The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane Proteins

<i>Salmonella</i> is a common pathogen which can secrete outer membrane vesicles (OMVs). However, the effect of OMVs from <i>Salmonella enterica</i> Serovar Typhimurium (<i>S.</i> Typhimurium) of poultry origin on cells of the chicken innate immune system is not w...

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Main Authors: Hongxiao Cui, Yajun Sun, Hua Lin, Yan Zhao, Xin Zhao
Format: Article
Language:English
Published: MDPI AG 2022-03-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/11/3/339
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author Hongxiao Cui
Yajun Sun
Hua Lin
Yan Zhao
Xin Zhao
author_facet Hongxiao Cui
Yajun Sun
Hua Lin
Yan Zhao
Xin Zhao
author_sort Hongxiao Cui
collection DOAJ
description <i>Salmonella</i> is a common pathogen which can secrete outer membrane vesicles (OMVs). However, the effect of OMVs from <i>Salmonella enterica</i> Serovar Typhimurium (<i>S.</i> Typhimurium) of poultry origin on cells of the chicken innate immune system is not well known. In this study, <i>S.</i> Typhimurium OMVs were first isolated from three different poultry strains of <i>Salmonella</i>, <i>Salmonella</i> CVCC542, SALA, and SALB. In order to investigate the effect of OMVs on the maturation of monocytes into macrophages, both bone marrow-derived (BMD) monocytes and macrophage cell line HD11 cells were used. OMVs promoted the formation of monocyte dendrites in both types of cells, enabled BMD cells to become larger, and stimulated expression of LPS-induced TNF-αfactor (LITAF), IL-6, and inducible nitric oxide synthase (iNOS) genes in HD11 cells. These results demonstrated the capability of OMVs to promote the development of chicken monocytes into macrophages and the maturation of macrophages. In order to study the effect of OMVs on the phagocytosis of macrophages, chicken spleen-derived monocytes and HD11 cells were used. Phagocytosis of FITC-<i>Salmonella</i> and FITC-dextran by these two types of cells was enhanced after stimulation with OMVs. To determine which components in OMVs were responsible for the above observed results, OMVs were treated with proteinase K(PK) or polymyxin B (PMB). Both treatments reduced the phagocytosis of FITC-<i>Salmonella</i> by HD11 cells and chicken spleen mononuclear cells and reduced the secretion of IL-1β, LITAF, and IL-6 cytokines. These results demonstrated that <i>Salmonella</i> OMVs activated chicken macrophages and spleen mononuclear cells and the activation was achieved mainly through lipopolysaccharides and membrane proteins.
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spelling doaj.art-a767fff2a22a4d4faca0c8ed785bad6b2023-11-30T21:52:40ZengMDPI AGPathogens2076-08172022-03-0111333910.3390/pathogens11030339The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane ProteinsHongxiao Cui0Yajun Sun1Hua Lin2Yan Zhao3Xin Zhao4College of Animal Science and Technology, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, Xianyang 712100, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, Xianyang 712100, China<i>Salmonella</i> is a common pathogen which can secrete outer membrane vesicles (OMVs). However, the effect of OMVs from <i>Salmonella enterica</i> Serovar Typhimurium (<i>S.</i> Typhimurium) of poultry origin on cells of the chicken innate immune system is not well known. In this study, <i>S.</i> Typhimurium OMVs were first isolated from three different poultry strains of <i>Salmonella</i>, <i>Salmonella</i> CVCC542, SALA, and SALB. In order to investigate the effect of OMVs on the maturation of monocytes into macrophages, both bone marrow-derived (BMD) monocytes and macrophage cell line HD11 cells were used. OMVs promoted the formation of monocyte dendrites in both types of cells, enabled BMD cells to become larger, and stimulated expression of LPS-induced TNF-αfactor (LITAF), IL-6, and inducible nitric oxide synthase (iNOS) genes in HD11 cells. These results demonstrated the capability of OMVs to promote the development of chicken monocytes into macrophages and the maturation of macrophages. In order to study the effect of OMVs on the phagocytosis of macrophages, chicken spleen-derived monocytes and HD11 cells were used. Phagocytosis of FITC-<i>Salmonella</i> and FITC-dextran by these two types of cells was enhanced after stimulation with OMVs. To determine which components in OMVs were responsible for the above observed results, OMVs were treated with proteinase K(PK) or polymyxin B (PMB). Both treatments reduced the phagocytosis of FITC-<i>Salmonella</i> by HD11 cells and chicken spleen mononuclear cells and reduced the secretion of IL-1β, LITAF, and IL-6 cytokines. These results demonstrated that <i>Salmonella</i> OMVs activated chicken macrophages and spleen mononuclear cells and the activation was achieved mainly through lipopolysaccharides and membrane proteins.https://www.mdpi.com/2076-0817/11/3/339bone marrow-derived monocytesHD11spleen mononuclear cellsOMVsLPS<i>S.</i> Typhimurium
spellingShingle Hongxiao Cui
Yajun Sun
Hua Lin
Yan Zhao
Xin Zhao
The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane Proteins
Pathogens
bone marrow-derived monocytes
HD11
spleen mononuclear cells
OMVs
LPS
<i>S.</i> Typhimurium
title The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane Proteins
title_full The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane Proteins
title_fullStr The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane Proteins
title_full_unstemmed The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane Proteins
title_short The Outer Membrane Vesicles of <i>Salmonella enterica</i> Serovar Typhimurium Activate Chicken Immune Cells through Lipopolysaccharides and Membrane Proteins
title_sort outer membrane vesicles of i salmonella enterica i serovar typhimurium activate chicken immune cells through lipopolysaccharides and membrane proteins
topic bone marrow-derived monocytes
HD11
spleen mononuclear cells
OMVs
LPS
<i>S.</i> Typhimurium
url https://www.mdpi.com/2076-0817/11/3/339
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