α-Synuclein and huntingtin exon 1 amyloid fibrils bind laterally to the cellular membrane

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Monsellier, Elodie ^a   Bousset, Luc ^a   Melki, Ronald ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; HTT PROTEIN, HUMAN; HUNTINGTIN; LIPOSOME; PROTEIN AGGREGATE; PROTEIN BINDING; RECOMBINANT PROTEIN;

ANIMAL; BRAIN; CELL LINE; CELL MEMBRANE; CHEMISTRY; EXON; GENETICS; HUMAN; LIPID METABOLISM; METABOLISM; MOUSE; PERMEABILITY; PROTEIN CONFORMATION; PROTEIN DEGRADATION;

ALPHA-SYNUCLEIN; AMYLOID; ANIMALS; BRAIN; CELL LINE; CELL MEMBRANE; EXONS; HUMANS; HUNTINGTIN PROTEIN; LIPID METABOLISM; MICE; PERMEABILITY; PROTEIN AGGREGATES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEOLYSIS; RECOMBINANT PROTEINS; UNILAMELLAR LIPOSOMES;

EID: 84955107741     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19180     Document Type: Article

References (45)

1. Knowles, T. P. J., Vendruscolo, M., Dobson, C. M. The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 15, 384-396 (2014).
2. Ren, P.-H. et al. Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine aggregates. Nat. Cell Biol. 11, 219-225 (2009).
3. Angot, E. et al. Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo. PLoS One 7, 23-27 (2012).
4. Peelaerts, W. et al.-Synuclein strains cause distinct synucleinopathies after local and systemic administration. Nature 522, 340-344 (2015).
5. Holmes, B. B. et al. Proteopathic tau seeding predicts tauopathy in vivo. Proc. Natl. Acad. Sci. 111, E4376-E4385 (2014).
6. Nonaka, T. et al. Prion-like properties of pathological TDP-43 aggregates from diseased brains. Cell Rep. 4, 124-134 (2013).
7. Costanzo, M., Zurzolo, C. The cell biology of prion-like spread of protein aggregates: mechanisms and implication in neurodegeneration. Biochem. J. 452, 1-17 (2013).
8. Costanzo, M. et al. Transfer of polyglutamine aggregates in neuronal cells occurs in tunneling nanotubes. J. Cell Sci. 126, 3678-3685 (2013).
9. Brundin, P., Melki, R., Kopito, R. Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat. Rev. Mol. Cell Biol. 11, 301-307 (2010).
10. Trevino, R. S. et al. Fibrillar structure and charge determine the interaction of polyglutamine protein aggregates with the cell surface. J. Biol. Chem. 287, 29722-29728 (2012).
11. Milanesi, L. et al. Direct three-dimensional visualization of membrane disruption by amyloid fibrils. Proc. Natl. Acad. Sci. 109, 20455-20460 (2012).
12. Laurén, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., Strittmatter, S. M. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457, 1128-1132 (2009).
13. Hamilton, A., Zamponi, G. W., Ferguson, S. S. G. Glutamate receptors function as scaffolds for the regulation of-amyloid and cellular prion protein signaling complexes. Mol. Brain 8, 1-9 (2015).
14. Shrivastava, A. N. et al. synuclein assemblies sequester neuronal 3-Na+/K+-ATPase and impair Na+ gradient. EMBO J. 34, 2408-2423 (2015).
15. Bousset, L. et al. Structural and functional characterization of two alpha-synuclein strains. Nat. Commun. 4, 2575 (2013).
16. Evangelisti, E. et al. Membrane lipid composition and its physicochemical properties define cell vulnerability to aberrant protein oligomers. J. Cell Sci. 125, 2416-2427 (2012).
17. Bucciantini, M. et al. Toxic effects of amyloid fibrils on cell membranes: the importance of ganglioside GM1. FASEB J. 26, 818-831 (2012).
18. Chaibva, M., Burke, K. A., Legleiter, J. Curvature enhances binding and aggregation of huntingtin at lipid membranes. Biochemistry 53, 2355-2365 (2014).
19. Garten, M. et al. Methyl-branched lipids promote the membrane adsorption of-synuclein by enhancing shallow lipid-packing defects. Phys. Chem. Chem. Phys. 17, 15589-15597 (2015).
20. Xue, W. F. et al. Fibril fragmentation enhances amyloid cytotoxicity. J. Biol. Chem. 284, 34272-34282 (2009).
21. Julien, O. et al. Unraveling the mechanism of cell death induced by chemical fibrils. Nat. Chem. Biol. 10, 969-976 (2014).
