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Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection
Iron and copper chelation restricts Plasmodium growth in vitro and in mammalian hosts. The parasite alters metal homeostasis in red blood cells to its favor, for example metabolizing hemoglobin to hemozoin. Metal interactions with the mosquito have not, however, been studied. Here, we describe the m...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8221525/ https://www.ncbi.nlm.nih.gov/pubmed/34161336 http://dx.doi.org/10.1371/journal.pntd.0009509 |
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author | Maya-Maldonado, Krystal Cardoso-Jaime, Victor González-Olvera, Gabriela Osorio, Beatriz Recio-Tótoro, Benito Manrique-Saide, Pablo Rodríguez-Sánchez, Iram Pablo Lanz-Mendoza, Humberto Missirlis, Fanis Hernández-Hernández, Fidel de la Cruz |
author_facet | Maya-Maldonado, Krystal Cardoso-Jaime, Victor González-Olvera, Gabriela Osorio, Beatriz Recio-Tótoro, Benito Manrique-Saide, Pablo Rodríguez-Sánchez, Iram Pablo Lanz-Mendoza, Humberto Missirlis, Fanis Hernández-Hernández, Fidel de la Cruz |
author_sort | Maya-Maldonado, Krystal |
collection | PubMed |
description | Iron and copper chelation restricts Plasmodium growth in vitro and in mammalian hosts. The parasite alters metal homeostasis in red blood cells to its favor, for example metabolizing hemoglobin to hemozoin. Metal interactions with the mosquito have not, however, been studied. Here, we describe the metallomes of Anopheles albimanus and Aedes aegypti throughout their life cycle and following a blood meal. Consistent with previous reports, we found evidence of maternal iron deposition in embryos of Ae. aegypti, but less so in An. albimanus. Sodium, potassium, iron, and copper are present at higher concentrations during larval developmental stages. Two An. albimanus phenotypes that differ in their susceptibility to Plasmodium berghei infection were studied. The susceptible white stripe (ws) phenotype was named after a dorsal white stripe apparent during larval stages 3, 4, and pupae. During larval stage 3, ws larvae accumulate more iron and copper than the resistant brown stripe (bs) phenotype counterparts. A similar increase in copper and iron accumulation was also observed in the susceptible ws, but not in the resistant bs phenotype following P. berghei infection. Feeding ws mosquitoes with extracellular iron and copper chelators before and after receiving Plasmodium-infected blood protected from infection and simultaneously affected follicular development in the case of iron chelation. Unexpectedly, the application of the iron chelator to the bs strain reverted resistance to infection. Besides a drop in iron, iron-chelated bs mosquitoes experienced a concomitant loss of copper. Thus, the effect of metal chelation on P. berghei infectivity was strain-specific. |
format | Online Article Text |
id | pubmed-8221525 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-82215252021-07-07 Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection Maya-Maldonado, Krystal Cardoso-Jaime, Victor González-Olvera, Gabriela Osorio, Beatriz Recio-Tótoro, Benito Manrique-Saide, Pablo Rodríguez-Sánchez, Iram Pablo Lanz-Mendoza, Humberto Missirlis, Fanis Hernández-Hernández, Fidel de la Cruz PLoS Negl Trop Dis Research Article Iron and copper chelation restricts Plasmodium growth in vitro and in mammalian hosts. The parasite alters metal homeostasis in red blood cells to its favor, for example metabolizing hemoglobin to hemozoin. Metal interactions with the mosquito have not, however, been studied. Here, we describe the metallomes of Anopheles albimanus and Aedes aegypti throughout their life cycle and following a blood meal. Consistent with previous reports, we found evidence of maternal iron deposition in embryos of Ae. aegypti, but less so in An. albimanus. Sodium, potassium, iron, and copper are present at higher concentrations during larval developmental stages. Two An. albimanus phenotypes that differ in their susceptibility to Plasmodium berghei infection were studied. The susceptible white stripe (ws) phenotype was named after a dorsal white stripe apparent during larval stages 3, 4, and pupae. During larval stage 3, ws larvae accumulate more iron and copper than the resistant brown stripe (bs) phenotype counterparts. A similar increase in copper and iron accumulation was also observed in the susceptible ws, but not in the resistant bs phenotype following P. berghei infection. Feeding ws mosquitoes with extracellular iron and copper chelators before and after receiving Plasmodium-infected blood protected from infection and simultaneously affected follicular development in the case of iron chelation. Unexpectedly, the application of the iron chelator to the bs strain reverted resistance to infection. Besides a drop in iron, iron-chelated bs mosquitoes experienced a concomitant loss of copper. Thus, the effect of metal chelation on P. berghei infectivity was strain-specific. Public Library of Science 2021-06-23 /pmc/articles/PMC8221525/ /pubmed/34161336 http://dx.doi.org/10.1371/journal.pntd.0009509 Text en © 2021 Maya-Maldonado et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Maya-Maldonado, Krystal Cardoso-Jaime, Victor González-Olvera, Gabriela Osorio, Beatriz Recio-Tótoro, Benito Manrique-Saide, Pablo Rodríguez-Sánchez, Iram Pablo Lanz-Mendoza, Humberto Missirlis, Fanis Hernández-Hernández, Fidel de la Cruz Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection |
title | Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection |
title_full | Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection |
title_fullStr | Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection |
title_full_unstemmed | Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection |
title_short | Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection |
title_sort | mosquito metallomics reveal copper and iron as critical factors for plasmodium infection |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8221525/ https://www.ncbi.nlm.nih.gov/pubmed/34161336 http://dx.doi.org/10.1371/journal.pntd.0009509 |
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