Fibril growth and seeding capacity play key roles in α-synuclein-mediated apoptotic cell death

Cell Death and Differentiation

Volumn 22, Issue 12, 2015, Pages 2107-2122

  Mahul Mellier, A L ^a   Vercruysse, F ^a   MacO, B ^a   Ait Bouziad, N ^a   De Roo, M ^b   Muller, D ^b   Lashuel, H A ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; BETA SYNUCLEIN; CASPASE 3; CASPASE 8; CASPASE 9; DNA; NEURON SPECIFIC NUCLEAR PROTEIN; TOLCAPONE; RECOMBINANT PROTEIN; TAU PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CELL LYSATE; CELL POPULATION; CELL SURFACE; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA FRAGMENTATION; ENZYME ACTIVATION; ENZYME INHIBITION; EX VIVO STUDY; GLIA CELL; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; MEMBRANE DAMAGE; MOLECULAR MODEL; MOLECULAR WEIGHT; MOUSE; NERVE CELL; NERVE CELL GROWTH; NERVE CELL MEMBRANE; NEUROBLASTOMA CELL LINE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; GENETICS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; TRANSMISSION ELECTRON MICROSCOPY;

ALPHA-SYNUCLEIN; ANIMALS; APOPTOSIS; CASPASE 3; CASPASE 8; CASPASE 9; CELLS, CULTURED; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; RECOMBINANT PROTEINS; TAU PROTEINS;

EID: 84947034456     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.79     Document Type: Article

References (67)

