Induction of de novo a-synuclein fibrillization in a neuronal model for Parkinson's disease

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 7, 2016, Pages E912-E921

  Fares, Mohamed Bilal ^a   Maco, Bohumil ^a   Oueslati, Abid ^a   Rockenstein, Edward ^b   Ninkina, Natalia ^c   Buchman, Vladimir L ^c   Masliah, Eliezer ^b   Lashuel, Hilal A ^a,d  

^a EPFL   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d HAMAD BIN KHALIFA UNIVERSITY   (Qatar)

Author keywords

Aggregation; Alpha synuclein; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; UBIQUITIN;

ANIMAL CELL; ARTICLE; BRAIN HOMOGENATE; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOSOME; FIBER; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOGOLD LABELING; IMMUNOREACTIVITY; IN VIVO STUDY; LYSOSOME; MOUSE; NERVE CELL; NERVE ENDING; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; ULTRASTRUCTURE; ANIMAL; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM;

ALPHA-SYNUCLEIN; ANIMALS; DISEASE MODELS, ANIMAL; MICE; MICE, KNOCKOUT; NEURONS; PARKINSON DISEASE;

EID: 84959020553     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1512876113     Document Type: Article

References (63)

1. Spillantini MG, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388(6645): 839-840.
2. Lashuel HA, Overk CR, Oueslati A, Masliah E (2013) The many faces of a-synuclein: From structure and toxicity to therapeutic target. Nat Rev Neurosci 14(1): 38-48.
3. Dawson TM, Ko HS, Dawson VL (2010) Genetic animal models of Parkinson's disease. Neuron 66(5): 646-661.
4. Feany MB, Bender WW (2000) A Drosophila model of Parkinson's disease. Nature 404(6776): 394-398.
5. Cabin DE, et al. (2005) Exacerbated synucleinopathy in mice expressing A53T SNCA on a Snca null background. Neurobiol Aging 26(1): 25-35.
6. Tofaris GK, et al. (2006) Pathological changes in dopaminergic nerve cells of the substantia nigra and olfactory bulb in mice transgenic for truncated human alphasynuclein( 1-120): Implications for Lewy body disorders. J Neurosci 26(15): 3942-3950.
7. Rochet JC, Conway KA, Lansbury PT, Jr (2000) Inhibition of fibrillization and accumulation of prefibrillar oligomers in mixtures of human and mouse alpha-synuclein. Biochemistry 39(35): 10619-10626.
8. Petrucelli L, et al. (2002) Parkin protects against the toxicity associated with mutant alpha-synuclein: Proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36(6): 1007-1019.
9. McLean PJ, Kawamata H, Hyman BT (2001) Alpha-synuclein-enhanced green fluorescent protein fusion proteins form proteasome sensitive inclusions in primary neurons. Neuroscience 104(3): 901-912.
10. Fares MB, et al. (2014) The novel Parkinson's disease linked mutation G51D attenuates in vitro aggregation and membrane binding of a-synuclein, and enhances its secretion and nuclear localization in cells. Hum Mol Genet 23(17): 4491-4509.
11. Khalaf O, et al. (2014) The H50Q mutation enhances a-synuclein aggregation, secretion, and toxicity. J Biol Chem 289(32): 21856-21876.
12. Specht CG, Schoepfer R (2001) Deletion of the alpha-synuclein locus in a subpopulation of C57BL/6J inbred mice. BMC Neurosci 2: 11-19.
13. Abeliovich A, et al. (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25(1): 239-252.
14. Tabrizi SJ, et al. (2000) Expression of mutant alpha-synuclein causes increased susceptibility to dopamine toxicity. Hum Mol Genet 9(18): 2683-2689.
15. Opazo F, Krenz A, Heermann S, Schulz JB, Falkenburger BH (2008) Accumulation and clearance of alpha-synuclein aggregates demonstrated by time-lapse imaging. J Neurochem 106(2): 529-540.
16. Tofaris GK, Layfield R, SpillantiniMG (2001) alpha-synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett 509(1): 22-26.
17. Engelender S, et al. (1999) Synphilin-1 associates with alpha-synuclein and promotes the formation of cytosolic inclusions. Nat Genet 22(1): 110-114.
