Published February 16, 2022 | Version Supplemental Material
Journal Article Open

Extended β-Strands Contribute to Reversible Amyloid Formation

Abstract

The assembly of proteins into fibrillar amyloid structures was once considered to be pathologic and essentially irreversible. Recent studies reveal amyloid-like structures that form reversibly, derived from protein low-complexity domains which function in cellular metabolism. Here, by comparing atomic-level structures of reversible and irreversible amyloid fibrils, we find that the β-sheets of reversible fibrils are enriched in flattened (as opposed to pleated) β-sheets formed by stacking of extended β-strands. Quantum mechanical calculations show that glycine residues favor extended β-strands which may be stabilized by intraresidue interactions between the amide proton and the carbonyl oxygen, known as C5 hydrogen-bonds. Larger residue side chains favor shorter strands and pleated sheets. These findings highlight a structural element that may regulate reversible amyloid assembly.

Additional Information

© 2022 American Chemical Society. Received: September 13, 2021; Accepted: January 14, 2022; Published: February 8, 2022. KAM is supported by the UCLA-Caltech Medical Scientist Training Program (GM08042). KAM and DE are supported by the UCLA Chemistry-Biology Interface training grant (USPHS National Research Service Award 5T32GM008496). We thank Duilio Cascio and the UCLA DOE Macromolecular Crystallization Core facility. Funding for this work is provided by the Howard Hughes Medical Institute and NIH. This work is based upon research conducted at the Northeastern Collaborative Access Team beamlines, which are funded by the National Institute of General Medical Sciences from the National Institutes of Health (P30 GM124165). The Eiger 16M detector on the 24-ID-E beamline is funded by a NIH-ORIP HEI grant (S10OD021527). This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. We also thank NIH AG 054022, AG070895, and AG 048120 and DOE DE-FC02-02ER63421 for support. Author Contributions. Project was conceived and designed by KAM and DEisenberg. KAM performed structure analysis with assistance from CJH. DEvans carried out all quantum calculations, with guidance from KNH. MPH wrote script to calculate atomic distances. MPH and MRS crystallized and determined the Nup54 structure. Manuscript was written by KAM and DEisenberg with contributions from all other authors. All images for main text and supplemental figures were created in their entirety by KAM and DEvans. KAM and DEvans contributed equally. The authors declare the following competing financial interest(s): DSE is a SAB chair and equity holder of ADRx, Inc.

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Additional details

Identifiers

Eprint ID
113333
Resolver ID
CaltechAUTHORS:20220208-948240000

Funding

NIH Predoctoral Fellowship
GM08042
NIH Predoctoral Fellowship
5T32GM008496
Howard Hughes Medical Institute (HHMI)
NIH
P30 GM124165
NIH
S10OD021527
Department of Energy (DOE)
DE-AC02-06CH11357
NIH
AG 054022
NIH
AG 070895
NIH
AG 048120
Department of Energy (DOE)
DE-FC02-02ER63421

Dates

Created
2022-02-08
Created from EPrint's datestamp field
Updated
2022-03-10
Created from EPrint's last_modified field