Insights into the molecular mechanism of amyloid filament formation: Segmental folding of α-synuclein on lipid membranes.


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
05 2021
Historique:
received: 17 12 2020
accepted: 25 03 2021
entrez: 15 5 2021
pubmed: 16 5 2021
medline: 16 4 2022
Statut: epublish

Résumé

Recent advances in the structural biology of disease-relevant α-synuclein fibrils have revealed a variety of structures, yet little is known about the process of fibril aggregate formation. Characterization of intermediate species that form during aggregation is crucial; however, this has proven very challenging because of their transient nature, heterogeneity, and low population. Here, we investigate the aggregation of α-synuclein bound to negatively charged phospholipid small unilamellar vesicles. Through a combination of kinetic and structural studies, we identify key time points in the aggregation process that enable targeted isolation of prefibrillar and early fibrillar intermediates. By using solid-state nuclear magnetic resonance, we show the gradual buildup of structural features in an α-synuclein fibril filament, revealing a segmental folding process. We identify distinct membrane-binding domains in α-synuclein aggregates, and the combined data are used to present a comprehensive mechanism of the folding of α-synuclein on lipid membranes.

Identifiants

pubmed: 33990334
pii: 7/20/eabg2174
doi: 10.1126/sciadv.abg2174
pmc: PMC8121418
pii:
doi:

Substances chimiques

Amyloid 0
Phospholipids 0
alpha-Synuclein 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

Références

Proc Natl Acad Sci U S A. 2015 Apr 21;112(16):E1994-2003
pubmed: 25855634
Nat Chem Biol. 2020 Jun;16(6):653-659
pubmed: 32152544
Nature. 1997 Aug 28;388(6645):839-40
pubmed: 9278044
Biophys J. 2016 Jun 21;110(12):2710-2719
pubmed: 27332129
J Biomol NMR. 1995 Nov;6(3):277-93
pubmed: 8520220
Nat Struct Mol Biol. 2016 May;23(5):409-15
pubmed: 27018801
J Am Chem Soc. 2003 Nov 26;125(47):14222-3
pubmed: 14624539
Nat Neurosci. 2019 Jul;22(7):1099-1109
pubmed: 31235907
J Phys Chem B. 2017 Mar 2;121(8):1783-1792
pubmed: 28075583
J Biomol NMR. 1994 Mar;4(2):171-80
pubmed: 8019132
Biochim Biophys Acta Proteins Proteom. 2019 May;1867(5):468-482
pubmed: 30315896
Proteins. 2005 Jun 1;59(4):687-96
pubmed: 15815974
Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):19666-71
pubmed: 19066219
Biomol NMR Assign. 2014 Oct;8(2):395-404
pubmed: 24114178
J Phys Chem B. 2017 Sep 28;121(38):8926-8934
pubmed: 28851223
Bioinformatics. 2015 Apr 15;31(8):1325-7
pubmed: 25505092
Nat Commun. 2014 Dec 19;5:5857
pubmed: 25524885
J Biomol NMR. 2009 Nov;45(3):319-27
pubmed: 19779834
Nat Protoc. 2016 Feb;11(2):252-72
pubmed: 26741409
J Mol Biol. 2009 Jun 5;389(2):413-24
pubmed: 19285989
Proc Natl Acad Sci U S A. 2016 Jun 28;113(26):7065-70
pubmed: 27298346
Chem Soc Rev. 2017 Oct 30;46(21):6492-6531
pubmed: 28702523
J Biol Chem. 2000 Nov 3;275(44):34393-8
pubmed: 10952980
J Am Chem Soc. 2012 Mar 21;134(11):5090-9
pubmed: 22352310
J Biomol NMR. 2009 Aug;44(4):213-23
pubmed: 19548092
Nat Commun. 2016 Sep 19;7:12563
pubmed: 27640673
J Am Chem Soc. 2014 Mar 12;136(10):3859-68
pubmed: 24527756
Brain. 1987 Oct;110 ( Pt 5):1131-53
pubmed: 2823957
Elife. 2019 Dec 09;8:
pubmed: 31815671
Nat Struct Mol Biol. 2020 Mar;27(3):249-259
pubmed: 32157247
Chemphyschem. 2019 Jan 21;20(2):302-310
pubmed: 30452110
J Neurol Neurosurg Psychiatry. 1969 Feb;32(1):28-34
pubmed: 5774131
Biomolecules. 2015 Mar 25;5(2):282-305
pubmed: 25816357
Int J Biol Macromol. 2013 Jul;58:190-8
pubmed: 23562552
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Phys Chem B. 2018 Oct 11;122(40):9302-9313
pubmed: 30211552
Angew Chem Int Ed Engl. 2018 Nov 12;57(46):15262-15266
pubmed: 30184304
J Neurochem. 2019 Sep;150(5):475-486
pubmed: 31269263
J Mol Biol. 2002 Sep 13;322(2):383-93
pubmed: 12217698
J Am Chem Soc. 2011 Dec 7;133(48):19366-75
pubmed: 21978222
Nat Commun. 2018 Sep 6;9(1):3609
pubmed: 30190461
Acta Neuropathol. 2000 Apr;99(4):352-7
pubmed: 10787032
Nat Commun. 2014 May 29;5:3827
pubmed: 24871041
Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5975-9
pubmed: 8650204
N Engl J Med. 2015 Jan 15;372(3):249-63
pubmed: 25587949
Proc Natl Acad Sci U S A. 2020 Feb 18;117(7):3592-3602
pubmed: 32015135
J Mol Biol. 2001 Apr 6;307(4):1061-73
pubmed: 11286556
Biochem J. 2012 May 1;443(3):719-26
pubmed: 22316405
J Magn Reson. 2019 Aug;305:1-4
pubmed: 31158790
FEBS Lett. 1994 May 23;345(1):27-32
pubmed: 8194594
Nat Chem Biol. 2015 Mar;11(3):229-34
pubmed: 25643172
Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10427-32
pubmed: 16020533
J Phys Chem Lett. 2014 Sep 18;5(18):3211-5
pubmed: 26276334
Biophys J. 2013 Sep 3;105(5):1192-8
pubmed: 24010662
Nature. 2020 Sep;585(7825):464-469
pubmed: 32461689
J Am Chem Soc. 2007 Sep 26;129(38):11791-801
pubmed: 17725352
J Mol Biol. 2002 Oct 4;322(5):1089-102
pubmed: 12367530
J Biol Chem. 2001 Jan 26;276(4):2380-6
pubmed: 11060312
ACS Chem Neurosci. 2017 Mar 15;8(3):538-547
pubmed: 28292187
Int J Mol Sci. 2018 Aug 23;19(9):
pubmed: 30142878
Chembiochem. 2008 Oct 13;9(15):2411-6
pubmed: 18821550
Science. 2017 Dec 15;358(6369):1440-1443
pubmed: 29242346
J Mol Biol. 2009 Jul 24;390(4):775-90
pubmed: 19481095
Q Rev Biophys. 2014 Feb;47(1):1-48
pubmed: 24443929
J Am Chem Soc. 2014 Sep 3;136(35):12489-97
pubmed: 25102442

