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Multivariate chemogenomic screening prioritizes new macrofilaricidal leads

Development of direct acting macrofilaricides for the treatment of human filariases is hampered by limitations in screening throughput imposed by the parasite life cycle. In vitro adult screens typically assess single phenotypes without prior enrichment for chemicals with antifilarial potential. We...

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Autores principales: Wheeler, Nicolas J., Ryan, Kaetlyn T., Gallo, Kendra J., Henthorn, Clair R., Ericksen, Spencer S., Chan, John D., Zamanian, Mostafa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9839782/
https://www.ncbi.nlm.nih.gov/pubmed/36639423
http://dx.doi.org/10.1038/s42003-023-04435-8
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author Wheeler, Nicolas J.
Ryan, Kaetlyn T.
Gallo, Kendra J.
Henthorn, Clair R.
Ericksen, Spencer S.
Chan, John D.
Zamanian, Mostafa
author_facet Wheeler, Nicolas J.
Ryan, Kaetlyn T.
Gallo, Kendra J.
Henthorn, Clair R.
Ericksen, Spencer S.
Chan, John D.
Zamanian, Mostafa
author_sort Wheeler, Nicolas J.
collection PubMed
description Development of direct acting macrofilaricides for the treatment of human filariases is hampered by limitations in screening throughput imposed by the parasite life cycle. In vitro adult screens typically assess single phenotypes without prior enrichment for chemicals with antifilarial potential. We developed a multivariate screen that identified dozens of compounds with submicromolar macrofilaricidal activity, achieving a hit rate of >50% by leveraging abundantly accessible microfilariae. Adult assays were multiplexed to thoroughly characterize compound activity across relevant parasite fitness traits, including neuromuscular control, fecundity, metabolism, and viability. Seventeen compounds from a diverse chemogenomic library elicited strong effects on at least one adult trait, with differential potency against microfilariae and adults. Our screen identified five compounds with high potency against adults but low potency or slow-acting microfilaricidal effects, at least one of which acts through a novel mechanism. We show that the use of microfilariae in a primary screen outperforms model nematode developmental assays and virtual screening of protein structures inferred with deep learning. These data provide new leads for drug development, and the high-content and multiplex assays set a new foundation for antifilarial discovery.
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spelling pubmed-98397822023-01-15 Multivariate chemogenomic screening prioritizes new macrofilaricidal leads Wheeler, Nicolas J. Ryan, Kaetlyn T. Gallo, Kendra J. Henthorn, Clair R. Ericksen, Spencer S. Chan, John D. Zamanian, Mostafa Commun Biol Article Development of direct acting macrofilaricides for the treatment of human filariases is hampered by limitations in screening throughput imposed by the parasite life cycle. In vitro adult screens typically assess single phenotypes without prior enrichment for chemicals with antifilarial potential. We developed a multivariate screen that identified dozens of compounds with submicromolar macrofilaricidal activity, achieving a hit rate of >50% by leveraging abundantly accessible microfilariae. Adult assays were multiplexed to thoroughly characterize compound activity across relevant parasite fitness traits, including neuromuscular control, fecundity, metabolism, and viability. Seventeen compounds from a diverse chemogenomic library elicited strong effects on at least one adult trait, with differential potency against microfilariae and adults. Our screen identified five compounds with high potency against adults but low potency or slow-acting microfilaricidal effects, at least one of which acts through a novel mechanism. We show that the use of microfilariae in a primary screen outperforms model nematode developmental assays and virtual screening of protein structures inferred with deep learning. These data provide new leads for drug development, and the high-content and multiplex assays set a new foundation for antifilarial discovery. Nature Publishing Group UK 2023-01-13 /pmc/articles/PMC9839782/ /pubmed/36639423 http://dx.doi.org/10.1038/s42003-023-04435-8 Text en © The Author(s) 2023 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
Wheeler, Nicolas J.
Ryan, Kaetlyn T.
Gallo, Kendra J.
Henthorn, Clair R.
Ericksen, Spencer S.
Chan, John D.
Zamanian, Mostafa
Multivariate chemogenomic screening prioritizes new macrofilaricidal leads
title Multivariate chemogenomic screening prioritizes new macrofilaricidal leads
title_full Multivariate chemogenomic screening prioritizes new macrofilaricidal leads
title_fullStr Multivariate chemogenomic screening prioritizes new macrofilaricidal leads
title_full_unstemmed Multivariate chemogenomic screening prioritizes new macrofilaricidal leads
title_short Multivariate chemogenomic screening prioritizes new macrofilaricidal leads
title_sort multivariate chemogenomic screening prioritizes new macrofilaricidal leads
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9839782/
https://www.ncbi.nlm.nih.gov/pubmed/36639423
http://dx.doi.org/10.1038/s42003-023-04435-8
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