Amyloid-Membrane Interactions in Protein Misfolding Disorders: from Basic Mechanisms to Therapy

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Background

It is now well established that the aberrant conversion of peptides or proteins from their native functional states into toxic amyloid entities underlies the pathogenesis of a wide range of debilitating human diseases, collectively known as protein misfolding disorders (PMDs). A large body of evidence indicates that one of the main pathogenic factors in PMDs involves the interaction of amyloidogenic proteins with biomembranes. On the one hand, the two-dimensional surface and composition of a lipid membrane may strongly influence the misfolding and aggregation of amyloidogenic proteins into toxic structures. On the other, pathogenic molecular forms of amyloid proteins (typically, oligomeric assemblies) may directly compromise and disrupt the integrity of lipid membranes, via molecular mechanisms that are often reminiscent of antimicrobial peptides. Thus, underlying the cytotoxicity of amyloid peptides is a complex interplay of physico-pathologic mechanisms between the misfolded proteins and lipid biomembranes.

Most studies addressing the interaction of amyloidogenic proteins with lipid species in PMDs have made use of simple, model membrane systems. An important goal is therefore to understand how amyloid proteins behave in the presence of lipid compositions that more faithfully recapitulate the complex lipid constituents of cellular and organelle membranes, such as mitochondrial membranes. Of particular importance here are specific anionic lipids (e.g. cardiolipin), cholesterol, gangliosides and lipid rafts. Moreover, we need to elucidate those key structural elements that enable promiscuity of protein aggregates to bind and perturb biological membranes. We also need direct evidence that misfolded protein-membrane interactions are relevant to disease pathogenesis in vivo, including animal models. Delivering answers to these key questions will allow not only a detailed understanding of fundamental mechanisms, but will also be critical for our ability to identify novel therapeutic strategies aimed at targeting amyloidogenic protein-biomembrane interactions.

To date, more than 50 amyloidogenic proteins or peptides have been shown to cause PMDs – the most common diseases include amyloid-β and tau in Alzheimer’s disease, α-synuclein in Parkinson’s disease, and the islet amyloid polypeptide in type-2 Diabetes Mellitus. The focus of this Research Topic is on the aberrant interactions between amyloid protein species and biological membranes, and their role in the pathogenesis of PMDs. Relevant studies are therefore those providing valuable insights into the mechanisms and consequences of amyloidogenic protein-biomembrane interactions. Studies may also address the development of effective therapeutic strategies aimed at inhibiting amyloid protein aggregation and toxicity in the presence of a phospholipid interface. Valuable contributions may utilize computational approaches, in vitro reconstituted biomimetic systems, as well as in vivo cell biology and transgenic animal models. Original Research, Brief reports, Methods, Review and Mini-Review articles are welcome.

Important note: All contributions to this Research Topic must be within the scope of the section and journal to which they are submitted, as defined in their mission statements. Frontiers reserves the right to guide an out-of-scope manuscript to a more suitable section or journal at any stage of peer review.

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