Pale Body-Like Inclusion Formation and Neurodegeneration following Depletion of 26S Proteasomes in Mouse Brain Neurones are Independent of α-Synuclein

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Paine, Simon M L ^a,b,d   Anderson, Glenn ^b   Bedford, Karen ^c   Lawler, Karen ^d   Mayer, R John ^d   Lowe, James ^d   Bedford, Lynn ^d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c HULL ROYAL INFIRMARY   (United Kingdom)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; PROTEASOME;

ANIMAL CELL; ARTICLE; AUTOLYSOSOME; BIOGENESIS; BRAIN NERVE CELL; CELL INCLUSION; CONTROLLED STUDY; DEPLETION; DOPAMINERGIC NERVE CELL; HOMEOSTASIS; LEWY BODY; MALE; MITOCHONDRION; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PARKINSON DISEASE;

ALPHA-SYNUCLEIN; ANIMALS; AUTOPHAGY; BRAIN; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; INCLUSION BODIES; LEWY BODIES; LYSOSOMES; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; NEURONS; PARKINSON DISEASE; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

EID: 84873844495     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054711     Document Type: Article

References (76)

1. Douglas PM, Dillin A, (2010) Protein homeostasis and aging in neurodegeneration. J Cell Biol 190: 719-729.
2. Wakabayashi K, Tanji K, Odagiri S, Miki Y, Mori F, et al. (2012) The Lewy Body in Parkinson's Disease and Related Neurodegenerative Disorders. Mol Neurobiol DOI: 10.1007/s12035-012-8280-y.
3. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
4. Devine MJ, Gwinn K, Singleton A, Hardy J, (2011) Parkinson's disease and alpha-synuclein expression. Mov Disord 26: 2160-2168.
5. Martin I, Dawson VL, Dawson TM, (2011) Recent advances in the genetics of Parkinson's disease. Annu Rev Genomics Hum Genet 12: 301-325.
6. Beach TG, Adler CH, Lue L, Sue LI, Bachalakuri J, et al. (2009) Unified staging system for Lewy body disorders: correlation with nigrostriatal degeneration, cognitive impairment and motor dysfunction. Acta Neuropathol 117: 613-634.
7. Halliday GM, Holton JL, Revesz T, Dickson DW, (2011) Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathol 122: 187-204.
8. Duyckaerts C, Delatour B, Potier MC, (2009) Classification and basic pathology of Alzheimer disease. Acta Neuropathol 118: 5-36.
9. Schapira AH, Gegg M (2011) Mitochondrial contribution to Parkinson's disease pathogenesis. Parkinsons Dis DOI: 10.4061/2011/159160.
10. Keane PC, Kurzawa M, Blain PG, Morris CM (2011) Mitochondrial dysfunction in Parkinson's disease. Parkinsons Dis DOI: 10.4061/2011/716871.
11. Schapira AH, (2010) Complex I: inhibitors, inhibition and neurodegeneration. Exp Neurol 224: 331-335.
12. Dale GE, Probst A, Luthert P, Martin J, Anderton BH, et al. (1992) Relationships between Lewy bodies and pale bodies in Parkinson's disease. Acta Neuropathol 83: 525-529.
13. Bedford L, Hay D, Devoy A, Paine S, Powe DG, et al. (2008) Depletion of 26S proteasomes in mouse brain neurons causes neurodegeneration and Lewy-like inclusions resembling human pale bodies. J Neurosci 28: 8189-8198.
14. Clague MJ, Urbe S, (2010) Ubiquitin: same molecule, different degradation pathways. Cell 143: 682-685.
15. Lowe J, Blanchard A, Morrell K, Lennox G, Reynolds L, et al. (1988) Ubiquitin is a common factor in intermediate filament inclusion bodies of diverse type in man, including those of Parkinson's disease, Pick's disease, and Alzheimer's disease, as well as Rosenthal fibres in cerebellar astrocytomas, cytoplasmic bodies in muscle, and mallory bodies in alcoholic liver disease. J Pathol 155: 9-15.
16. Cook C, Petrucelli L, (2009) A critical evaluation of the ubiquitin-proteasome system in Parkinson's disease. Biochim Biophys Acta 1792: 664-675.
17. Wong E, Cuervo AM, (2010) Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 13: 805-811.
18. Ebrahimi-Fakhari D, Cantuti-Castelvetri I, Fan Z, Rockenstein E, Masliah E, et al. (2011) Distinct roles in vivo for the ubiquitin-proteasome system and the autophagy-lysosomal pathway in the degradation of alpha-synuclein. J Neurosci 31: 14508-14520.
19. Johnston JA, Ward CL, Kopito RR, (1998) Aggresomes: a cellular response to misfolded proteins. J Cell Biol 143: 1883-1898.
20. Olanow CW, Perl DP, DeMartino GN, McNaught KS, (2004) Lewy-body formation is an aggresome-related process: a hypothesis. Lancet Neurol 3: 496-503.
