Role of post-translational modifications on the alpha-synuclein aggregation-related pathogenesis of Parkinson's disease |
Yoo, Hajung
(Department of Biomedical Science, Graduate School of Biomedical Science and Engineering, Hanyang University)
Lee, Jeongmin (Department of Biomedical Science, Graduate School of Biomedical Science and Engineering, Hanyang University) Kim, Bokwang (Department of Biomedical Science, Graduate School of Biomedical Science and Engineering, Hanyang University) Moon, Heechang (Department of Biomedical Science, Graduate School of Biomedical Science and Engineering, Hanyang University) Jeong, Huisu (Department of Biomedical Science, Graduate School of Biomedical Science and Engineering, Hanyang University) Lee, Kyungmi (Department of Medicine, College of Medicine, Hanyang University) Song, Woo Jeung (Department of Medical Genetics, College of Medicine, Hanyang University) Hur, Junho K. (Department of Biomedical Science, Graduate School of Biomedical Science and Engineering, Hanyang University) Oh, Yohan (Department of Biomedical Science, Graduate School of Biomedical Science and Engineering, Hanyang University) |
1 | Bartels T, Kim NC, Luth ES and Selkoe DJ (2014) Nalpha-acetylation of alpha-synuclein increases its helical folding propensity, GM1 binding specificity and resistance to aggregation. PLoS One 9, e103727 DOI |
2 | Watson MD and Lee JC (2019) N-terminal acetylation affects alpha-synuclein fibril polymorphism. Biochemistry 58, 3630-3633 DOI |
3 | Dikiy I and Eliezer D (2014) N-terminal acetylation stabilizes N-terminal helicity in lipid- and micelle-bound alpha-synuclein and increases its affinity for physiological membranes. J Biol Chem 289, 3652-3665 DOI |
4 | Lorentzon E, Kumar R, Horvath I and Wittung-Stafshede P (2020) Differential effects of Cu(2+) and Fe(3+) ions on in vitro amyloid formation of biologically-relevant alpha-synuclein variants. Biometals 33, 97-106 DOI |
5 | Hejjaoui M, Haj-Yahya M, Kumar KS, Brik A and Lashuel HA (2011) Towards elucidation of the role of ubiquitination in the pathogenesis of Parkinson's disease with semisynthetic ubiquitinated alpha-synuclein. Angew Chem Int Ed Engl 50, 405-409 DOI |
6 | Gerez JA, Prymaczok NC, Rockenstein E et al (2019) A cullin-RING ubiquitin ligase targets exogenous alpha-synuclein and inhibits Lewy body-like pathology. Sci Transl Med 11, eaau6722 DOI |
7 | Ye Y, Klenerman D and Finley D (2020) N-terminal ubiquitination of amyloidogenic proteins triggers removal of their oligomers by the proteasome holoenzyme. J Mol Biol 432, 585-596 DOI |
8 | Moon SP, Balana AT, Galesic A, Rakshit A and Pratt MR (2020) Ubiquitination can change the structure of the alpha-synuclein amyloid fiber in a site selective fashion. J Org Chem 85, 1548-1555 DOI |
9 | Rott R, Szargel R, Shani V et al (2017) SUMOylation and ubiquitination reciprocally regulate alpha-synuclein degradation and pathological aggregation. Proc Natl Acad Sci U S A 114, 13176-13181 DOI |
10 | Wang S, Yang F, Petyuk VA et al (2017) Quantitative proteomics identifies altered O-GlcNAcylation of structural, synaptic and memory-associated proteins in Alzheimer's disease. J Pathol 243, 78-88 DOI |
11 | Luk KC, Song C, O'Brien P et al (2009) Exogenous alpha-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci U S A 106, 20051-20056 DOI |
12 | Pountney DL, Huang Y, Burns RJ et al (2003) SUMO-1 marks the nuclear inclusions in familial neuronal intra-nuclear inclusion disease. Exp Neurol 184, 436-446 DOI |
