<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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American Society for Microbiology
2021
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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) |
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malaria P. vivax metabolism mitochondria monocytes mitochondrial metabolism Microbiology QR1-502 |
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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 |
work_keys_str_mv |
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