21. Karbowski M, Neutzner A, (2012) Neurodegeneration as a consequence of failed mitochondrial maintenance. Acta Neuropathol 123: 157-171.
22. Karbowski M, Youle RJ, (2011) Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation. Curr Opin Cell Biol 23: 476-482.
23. Heo JM, Rutter J, (2011) Ubiquitin-dependent mitochondrial protein degradation. Int J Biochem Cell Biol 43: 1422-1426.
24. Narendra D, Tanaka A, Suen DF, Youle RJ, (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183: 795-803.
25. Chan NC, Chan DC, (2011) Parkin uses the UPS to ship off dysfunctional mitochondria. Autophagy 7: 771-772.
26. Devi L, Raghavendran V, Prabhu BM, Avadhani NG, Anandatheerthavarada HK, (2008) Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J Biol Chem 283: 9089-9100.
27. Nakamura K, Nemani VM, Azarbal F, Skibinski G, Levy JM, et al. (2011) Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein. J Biol Chem 286: 20710-20726.
28. Sai Y, Zou Z, Peng K, Dong Z, (2012) The Parkinson's disease-related genes act in mitochondrial homeostasis. Neurosci Biobehav Rev 36: 2034-2043.
29. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, et al. (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25: 239-252.
30. Bayer SA, Wills KV, Triarhou LC, Ghetti B, (1995) Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp Brain Res 105: 191-199.
31. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, et al. (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science 274: 1678-1683.
32. Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, et al. (1996) Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87: 1317-1326.
33. Baquet ZC, Williams D, Brody J, Smeyne RJ, (2009) A comparison of model-based (2D) and design-based (3D) stereological methods for estimating cell number in the substantia nigra pars compacta (SNpc) of the C57BL/6J mouse. Neuroscience 161: 1082-1090.
34. Rideout HJ, Lang-Rollin I, Stefanis L, (2004) Involvement of macroautophagy in the dissolution of neuronal inclusions. Int J Biochem Cell Biol 36: 2551-2562.
35. Iwata A, Riley BE, Johnston JA, Kopito RR, (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280: 40282-40292.
36. Mizushima N, (2004) Methods for monitoring autophagy. Int J Biochem Cell Biol 36: 2491-2502.
37. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175.
38. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, et al. (2011) Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 20: 1726-37.
39. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, et al. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131: 1149-1163.
40. Moscat J, Diaz-Meco MT (2009) To aggregate or not to aggregate? A new role for p62. EMBO Rep DOI: 10.1038/embor.2009.172.
41. Narendra D, Kane LA, Hauser DN, Fearnley IM, Youle RJ, (2010) p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 6: 1090-1106.
42. Dawson TM, Ko HS, Dawson VL, (2010) Genetic animal models of Parkinson's disease. Neuron 66: 646-661.
43. Chesselet MF, (2008) In vivo alpha-synuclein overexpression in rodents: a useful model of Parkinson's disease? Exp Neurol 209: 22-27.
44. Emmer KL, Waxman EA, Covy JP, Giasson BI, (2011) E46K human alpha-synuclein transgenic mice develop Lewy-like and tau pathology associated with age-dependent, detrimental motor impairment. J Biol Chem 286: 35104-35118.
45. McNaught KS, Perl DP, Brownell AL, Olanow CW, (2004) Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's disease. Ann Neurol 56: 149-162.
46. Bove J, Zhou C, Jackson-Lewis V, Taylor J, Chu Y, et al. (2006) Proteasome inhibition and Parkinson's disease modeling. Ann Neurol 60: 260-264.
47. Kordower JH, Kanaan NM, Chu Y, Suresh Babu R, Stansell J, 3rd, et al (2006) Failure of proteasome inhibitor administration to provide a model of Parkinson's disease in rats and monkeys. Ann Neurol 60: 264-268.
48. Schapira AH, Cleeter MW, Muddle JR, Workman JM, Cooper JM, et al. (2006) Proteasomal inhibition causes loss of nigral tyrosine hydroxylase neurons. Ann Neurol 60: 253-255.
49. Zeng BY, Bukhatwa S, Hikama A, Rose S, Jenner P, (2006) Reproducible nigral loss after systemic proteasomal inhibitor administration to rats. Annals of Neurology 60: 248-252.
