role of autophagy: From protein metabolism to bactericide. Cell Death Differ 12 (Suppl 2): 1535-1541.
78. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. 2004. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15: 1101-1111.
79. Mortimore GE, Lardeux BR, Adams CE. 1988. Regulation of microautophagy and basal protein turnover in rat liver. Effects of short-term starvation. J Biol Chem 263: 2506-2512.
80. Muchowski PJ. 2002. Protein misfolding, amyloid formation, and neurodegeneration: A critical role for molecular chaperones? Neuron 35: 9-12.
81. Navon A, Goldberg AL. 2001. Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol Cell 8: 1339-1349.
82. Nixon RA. 2006. Autophagy in neurodegenerative disease: Friend, foe or turncoat? Trends Neurosci 29: 528-535.
83. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM. 2005. Extensive involvement of autophagy in Alzheimer disease: An immuno-electron microscopy study. J Neuropathol Exp Neurol 64: 113-122.
84. Okada K, Wangpoengtrakul C, Osawa T, Toyokuni S, Tanaka K, Uchida K. 1999. 4-Hydroxy-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. Identification of proteasomes as target molecules. J Biol Chem 274: 23787-23793.
85. Olzmann JA, Chin LS. 2008. Parkin-mediated K63-linked polyubiquitination: A signal for targeting misfolded proteins to the aggresome-autophagy pathway. Autophagy 4: 85-87.
86. Paisan-Ruiz C, Jain S, Evans EW, Gilks WP, Simon J, van der Brug M, Lopez de Munain A, Aparicio S, Gil AM, Khan N, et al. 2004. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44: 595-600.
87. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939.
88. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D, Gygi SP. 2003. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21: 921-926.
89. Petrucelli L, O'Farrell C, Lockhart PJ, Baptista M, Kehoe K, Vink L, Choi P, Wolozin B, Farrer M, Hardy J, et al. 2002. Parkin protects against the toxicity associated with mutant α-synuclein: Proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36: 1007-1019.
90. Pickart CM. 2001. Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533.
91. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, et al. 2008. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid β accumulation in mice. J Clin Invest 118: 2190-2199.
92. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, et al. 1997. Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047.
93. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE. 2009. Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 78: 959-991.
94. Ramirez A, Heimbach A, Grundemann J, Stiller B, Hampshire D, Cid LP, GoebelI, Mubaidin AF, Wriekat AL, Roeper 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.
95. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, EastonDF, Duden R, O'Kane CJ, et al. 2004. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36: 585-595.
96. Rideout HJ, Larsen KE, Sulzer D, Stefanis L. 2001. Proteasomal inhibition leads to formation of ubiquitin/α-synuclein-immunoreactive inclusions in PC12 cells. J Neurochem 78: 899-908.
97. Riley BE, Kaiser SE, Shaler TA, Ng AC, Hara T, Hipp MS, Lage K, Xavier RJ, RyuKY, Taguchi K, et al. 2010. Ubiquitin accumulation in autophagy-deficient mice is dependent on the Nrf2-mediated stress response pathway: A potential role for protein aggregation in autophagic substrate selection. J Cell Biol 191: 537-552.
98. Ross CA, Poirier MA. 2004. Protein aggregation and neurodegenerative disease. Nat Med 10 (Suppl): S10-S17.
99. Saito Y, Suzuki K, Hulette CM, Murayama S. 2004. Aberrant phosphorylation of α-synuclein in human Niemann-Pick type C1 disease. J Neuropathol Exp Neurol 63: 323-328.
100. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, GuimaraesA, DeTure M, Ramsden M, McGowan E, et al. 2005. Tau suppression in a neurodegenerative mouse model improves memory function. Science 309: 476-481.
101. Sarkar S, Perlstein EO, Imarisio S, Pineau S, Cordenier A, Maglathlin RL, Webster JA, Lewis TA, O'Kane CJ, Schreiber SL, et al. 2007. Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat Chem Biol 3: 331-338.
102. Schlossmacher MG, Frosch MP, Gai WP, Medina M, Sharma N, Forno L, OchiishiT, Shimura H, Sharon R, Hattori N, et al. 2002. Parkin localizes to the Lewy bodies of Parkinson disease and dementia with Lewy bodies. Am J Pathol 160: 1655-1667.
103. Schwartz AL, Ciechanover A. 1999. The ubiquitin-proteasome pathway and pathogenesis of human diseases. Annu Rev Med 50: 57-74.
104. Seibenhener ML, Geetha T, Wooten MW. 2007. Sequestosome 1/p62-more than just a scaffold. FEBS Lett 581: 175-179.
105. Shamoto-Nagai M, Maruyama W, Kato Y, Isobe K, Tanaka M, Naoi M, Osawa T. 2003. An inhibitor of mitochondrial complex I, rotenone, inactivates proteasome by oxidative modification and induces aggregation of oxidized proteins in SH-SY5Y cells. J Neurosci Res 74: 589-597.
106. Shimura H, Hattori N, Kubo S, Mizuno Y, Asakawa S, Minoshima S, Shimizu N, Iwai K, Chiba T, Tanaka K, et al. 2000. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 25: 302-305.
107. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, HulihanM, Peuralinna T, Dutra A, Nussbaum R, et al. 2003. α-Synuclein locus triplication causes Parkinson's disease. Science 302: 841.
