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Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection

Parasitic enteric nematodes induce a type 2 immune response characterized by increased production of Th2 cytokines, IL-4 and IL-13, and recruitment of alternatively activated macrophages (M2) to the site of infection. Nematode infection is associated with changes in epithelial permeability and inhib...

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Autores principales: Notari, Luigi, Riera, Diana C., Sun, Rex, Bohl, Jennifer A., McLean, Leon P., Madden, Kathleen B., van Rooijen, Nico, Vanuytsel, Tim, Urban, Joseph F., Zhao, Aiping, Shea-Donohue, Terez
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3900397/
https://www.ncbi.nlm.nih.gov/pubmed/24465430
http://dx.doi.org/10.1371/journal.pone.0084763
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author Notari, Luigi
Riera, Diana C.
Sun, Rex
Bohl, Jennifer A.
McLean, Leon P.
Madden, Kathleen B.
van Rooijen, Nico
Vanuytsel, Tim
Urban, Joseph F.
Zhao, Aiping
Shea-Donohue, Terez
author_facet Notari, Luigi
Riera, Diana C.
Sun, Rex
Bohl, Jennifer A.
McLean, Leon P.
Madden, Kathleen B.
van Rooijen, Nico
Vanuytsel, Tim
Urban, Joseph F.
Zhao, Aiping
Shea-Donohue, Terez
author_sort Notari, Luigi
collection PubMed
description Parasitic enteric nematodes induce a type 2 immune response characterized by increased production of Th2 cytokines, IL-4 and IL-13, and recruitment of alternatively activated macrophages (M2) to the site of infection. Nematode infection is associated with changes in epithelial permeability and inhibition of sodium-linked glucose absorption, but the role of M2 in these effects is unknown. Clodronate-containing liposomes were administered prior to and during nematode infection to deplete macrophages and prevent the development of M2 in response to infection with Nippostrongylus brasiliensis. The inhibition of epithelial glucose absorption that is associated with nematode infection involved a macrophage-dependent reduction in SGLT1 activity, with no change in receptor expression, and a macrophage-independent down-regulation of GLUT2 expression. The reduced transport of glucose into the enterocyte is compensated partially by an up-regulation of the constitutive GLUT1 transporter consistent with stress-induced activation of HIF-1α. Thus, nematode infection results in a “lean” epithelial phenotype that features decreased SGLT1 activity, decreased expression of GLUT2 and an emergent dependence on GLUT1 for glucose uptake into the enterocyte. Macrophages do not play a role in enteric nematode infection-induced changes in epithelial barrier function. There is a greater contribution, however, of paracellular absorption of glucose to supply the energy demands of host resistance. These data provide further evidence of the ability of macrophages to alter glucose metabolism of neighboring cells.
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spelling pubmed-39003972014-01-24 Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection Notari, Luigi Riera, Diana C. Sun, Rex Bohl, Jennifer A. McLean, Leon P. Madden, Kathleen B. van Rooijen, Nico Vanuytsel, Tim Urban, Joseph F. Zhao, Aiping Shea-Donohue, Terez PLoS One Research Article Parasitic enteric nematodes induce a type 2 immune response characterized by increased production of Th2 cytokines, IL-4 and IL-13, and recruitment of alternatively activated macrophages (M2) to the site of infection. Nematode infection is associated with changes in epithelial permeability and inhibition of sodium-linked glucose absorption, but the role of M2 in these effects is unknown. Clodronate-containing liposomes were administered prior to and during nematode infection to deplete macrophages and prevent the development of M2 in response to infection with Nippostrongylus brasiliensis. The inhibition of epithelial glucose absorption that is associated with nematode infection involved a macrophage-dependent reduction in SGLT1 activity, with no change in receptor expression, and a macrophage-independent down-regulation of GLUT2 expression. The reduced transport of glucose into the enterocyte is compensated partially by an up-regulation of the constitutive GLUT1 transporter consistent with stress-induced activation of HIF-1α. Thus, nematode infection results in a “lean” epithelial phenotype that features decreased SGLT1 activity, decreased expression of GLUT2 and an emergent dependence on GLUT1 for glucose uptake into the enterocyte. Macrophages do not play a role in enteric nematode infection-induced changes in epithelial barrier function. There is a greater contribution, however, of paracellular absorption of glucose to supply the energy demands of host resistance. These data provide further evidence of the ability of macrophages to alter glucose metabolism of neighboring cells. Public Library of Science 2014-01-23 /pmc/articles/PMC3900397/ /pubmed/24465430 http://dx.doi.org/10.1371/journal.pone.0084763 Text en https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
spellingShingle Research Article
Notari, Luigi
Riera, Diana C.
Sun, Rex
Bohl, Jennifer A.
McLean, Leon P.
Madden, Kathleen B.
van Rooijen, Nico
Vanuytsel, Tim
Urban, Joseph F.
Zhao, Aiping
Shea-Donohue, Terez
Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection
title Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection
title_full Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection
title_fullStr Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection
title_full_unstemmed Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection
title_short Role of Macrophages in the Altered Epithelial Function during a Type 2 Immune Response Induced by Enteric Nematode Infection
title_sort role of macrophages in the altered epithelial function during a type 2 immune response induced by enteric nematode infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3900397/
https://www.ncbi.nlm.nih.gov/pubmed/24465430
http://dx.doi.org/10.1371/journal.pone.0084763
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