22. Suopanki, J. et al. Interaction of huntingtin fragments with brain membranes-clues to early dysfunction in Huntington's disease. J. Neurochem. 96, 870-84 (2006).
23. Engel, M. F. M. et al. Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane. Proc. Natl. Acad. Sci. USA 105, 6033-6038 (2008).
24. Xue, W., Radford, S. E. An imaging and systems modeling approach to fibril breakage enables prediction of amyloid behavior. Biophys. J. 105, 2811-2819 (2013).
25. Knowles, T. P. J. et al. Observation of spatial propagation of amyloid assembly from single nuclei. Proc. Natl. Acad. Sci. 108, 14746-14751 (2011).
26. Knowles, T. P. J. et al. An analytical solution to the kinetics of breakable filament assembly. Science 326, 1533-1537 (2009).
27. Wu, J. W. et al. Small misfolded tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J. Biol. Chem. 288, 1856-1870 (2013).
28. Biancalana, M., Koide, S. Molecular mechanism of Thioflavin-T binding to amyloid fibrils. Biochim. Biophys. Acta 1804, 1405-1412 (2010).
29. Pieri, L., Madiona, K., Bousset, L., Melki, R. Fibrillar-synuclein and huntingtin exon 1 assemblies are toxic to the cells. Biophys. J. 102, 2894-2905 (2012).
30. Ruiz-Arlandis, G., Pieri, L., Bousset, L., Melki, R. Binding, internalization and fate of Huntingtin Exon1 fibrillar assemblies in mitotic and non-mitotic neuroblastoma cells. Neuropathol. Appl. Neurobiol. In press (2015).
31. Couceiro, J. et al. Sequence-dependent internalization of aggregating peptides. J. Biol. Chem. 290, 242-258 (2015).
32. Kegel, K. B. et al. Polyglutamine expansion in huntingtin alters its interaction with phospholipids. J. Neurochem. 110, 1585-1597 (2009).
33. Grey, M., Linse, S., Nilsson, H., Brundin, P., Sparr, E. Membrane interaction of-synuclein in different aggregation states. J. Parkinsons. Dis. 1, 359-371 (2011).
34. Burke, K. A., Yates, E. A., Legleiter, J. Amyloid-forming proteins alter the local mechanical properties of lipid membranes. Biochemistry 52, 808-817 (2013).
35. Holmes, B. B. et al. Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc. Natl. Acad. Sci. 110, E3138-E3147 (2013).
36. Burke, K. A., Kauffman, K. J., Umbaugh, C. S., Frey, S. L., Legleiter, J. The interaction of polyglutamine peptides with lipid membranes is regulated by flanking sequences associated with huntingtin. J. Biol. Chem. 288, 14993-15005 (2013).
37. Michalek, M., Salnikov, E. S., Werten, S., Bechinger, B. Membrane interactions of the amphipathic amino terminus of huntingtin. Biochemistry 52, 847-858 (2013).
38. Michalek, M., Salnikov, E. S., Bechinger, B. Structure and topology of the huntingtin 1-17 membrane anchor by a combined solution and solid-state NMR approach. Biophys. J. 105, 699-710 (2013).
39. Fusco, G. et al. Direct observation of the three regions in-synuclein that determine its membrane-bound behaviour. Nat. Commun. 5, 3827 (2014).
40. Sivanandam, V. N. et al. The aggregation-enhancing huntingtin N-terminus is helical in amyloid fibrils. J. Am. Chem. Soc. 133, 4558-4566 (2011).
41. Pemberton, S., Melki, R. The interaction of Hsc70 protein with fibrillar alpha-Synuclein and its therapeutic potential in Parkinson's disease. Commun Integr Biol 5, 94-95 (2012).
42. Melki, R. Role of different alpha-Synuclein strains in synucleinopathies, similarities with other neurodegenerative diseases. J. Parkinsons. Dis. 5, 217-227 (2015).
43. Ghee, M., Melki, R., Michot, N., Mallet, J. PA700, the regulatory complex of the 26S proteasome, interferes with alpha-synuclein assembly. FEBS J. 272, 4023-4033 (2005).
44. Monsellier, E., Redeker, V., Ruiz-Arlandis, G., Bousset, L., Melki, R. Molecular interaction between the chaperone Hsc70 and the N-terminal flank of huntingtin exon 1 modulates aggregation. J. Biol. Chem. 290, 2560-2576 (2015).
45. Wanker, E. E. et al. Membrane filter assay for detection of amyloid-like polyglutamine-containing protein aggregates. Methods Enzymol. 309, 375-386 (1999).