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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Published in:PLOS Neglected Tropical Diseases
Main Authors: 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
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2021
Subjects:
Online Access:https://doi.org/10.1371/journal.pntd.0009509
https://doaj.org/article/dbe9eeb4d81b4a2ca57b85a7c8d2251b
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spelling 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
collection 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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