18. Lee HJ, Shin SY, Choi C, Lee YH, Lee SJ (2002) Formation and removal of alpha-synuclein aggregates in cells exposed to mitochondrial inhibitors. J Biol Chem 277(7): 5411-5417.
19. Paxinou E, et al. (2001) Induction of alpha-synuclein aggregation by intracellular nitrative insult. J Neurosci 21(20): 8053-8061.
20. Fujiwara H, et al. (2002) alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4(2): 160-164.
21. Hasegawa M, et al. (2002) Phosphorylated alpha-synuclein is ubiquitinated in alphasynucleinopathy lesions. J Biol Chem 277(50): 49071-49076.
22. Volpicelli-Daley LA, et al. (2011) Exogenous a-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 72(1): 57-71.
23. Irwin DJ, Lee VM, Trojanowski JQ (2013) Parkinson's disease dementia: Convergence of a-synuclein, tau and amyloid-ß pathologies. Nat Rev Neurosci 14(9): 626-636.
24. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, GoedertM (1998) alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc Natl Acad Sci USA 95(11): 6469-6473.
25. McKinney SA, Murphy CS, Hazelwood KL, Davidson MW, Looger LL (2009) A bright and photostable photoconvertible fluorescent protein. Nat Methods 6(2): 131-133.
26. Roberti MJ, Jovin TM, Jares-Erijman E (2011) Confocal fluorescence anisotropy and FRAP imaging of a-synuclein amyloid aggregates in living cells. PLoS One 6(8): E23338.
27. Oueslati A, Fournier M, Lashuel HA (2010) Role of post-translational modifications in modulating the structure, function and toxicity of alpha-synuclein: Implications for Parkinson's disease pathogenesis and therapies. Prog Brain Res 183: 115-145.
28. Paleologou KE, et al. (2010) Phosphorylation at S87 is enhanced in synucleinopathies, inhibits alpha-synuclein oligomerization, and influences synuclein-membrane interactions. J Neurosci 30(9): 3184-3198.
29. Oueslati A, Paleologou KE, Schneider BL, Aebischer P, Lashuel HA (2012) Mimicking phosphorylation at serine 87 inhibits the aggregation of human a-synuclein and protects against its toxicity in a rat model of Parkinson's disease. J Neurosci 32(5): 1536-1544.
30. Di Giovanni S, et al. (2010) Entacapone and tolcapone, two catechol O-methyltransferase inhibitors, block fibril formation of alpha-synuclein and beta-amyloid and protect against amyloid-induced toxicity. J Biol Chem 285(20): 14941-14954.
31. Chandra S, et al. (2004) Double-knockout mice for alpha- and beta-synucleins: Effect on synaptic functions. Proc Natl Acad Sci USA 101(41): 14966-14971.
32. Buchman VL, et al. (1998) Persyn, a member of the synuclein family, has a distinct pattern of expression in the developing nervous system. J Neurosci 18(22): 9335-9341.
33. Anwar S, et al. (2011) Functional alterations to the nigrostriatal system in mice lacking all three members of the synuclein family. J Neurosci 31(20): 7264-7274.
34. Li J, Henning Jensen P, Dahlström A (2002) Differential localization of alpha-, betaand gamma-synucleins in the rat CNS. Neuroscience 113(2): 463-478.
35. Masliah E, et al. (2000) Dopaminergic loss and inclusion body formation in alphasynuclein mice: Implications for neurodegenerative disorders. Science 287(5456): 1265-1269.
36. Nishimura M, et al. (1994) Synaptophysin and chromogranin A immunoreactivities of Lewy bodies in Parkinson's disease brains. Brain Res 634(2): 339-344.
37. Hashimoto M, Rockenstein E, Mante M, Mallory M, Masliah E (2001) beta-Synuclein inhibits alpha-synuclein aggregation: A possible role as an anti-Parkinsonian factor. Neuron 32(2): 213-223.
38. Ko LW, Ko HH, Lin WL, Kulathingal JG, Yen SH (2008) Aggregates assembled from overexpression of wild-type alpha-synuclein are not toxic to human neuronal cells. J Neuropathol Exp Neurol 67(11): 1084-1096.
39. Tanaka M, et al. (2004) Aggresomes formed by alpha-synuclein and synphilin-1 are cytoprotective. J Biol Chem 279(6): 4625-4631.
40. Luk KC, et al. (2012) Pathological a-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338(6109): 949-953.
41. Masuda-Suzukake M, et al. (2014) Pathological alpha-synuclein propagates through neural networks. Acta Neuropathol Commun 2: 88-99.
