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...
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2021
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ftdoajarticles:oai:doaj.org/article:dbe9eeb4d81b4a2ca57b85a7c8d2251b 2023-05-15T15:10:58+02:00 Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection. Krystal Maya-Maldonado Victor Cardoso-Jaime Gabriela González-Olvera Beatriz Osorio Benito Recio-Tótoro Pablo Manrique-Saide Iram Pablo Rodríguez-Sánchez Humberto Lanz-Mendoza Fanis Missirlis Fidel de la Cruz Hernández-Hernández 2021-06-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0009509 https://doaj.org/article/dbe9eeb4d81b4a2ca57b85a7c8d2251b EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0009509 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0009509 https://doaj.org/article/dbe9eeb4d81b4a2ca57b85a7c8d2251b PLoS Neglected Tropical Diseases, Vol 15, Iss 6, p e0009509 (2021) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2021 ftdoajarticles https://doi.org/10.1371/journal.pntd.0009509 2022-12-31T07:46:16Z 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. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic Stripe ENVELOPE(9.914,9.914,63.019,63.019) PLOS Neglected Tropical Diseases 15 6 e0009509 |
institution |
Open Polar |
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Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 |
spellingShingle |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 Krystal Maya-Maldonado Victor Cardoso-Jaime Gabriela González-Olvera Beatriz Osorio Benito Recio-Tótoro Pablo Manrique-Saide Iram Pablo Rodríguez-Sánchez Humberto Lanz-Mendoza Fanis Missirlis Fidel de la Cruz Hernández-Hernández Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection. |
topic_facet |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 |
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 |
Article in Journal/Newspaper |
author |
Krystal Maya-Maldonado Victor Cardoso-Jaime Gabriela González-Olvera Beatriz Osorio Benito Recio-Tótoro Pablo Manrique-Saide Iram Pablo Rodríguez-Sánchez Humberto Lanz-Mendoza Fanis Missirlis Fidel de la Cruz Hernández-Hernández |
author_facet |
Krystal Maya-Maldonado Victor Cardoso-Jaime Gabriela González-Olvera Beatriz Osorio Benito Recio-Tótoro Pablo Manrique-Saide Iram Pablo Rodríguez-Sánchez Humberto Lanz-Mendoza Fanis Missirlis Fidel de la Cruz Hernández-Hernández |
author_sort |
Krystal Maya-Maldonado |
title |
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_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_sort |
mosquito metallomics reveal copper and iron as critical factors for plasmodium infection. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2021 |
url |
https://doi.org/10.1371/journal.pntd.0009509 https://doaj.org/article/dbe9eeb4d81b4a2ca57b85a7c8d2251b |
long_lat |
ENVELOPE(9.914,9.914,63.019,63.019) |
geographic |
Arctic Stripe |
geographic_facet |
Arctic Stripe |
genre |
Arctic |
genre_facet |
Arctic |
op_source |
PLoS Neglected Tropical Diseases, Vol 15, Iss 6, p e0009509 (2021) |
op_relation |
https://doi.org/10.1371/journal.pntd.0009509 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0009509 https://doaj.org/article/dbe9eeb4d81b4a2ca57b85a7c8d2251b |
op_doi |
https://doi.org/10.1371/journal.pntd.0009509 |
container_title |
PLOS Neglected Tropical Diseases |
container_volume |
15 |
container_issue |
6 |
container_start_page |
e0009509 |
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1766341897927786496 |