50. Hawlitschka A, Haas SJ, Schmitt O, Weiss DG, Wree A, (2007) Effects of systemic PSI administration on catecholaminergic cells in the brain, adrenal medulla and carotid body in Wistar rats. Brain Res 1173: 137-144.
51. Jantas D, Lorenc-Koci E, Kubera M, Lason W, (2011) Neuroprotective effects of MAPK/ERK1/2 and calpain inhibitors on lactacystin-induced cell damage in primary cortical neurons. Neurotoxicology 32: 845-856.
52. Bennett MC, Bishop JF, Leng Y, Chock PB, Chase TN, et al. (1999) Degradation of alpha-synuclein by proteasome. J Biol Chem 274: 33855-33858.
53. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC, (2003) Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 278: 25009-25013.
54. Shin Y, Klucken J, Patterson C, Hyman BT, McLean PJ, (2005) The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J Biol Chem 280: 23727-23734.
55. Voges D, Zwickl P, Baumeister W, (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68: 1015-1068.
56. Pickart CM, Cohen RE, (2004) Proteasomes and their kin: proteases in the machine age. Nat Rev Mol Cell Biol 5: 177-187.
57. Schmidt M, Hanna J, Elsasser S, Finley D, (2005) Proteasome-associated proteins: regulation of a proteolytic machine. Biol Chem 386: 725-737.
58. Demartino GN, Gillette TG, (2007) Proteasomes: machines for all reasons. Cell 129: 659-62.
59. Tofaris GK, Layfield R, Spillantini MG, (2001) alpha-Synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett 509: 22-26.
60. Fornai F, Schluter OM, Lenzi P, Gesi M, Ruffoli R, et al. (2005) Parkinson-like syndrome induced by continuous MPTP infusion: convergent roles of the ubiquitin-proteasome system and alpha-synuclein. Proc Natl Acad Sci U S A 102: 3413-3418.
61. Liu W, Vives-Bauza C, Acin-Perez R, Yamamoto A, Tan Y, et al. (2009) PINK1 defect causes mitochondrial dysfunction, proteasomal deficit and alpha-synuclein aggregation in cell culture models of Parkinson's disease. PLoS One 4: e4597.
62. Wills J, Credle J, Oaks AW, Duka V, Lee JH, et al. (2012) Paraquat, but Not Maneb, Induces Synucleinopathy and Tauopathy in Striata of Mice through Inhibition of Proteasomal and Autophagic Pathways. PLoS One 7: e30745.
63. Lindersson E, Beedholm R, Hojrup P, Moos T, Gai W, et al. (2004) Proteasomal inhibition by alpha-synuclein filaments and oligomers. J Biol Chem 279: 12924-12934.
64. Zhang NY, Tang Z, Liu CW, (2008) alpha-Synuclein protofibrils inhibit 26 S proteasome-mediated protein degradation: understanding the cytotoxicity of protein protofibrils in neurodegenerative disease pathogenesis. J Biol Chem 283: 20288-20298.
65. Chen L, Thiruchelvam MJ, Madura K, Richfield EK, (2006) Proteasome dysfunction in aged human alpha-synuclein transgenic mice. Neurobiol Dis 23: 120-126.
66. Emmanouilidou E, Stefanis L, Vekrellis K, (2010) Cell-produced alpha-synuclein oligomers are targeted to, and impair, the 26S proteasome. Neurobiol Aging 31: 953-968.
67. Hardy J, (2010) Genetic analysis of pathways to Parkinson disease. Neuron 68: 201-206.
68. Gibb WR, Lees AJ, (1989) Prevalence of Lewy bodies in Alzheimer's disease. Ann Neurol 26: 691-693.
69. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, et al. (2004) The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55: 164-173.
70. Dickson DW, Fujishiro H, DelleDonne A, Menke J, Ahmed Z, et al. (2008) Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease. Acta Neuropathol 115: 437-444.
71. Leverenz JB, Umar I, Wang Q, Montine TJ, McMillan PJ, et al. (2007) Proteomic identification of novel proteins in cortical lewy bodies. Brain Pathol 17: 139-145.
72. Yoshii SR, Kishi C, Ishihara N, Mizushima N, (2011) Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J Biol Chem 286: 19630-19640.
73. Nakamura K, Nemani VM, Wallender EK, Kaehlcke K, Ott M, et al. (2008) Optical reporters for the conformation of alpha-synuclein reveal a specific interaction with mitochondria. J Neurosci 28: 12305-12317.
74. Kamp F, Exner N, Lutz AK, Wender N, Hegermann J, et al. (2010) Inhibition of mitochondrial fusion by alpha-synuclein is rescued by PINK1, Parkin and DJ-1. Embo J 29: 3571-3589.
75. Zigoneanu IG, Yang YJ, Krois AS, Haque ME, Pielak GJ, (2011) Interaction of alpha-synuclein with vesicles that mimic mitochondrial membranes. Biochim Biophys Acta 1818: 512-519.
76. Martin LJ, Pan Y, Price AC, Sterling W, Copeland NG, et al. (2006) Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. J Neurosci 26: 41-50.