<named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes

ABSTRACT Monocytes play an important role in the host defense against Plasmodium vivax as the main source of inflammatory cytokines and mitochondrial reactive oxygen species (mROS). Here, we show that monocyte metabolism is altered during human P. vivax malaria, with mitochondria playing a major fun...

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Autores principales: Suelen Queiroz Diniz, Andréa Teixeira-Carvalho, Maria Marta Figueiredo, Pedro Augusto Carvalho Costa, Bruno Coelho Rocha, Olindo Assis Martins-Filho, Ricardo Gonçalves, Dhélio Batista Pereira, Mauro Shugiro Tada, Fabiano Oliveira, Ricardo Tostes Gazzinelli, Lis Ribeiro do Valle Antonelli
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Publicado: American Society for Microbiology 2021
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Acceso en línea:https://doaj.org/article/cc51a8d6d04642acb3c7b1691c5ba420
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spelling oai:doaj.org-article:cc51a8d6d04642acb3c7b1691c5ba4202021-11-10T18:37:51Z<named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes10.1128/mBio.01247-212150-7511https://doaj.org/article/cc51a8d6d04642acb3c7b1691c5ba4202021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01247-21https://doaj.org/toc/2150-7511ABSTRACT Monocytes play an important role in the host defense against Plasmodium vivax as the main source of inflammatory cytokines and mitochondrial reactive oxygen species (mROS). Here, we show that monocyte metabolism is altered during human P. vivax malaria, with mitochondria playing a major function in this switch. The process involves a reprograming in which the cells increase glucose uptake and produce ATP via glycolysis instead of oxidative phosphorylation. P. vivax infection results in dysregulated mitochondrial gene expression and in altered membrane potential leading to mROS increase rather than ATP production. When monocytes were incubated with P. vivax-infected reticulocytes, mitochondria colocalized with phagolysosomes containing parasites representing an important source mROS. Importantly, the mitochondrial enzyme superoxide dismutase 2 (SOD2) is simultaneously induced in monocytes from malaria patients. Taken together, the monocyte metabolic reprograming with an increased mROS production may contribute to protective responses against P. vivax while triggering immunomodulatory mechanisms to circumvent tissue damage. IMPORTANCE Plasmodium vivax is the most widely distributed causative agent of human malaria. To achieve parasite control, the human immune system develops a substantial inflammatory response that is also responsible for the symptoms of the disease. Among the cells involved in this response, monocytes play an important role. Here, we show that monocyte metabolism is altered during malaria, with its mitochondria playing a major function in this switch. This change involves a reprograming process in which the cells increase glucose uptake and produce ATP via glycolysis instead of oxidative phosphorylation. The resulting altered mitochondrial membrane potential leads to an increase in mitochondrial reactive oxygen species rather than ATP. These data suggest that agents that change metabolism should be investigated and used with caution during malaria.Suelen Queiroz DinizAndréa Teixeira-CarvalhoMaria Marta FigueiredoPedro Augusto Carvalho CostaBruno Coelho RochaOlindo Assis Martins-FilhoRicardo GonçalvesDhélio Batista PereiraMauro Shugiro TadaFabiano OliveiraRicardo Tostes GazzinelliLis Ribeiro do Valle AntonelliAmerican Society for MicrobiologyarticlemalariaP. vivaxmetabolismmitochondriamonocytesmitochondrial metabolismMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution DOAJ
collection DOAJ
language EN
topic malaria
P. vivax
metabolism
mitochondria
monocytes
mitochondrial metabolism
Microbiology
QR1-502
spellingShingle malaria
P. vivax
metabolism
mitochondria
monocytes
mitochondrial metabolism
Microbiology
QR1-502
Suelen Queiroz Diniz
Andréa Teixeira-Carvalho
Maria Marta Figueiredo
Pedro Augusto Carvalho Costa
Bruno Coelho Rocha
Olindo Assis Martins-Filho
Ricardo Gonçalves
Dhélio Batista Pereira
Mauro Shugiro Tada
Fabiano Oliveira
Ricardo Tostes Gazzinelli
Lis Ribeiro do Valle Antonelli
<named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes
description ABSTRACT Monocytes play an important role in the host defense against Plasmodium vivax as the main source of inflammatory cytokines and mitochondrial reactive oxygen species (mROS). Here, we show that monocyte metabolism is altered during human P. vivax malaria, with mitochondria playing a major function in this switch. The process involves a reprograming in which the cells increase glucose uptake and produce ATP via glycolysis instead of oxidative phosphorylation. P. vivax infection results in dysregulated mitochondrial gene expression and in altered membrane potential leading to mROS increase rather than ATP production. When monocytes were incubated with P. vivax-infected reticulocytes, mitochondria colocalized with phagolysosomes containing parasites representing an important source mROS. Importantly, the mitochondrial enzyme superoxide dismutase 2 (SOD2) is simultaneously induced in monocytes from malaria patients. Taken together, the monocyte metabolic reprograming with an increased mROS production may contribute to protective responses against P. vivax while triggering immunomodulatory mechanisms to circumvent tissue damage. IMPORTANCE Plasmodium vivax is the most widely distributed causative agent of human malaria. To achieve parasite control, the human immune system develops a substantial inflammatory response that is also responsible for the symptoms of the disease. Among the cells involved in this response, monocytes play an important role. Here, we show that monocyte metabolism is altered during malaria, with its mitochondria playing a major function in this switch. This change involves a reprograming process in which the cells increase glucose uptake and produce ATP via glycolysis instead of oxidative phosphorylation. The resulting altered mitochondrial membrane potential leads to an increase in mitochondrial reactive oxygen species rather than ATP. These data suggest that agents that change metabolism should be investigated and used with caution during malaria.
format article
author Suelen Queiroz Diniz
Andréa Teixeira-Carvalho
Maria Marta Figueiredo
Pedro Augusto Carvalho Costa
Bruno Coelho Rocha
Olindo Assis Martins-Filho
Ricardo Gonçalves
Dhélio Batista Pereira
Mauro Shugiro Tada
Fabiano Oliveira
Ricardo Tostes Gazzinelli
Lis Ribeiro do Valle Antonelli
author_facet Suelen Queiroz Diniz
Andréa Teixeira-Carvalho
Maria Marta Figueiredo
Pedro Augusto Carvalho Costa
Bruno Coelho Rocha
Olindo Assis Martins-Filho
Ricardo Gonçalves
Dhélio Batista Pereira
Mauro Shugiro Tada
Fabiano Oliveira
Ricardo Tostes Gazzinelli
Lis Ribeiro do Valle Antonelli
author_sort Suelen Queiroz Diniz
title <named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes
title_short <named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes
title_full <named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes
title_fullStr <named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes
title_full_unstemmed <named-content content-type="genus-species">Plasmodium vivax</named-content> Infection Alters Mitochondrial Metabolism in Human Monocytes
title_sort <named-content content-type="genus-species">plasmodium vivax</named-content> infection alters mitochondrial metabolism in human monocytes
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/cc51a8d6d04642acb3c7b1691c5ba420
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