42. Paumier KL, et al. (2015) Intrastriatal injection of pre-formed mouse a-synuclein fibrils into rats triggers a-synuclein pathology and bilateral nigrostriatal degeneration. Neurobiol Dis 82: 185-199.
43. B?temps D, et al. (2014) Alpha-synuclein spreading in M83 mice brain revealed by detection of pathological a-synuclein by enhanced ELISA. Acta Neuropathol Commun 2: 29-42.
44. Luk KC, et al. (2012) Intracerebral inoculation of pathological a-synuclein initiates a rapidly progressive neurodegenerative a-synucleinopathy in mice. J ExpMed 209(5): 975-986.
45. Sacino AN, et al. (2014) Brain injection of a-synuclein induces multiple proteinopathies, gliosis, and a neuronal injury marker. J Neurosci 34(37): 12368-12378.
46. Peelaerts W, et al. (2015) a-Synuclein strains cause distinct synucleinopathies after local and systemic administration. Nature 522(7556): 340-344.
47. Sacino AN, et al. (2014) Intramuscular injection of a-synuclein induces CNS a-synuclein pathology and a rapid-onset motor phenotype in transgenic mice. Proc Natl Acad Sci USA 111(29): 10732-10737.
48. Sacino AN, et al. (2013) Induction of CNS a-synuclein pathology by fibrillar and nonamyloidogenic recombinant a-synuclein. Acta Neuropathol Commun 1(1): 38-51.
49. Hasegawa K, Yamaguchi I, Omata S, Gejyo F, Naiki H (1999) Interaction between A beta(1-42) and A beta(1-40) in Alzheimer's beta-amyloid fibril formation in vitro. Biochemistry 38(47): 15514-15521.
50. Eaton WA, Hofrichter J (1995) The biophysics of sickle cell hydroxyurea therapy. Science 268(5214): 1142-1143.
51. Hammarström P, Schneider F, Kelly JW (2001) Trans-suppression of misfolding in an amyloid disease. Science 293(5539): 2459-2462.
52. Sousa MM, et al. (2002) Evidence for early cytotoxic aggregates in transgenic mice for human transthyretin Leu55Pro. Am J Pathol 161(5): 1935-1948.
53. Cao P, Meng F, Abedini A, Raleigh DP (2010) The ability of rodent islet amyloid polypeptide to inhibit amyloid formation by human islet amyloid polypeptide has important implications for the mechanism of amyloid formation and the design of inhibitors. Biochemistry 49(5): 872-881.
54. Sellin D, Yan LM, Kapurniotu A, Winter R (2010) Suppression of IAPP fibrillation at anionic lipid membranes via IAPP-derived amyloid inhibitors and insulin. Biophys Chem 150(1-3): 73-79.
55. Uversky VN, et al. (2002) Biophysical properties of the synucleins and their propensities to fibrillate: Inhibition of alpha-synuclein assembly by beta- and gammasynucleins. J Biol Chem 277(14): 11970-11978.
56. Park JY, Lansbury PT, Jr (2003) Beta-synuclein inhibits formation of alpha-synuclein protofibrils: A possible therapeutic strategy against Parkinson's disease. Biochemistry 42(13): 3696-3700.
57. Fan Y, et al. (2006) Beta-synuclein modulates alpha-synuclein neurotoxicity by reducing alpha-synuclein protein expression. Hum Mol Genet 15(20): 3002-3011.
58. Robertson DC, et al. (2004) Developmental loss and resistance to MPTP toxicity of dopaminergic neurones in substantia nigra pars compacta of gamma-synuclein, alpha- synuclein and double alpha/gamma-synuclein null mutant mice. J Neurochem 89(5): 1126-1136.
59. Cookson MR (2009) alpha-Synuclein and neuronal cell death. Mol Neurodegener 4: 9-22.
60. Fauvet B, et al. (2012) Characterization of semisynthetic and naturally Na-acetylated a-synuclein in vitro and in intact cells: Implications for aggregation and cellular properties of a-synuclein. J Biol Chem 287(34): 28243-28262.
61. Tenreiro S, et al. (2014) Phosphorylation modulates clearance of alpha-synuclein inclusions in a yeast model of Parkinson's disease. PLoS Genet 10(5): E1004302.
62. Hoi H, et al. (2010) A monomeric photoconvertible fluorescent protein for imaging of dynamic protein localization. J Mol Biol 401(5): 776-791.
63. Klivenyi P, et al. (2006) Mice lacking alpha-synuclein are resistant to mitochondrial toxins. Neurobiol Dis 21(3): 541-548.