13 | Kim YM, Jang WH, Quezado MM et al (2011) Proteasome inhibition induces alpha-synuclein SUMOylation and aggregate formation. J Neurol Sci 307, 157-161 DOI |
14 | Abeywardana T and Pratt MR (2015) Extent of inhibition of alpha-synuclein aggregation in vitro by SUMOylation is conjugation site- and SUMO isoform-selective. Biochemistry 54, 959-961 DOI |
15 | Haj-Yahya M, Fauvet B, Herman-Bachinsky Y et al (2013) Synthetic polyubiquitinated alpha-Synuclein reveals important insights into the roles of the ubiquitin chain in regulating its pathophysiology. Proc Natl Acad Sci U S A 110, 17726-17731 DOI |
16 | Krumova P, Meulmeester E, Garrido M et al (2011) Sumoylation inhibits alpha-synuclein aggregation and toxicity. J Cell Biol 194, 49-60 DOI |
17 | Baba M, Nakajo S, Tu PH et al (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 152, 879-884 |
18 | Muntane G, Ferrer I and Martinez-Vicente M (2012) alpha-synuclein phosphorylation and truncation are normal events in the adult human brain. Neuroscience 200, 106-119 DOI |
19 | Iyer A, Roeters SJ, Kogan V, Woutersen S, Claessens M and Subramaniam V (2017) C-terminal truncated alpha-synuclein fibrils contain strongly twisted beta-sheets. J Am Chem Soc 139, 15392-15400 DOI |
20 | Hoyer W, Cherny D, Subramaniam V and Jovin TM (2004) Impact of the acidic C-terminal region comprising amino acids 109-140 on alpha-synuclein aggregation in vitro. Biochemistry 43, 16233-16242 DOI |
21 | Klein C and Westenberger A (2012) Genetics of Parkinson's disease. Cold Spring Harb Perspect Med 2, a008888 DOI |
22 | Giasson BI, Duda JE, Murray IV et al (2000) Oxidative damage linked to neurodegeneration by selective alphasynuclein nitration in synucleinopathy lesions. Science 290, 985-989 DOI |
23 | Waxman EA and Giasson BI (2008) Specificity and regulation of casein kinase-mediated phosphorylation of alpha-synuclein. J Neuropathol Exp Neurol 67, 402-416 DOI |
24 | Munch G, Luth HJ, Wong A et al (2000) Crosslinking of alpha-synuclein by advanced glycation endproducts--an early pathophysiological step in Lewy body formation? J Chem Neuroanat 20, 253-257 DOI |
25 | Li W, West N, Colla E et al (2005) Aggregation promoting C-terminal truncation of alpha-synuclein is a normal cellular process and is enhanced by the familial Parkinson's disease-linked mutations. Proc Natl Acad Sci U S A 102, 2162-2167 DOI |
26 | Maltsev AS, Ying J and Bax A (2012) Impact of N-terminal acetylation of alpha-synuclein on its random coil and lipid binding properties. Biochemistry 51, 5004-5013 DOI |
27 | Lima VA, do Nascimento LA, Eliezer D and Follmer C (2019) Role of Parkinson's disease-linked mutations and N-terminal acetylation on the oligomerization of alpha-synuclein Induced by 3,4-dihydroxyphenylacetaldehyde. ACS Chem Neurosci 10, 690-703 DOI |
28 | Mishizen-Eberz AJ, Norris EH, Giasson BI et al (2005) Cleavage of alpha-synuclein by calpain: potential role in degradation of fibrillized and nitrated species of alpha-synuclein. Biochemistry 44, 7818-7829 DOI |
29 | Mishizen-Eberz AJ, Guttmann RP, Giasson BI et al (2003) Distinct cleavage patterns of normal and pathologic forms of alpha-synuclein by calpain I in vitro. J Neurochem 86, 836-847 DOI |
30 | Kasai T, Tokuda T, Yamaguchi N et al (2008) Cleavage of normal and pathological forms of alpha-synuclein by neurosin in vitro. Neurosci Lett 436, 52-56 DOI |
31 | Polymeropoulos MH, Lavedan C, Leroy E et al (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047 DOI |
