Serine phosphorylation mimics of Aβ form distinct, non-cross-seeding fibril morphs
(2024) In Chemical Science 15(45). p.19142-19159- Abstract
The self-assembly of amyloid-β peptide (Aβ) into fibrils and oligomers is linked to Alzheimer's disease (AD). Fibrillar aggregates in AD patient's brains contain several post-translational modifications, including phosphorylation at positions 8 and 26. These play a key role in modifying the aggregation propensity of Aβ, yet how they affect the mechanism of aggregation is only poorly understood. Here we elucidate the aggregation mechanism of Aβ42 peptides with phosphomimic mutations at these positions, with glutamine mimicking the size, and glutamate mimicking both the size and charge effect. We find that all variants are less aggregation-prone than wild-type Aβ42 with the glutamate mutants showing the largest reduction. Secondary... (More)
The self-assembly of amyloid-β peptide (Aβ) into fibrils and oligomers is linked to Alzheimer's disease (AD). Fibrillar aggregates in AD patient's brains contain several post-translational modifications, including phosphorylation at positions 8 and 26. These play a key role in modifying the aggregation propensity of Aβ, yet how they affect the mechanism of aggregation is only poorly understood. Here we elucidate the aggregation mechanism of Aβ42 peptides with phosphomimic mutations at these positions, with glutamine mimicking the size, and glutamate mimicking both the size and charge effect. We find that all variants are less aggregation-prone than wild-type Aβ42 with the glutamate mutants showing the largest reduction. Secondary nucleation is the dominant nucleation route for all variants, as confirmed using seeding experiments; however, its rate is reduced by about an order of magnitude or more for all variants relative to wild-type. S26Q and S26E fibrils fail to catalyse nucleation of wild-type monomers and vice versa, while the S8 variants co-aggregate more readily with wild-type. Ultrastructural analyses by cryo-electron microscopy and small angle X-ray scattering reveal an altered structure with longer node-to-node distance and smaller cross-section dimensions of S26Q fibrils. These results imply that structural compatibility between fibrils and monomer is a key determinant in secondary nucleation, and that small modifications can alter the preferred fibril structure, and thus its potential to induce aggregation of other variants. Overall, our results indicate that phosphorylation could play a key role in controlling aggregation propensity and may lead to the formation of distinct, non-cross-seeding fibril populations.
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- author
- Sanagavarapu, Kalyani LU ; Meisl, Georg ; Lattanzi, Veronica LU ; Bernfur, Katja LU ; Frohm, Birgitta LU ; Olsson, Ulf LU ; Knowles, Tuomas P.J. ; Malmendal, Anders LU and Linse, Sara LU
- organization
-
- Biochemistry and Structural Biology
- MultiPark: Multidisciplinary research focused on Parkinson's disease
- Physical Chemistry
- Biophysical Chemistry
- NanoLund: Centre for Nanoscience
- LTH Profile Area: Nanoscience and Semiconductor Technology
- LU Profile Area: Proactive Ageing
- LU Profile Area: Light and Materials
- publishing date
- 2024-10-11
- type
- Contribution to journal
- publication status
- published
- subject
- in
- Chemical Science
- volume
- 15
- issue
- 45
- pages
- 18 pages
- publisher
- Royal Society of Chemistry
- external identifiers
-
- scopus:85208809780
- pmid:39494375
- ISSN
- 2041-6520
- DOI
- 10.1039/d3sc06343g
- language
- English
- LU publication?
- yes
- additional info
- Publisher Copyright: © 2024 The Royal Society of Chemistry.
- id
- df46f520-cf42-403f-aedc-e03c06230aee
- date added to LUP
- 2025-01-14 13:10:59
- date last changed
- 2025-07-02 03:19:39
@article{df46f520-cf42-403f-aedc-e03c06230aee, abstract = {{<p>The self-assembly of amyloid-β peptide (Aβ) into fibrils and oligomers is linked to Alzheimer's disease (AD). Fibrillar aggregates in AD patient's brains contain several post-translational modifications, including phosphorylation at positions 8 and 26. These play a key role in modifying the aggregation propensity of Aβ, yet how they affect the mechanism of aggregation is only poorly understood. Here we elucidate the aggregation mechanism of Aβ42 peptides with phosphomimic mutations at these positions, with glutamine mimicking the size, and glutamate mimicking both the size and charge effect. We find that all variants are less aggregation-prone than wild-type Aβ42 with the glutamate mutants showing the largest reduction. Secondary nucleation is the dominant nucleation route for all variants, as confirmed using seeding experiments; however, its rate is reduced by about an order of magnitude or more for all variants relative to wild-type. S26Q and S26E fibrils fail to catalyse nucleation of wild-type monomers and vice versa, while the S8 variants co-aggregate more readily with wild-type. Ultrastructural analyses by cryo-electron microscopy and small angle X-ray scattering reveal an altered structure with longer node-to-node distance and smaller cross-section dimensions of S26Q fibrils. These results imply that structural compatibility between fibrils and monomer is a key determinant in secondary nucleation, and that small modifications can alter the preferred fibril structure, and thus its potential to induce aggregation of other variants. Overall, our results indicate that phosphorylation could play a key role in controlling aggregation propensity and may lead to the formation of distinct, non-cross-seeding fibril populations.</p>}}, author = {{Sanagavarapu, Kalyani and Meisl, Georg and Lattanzi, Veronica and Bernfur, Katja and Frohm, Birgitta and Olsson, Ulf and Knowles, Tuomas P.J. and Malmendal, Anders and Linse, Sara}}, issn = {{2041-6520}}, language = {{eng}}, month = {{10}}, number = {{45}}, pages = {{19142--19159}}, publisher = {{Royal Society of Chemistry}}, series = {{Chemical Science}}, title = {{Serine phosphorylation mimics of Aβ form distinct, non-cross-seeding fibril morphs}}, url = {{http://dx.doi.org/10.1039/d3sc06343g}}, doi = {{10.1039/d3sc06343g}}, volume = {{15}}, year = {{2024}}, }