1. Goedert M, Spillantini MG, Del Tredici K, Braak H. 100 years of Lewy pathology. Nat Rev Neurol 2013; 9: 13-24.
2. Lashuel HA, Overk CR, Oueslati A, Masliah E. The many faces of alpha-synuclein: from structure and toxicity to therapeutic target. Nat Rev Neurosci 2013; 14: 38-48.
3. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ et al. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 2008; 14: 501-503.
4. Kordower JH, Chu Y, Hauser RA, Olanow CW, Freeman TB. Transplanted dopaminergic neurons develop PD pathologic changes: a second case report. Mov Disord 2008; 23: 2303-2306.
5. Mollenhauer B, Trautmann E, Taylor P, Manninger P, Sixel-Doring F, Ebentheuer J et al. Total CSF alpha-synuclein is lower in de novo Parkinson patients than in healthy subjects. Neurosci Lett 2013; 532: 44-48.
6. Lee HJ, Patel S, Lee SJ. Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. J Neurosci 2005; 25: 6016-6024.
7. Marques O, Outeiro TF. Alpha-synuclein: from secretion to dysfunction and death. Cell Death Dis 2012; 3: e350.
8. Lee HJ, Bae EJ, Lee SJ. Extracellular alpha-synuclein-a novel and crucial factor in Lewy body diseases. Nat Rev Neurol 2014; 10: 92-98.
9. Emmanouilidou E, Melachroinou K, Roumeliotis T, Garbis SD, Ntzouni M, Margaritis LH et al. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci 2010; 30: 6838-6851.
10. Alvarez-Erviti L, Seow Y, Schapira AH, Gardiner C, Sargent IL, Wood MJ et al. Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission. Neurobiol Dis 2011; 42: 360-367.
11. Winner B, Jappelli R, Maji SK, Desplats PA, Boyer L, Aigner S et al. In vivo demonstration that alpha-synuclein oligomers are toxic. Proc Natl Acad Sci USA 2011; 108: 4194-4199.
12. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L et al. Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci USA 2009; 106: 13010-13015.
13. Luk KC, Kehm VM, Zhang B, O'Brien P, Trojanowski JQ, Lee VM. Intracerebral inoculation of pathological alpha-synuclein initiates a rapidly progressive neurodegenerative alphasynucleinopathy in mice. J Exp Med 2012; 209: 975-986.
14. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ et al. Pathological alphasynuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science (New York, NY) 2012; 338: 949-953.
15. Recasens A, Dehay B, Bove J, Carballo-Carbajal I, Dovero S, Perez-Villalba A et al. Lewy body extracts from Parkinson disease brains trigger alpha-synuclein pathology and neurodegeneration in mice and monkeys. Ann Neurol 2014; 75: 351-362.
16. Hansen C, Angot E, Bergstrom AL, Steiner JA, Pieri L, Paul G et al. alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 2011; 121: 715-725.
17. Volpicelli-Daley LA, Luk KC, Patel TP, Tanik SA, Riddle DM, Stieber A et al. Exogenous alpha-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 2011; 72: 57-71.
18. Luk KC, Song C, O'Brien P, Stieber A, Branch JR, Brunden KR et al. Exogenous alphasynuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci USA 2009; 106: 20051-20056.
19. Alvarez-Erviti L, Couch Y, Richardson J, Cooper JM, Wood MJ. Alpha-synuclein release by neurons activates the inflammatory response in a microglial cell line. Neurosci Res 2011; 69: 337-342.
20. Zhang W, Wang T, Pei Z, Miller DS, Wu X, Block ML et al. Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J 2005; 19: 533-542.
21. Lee HJ, Suk JE, Patrick C, Bae EJ, Cho JH, Rho S et al. Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J Biol Chem 2010; 285: 9262-9272.
22. Di Giovanni S, Eleuteri S, Paleologou KE, Yin G, Zweckstetter M, Carrupt PA et al. 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 2010; 285: 14941-14954.
23. El-Agnaf OM, Jakes R, Curran MD, Middleton D, Ingenito R, Bianchi E et al. Aggregates from mutant and wild-type alpha-synuclein proteins and NAC peptide induce apoptotic cell death in human neuroblastoma cells by formation of beta-sheet and amyloid-like filaments. FEBS Lett 1998; 440: 71-75.
24. Wright JA, Wang X, Brown DR. Unique copper-induced oligomers mediate alpha-synuclein toxicity. FASEB J 2009; 23: 2384-2393.