32 | Emamzadeh FN (2016) Alpha-synuclein structure, functions, and interactions. J Res Med Sci 21, 29 DOI |
33 | McCann H, Stevens CH, Cartwright H and Halliday GM (2014) alpha-Synucleinopathy phenotypes. Parkinsonism Relat Disord 20 Suppl 1, S62-S67 DOI |
34 | Li JY, Englund E, Holton JL et al (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14, 501-503 DOI |
35 | Terada M, Suzuki G, Nonaka T, Kametani F, Tamaoka A and Hasegawa M (2018) The effect of truncation on prion-like properties of alpha-synuclein. J Biol Chem 293, 13910-13920 DOI |
36 | Brahmachari S, Ge P, Lee SH et al (2016) Activation of tyrosine kinase c-Abl contributes to alpha-synuclein-induced neurodegeneration. J Clin Invest 126, 2970-2988 DOI |
37 | Dufty BM, Warner LR, Hou ST et al (2007) Calpain-cleavage of alpha-synuclein: connecting proteolytic processing to disease-linked aggregation. Am J Pathol 170, 1725-1738 DOI |
38 | Bartels T, Choi JG and Selkoe DJ (2011) alpha-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477, 107-110 DOI |
39 | Fusco G, Chen SW, Williamson PTF et al (2017) Structural basis of membrane disruption and cellular toxicity by alpha-synuclein oligomers. Science 358, 1440-1443 DOI |
40 | Yasuda T, Nakata Y and Mochizuki H (2013) alpha-Synuclein and neuronal cell death. Mol Neurobiol 47, 466-483 DOI |
41 | Benskey MJ, Perez RG and Manfredsson FP (2016) The contribution of alpha synuclein to neuronal survival and function - Implications for Parkinson's disease. J Neurochem 137, 331-359 DOI |
42 | Sherer TB, Betarbet R, Stout AK et al (2002) An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered alpha-synuclein metabolism and oxidative damage. J Neurosci 22, 7006-7015 DOI |
43 | Scudamore O and Ciossek T (2018) Increased oxidative stress exacerbates alpha-synuclein aggregation in vivo. J Neuropathol Exp Neurol 77, 443-453 DOI |
44 | Musgrove RE, Helwig M, Bae EJ et al (2019) Oxidative stress in vagal neurons promotes parkinsonian pathology and intercellular alpha-synuclein transfer. J Clin Invest 129, 3738-3753 DOI |
45 | Xilouri M, Brekk OR and Stefanis L (2013) alpha-Synuclein and protein degradation systems: a reciprocal relationship. Mol Neurobiol 47, 537-551 DOI |
46 | Tuttle MD, Comellas G, Nieuwkoop AJ et al (2016) Solid-state NMR structure of a pathogenic fibril of full-length human alpha-synuclein. Nat Struct Mol Biol 23, 409-415 DOI |
47 | Ni X, McGlinchey RP, Jiang J and Lee JC (2019) Structural insights into alpha-synuclein fibril polymorphism: Effects of Parkinson's disease-related C-terminal truncations. J Mol Biol 431, 3913-3919 DOI |
48 | Anderson JP, Walker DE, Goldstein JM et al (2006) Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease. J Biol Chem 281, 29739-29752 DOI |
49 | Machiya Y, Hara S, Arawaka S et al (2010) Phosphorylated alpha-synuclein at Ser-129 is targeted to the proteasome pathway in a ubiquitin-independent manner. J Biol Chem 285, 40732-40744 DOI |
50 | Alfaro JF, Gong CX, Monroe ME et al (2012) Tandem mass spectrometry identifies many mouse brain O-GlcNA-cylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc Natl Acad Sci U S A 109, 7280-7285 DOI |
51 | Yamin G, Uversky VN and Fink AL (2003) Nitration inhibits fibrillation of human alpha-synuclein in vitro by formation of soluble oligomers. FEBS Lett 542, 147-152 DOI |
52 | Seo J and Lee KJ (2004) Post-translational modifications and their biological functions: proteomic analysis and systematic approaches. J Biochem Mol Biol 37, 35-44 |
