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Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow

A reduced removal of dysfunctional mitochondria is common to aging and age-related neurodegenerative pathologies such as Alzheimer’s disease (AD). Strategies for treating such impaired mitophagy would benefit from the identification of mitophagy modulators. Here we report the combined use of unsuper...

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Autores principales: Xie, Chenglong, Zhuang, Xu-Xu, Niu, Zhangming, Ai, Ruixue, Lautrup, Sofie, Zheng, Shuangjia, Jiang, Yinghui, Han, Ruiyu, Gupta, Tanima Sen, Cao, Shuqin, Lagartos-Donate, Maria Jose, Cai, Cui-Zan, Xie, Li-Ming, Caponio, Domenica, Wang, Wen-Wen, Schmauck-Medina, Tomas, Zhang, Jianying, Wang, He-ling, Lou, Guofeng, Xiao, Xianglu, Zheng, Wenhua, Palikaras, Konstantinos, Yang, Guang, Caldwell, Kim A., Caldwell, Guy A., Shen, Han-Ming, Nilsen, Hilde, Lu, Jia-Hong, Fang, Evandro F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8782726/
https://www.ncbi.nlm.nih.gov/pubmed/34992270
http://dx.doi.org/10.1038/s41551-021-00819-5
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author Xie, Chenglong
Zhuang, Xu-Xu
Niu, Zhangming
Ai, Ruixue
Lautrup, Sofie
Zheng, Shuangjia
Jiang, Yinghui
Han, Ruiyu
Gupta, Tanima Sen
Cao, Shuqin
Lagartos-Donate, Maria Jose
Cai, Cui-Zan
Xie, Li-Ming
Caponio, Domenica
Wang, Wen-Wen
Schmauck-Medina, Tomas
Zhang, Jianying
Wang, He-ling
Lou, Guofeng
Xiao, Xianglu
Zheng, Wenhua
Palikaras, Konstantinos
Yang, Guang
Caldwell, Kim A.
Caldwell, Guy A.
Shen, Han-Ming
Nilsen, Hilde
Lu, Jia-Hong
Fang, Evandro F.
author_facet Xie, Chenglong
Zhuang, Xu-Xu
Niu, Zhangming
Ai, Ruixue
Lautrup, Sofie
Zheng, Shuangjia
Jiang, Yinghui
Han, Ruiyu
Gupta, Tanima Sen
Cao, Shuqin
Lagartos-Donate, Maria Jose
Cai, Cui-Zan
Xie, Li-Ming
Caponio, Domenica
Wang, Wen-Wen
Schmauck-Medina, Tomas
Zhang, Jianying
Wang, He-ling
Lou, Guofeng
Xiao, Xianglu
Zheng, Wenhua
Palikaras, Konstantinos
Yang, Guang
Caldwell, Kim A.
Caldwell, Guy A.
Shen, Han-Ming
Nilsen, Hilde
Lu, Jia-Hong
Fang, Evandro F.
author_sort Xie, Chenglong
collection PubMed
description A reduced removal of dysfunctional mitochondria is common to aging and age-related neurodegenerative pathologies such as Alzheimer’s disease (AD). Strategies for treating such impaired mitophagy would benefit from the identification of mitophagy modulators. Here we report the combined use of unsupervised machine learning (involving vector representations of molecular structures, pharmacophore fingerprinting and conformer fingerprinting) and a cross-species approach for the screening and experimental validation of new mitophagy-inducing compounds. From a library of naturally occurring compounds, the workflow allowed us to identify 18 small molecules, and among them two potent mitophagy inducers (Kaempferol and Rhapontigenin). In nematode and rodent models of AD, we show that both mitophagy inducers increased the survival and functionality of glutamatergic and cholinergic neurons, abrogated amyloid-β and tau pathologies, and improved the animals’ memory. Our findings suggest the existence of a conserved mechanism of memory loss across the AD models, this mechanism being mediated by defective mitophagy. The computational–experimental screening and validation workflow might help uncover potent mitophagy modulators that stimulate neuronal health and brain homeostasis.
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spelling pubmed-87827262022-02-04 Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow Xie, Chenglong Zhuang, Xu-Xu Niu, Zhangming Ai, Ruixue Lautrup, Sofie Zheng, Shuangjia Jiang, Yinghui Han, Ruiyu Gupta, Tanima Sen Cao, Shuqin Lagartos-Donate, Maria Jose Cai, Cui-Zan Xie, Li-Ming Caponio, Domenica Wang, Wen-Wen Schmauck-Medina, Tomas Zhang, Jianying Wang, He-ling Lou, Guofeng Xiao, Xianglu Zheng, Wenhua Palikaras, Konstantinos Yang, Guang Caldwell, Kim A. Caldwell, Guy A. Shen, Han-Ming Nilsen, Hilde Lu, Jia-Hong Fang, Evandro F. Nat Biomed Eng Article A reduced removal of dysfunctional mitochondria is common to aging and age-related neurodegenerative pathologies such as Alzheimer’s disease (AD). Strategies for treating such impaired mitophagy would benefit from the identification of mitophagy modulators. Here we report the combined use of unsupervised machine learning (involving vector representations of molecular structures, pharmacophore fingerprinting and conformer fingerprinting) and a cross-species approach for the screening and experimental validation of new mitophagy-inducing compounds. From a library of naturally occurring compounds, the workflow allowed us to identify 18 small molecules, and among them two potent mitophagy inducers (Kaempferol and Rhapontigenin). In nematode and rodent models of AD, we show that both mitophagy inducers increased the survival and functionality of glutamatergic and cholinergic neurons, abrogated amyloid-β and tau pathologies, and improved the animals’ memory. Our findings suggest the existence of a conserved mechanism of memory loss across the AD models, this mechanism being mediated by defective mitophagy. The computational–experimental screening and validation workflow might help uncover potent mitophagy modulators that stimulate neuronal health and brain homeostasis. Nature Publishing Group UK 2022-01-06 2022 /pmc/articles/PMC8782726/ /pubmed/34992270 http://dx.doi.org/10.1038/s41551-021-00819-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Xie, Chenglong
Zhuang, Xu-Xu
Niu, Zhangming
Ai, Ruixue
Lautrup, Sofie
Zheng, Shuangjia
Jiang, Yinghui
Han, Ruiyu
Gupta, Tanima Sen
Cao, Shuqin
Lagartos-Donate, Maria Jose
Cai, Cui-Zan
Xie, Li-Ming
Caponio, Domenica
Wang, Wen-Wen
Schmauck-Medina, Tomas
Zhang, Jianying
Wang, He-ling
Lou, Guofeng
Xiao, Xianglu
Zheng, Wenhua
Palikaras, Konstantinos
Yang, Guang
Caldwell, Kim A.
Caldwell, Guy A.
Shen, Han-Ming
Nilsen, Hilde
Lu, Jia-Hong
Fang, Evandro F.
Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow
title Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow
title_full Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow
title_fullStr Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow
title_full_unstemmed Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow
title_short Amelioration of Alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow
title_sort amelioration of alzheimer’s disease pathology by mitophagy inducers identified via machine learning and a cross-species workflow
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8782726/
https://www.ncbi.nlm.nih.gov/pubmed/34992270
http://dx.doi.org/10.1038/s41551-021-00819-5
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