25. Lee EN, Cho HJ, Lee CH, Lee D, Chung KC, Paik SR. Phthalocyanine tetrasulfonates affect the amyloid formation and cytotoxicity of alpha-synuclein. Biochemistry 2004; 43: 3704-3715.
26. Jan A, Hartley DM, Lashuel HA. Preparation and characterization of toxic Abeta aggregates for structural and functional studies in Alzheimer's disease research. Nat Protoc 2010; 5: 1186-1209.
27. Jan A, Gokce O, Luthi-Carter R, Lashuel HA. The ratio of monomeric to aggregated forms of Abeta40 and Abeta42 is an important determinant of amyloid-beta aggregation, fibrillogenesis, and toxicity. J Biol Chem 2008; 283: 28176-28189.
28. Fauvet B, Mbefo MK, Fares MB, Desobry C, Michael S, Ardah MT et al. alpha-Synuclein in central nervous system and from erythrocytes, mammalian cells, and Escherichia coli exists predominantly as disordered monomer. J Biol Chem 2012; 287: 15345-15364.
29. Yamakawa K, Izumi Y, Takeuchi H, Yamamoto N, Kume T, Akaike A et al. Dopamine facilitates alpha-synuclein oligomerization in human neuroblastoma SH-SY5Y cells. Biochem Biophys Res Commun 2010; 391: 129-134.
30. Fagerqvist T, Nasstrom T, Ihse E, Lindstrom V, Sahlin C, Tucker SM et al. Off-pathway alphasynuclein oligomers seem to alter alpha-synuclein turnover in a cell model but lack seeding capability in vivo. Amyloid 2013; 20: 233-244.
31. Lee HJ, Baek SM, Ho DH, Suk JE, Cho ED, Lee SJ. Dopamine promotes formation and secretion of non-fibrillar alpha-synuclein oligomers. Exp Mol Med 2011; 43: 216-222.
32. Luk KC, Lee VM. Modeling Lewy pathology propagation in Parkinson's disease. Parkinsonism Relat Disord 2014; 20: S85-S87.
33. Jan A, Adolfsson O, Allaman I, Buccarello AL, Magistretti PJ, Pfeifer A et al. Abeta42 neurotoxicity is mediated by ongoing nucleated polymerization process rather than by discrete Abeta42 species. J Biol Chem 2011; 286: 8585-8596.
34. Wogulis M, Wright S, Cunningham D, Chilcote T, Powell K, Rydel RE. Nucleation-dependent polymerization is an essential component of amyloid-mediated neuronal cell death. J Neurosci 2005; 25: 1071-1080.
35. Biere AL, Wood SJ, Wypych J, Steavenson S, Jiang Y, Anafi D et al. Parkinson's diseaseassociated alpha-synuclein is more fibrillogenic than beta-and gamma-synuclein and cannot cross-seed its homologs. J Biol Chem 2000; 275: 34574-34579.
36. Tsigelny IF, Bar-On P, Sharikov Y, Crews L, Hashimoto M, Miller MA et al. Dynamics of alpha-synuclein aggregation and inhibition of pore-like oligomer development by betasynuclein. FEBS J 2007; 274: 1862-1877.
37. Hashimoto M, Rockenstein E, Mante M, Mallory M, Masliah E. beta-Synuclein inhibits alphasynuclein aggregation: a possible role as an anti-parkinsonian factor. Neuron 2001; 32: 213-223.
38. Giasson BI, Forman MS, Higuchi M, Golbe LI, Graves CL, Kotzbauer PT et al. Initiation and synergistic fibrillization of tau and alpha-synuclein. Science (New York, NY) 2003; 300: 636-640.
39. Cook NP, Kilpatrick K, Segatori L, Marti AA. Detection of alpha-synuclein amyloidogenic aggregates in vitro and in cells using light-switching dipyridophenazine ruthenium(II) complexes. J Am Chem Soc 2012; 134: 20776-20782.
40. Kilpatrick K, Novoa JA, Hancock T, Guerriero CJ, Wipf P, Brodsky JL et al. Chemical induction of Hsp70 reduces alpha-synuclein aggregation in neuroglioma cells. ACS Chem Biol 2013; 8: 1460-1468.
41. Shen D, Coleman J, Chan E, Nicholson TP, Dai L, Sheppard PW et al. Novel cell-and tissuebased assays for detecting misfolded and aggregated protein accumulation within aggresomes and inclusion bodies. Cell Biochem Biophys 2011; 60: 173-185.
42. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012; 19: 107-120.
43. Forloni G, Bertani I, Calella AM, Thaler F, Invernizzi R. Alpha-synuclein and Parkinson's disease: selective neurodegenerative effect of alpha-synuclein fragment on dopaminergic neurons in vitro and in vivo. Ann Neurol 2000; 47: 632-640.
44. Lee HJ, Choi C, Lee SJ. Membrane-bound alpha-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form. J Biol Chem2002; 277: 671-678.
45. Hertel C, Hauser N, Schubenel R, Seilheimer B, Kemp JA. Beta-amyloid-induced cell toxicity: enhancement of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromidedependent cell death. J Neurochem 1996; 67: 272-276.
