The role of hydrophobic collapse in cytotoxic and functional amyloid oligomerization

疏水塌缩在细胞毒性和功能性淀粉样蛋白寡聚化中的作用

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Abstract

"Amyloid" refers to an insoluble, highly organized protein fibril composed of intermolecular β sheets, known as a cross-β motif. Amyloidogenic proteins are generally driven to aggregate into tightly packed fibrils. Some amyloids are functional, often being utilized as hormone storage reservoirs. The functional, paracrine signaling neuropeptide β-endorphin (βE) is stored and released to modulate pain responses. Conversely, the function of amyloid-β (Aβ), involved in Alzheimer's disease, is uncertain-but substantial evidence exists of its role in neuronal cell apoptosis. Although both peptides are mechanistically linked in their propensity to adopt fibrillar structures, the biophysical characteristics that drive divergence in cytotoxic potential are not well understood. To probe the conformational dynamics and mechanisms of functional and cytotoxic oligomer formation, we utilized all-atom molecular dynamics to simulate the formation of monomeric and hexameric Aβ(42) and βE(31). Monomeric Aβ(42) and βE(31) selectively sampled β strand motifs comprising hydrophobic residues, adopting a collapsed state. Cluster analysis indicates that βE(31) hexamers were more conformationally diverse than those sampled by Aβ(42), suggesting that βE(31) exhibits more signatures of disorder. Aβ(42) hexamer formation was driven by hydrophobic packing of collapsed β strand motifs, where βE(31) hexamer peptide subunits remained structurally plastic and solvent accessible. Mutation of Aβ(42) disrupting the C-terminal hydrophobic sequence inhibited hydrophobic β strand formation, reduced aggregation propensity, and increased solvent accessibility, suggesting that retention of a collapsed state is critical for aberrant oligomer formation. This work provides a preliminary view of cytotoxic and functional oligomer morphologies at atomistic resolution, gaining insights into the biophysical aspects of early aggregation events of amyloids.

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