108. Sitte N, Huber M, Grune T, Ladhoff A, Doecke WD, Von Zglinicki T, Davies KJ. 2000a. Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J 14: 1490-1498.
109. Sitte N, Merker K, Von Zglinicki T, Grune T, Davies KJ. 2000b. Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: Part I-effects of proliferative senescence. FASEB J 14: 2495-2502.
110. Snyder H, Mensah K, Theisler C, Lee J, Matouschek A, Wolozin B. 2003. Aggregated and monomeric α-synuclein bind to the S6′ proteasomal protein and inhibit proteasomal function. J Biol Chem 278: 11753-11759.
111. Spencer B, Potkar R, Trejo M, Rockenstein E, Patrick C, Gindi R, Adame A, Wyss-Coray T, Masliah E. 2009. Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in α-synuclein models of Parkinson's and Lewy body diseases. J Neurosci 29: 13578-13588.
112. Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA. 2001. Expression of A53T mutant but not wild-type α-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.
113. Tan JM, Wong ES, Kirkpatrick DS, Pletnikova O, Ko HS, Tay SP, Ho MW, Troncoso J, Gygi SP, Lee MK, et al. 2008. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet 17: 431-439.
114. Tayebi N, Callahan M, Madike V, Stubblefield BK, Orvisky E, Krasnewich D, Fillano JJ, Sidransky E. 2001. Gaucher disease and parkinsonism: A phenotypic and genotypic characterization. Mol Genet Metab 73: 313-321.
115. Terman A, Brunk UT. 2004. Lipofuscin. Int J Biochem Cell Biol 36: 1400-1404.
116. Tessari I, Bisaglia M, Valle F, Samori B, Bergantino E, Mammi S, Bubacco L. 2008. The reaction of α-synuclein with tyrosinase: Possible implications for Parkinson disease. J Biol Chem 283: 16808-16817.
117. Tofaris GK, Layfield R, Spillantini MG. 2001. α-Synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett 509: 22-26.
118. Ullrich O, Reinheckel T, Sitte N, Grune T. 1999. Degradation of hypochlorite-damaged glucose-6-phosphate dehydrogenase by the 20S proteasome. Free Radic Biol Med 27: 487-492.
119. Uversky VN, Li J, Fink AL. 2001. Pesticides directly accelerate the rate of α-synuclein fibril formation: A possible factor in Parkinson's disease. FEBS Lett 500: 105-108.
120. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, et al. 2004. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304: 1158-1160.
121. Varkonyi J, Rosenbaum H, Baumann N, MacKenzie JJ, Simon Z, Aharon-Peretz J, Walker JM, Tayebi N, Sidransky E. 2003. Gaucher disease associated with parkinsonism: Four further case reports. Am J Med Genet A 116A: 348-351.
122. Voges D, Zwickl P, Baumeister W. 1999. The 26S proteasome: A molecular machine designed for controlled proteolysis. Annu Rev Biochem 68: 1015-1068.
123. Wang XF, Li S, Chou AP, Bronstein JM. 2006. Inhibitory effects of pesticides on proteasome activity: Implication in Parkinson's disease. Neurobiol Dis 23: 198-205.
124. Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM. 1999. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 23: 425-428.
125. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC. 2003. α-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 278: 25009-25013.
126. Williams DR, Hadeed A, al-Din AS, Wreikat AL, Lees AJ. 2005. Kufor Rakeb disease: Autosomal recessive, levodopa-responsive parkinsonism with pyramidal degeneration, supranuclear gaze palsy, and dementia. Mov Disord 20: 1264-1271.
127. Williams A, Jahreiss L, Sarkar S, Saiki S, Menzies FM, Ravikumar B, RubinszteinDC. 2006. Aggregate-prone proteins are cleared from the cytosol by autophagy: Therapeutic implications. Curr Top Dev Biol 76: 89-101.
128. Xilouri M, Vogiatzi T, Vekrellis K, Park D, Stefanis L. 2009. Abberant α-synuclein confers toxicity to neurons in part through inhibition of chaperone-mediated autophagy. PLoS One 4: e5515.
129. Yamamoto A, Lucas JJ, Hen R. 2000. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 101: 57-66.
130. Yang Q, She H, Gearing M, Colla E, Lee M, Shacka JJ, Mao Z. 2009. Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Science 323: 124-127.
131. Yorimitsu T, Klionsky DJ. 2005. Autophagy: Molecular machinery for self-eating. Cell Death Differ 12 (Suppl 2): 1542-1552.
132. Yu WH, Dorado B, Figueroa HY, Wang L, Planel E, Cookson MR, Clark LN, DuffKE. 2009. Metabolic activity determines efficacy of macroautophagic clearance of pathological oligomeric α-synuclein. Am J Pathol 175: 736-747.
133. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, Hoenicka J, Rodriguez O, Atares B, et al. 2004. The new mutation, E46K, of α-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55: 164-173.
134. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, Dawson TM. 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 97: 13354-13359.
135. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, Kachergus J, Hulihan M, Uitti RJ, Calne DB, et al. 2004. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44: 601-607.
136. Zu T, Duvick LA, Kaytor MD, Berlinger MS, Zoghbi HY, Clark HB, Orr HT. 2004. Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. J Neurosci 24: 8853-8861.