Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life Cycle

A recently developed artemisinin-quinoline hybrid, named 163A, has been shown to display potent activity against the asexual blood stage of <i>Plasmodium</i>, the malaria parasite. In this study, we determined its in vitro cytotoxicity to mammalian cells, its potency to suppress <i>...

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Main Authors: Helenita C. Quadros, Aysun Çapcı, Lars Herrmann, Sarah D’Alessandro, Diana Fontinha, Raquel Azevedo, Wilmer Villarreal, Nicoletta Basilico, Miguel Prudêncio, Svetlana B. Tsogoeva, Diogo R. M. Moreira
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Pharmaceuticals
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Online Access:https://www.mdpi.com/1424-8247/14/11/1129
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author Helenita C. Quadros
Aysun Çapcı
Lars Herrmann
Sarah D’Alessandro
Diana Fontinha
Raquel Azevedo
Wilmer Villarreal
Nicoletta Basilico
Miguel Prudêncio
Svetlana B. Tsogoeva
Diogo R. M. Moreira
author_facet Helenita C. Quadros
Aysun Çapcı
Lars Herrmann
Sarah D’Alessandro
Diana Fontinha
Raquel Azevedo
Wilmer Villarreal
Nicoletta Basilico
Miguel Prudêncio
Svetlana B. Tsogoeva
Diogo R. M. Moreira
author_sort Helenita C. Quadros
collection DOAJ
description A recently developed artemisinin-quinoline hybrid, named 163A, has been shown to display potent activity against the asexual blood stage of <i>Plasmodium</i>, the malaria parasite. In this study, we determined its in vitro cytotoxicity to mammalian cells, its potency to suppress <i>P. berghei</i> hepatic infection and to decrease the viability of <i>P. falciparum</i> gametocytes, in addition to determining whether the drug exhibits efficacy of a <i>P. berghei</i> infection in mice. This hybrid compound has a low level of cytotoxicity to mammalian cells and, conversely, a high level of selectivity. It is potent in the prevention of hepatic stage development as well as in killing gametocytes, denoting a potential blockage of malaria transmission. The hybrid presents a potent inhibitory activity for beta-hematin crystal formation, in which subsequent assays revealed that its endoperoxide component undergoes bioactivation by reductive reaction with ferrous heme towards the formation of heme-drug adducts; in parallel, the 7-chloroquinoline component has binding affinity for ferric hemin. Both structural components of the hybrid co-operate to enhance the inhibition of beta-hematin, and this bitopic ligand property is essential for arresting the growth of asexual blood parasites. We demonstrated the in vivo efficacy of the hybrid as an erythrocytic schizonticide agent in comparison to a chloroquine/artemisinin combination therapy. Collectively, the findings suggest that the bitopic property of the hybrid is highly operative on heme detoxification suppression, and this provides compelling evidence for explaining the action of the hybrid on the asexual blood stage. For sporozoite and gametocyte stages, the hybrid conserves the potency typically observed for endoperoxide drugs, and this is possibly achieved due to the redox chemistry of endoperoxide components with ferrous heme.