53 | Kang L, Moriarty GM, Woods LA, Ashcroft AE, Radford SE and Baum J (2012) N-terminal acetylation of alpha-synuclein induces increased transient helical propensity and decreased aggregation rates in the intrinsically disordered monomer. Protein Sci 21, 911-917 DOI |
54 | Sevcsik E, Trexler AJ, Dunn JM and Rhoades E (2011) Allostery in a disordered protein: oxidative modifications to alpha-synuclein act distally to regulate membrane binding. J Am Chem Soc 133, 7152-7158 DOI |
55 | Pronin AN, Morris AJ, Surguchov A and Benovic JL (2000) Synucleins are a novel class of substrates for G protein-coupled receptor kinases. J Biol Chem 275, 26515-26522 DOI |
56 | Mbefo MK, Paleologou KE, Boucharaba A et al (2010) Phosphorylation of synucleins by members of the Pololike kinase family. J Biol Chem 285, 2807-2822 DOI |
57 | Li Y, Zhao C, Luo F et al (2018) Amyloid fibril structure of alpha-synuclein determined by cryo-electron microscopy. Cell Res 28, 897-903 DOI |
58 | Morris M, Knudsen GM, Maeda S et al (2015) Tau posttranslational modifications in wild-type and human amyloid precursor protein transgenic mice. Nat Neurosci 18, 1183-1189 DOI |
59 | Marotta NP, Lin YH, Lewis YE et al (2015) O-GlcNAc modification blocks the aggregation and toxicity of the protein alpha-synuclein associated with Parkinson's disease. Nat Chem 7, 913-920 DOI |
60 | Sato H, Arawaka S, Hara S et al (2011) Authentically phosphorylated alpha-synuclein at Ser129 accelerates neurodegeneration in a rat model of familial Parkinson's disease. J Neurosci 31, 16884-16894 DOI |
61 | Burai R, Ait-Bouziad N, Chiki A and Lashuel HA (2015) Elucidating the role of site-specific nitration of alpha-synuclein in the pathogenesis of Parkinson's disease via protein semisynthesis and mutagenesis. J Am Chem Soc 137, 5041-5052 DOI |
62 | Lewis YE, Galesic A, Levine PM et al (2017) O-GlcNAcylation of alpha-synuclein at serine 87 reduces aggregation without affecting membrane binding. ACS Chem Biol 12, 1020-1027 DOI |
63 | Sharma N, Rao SP and Kalivendi SV (2019) The deglycase activity of DJ-1 mitigates alpha-synuclein glycation and aggregation in dopaminergic cells: Role of oxidative stress mediated downregulation of DJ-1 in Parkinson's disease. Free Radic Biol Med 135, 28-37 DOI |
64 | Hodara R, Norris EH, Giasson BI et al (2004) Functional consequences of alpha-synuclein tyrosine nitration: diminished binding to lipid vesicles and increased fibril formation. J Biol Chem 279, 47746-47753 DOI |
65 | Chen SW, Drakulic S, Deas E et al (2015) Structural characterization of toxic oligomers that are kinetically trapped during alpha-synuclein fibril formation. Proc Natl Acad Sci U S A 112, E1994-E2003 |
66 | Chen L, Wei Y, Wang X and He R (2010) Ribosylation rapidly induces alpha-synuclein to form highly cytotoxic molten globules of advanced glycation end products. PLoS One 5, e9052 DOI |
67 | Marino L, Ramis R, Casasnovas R et al (2020) Unravelling the effect of N(epsilon)-(carboxyethyl)lysine on the conformation, dynamics and aggregation propensity of alpha-synuclein. Chem Sci 11, 3332-3344 DOI |
68 | Lee D, Park CW, Paik SR and Choi KY (2009) The modification of alpha-synuclein by dicarbonyl compounds inhibits its fibril-forming process. Biochim Biophys Acta 1794, 421-430 DOI |
69 | Norris EH, Giasson BI, Ischiropoulos H and Lee VM (2003) Effects of oxidative and nitrative challenges on alpha-synuclein fibrillogenesis involve distinct mechanisms of protein modifications. J Biol Chem 278, 27230-27240 DOI |
