Cargando…

Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function

Metabolic adaptations shape immune cell function. In the acute response, a metabolic switch towards glycolysis is necessary for mounting a proinflammatory response. During the clinical course of sepsis, both suppression and activation of immune responses take place simultaneously. Leukocytes from se...

Descripción completa

Detalles Bibliográficos
Autores principales: Ferreira, Bianca Lima, Sousa, Mônica Bragança, Leite, Giuseppe Gianini Figueirêdo, Brunialti, Milena Karina Colo, Nishiduka, Erika Sayuri, Tashima, Alexandre Keiji, van der Poll, Tom, Salomão, Reinaldo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9718365/
https://www.ncbi.nlm.nih.gov/pubmed/36466921
http://dx.doi.org/10.3389/fimmu.2022.1051514
_version_ 1784843077358190592
author Ferreira, Bianca Lima
Sousa, Mônica Bragança
Leite, Giuseppe Gianini Figueirêdo
Brunialti, Milena Karina Colo
Nishiduka, Erika Sayuri
Tashima, Alexandre Keiji
van der Poll, Tom
Salomão, Reinaldo
author_facet Ferreira, Bianca Lima
Sousa, Mônica Bragança
Leite, Giuseppe Gianini Figueirêdo
Brunialti, Milena Karina Colo
Nishiduka, Erika Sayuri
Tashima, Alexandre Keiji
van der Poll, Tom
Salomão, Reinaldo
author_sort Ferreira, Bianca Lima
collection PubMed
description Metabolic adaptations shape immune cell function. In the acute response, a metabolic switch towards glycolysis is necessary for mounting a proinflammatory response. During the clinical course of sepsis, both suppression and activation of immune responses take place simultaneously. Leukocytes from septic patients present inhibition of cytokine production while other functions such as phagocytosis and production of reactive oxygen species (ROS) are preserved, similarly to the in vitro endotoxin tolerance model, where a first stimulation with lipopolysaccharide (LPS) affects the response to a second stimulus. Here, we sought to investigate how cellular metabolism is related to the modulation of immune responses in sepsis and endotoxin tolerance. Proteomic analysis in peripheral blood mononuclear cells (PBMCs) from septic patients obtained at intensive care unit admission showed an upregulation of proteins related to glycolysis, the pentose phosphate pathway (PPP), production of ROS and nitric oxide, and downregulation of proteins in the tricarboxylic acid cycle and oxidative phosphorylation compared to healthy volunteers. Using the endotoxin-tolerance model in PBMCs from healthy subjects, we observed increased lactate production in control cells upon LPS stimulation, while endotoxin-tolerant cells presented inhibited tumor necrosis factor-α and lactate production along with preserved phagocytic capacity. Inhibition of glycolysis and PPP led to impairment of phagocytosis and cytokine production both in control and in endotoxin-tolerant cells. These data indicate that glucose metabolism supports leukocyte functions even in a condition of endotoxin tolerance.
format Online
Article
Text
id pubmed-9718365
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-97183652022-12-03 Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function Ferreira, Bianca Lima Sousa, Mônica Bragança Leite, Giuseppe Gianini Figueirêdo Brunialti, Milena Karina Colo Nishiduka, Erika Sayuri Tashima, Alexandre Keiji van der Poll, Tom Salomão, Reinaldo Front Immunol Immunology Metabolic adaptations shape immune cell function. In the acute response, a metabolic switch towards glycolysis is necessary for mounting a proinflammatory response. During the clinical course of sepsis, both suppression and activation of immune responses take place simultaneously. Leukocytes from septic patients present inhibition of cytokine production while other functions such as phagocytosis and production of reactive oxygen species (ROS) are preserved, similarly to the in vitro endotoxin tolerance model, where a first stimulation with lipopolysaccharide (LPS) affects the response to a second stimulus. Here, we sought to investigate how cellular metabolism is related to the modulation of immune responses in sepsis and endotoxin tolerance. Proteomic analysis in peripheral blood mononuclear cells (PBMCs) from septic patients obtained at intensive care unit admission showed an upregulation of proteins related to glycolysis, the pentose phosphate pathway (PPP), production of ROS and nitric oxide, and downregulation of proteins in the tricarboxylic acid cycle and oxidative phosphorylation compared to healthy volunteers. Using the endotoxin-tolerance model in PBMCs from healthy subjects, we observed increased lactate production in control cells upon LPS stimulation, while endotoxin-tolerant cells presented inhibited tumor necrosis factor-α and lactate production along with preserved phagocytic capacity. Inhibition of glycolysis and PPP led to impairment of phagocytosis and cytokine production both in control and in endotoxin-tolerant cells. These data indicate that glucose metabolism supports leukocyte functions even in a condition of endotoxin tolerance. Frontiers Media S.A. 2022-11-18 /pmc/articles/PMC9718365/ /pubmed/36466921 http://dx.doi.org/10.3389/fimmu.2022.1051514 Text en Copyright © 2022 Ferreira, Sousa, Leite, Brunialti, Nishiduka, Tashima, van der Poll and Salomão https://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
Ferreira, Bianca Lima
Sousa, Mônica Bragança
Leite, Giuseppe Gianini Figueirêdo
Brunialti, Milena Karina Colo
Nishiduka, Erika Sayuri
Tashima, Alexandre Keiji
van der Poll, Tom
Salomão, Reinaldo
Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function
title Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function
title_full Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function
title_fullStr Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function
title_full_unstemmed Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function
title_short Glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function
title_sort glucose metabolism is upregulated in the mononuclear cell proteome during sepsis and supports endotoxin-tolerant cell function
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9718365/
https://www.ncbi.nlm.nih.gov/pubmed/36466921
http://dx.doi.org/10.3389/fimmu.2022.1051514
work_keys_str_mv AT ferreirabiancalima glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction
AT sousamonicabraganca glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction
AT leitegiuseppegianinifigueiredo glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction
AT brunialtimilenakarinacolo glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction
AT nishidukaerikasayuri glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction
AT tashimaalexandrekeiji glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction
AT vanderpolltom glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction
AT salomaoreinaldo glucosemetabolismisupregulatedinthemononuclearcellproteomeduringsepsisandsupportsendotoxintolerantcellfunction