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spelling doaj.art-0c90374b919e4727a3854b15ff3c116b2023-11-23T00:55:40ZengMDPI AGPharmaceuticals1424-82472021-11-011411112910.3390/ph14111129Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life CycleHelenita C. Quadros0Aysun Çapcı1Lars Herrmann2Sarah D’Alessandro3Diana Fontinha4Raquel Azevedo5Wilmer Villarreal6Nicoletta Basilico7Miguel Prudêncio8Svetlana B. Tsogoeva9Diogo R. M. Moreira10Instituto Gonçalo Moniz, Fundação Oswaldo Cruz (Fiocruz), Salvador 40296-710, BrazilOrganic Chemistry Chair I and Interdisciplinary Center for Molecular Materials (ICMM), Friedrich-Alexander University of Erlangen-Nürnberg, Nikolaus Fiebiger-Straße 10, 91058 Erlangen, GermanyOrganic Chemistry Chair I and Interdisciplinary Center for Molecular Materials (ICMM), Friedrich-Alexander University of Erlangen-Nürnberg, Nikolaus Fiebiger-Straße 10, 91058 Erlangen, GermanyDipartimento di Scienze Farmacologiche e Biomolecolari, Università degli Studi di Milano, 20133 Milan, ItalyInstituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028 Lisboa, PortugalInstituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028 Lisboa, PortugalGrupo de Química Inorgânica Medicinal e Reações Aplicadas, Instituto de Química, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre 91501-970, BrazilDipartimento di Scienze Biomediche, Chirurgiche e Odontoiatriche, Universitá degli Studi di Milano, 20133 Milan, ItalyInstituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028 Lisboa, PortugalOrganic Chemistry Chair I and Interdisciplinary Center for Molecular Materials (ICMM), Friedrich-Alexander University of Erlangen-Nürnberg, Nikolaus Fiebiger-Straße 10, 91058 Erlangen, GermanyInstituto Gonçalo Moniz, Fundação Oswaldo Cruz (Fiocruz), Salvador 40296-710, BrazilA recently developed artemisinin-quinoline hybrid, named 163A, has been shown to display potent activity against the asexual blood stage of <i>Plasmodium</i>, the malaria parasite. In this study, we determined its in vitro cytotoxicity to mammalian cells, its potency to suppress <i>P. berghei</i> hepatic infection and to decrease the viability of <i>P. falciparum</i> gametocytes, in addition to determining whether the drug exhibits efficacy of a <i>P. berghei</i> infection in mice. This hybrid compound has a low level of cytotoxicity to mammalian cells and, conversely, a high level of selectivity. It is potent in the prevention of hepatic stage development as well as in killing gametocytes, denoting a potential blockage of malaria transmission. The hybrid presents a potent inhibitory activity for beta-hematin crystal formation, in which subsequent assays revealed that its endoperoxide component undergoes bioactivation by reductive reaction with ferrous heme towards the formation of heme-drug adducts; in parallel, the 7-chloroquinoline component has binding affinity for ferric hemin. Both structural components of the hybrid co-operate to enhance the inhibition of beta-hematin, and this bitopic ligand property is essential for arresting the growth of asexual blood parasites. We demonstrated the in vivo efficacy of the hybrid as an erythrocytic schizonticide agent in comparison to a chloroquine/artemisinin combination therapy. Collectively, the findings suggest that the bitopic property of the hybrid is highly operative on heme detoxification suppression, and this provides compelling evidence for explaining the action of the hybrid on the asexual blood stage. For sporozoite and gametocyte stages, the hybrid conserves the potency typically observed for endoperoxide drugs, and this is possibly achieved due to the redox chemistry of endoperoxide components with ferrous heme.https://www.mdpi.com/1424-8247/14/11/1129malaria<i>Plasmodium</i>hemozoinheterobivalentartemisininhybrids
spellingShingle Helenita C. Quadros
Aysun Çapcı
Lars Herrmann
Sarah D’Alessandro
Diana Fontinha
Raquel Azevedo
Wilmer Villarreal
Nicoletta Basilico
Miguel Prudêncio
Svetlana B. Tsogoeva
Diogo R. M. Moreira
Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life Cycle
Pharmaceuticals
malaria
<i>Plasmodium</i>
hemozoin
heterobivalent
artemisinin
hybrids
title Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life Cycle
title_full Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life Cycle
title_fullStr Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life Cycle
title_full_unstemmed Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life Cycle
title_short Studies of Potency and Efficacy of an Optimized Artemisinin-Quinoline Hybrid against Multiple Stages of the <i>Plasmodium</i> Life Cycle
title_sort studies of potency and efficacy of an optimized artemisinin quinoline hybrid against multiple stages of the i plasmodium i life cycle
topic malaria
<i>Plasmodium</i>
hemozoin
heterobivalent
artemisinin
hybrids
url https://www.mdpi.com/1424-8247/14/11/1129
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