70 | Qiao HH, Zhu LN, Wang Y et al (2019) Implications of alpha-synuclein nitration at tyrosine 39 in methamphetamine-induced neurotoxicity in vitro and in vivo. Neural Regen Res 14, 319-327 DOI |
71 | Fujiwara H, Hasegawa M, Dohmae N et al (2002) alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4, 160-164 DOI |
72 | Vicente Miranda H, Szego EM, Oliveira LMA et al (2017) Glycation potentiates alpha-synuclein-associated neurodegeneration in synucleinopathies. Brain 140, 1399-1419 DOI |
73 | van der Wateren IM, Knowles TPJ, Buell AK, Dobson CM and Galvagnion C (2018) C-terminal truncation of alpha-synuclein promotes amyloid fibril amplification at physiological pH. Chem Sci 9, 5506-5516 DOI |
74 | Negro A, Brunati AM, Donella-Deana A, Massimino ML and Pinna LA (2002) Multiple phosphorylation of alpha-synuclein by protein tyrosine kinase Syk prevents eosininduced aggregation. FASEB J 16, 210-212 |
75 | Shin WH and Chung KC (2020) Death-associated protein kinase 1 phosphorylates alpha-synuclein at Ser129 and exacerbates rotenone-induced toxic aggregation of alpha-synuclein in dopaminergic SH-SY5Y cells. Exp Neurobiol 29, 207-218 DOI |
76 | Nakamura T, Yamashita H, Takahashi T and Nakamura S (2001) Activated Fyn phosphorylates alpha-synuclein at tyrosine residue 125. Biochem Biophys Res Commun 280, 1085-1092 DOI |
77 | Ellis CE, Schwartzberg PL, Grider TL, Fink DW and Nussbaum RL (2001) alpha-synuclein is phosphorylated by members of the Src family of protein-tyrosine kinases. J Biol Chem 276, 3879-3884 DOI |
78 | Sorrentino ZA, Hass E, Vijayaraghavan N et al (2020) Carboxy-terminal truncation and phosphorylation of alpha-synuclein elongates survival in a prion-like seeding mouse model of synucleinopathy. Neurosci Lett 732, 135017 DOI |
79 | Stefanis L, Emmanouilidou E, Pantazopoulou M, Kirik D, Vekrellis K and Tofaris GK (2019) How is alpha-synuclein cleared from the cell? J Neurochem 150, 577-590 DOI |
80 | Shin Y, Klucken J, Patterson C, Hyman BT and 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 DOI |
81 | Tetzlaff JE, Putcha P, Outeiro TF et al (2008) CHIP targets toxic alpha-Synuclein oligomers for degradation. J Biol Chem 283, 17962-17968 DOI |
82 | Nishie M, Mori F, Yoshimoto M, Takahashi H and Wakabayashi K (2004) A quantitative investigation of neuronal cytoplasmic and intranuclear inclusions in the pontine and inferior olivary nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 30, 546-554 DOI |
83 | Waxman EA and Giasson BI (2011) Characterization of kinases involved in the phosphorylation of aggregated alpha-synuclein. J Neurosci Res 89, 231-247 DOI |
84 | Spillantini MG, Crowther RA, 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 U S A 95, 6469-6473 DOI |
85 | Trojanowski JQ, Revesz T and Neuropathology Working Group on MSA (2007) Proposed neuropathological criteria for the post mortem diagnosis of multiple system atrophy. Neuropathol Appl Neurobiol 33, 615-620 DOI |
86 | Fauvet B, Mbefo MK, Fares MB et al (2012) alpha-Synuclein in central nervous system and from erythrocytes, mammalian cells, and Escherichia coli exists predominantly as disordered monomer. J Biol Chem 287, 15345-15364 DOI |
87 | Cremades N, Cohen SI, Deas E et al (2012) Direct observation of the interconversion of normal and toxic forms of alpha-synuclein. Cell 149, 1048-1059 DOI |
88 | Mahul-Mellier AL, Burtscher J, Maharjan N et al (2020) The process of Lewy body formation, rather than simply alpha-synuclein fibrillization, is one of the major drivers of neurodegeneration. Proc Natl Acad Sci U S A 117, 4971-4982 DOI |
