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A novel peptide‐based tau aggregation inhibitor as a potential therapeutic for Alzheimer's disease and other tauopathies

A novel peptide‐based tau aggregation inhibitor as a potential therapeutic for Alzheimer's disease and other tauopathies
A novel peptide‐based tau aggregation inhibitor as a potential therapeutic for Alzheimer's disease and other tauopathies

INTRODUCTION: As aggregation underpins Tau toxicity, aggregation inhibitor peptides may have disease-modifying potential. They are therefore currently being designed and target either the 306VQIVYK 311 aggregation-promoting hotspot found in all Tau isoforms or the 275VQIINK 280 aggregation-promoting hotspot found in 4R isoforms. However, for any Tau aggregation inhibitor to potentially be clinically relevant for other tauopathies, it should target both hotspots to suppress aggregation of Tau isoforms, be stable, cross the blood-brain barrier, and rescue aggregation-dependent Tau phenotypes in vivo. METHODS: We developed a retro-inverso, stable D-amino peptide, RI-AG03 [Ac-rrrrrrrrGpkyk(ac)iqvGr-NH2], based on the 306VQIVYK 311 hotspots which exhibit these disease-relevant attributes. RESULTS: Unlike other aggregation inhibitors, RI-AG03 effectively suppresses aggregation of multiple Tau species containing both hotspots in vitro and in vivo, is non-toxic, and suppresses aggregation-dependent neurodegenerative and behavioral phenotypes. DISCUSSION: RI-AG03 therefore meets many clinically relevant requirements for an anti-aggregation Tau therapeutic and should be explored further for its disease-modifying potential for Tauopathies. Highlights: Our manuscript describes the development of a novel peptide inhibitor of Tau aggregation, a retro-inverso, stable D-amino peptide called RI-AG03 that displays many clinically relevant attributes. We show its efficacy in preventing Tau aggregation in both in vitro and in vivo experimental models while being non-toxic to cells. RI-AG03 also rescues a biosensor cell line that stably expresses Tau repeat domains with the P301S mutation fused to Cer/Clo and rescues aggregation-dependent phenotypes in vivo, suppressing neurodegeneration and extending lifespan. Collectively our data describe several properties and attributes of RI-AG03 that make it a promising disease-modifying candidate to explore for reducing pathogenic Tau aggregation in Tauopathies such as Alzheimer's disease. Given the real interest in reducing Tau aggregation and the potential clinical benefit of using such agents in clinical practice, RI-AG03 should be investigated further for the treatment of Tauopathies after validation in mammalian models. Tau aggregation inhibitors are the obvious first choice as Tau-based therapies as much of Tau-mediated toxicity is aggregation dependent. Indeed, there are many research efforts focusing on this therapeutic strategy with aggregation inhibitors being designed against one of the two aggregation-promoting hotspots of the Tau protein. To our knowledge, RI-AG03 is the only peptide aggregation inhibitor that inhibits aggregation of Tau by targeting both aggregation-promoting hotspot motifs simultaneously. As such, we believe that our study will have a significant impact on drug discovery efforts in this arena.

Alzheimer's disease, Drosophila, VQIINK, VQIVYK, aggregation, amino-acid, dementia, drug development, in silico, in vitro, in vivo, inhibitor, melanogaster, peptide, tau, tauopathies, therapeutic
1552-5260
7788-7804
Aggidis, Anthony
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Devitt, George
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Zhang, Yongrui
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Chatterjee, Shreyasi
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Townsend, David
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Fullwood, Nigel James
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Ruiz-Ortega, Eva Daniela
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Tarutani, Airi
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Hasegawa, Masato
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Cooper, Amber
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Williamson, Philip T.F.
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Mendoza-Oliva, Ayde
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Diamond, Marc
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Mudher, Amritpal
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Allsop, David
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Aggidis, Anthony
fe18cad3-96e3-410a-a205-6ae142bf6543
Devitt, George
088c46c0-9dcf-4c83-acfd-16c6c9d0ca88
Zhang, Yongrui
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Chatterjee, Shreyasi
8794dd52-b2da-42cb-ac03-374fe00214d6
Townsend, David
7dce2ccc-059f-452f-8929-9fa8b9bdd2f0
Fullwood, Nigel James
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Ruiz-Ortega, Eva Daniela
0733ab6e-0574-42ac-9a79-d35482df9da8
Tarutani, Airi
c3144843-2cb3-45b6-9c17-6ce29920bb30
Hasegawa, Masato
c4d04d0a-79df-4def-93d5-72dd74967c1f
Cooper, Amber
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Williamson, Philip T.F.
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Mendoza-Oliva, Ayde
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Diamond, Marc
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Mudher, Amritpal
ce0ccb35-ac49-4b6c-92b4-8dd5e78ac119
Allsop, David
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Aggidis, Anthony, Devitt, George, Zhang, Yongrui, Chatterjee, Shreyasi, Townsend, David, Fullwood, Nigel James, Ruiz-Ortega, Eva Daniela, Tarutani, Airi, Hasegawa, Masato, Cooper, Amber, Williamson, Philip T.F., Mendoza-Oliva, Ayde, Diamond, Marc, Mudher, Amritpal and Allsop, David (2024) A novel peptide‐based tau aggregation inhibitor as a potential therapeutic for Alzheimer's disease and other tauopathies. Alzheimer's & Dementia, 20 (11), 7788-7804. (doi:10.1002/alz.14246).