46. Soriano FX, Galbete JL, Forloni G. Effect of beta-amyloid on endothelial cells: lack of direct toxicity, enhancement of MTT-induced cell death and intracellular accumulation. Neurochem Int 2003; 43: 251-261.
47. Kane MD, Schwarz RD, St Pierre L, Watson MD, Emmerling MR, Boxer PA et al. Inhibitors of V-type ATPases, bafilomycin A1 and concanamycin A, protect against beta-amyloidmediated effects on 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 1999; 72: 1939-1947.
48. Brandner S, Isenmann S, Raeber A, Fischer M, Sailer A, Kobayashi Y et al. Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 1996; 379: 339-343.
49. Holmes BB, DeVos SL, Kfoury N, Li M, Jacks R, Yanamandra K et al. Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci USA 2013; 110: E3138-E3147.
50. Liu IH, Uversky VN, Munishkina LA, Fink AL, Halfter W, Cole GJ. Agrin binds alpha-synuclein and modulates alpha-synuclein fibrillation. Glycobiology 2005; 15: 1320-1331.
51. Cohlberg JA, Li J, Uversky VN, Fink AL. Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from alpha-synuclein in vitro. Biochemistry 2002; 41: 1502-1511.
52. Reynolds NP, Soragni A, Rabe M, Verdes D, Liverani E, Handschin S et al. Mechanism of membrane interaction and disruption by alpha-synuclein. J Am Chem Soc 2011; 133: 19366-19375.
53. Galvagnion C, Buell AK, Meisl G, Michaels TC, Vendruscolo M, Knowles TP et al. Lipid vesicles trigger alpha-synuclein aggregation by stimulating primary nucleation. Nat Chem Biol 2015; 11: 229-234.
54. Buell AK, Galvagnion C, Gaspar R, Sparr E, Vendruscolo M, Knowles TP et al. Solution conditions determine the relative importance of nucleation and growth processes in alpha-synuclein aggregation. Proc Natl Acad Sci USA 2014; 111: 7671-7676.
55. Jeong JS, Ansaloni A, Mezzenga R, Lashuel HA, Dietler G. Novel mechanistic insight into the molecular basis of amyloid polymorphism and secondary nucleation during amyloid formation. J Mol Biol 2013; 425: 1765-1781.
56. Cohen SI, Linse S, Luheshi LM, Hellstrand E, White DA, Rajah L et al. Proliferation of amyloid-beta42 aggregates occurs through a secondary nucleation mechanism. Proc Natl Acad Sci USA 2013; 110: 9758-9763.
57. Chaudhary H, Stefanovic AN, Subramaniam V, Claessens MM. Membrane interactions and fibrillization of alpha-synuclein play an essential role in membrane disruption. FEBS Lett 2014; 588: 4457-4463.
58. Pacheco CR, Morales CN, Ramirez AE, Munoz FJ, Gallegos SS, Caviedes PA et al. Extracellular alpha-synuclein alters synaptic transmission in brain neurons by perforating the neuronal plasma membrane. J Neurochem 2015; 132: 731-741.
59. Choi WS, Eom DS, Han BS, Kim WK, Han BH, Choi EJ et al. Phosphorylation of p38 MAPK induced by oxidative stress is linked to activation of both caspase-8-and-9-mediated apoptotic pathways in dopaminergic neurons. J Biol Chem 2004; 279: 20451-20460.
60. Viswanath V, Wu Y, Boonplueang R, Chen S, Stevenson FF, Yantiri F et al. Caspase-9 activation results in downstream caspase-8 activation and bid cleavage in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson's disease. J Neurosci 2001; 21: 9519-9528.
61. Ouberai MM, Wang J, Swann MJ, Galvagnion C, Guilliams T, Dobson CM et al. alpha-Synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane remodeling. J Biol Chem 2013; 288: 20883-20895.
62. Lashuel HA, Hartley D, Petre BM, Walz T, Lansbury Jr PT. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 2002; 418: 291.
63. Harbison NW, Bhattacharya S, Eliezer D. Assigning backbone NMR resonances for full length tau isoforms: efficient compromise between manual assignments and reduced dimensionality. PLoS One 2012; 7: e34679.
64. Steiner P, Sarria JC, Glauser L, Magnin S, Catsicas S, Hirling H. Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD. J Cell Biol 2002; 157: 1197-1209.
65. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991; 37: 173-182.
66. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119: 493-501.
67. Cappai R, Leck SL, Tew DJ, Williamson NA, Smith DP, Galatis D et al. Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway. FASEB J 2005; 19: 1377-1379.