89 | Chen L and Feany MB (2005) Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. Nat Neurosci 8, 657-663 DOI |
90 | Chen L, Periquet M, Wang X et al (2009) Tyrosine and serine phosphorylation of alpha-synuclein have opposing effects on neurotoxicity and soluble oligomer formation. J Clin Invest 119, 3257-3265 DOI |
91 | Okochi M, Walter J, Koyama A et al (2000) Constitutive phosphorylation of the Parkinson's disease associated alpha-synuclein. J Biol Chem 275, 390-397 DOI |
92 | Paleologou KE, Oueslati A, Shakked G et al (2010) Phosphorylation at S87 is enhanced in synucleinopathies, inhibits alpha-synuclein oligomerization, and influences synuclein-membrane interactions. J Neurosci 30, 3184-3198 DOI |
93 | Smith WW, Margolis RL, Li X et al (2005) Alpha-synuclein phosphorylation enhances eosinophilic cytoplasmic inclusion formation in SH-SY5Y cells. J Neurosci 25, 5544-5552 DOI |
94 | Ding J, Wang Y, Huang J et al (2020) Role of alpha-synuclein phosphorylation at Serine 129 in methamphetamine-induced neurotoxicity in vitro and in vivo. Neuroreport 31, 787-797 |
95 | Oueslati A, Schneider BL, Aebischer P and Lashuel HA (2013) Polo-like kinase 2 regulates selective autophagic alpha-synuclein clearance and suppresses its toxicity in vivo. Proc Natl Acad Sci U S A 110, E3945-E3954 |
96 | Rott R, Szargel R, Haskin J et al (2008) Monoubiquitylation of alpha-synuclein by seven in absentia homolog (SIAH) promotes its aggregation in dopaminergic cells. J Biol Chem 283, 3316-3328 DOI |
97 | Lee JT, Wheeler TC, Li L and Chin LS (2008) Ubiquitination of alpha-synuclein by Siah-1 promotes alpha-synuclein aggregation and apoptotic cell death. Hum Mol Genet 17, 906-917 DOI |
98 | Oh Y, Kim YM, Mouradian MM and Chung KC (2011) Human Polycomb protein 2 promotes alpha-synuclein aggregate formation through covalent SUMOylation. Brain Res 1381, 78-89 DOI |
99 | Prasad V, Wasser Y, Hans F et al (2019) Monitoring alpha-synuclein multimerization in vivo. FASEB J 33, 2116-2131 DOI |
100 | Lashuel HA, Petre BM, Wall J et al (2002) Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J Mol Biol 322, 1089-1102 DOI |
101 | Oueslati A, Paleologou KE, Schneider BL, Aebischer P and Lashuel HA (2012) Mimicking phosphorylation at serine 87 inhibits the aggregation of human alpha-synuclein and protects against its toxicity in a rat model of Parkinson's disease. J Neurosci 32, 1536-1544 DOI |
102 | Tofaris GK, Kim HT, Hourez R, Jung JW, Kim KP and Goldberg AL (2011) Ubiquitin ligase Nedd4 promotes alpha-synuclein degradation by the endosomal-lysosomal pathway. Proc Natl Acad Sci U S A 108, 17004-17009 DOI |
103 | Levine PM, Galesic A, Balana AT et al (2019) alpha-Synuclein O-GlcNAcylation alters aggregation and toxicity, revealing certain residues as potential inhibitors of Parkinson's disease. Proc Natl Acad Sci U S A 116, 1511-1519 DOI |
104 | Davies SE, Hallett PJ, Moens T et al (2014) Enhanced ubiquitin-dependent degradation by Nedd4 protects against alpha-synuclein accumulation and toxicity in animal models of Parkinson's disease. Neurobiol Dis 64, 79-87 DOI |
105 | Danzer KM, Haasen D, Karow AR et al (2007) Different species of alpha-synuclein oligomers induce calcium influx and seeding. J Neurosci 27, 9220-9232 DOI |
106 | Peelaerts W, Bousset L, Van der Perren A et al (2015) alpha-Synuclein strains cause distinct synucleinopathies after local and systemic administration. Nature 522, 340-344 DOI |
