Structural convergence and membrane interactions of Aβ1-42 along the primary nucleation process studied by solid state NMR

Abstract Non-specific disruption of cellular membranes induced by amyloidogenic aggregation of β-amyloid (Aβ) peptides remains a viable cytotoxicity mechanism in Alzheimer’s disease (AD). Obtaining structural information about the intermediate states of Aβ-membrane systems and their molecular intera...

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Main Authors: Maurine K. Kengwerere, June M. Kenyaga, Peng Xiao, Shubha S. Gunaga, Faith J. Scott, Xyomara Wutoh-Hughes, James Wang, Brian Lum, Yan Sun, Frederic Mentink-Vigier, Tuo Wang, Wei Qiang
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Communications Chemistry
Online Access:https://doi.org/10.1038/s42004-025-01537-8
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Summary:Abstract Non-specific disruption of cellular membranes induced by amyloidogenic aggregation of β-amyloid (Aβ) peptides remains a viable cytotoxicity mechanism in Alzheimer’s disease (AD). Obtaining structural information about the intermediate states of Aβ-membrane systems and their molecular interactions is challenging due to their heterogeneity and low abundance. Here, we systematically study the molecular interactions of membrane-associated Aβ1-42 peptides using solid-state nuclear magnetic resonance (ssNMR) spectroscopy, focusing on the primary nucleation phase of the fibrillation process. Compared to the less pathogenic Aβ1-40 peptide, Aβ1-42 forms smaller oligomers prior to fibrillation, as evidenced by a higher overall population of lipid-proximity peptides. Aβ1-42 also exhibits more pronounced residue-specific contacts with phospholipid headgroups compared to Aβ1-40, with multiple lipid-proximity segments throughout the entire primary sequence. The segments involved in initial inter-strand assembly overlap with those located near the lipid headgroups in Aβ1-42, whereas these two segments are distinct in Aβ1-40. ssNMR spectroscopy with sensitivity enhanced by Dynamic nuclear polarization (DNP) confirmed local secondary structural convergence during the nucleation process of Aβ1-42 and the presence of long-range tertiary contacts at early stages of nucleation. Overall, our results provide a molecular-level understanding of the Aβ1-42 nucleation process in a membrane-like environment and its membrane-disrupting intermediates. The comparison between Aβ1-42 and Aβ1-40 explains its higher cytotoxicity from the perspective of membrane disruption.
ISSN:2399-3669