Record type: Article

Abstract

INTRODUCTION: As aggregation underpins Tau toxicity, aggregation inhibitor peptides may have disease-modifying potential. They are therefore currently being designed and target either the 306VQIVYK 311 aggregation-promoting hotspot found in all Tau isoforms or the 275VQIINK 280 aggregation-promoting hotspot found in 4R isoforms. However, for any Tau aggregation inhibitor to potentially be clinically relevant for other tauopathies, it should target both hotspots to suppress aggregation of Tau isoforms, be stable, cross the blood-brain barrier, and rescue aggregation-dependent Tau phenotypes in vivo. METHODS: We developed a retro-inverso, stable D-amino peptide, RI-AG03 [Ac-rrrrrrrrGpkyk(ac)iqvGr-NH2], based on the 306VQIVYK 311 hotspots which exhibit these disease-relevant attributes. RESULTS: Unlike other aggregation inhibitors, RI-AG03 effectively suppresses aggregation of multiple Tau species containing both hotspots in vitro and in vivo, is non-toxic, and suppresses aggregation-dependent neurodegenerative and behavioral phenotypes. DISCUSSION: RI-AG03 therefore meets many clinically relevant requirements for an anti-aggregation Tau therapeutic and should be explored further for its disease-modifying potential for Tauopathies. Highlights: Our manuscript describes the development of a novel peptide inhibitor of Tau aggregation, a retro-inverso, stable D-amino peptide called RI-AG03 that displays many clinically relevant attributes. We show its efficacy in preventing Tau aggregation in both in vitro and in vivo experimental models while being non-toxic to cells. RI-AG03 also rescues a biosensor cell line that stably expresses Tau repeat domains with the P301S mutation fused to Cer/Clo and rescues aggregation-dependent phenotypes in vivo, suppressing neurodegeneration and extending lifespan. Collectively our data describe several properties and attributes of RI-AG03 that make it a promising disease-modifying candidate to explore for reducing pathogenic Tau aggregation in Tauopathies such as Alzheimer's disease. Given the real interest in reducing Tau aggregation and the potential clinical benefit of using such agents in clinical practice, RI-AG03 should be investigated further for the treatment of Tauopathies after validation in mammalian models. Tau aggregation inhibitors are the obvious first choice as Tau-based therapies as much of Tau-mediated toxicity is aggregation dependent. Indeed, there are many research efforts focusing on this therapeutic strategy with aggregation inhibitors being designed against one of the two aggregation-promoting hotspots of the Tau protein. To our knowledge, RI-AG03 is the only peptide aggregation inhibitor that inhibits aggregation of Tau by targeting both aggregation-promoting hotspot motifs simultaneously. As such, we believe that our study will have a significant impact on drug discovery efforts in this arena.

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Accepted/In Press date: 13 August 2024
Published date: 3 October 2024
Additional Information: © 2024 The Author(s). Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.
Keywords: Alzheimer's disease, Drosophila, VQIINK, VQIVYK, aggregation, amino-acid, dementia, drug development, in silico, in vitro, in vivo, inhibitor, melanogaster, peptide, tau, tauopathies, therapeutic

Identifiers

Local EPrints ID: 495993
URI: http://eprints.soton.ac.uk/id/eprint/495993
ISSN: 1552-5260
PURE UUID: 742ccac6-0ff1-4003-804e-cb2ef0beb6f4
ORCID for George Devitt: ORCID iD orcid.org/0000-0001-7179-4459
ORCID for Philip T.F. Williamson: ORCID iD orcid.org/0000-0002-0231-8640

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Date deposited: 28 Nov 2024 17:53
Last modified: 30 Nov 2024 03:03

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Contributors

Author: Anthony Aggidis
Author: George Devitt ORCID iD
Author: Yongrui Zhang
Author: Shreyasi Chatterjee
Author: David Townsend
Author: Nigel James Fullwood
Author: Airi Tarutani
Author: Masato Hasegawa
Author: Amber Cooper
Author: Ayde Mendoza-Oliva
Author: Marc Diamond
Author: Amritpal Mudher
Author: David Allsop

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