Conformational Dynamics of α‑Synuclein during the Interaction with Phospholipid Nanodiscs by Millisecond Hydrogen–Deuterium Exchange Mass Spectrometry

Both normal and pathological functions of α-synuclein (αSN), an abundant protein in the central and peripheral nervous system, have been linked to its interaction with membrane lipid bilayers. The ability to characterize structural transitions of αSN upon membrane complexation will clarify molecular...

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Published inJournal of the American Society for Mass Spectrometry Vol. 32; no. 5; pp. 1169 - 1179
Main Authors Oganesyan, Irina, Lento, Cristina, Tandon, Anurag, Wilson, Derek J
Format Journal Article
LanguageEnglish
Published United States American Chemical Society 05.05.2021
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Abstract Both normal and pathological functions of α-synuclein (αSN), an abundant protein in the central and peripheral nervous system, have been linked to its interaction with membrane lipid bilayers. The ability to characterize structural transitions of αSN upon membrane complexation will clarify molecular mechanisms associated with αSN-linked pathologies, including Parkinson’s disease (PD), multiple systems atrophy, and other synucleinopathies. In this work, time-resolved electrospray ionization hydrogen/deuterium exchange mass spectrometry (TRESI-HDX-MS) was employed to acquire a detailed picture of αSN’s conformational transitions as it undergoes complexation with nanodisc membrane mimics with different headgroup charges (zwitterionic DMPC and negative POPG). Using this approach, αSN interactions with DMPC nanodiscs were shown to be rapid exchanging and to have little impact on the αSN conformational ensemble. Interactions with nanodiscs containing lipids known to promote amyloidogenesis (e.g., POPG), on the other hand, were observed to induce substantial and specific changes in the αSN conformational ensemble. Ultimately, we identify a region corresponding residues 19–28 and 45–57 of the αSN sequence that is uniquely impacted by interactions with “amyloidogenic” lipid membranes, supporting the existing “broken-helix” model for α-synuclein/membrane interactions, but do not detect a “helical extension” that is also thought to play a role in αSN aggregation.
AbstractList Both normal and pathological functions of α-synuclein (αSN), an abundant protein in the central and peripheral nervous system, have been linked to its interaction with membrane lipid bilayers. The ability to characterize structural transitions of αSN upon membrane complexation will clarify molecular mechanisms associated with αSN-linked pathologies, including Parkinson’s disease (PD), multiple systems atrophy, and other synucleinopathies. In this work, time-resolved electrospray ionization hydrogen/deuterium exchange mass spectrometry (TRESI-HDX-MS) was employed to acquire a detailed picture of αSN’s conformational transitions as it undergoes complexation with nanodisc membrane mimics with different headgroup charges (zwitterionic DMPC and negative POPG). Using this approach, αSN interactions with DMPC nanodiscs were shown to be rapid exchanging and to have little impact on the αSN conformational ensemble. Interactions with nanodiscs containing lipids known to promote amyloidogenesis (e.g., POPG), on the other hand, were observed to induce substantial and specific changes in the αSN conformational ensemble. Ultimately, we identify a region corresponding residues 19–28 and 45–57 of the αSN sequence that is uniquely impacted by interactions with “amyloidogenic” lipid membranes, supporting the existing “broken-helix” model for α-synuclein/membrane interactions, but do not detect a “helical extension” that is also thought to play a role in αSN aggregation.
Author Wilson, Derek J
Oganesyan, Irina
Lento, Cristina
Tandon, Anurag
AuthorAffiliation Department of Chemistry
Centre for Research in Mass Spectrometry
Department of Medicine
University of Toronto
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33784451$$D View this record in MEDLINE/PubMed
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Keywords phospholipids nanodiscs
mass spectrometry
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α-synuclein
Parkinson’s disease
hydrogen−deuterium exchange
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Snippet Both normal and pathological functions of α-synuclein (αSN), an abundant protein in the central and peripheral nervous system, have been linked to its...
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Title Conformational Dynamics of α‑Synuclein during the Interaction with Phospholipid Nanodiscs by Millisecond Hydrogen–Deuterium Exchange Mass Spectrometry
URI http://dx.doi.org/10.1021/jasms.0c00463
https://www.ncbi.nlm.nih.gov/pubmed/33784451
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Volume 32
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