Auteurs

Leif Antonschmidt (L)

Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.

Rıza Dervişoğlu (R)

Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.

Vrinda Sant (V)

Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.
Department of Mechanical and Aerospace Engineering, University of California San Diego, San Diego, CA, USA.

Kumar Tekwani Movellan (K)

Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.

Ingo Mey (I)

Institute of Organic and Biomolecular Chemistry, Georg-August-Universität Göttingen, Göttingen, Germany.

Dietmar Riedel (D)

Laboratory of Electron Microscopy, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.

Claudia Steinem (C)

Institute of Organic and Biomolecular Chemistry, Georg-August-Universität Göttingen, Göttingen, Germany.
Biomolecular Chemistry Group, Max-Planck Institute for Dynamics and Self-Organization, Am Fassberg 17, 37077 Göttingen, Germany.
Cluster of Excellence "Multiscale Bioimaging: From Molecular Machines to Networks of Excitable Cells" (MBExC), University of Göttingen, Göttingen, Germany.

Stefan Becker (S)

Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany.

Loren B Andreas (LB)

Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany. land@nmr.mpibpc.mpg.de cigr@nmr.mpibpc.mpg.de.

Christian Griesinger (C)

Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany. land@nmr.mpibpc.mpg.de cigr@nmr.mpibpc.mpg.de.
Cluster of Excellence "Multiscale Bioimaging: From Molecular Machines to Networks of Excitable Cells" (MBExC), University of Göttingen, Göttingen, Germany.

Articles similaires

alpha-Synuclein Humans Animals Mice Lewy Body Disease

Amyloid accelerator polyphosphate fits as the mystery density in α-synuclein fibrils.

Philipp Huettemann, Pavithra Mahadevan, Justine Lempart et al.
1.00
Polyphosphates alpha-Synuclein Humans Amyloid Molecular Dynamics Simulation

Measurement of α-synuclein as protein cargo in plasma extracellular vesicles.

Tal Gilboa, Dmitry Ter-Ovanesyan, Shih-Chin Wang et al.
1.00
alpha-Synuclein Extracellular Vesicles Humans Phosphorylation Parkinson Disease
Escherichia coli Membrane Fluidity Temperature Escherichia coli Proteins Fatty Acids

Classifications MeSH