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DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei

Epigenetic mechanisms such as DNA methylation and histone post-translational modifications are fundamental for the phenotypic plasticity of insects during their interaction with the environment. In response to environmental cues, the methylation pattern in DNA is dynamically remodeled to achieve an...

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Autores principales: Claudio-Piedras, Fabiola, Recio-Tótoro, Benito, Condé, Renaud, Hernández-Tablas, Juan M., Hurtado-Sil, Gerardo, Lanz-Mendoza, Humberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6970940/
https://www.ncbi.nlm.nih.gov/pubmed/31993053
http://dx.doi.org/10.3389/fimmu.2019.03025
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author Claudio-Piedras, Fabiola
Recio-Tótoro, Benito
Condé, Renaud
Hernández-Tablas, Juan M.
Hurtado-Sil, Gerardo
Lanz-Mendoza, Humberto
author_facet Claudio-Piedras, Fabiola
Recio-Tótoro, Benito
Condé, Renaud
Hernández-Tablas, Juan M.
Hurtado-Sil, Gerardo
Lanz-Mendoza, Humberto
author_sort Claudio-Piedras, Fabiola
collection PubMed
description Epigenetic mechanisms such as DNA methylation and histone post-translational modifications are fundamental for the phenotypic plasticity of insects during their interaction with the environment. In response to environmental cues, the methylation pattern in DNA is dynamically remodeled to achieve an epigenetic control of gene expression. DNA methylation is the focus of study in insects for its evolutionarily conserved character; however, there is scant knowledge about the epigenetic regulation in vector mosquitoes, especially during their infection by parasites. The aim of the present study was to evaluate the participation of DNA methylation in the immune response of Anopheles albimanus to a Plasmodium infection. For this, we first investigated the presence of a fully functional DNA methylation system in A. albimanus by assessing its potential role in larval development. Subsequently, we evaluated the transcriptional response to Plasmodium berghei of two mosquito phenotypes with different degrees of susceptibility to the parasite, in a scenario where their global DNA methylation had been pharmacologically inhibited. Our study revealed that A. albimanus has a functional DNA methylation system that is essential to larval viability, and that is also responsive to feeding and parasite challenges. The pharmacological erasure of the methylome with azacytidine or decitabine abolished the divergent responses of both mosquito phenotypes, leading to a transcriptionally similar response upon parasite challenge. This response was more specific, and the infection load in both phenotypes was lowered. Our findings suggest that DNA methylation may constitute a key factor in vector competence, and a promising target for preventing malaria transmission.
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spelling pubmed-69709402020-01-28 DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei Claudio-Piedras, Fabiola Recio-Tótoro, Benito Condé, Renaud Hernández-Tablas, Juan M. Hurtado-Sil, Gerardo Lanz-Mendoza, Humberto Front Immunol Immunology Epigenetic mechanisms such as DNA methylation and histone post-translational modifications are fundamental for the phenotypic plasticity of insects during their interaction with the environment. In response to environmental cues, the methylation pattern in DNA is dynamically remodeled to achieve an epigenetic control of gene expression. DNA methylation is the focus of study in insects for its evolutionarily conserved character; however, there is scant knowledge about the epigenetic regulation in vector mosquitoes, especially during their infection by parasites. The aim of the present study was to evaluate the participation of DNA methylation in the immune response of Anopheles albimanus to a Plasmodium infection. For this, we first investigated the presence of a fully functional DNA methylation system in A. albimanus by assessing its potential role in larval development. Subsequently, we evaluated the transcriptional response to Plasmodium berghei of two mosquito phenotypes with different degrees of susceptibility to the parasite, in a scenario where their global DNA methylation had been pharmacologically inhibited. Our study revealed that A. albimanus has a functional DNA methylation system that is essential to larval viability, and that is also responsive to feeding and parasite challenges. The pharmacological erasure of the methylome with azacytidine or decitabine abolished the divergent responses of both mosquito phenotypes, leading to a transcriptionally similar response upon parasite challenge. This response was more specific, and the infection load in both phenotypes was lowered. Our findings suggest that DNA methylation may constitute a key factor in vector competence, and a promising target for preventing malaria transmission. Frontiers Media S.A. 2020-01-14 /pmc/articles/PMC6970940/ /pubmed/31993053 http://dx.doi.org/10.3389/fimmu.2019.03025 Text en Copyright © 2020 Claudio-Piedras, Recio-Tótoro, Condé, Hernández-Tablas, Hurtado-Sil and Lanz-Mendoza. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Claudio-Piedras, Fabiola
Recio-Tótoro, Benito
Condé, Renaud
Hernández-Tablas, Juan M.
Hurtado-Sil, Gerardo
Lanz-Mendoza, Humberto
DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei
title DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei
title_full DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei
title_fullStr DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei
title_full_unstemmed DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei
title_short DNA Methylation in Anopheles albimanus Modulates the Midgut Immune Response Against Plasmodium berghei
title_sort dna methylation in anopheles albimanus modulates the midgut immune response against plasmodium berghei
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6970940/
https://www.ncbi.nlm.nih.gov/pubmed/31993053
http://dx.doi.org/10.3389/fimmu.2019.03025
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