107 | Volpicelli-Daley LA, Luk KC, Patel TP et al (2011) Exogenous alpha-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 72, 57-71 DOI |
108 | Zhang J, Lei H, Chen Y et al (2017) Enzymatic O-GlcNA-cylation of alpha-synuclein reduces aggregation and increases SDS-resistant soluble oligomers. Neurosci Lett 655, 90-94 DOI |
109 | Vijayakumaran S, Nakamura Y, Henley JM and Pountney DL (2019) Ginkgolic acid promotes autophagy-dependent clearance of intracellular alpha-synuclein aggregates. Mol Cell Neurosci 101, 103416 DOI |
110 | Shahpasandzadeh H, Popova B, Kleinknecht A, Fraser PE, Outeiro TF and Braus GH (2014) Interplay between sumoylation and phosphorylation for protection against alpha-synuclein inclusions. J Biol Chem 289, 31224-31240 DOI |
111 | Campbell BC, McLean CA, Culvenor JG et al (2001) The solubility of alpha-synuclein in multiple system atrophy differs from that of dementia with Lewy bodies and Parkinson's disease. J Neurochem 76, 87-96 DOI |
112 | Murray IV, Giasson BI, Quinn SM et al (2003) Role of alpha-synuclein carboxy-terminus on fibril formation in vitro. Biochemistry 42, 8530-8540 DOI |
113 | Serpell LC, Berriman J, Jakes R, Goedert M and Crowther RA (2000) Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc Natl Acad Sci U S A 97, 4897-4902 DOI |
114 | Periquet M, Fulga T, Myllykangas L, Schlossmacher MG and Feany MB (2007) Aggregated alpha-synuclein mediates dopaminergic neurotoxicity in vivo. J Neurosci 27, 3338-3346 DOI |
115 | Zhang Z, Kang SS, Liu X et al (2017) Asparagine endopeptidase cleaves alpha-synuclein and mediates pathologic activities in Parkinson's disease. Nat Struct Mol Biol 24, 632-642 DOI |
116 | McGlinchey RP, Lacy SM, Huffer KE, Tayebi N, Sidransky E and Lee JC (2019) C-terminal alpha-synuclein truncations are linked to cysteine cathepsin activity in Parkinson's disease. J Biol Chem 294, 9973-9984 DOI |
117 | Tofaris GK, Garcia Reitbock P, Humby T et al (2006) Pathological changes in dopaminergic nerve cells of the substantia nigra and olfactory bulb in mice transgenic for truncated human alpha-synuclein(1-120): implications for Lewy body disorders. J Neurosci 26, 3942-3950 DOI |
118 | Marotta NP, Cherwien CA, Abeywardana T and Pratt MR (2012) O-GlcNAc modification prevents peptide-dependent acceleration of alpha-synuclein aggregation. ChemBioChem 13, 2665-2670 DOI |
119 | Ryan P, Xu M, Davey AK et al (2019) O-GlcNAc modification protects against protein misfolding and aggregation in neurodegenerative disease. ACS Chem Neurosci 10, 2209-2221 DOI |
120 | Braak H, Ghebremedhin E, Rub U, Bratzke H and Del Tredici K (2004) Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res 318, 121-134 DOI |
121 | Nakajo S, Tsukada K, Omata K, Nakamura Y and Nakaya K (1993) A new brain-specific 14-kDa protein is a phosphoprotein. Its complete amino acid sequence and evidence for phosphorylation. Eur J Biochem 217, 1057-1063 DOI |
122 | Moons R, Konijnenberg A, Mensch C et al (2020) Metal ions shape alpha-synuclein. Sci Rep 10, 16293 DOI |
123 | Burmann BM, Gerez JA, Matecko-Burmann I et al (2020) Regulation of alpha-synuclein by chaperones in mammalian cells. Nature 577, 127-132 DOI |
124 | Meier F, Abeywardana T, Dhall A et al (2012) Semisynthetic, site-specific ubiquitin modification of alpha-synuclein reveals differential effects on aggregation. J Am Chem Soc 134, 5468-5471 DOI |
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