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Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum

BACKGROUND: Besides feeding on blood, females of the malaria vector Anopheles gambiae sensu lato readily feed on natural sources of plant sugars. The impact of toxic secondary phytochemicals contained in plant-derived sugars on mosquito physiology and the development of Plasmodium parasites remains...

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Autores principales: Hien, Domonbabele F. D. S., Paré, Prisca S. L., Cooper, Amanda, Koama, Benjamin K., Guissou, Edwige, Yaméogo, Koudraogo B., Yerbanga, Rakiswendé S., Farrell, Iain W., Ouédraogo, Jean B., Gnankiné, Olivier, Ignell, Rickard, Cohuet, Anna, Dabiré, Roch K., Stevenson, Philip C., Lefèvre, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8444468/
https://www.ncbi.nlm.nih.gov/pubmed/34526119
http://dx.doi.org/10.1186/s13071-021-04992-z
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author Hien, Domonbabele F. D. S.
Paré, Prisca S. L.
Cooper, Amanda
Koama, Benjamin K.
Guissou, Edwige
Yaméogo, Koudraogo B.
Yerbanga, Rakiswendé S.
Farrell, Iain W.
Ouédraogo, Jean B.
Gnankiné, Olivier
Ignell, Rickard
Cohuet, Anna
Dabiré, Roch K.
Stevenson, Philip C.
Lefèvre, Thierry
author_facet Hien, Domonbabele F. D. S.
Paré, Prisca S. L.
Cooper, Amanda
Koama, Benjamin K.
Guissou, Edwige
Yaméogo, Koudraogo B.
Yerbanga, Rakiswendé S.
Farrell, Iain W.
Ouédraogo, Jean B.
Gnankiné, Olivier
Ignell, Rickard
Cohuet, Anna
Dabiré, Roch K.
Stevenson, Philip C.
Lefèvre, Thierry
author_sort Hien, Domonbabele F. D. S.
collection PubMed
description BACKGROUND: Besides feeding on blood, females of the malaria vector Anopheles gambiae sensu lato readily feed on natural sources of plant sugars. The impact of toxic secondary phytochemicals contained in plant-derived sugars on mosquito physiology and the development of Plasmodium parasites remains elusive. The focus of this study was to explore the influence of the alkaloid ricinine, found in the nectar of the castor bean Ricinus communis, on the ability of mosquitoes to transmit Plasmodium falciparum. METHODS: Females of Anopheles gambiae and its sibling species Anopheles coluzzii were exposed to ricinine through sugar feeding assays to assess the effect of this phytochemical on mosquito survival, level of P. falciparum infection and growth rate of the parasite. RESULTS: Ricinine induced a significant reduction in the longevity of both Anopheles species. Ricinine caused acceleration in the parasite growth rate with an earlier invasion of the salivary glands in both species. At a concentration of 0.04 g l(−1) in An. coluzzii, ricinine had no effect on mosquito infection, while 0.08 g l(−1) ricinine-5% glucose solution induced a 14% increase in An. gambiae infection rate. CONCLUSIONS: Overall, our findings reveal that consumption of certain nectar phytochemicals can have unexpected and contrasting effects on key phenotypic traits that govern the intensity of malaria transmission. Further studies will be required before concluding on the putative role of ricinine as a novel control agent, including the development of ricinine-based toxic and transmission-blocking sugar baits. Testing other secondary phytochemicals in plant nectar will provide a broader understanding of the impact which plants can have on the transmission of vector-borne diseases. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04992-z.
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spelling pubmed-84444682021-09-16 Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum Hien, Domonbabele F. D. S. Paré, Prisca S. L. Cooper, Amanda Koama, Benjamin K. Guissou, Edwige Yaméogo, Koudraogo B. Yerbanga, Rakiswendé S. Farrell, Iain W. Ouédraogo, Jean B. Gnankiné, Olivier Ignell, Rickard Cohuet, Anna Dabiré, Roch K. Stevenson, Philip C. Lefèvre, Thierry Parasit Vectors Research BACKGROUND: Besides feeding on blood, females of the malaria vector Anopheles gambiae sensu lato readily feed on natural sources of plant sugars. The impact of toxic secondary phytochemicals contained in plant-derived sugars on mosquito physiology and the development of Plasmodium parasites remains elusive. The focus of this study was to explore the influence of the alkaloid ricinine, found in the nectar of the castor bean Ricinus communis, on the ability of mosquitoes to transmit Plasmodium falciparum. METHODS: Females of Anopheles gambiae and its sibling species Anopheles coluzzii were exposed to ricinine through sugar feeding assays to assess the effect of this phytochemical on mosquito survival, level of P. falciparum infection and growth rate of the parasite. RESULTS: Ricinine induced a significant reduction in the longevity of both Anopheles species. Ricinine caused acceleration in the parasite growth rate with an earlier invasion of the salivary glands in both species. At a concentration of 0.04 g l(−1) in An. coluzzii, ricinine had no effect on mosquito infection, while 0.08 g l(−1) ricinine-5% glucose solution induced a 14% increase in An. gambiae infection rate. CONCLUSIONS: Overall, our findings reveal that consumption of certain nectar phytochemicals can have unexpected and contrasting effects on key phenotypic traits that govern the intensity of malaria transmission. Further studies will be required before concluding on the putative role of ricinine as a novel control agent, including the development of ricinine-based toxic and transmission-blocking sugar baits. Testing other secondary phytochemicals in plant nectar will provide a broader understanding of the impact which plants can have on the transmission of vector-borne diseases. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04992-z. BioMed Central 2021-09-15 /pmc/articles/PMC8444468/ /pubmed/34526119 http://dx.doi.org/10.1186/s13071-021-04992-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Hien, Domonbabele F. D. S.
Paré, Prisca S. L.
Cooper, Amanda
Koama, Benjamin K.
Guissou, Edwige
Yaméogo, Koudraogo B.
Yerbanga, Rakiswendé S.
Farrell, Iain W.
Ouédraogo, Jean B.
Gnankiné, Olivier
Ignell, Rickard
Cohuet, Anna
Dabiré, Roch K.
Stevenson, Philip C.
Lefèvre, Thierry
Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum
title Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum
title_full Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum
title_fullStr Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum
title_full_unstemmed Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum
title_short Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum
title_sort contrasting effects of the alkaloid ricinine on the capacity of anopheles gambiae and anopheles coluzzii to transmit plasmodium falciparum
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8444468/
https://www.ncbi.nlm.nih.gov/pubmed/34526119
http://dx.doi.org/10.1186/s13071-021-04992-z
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