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

Abstract

Salmonella is a common pathogen which can secrete outer membrane vesicles (OMVs). However, the effect of OMVs from Salmonella enterica Serovar Typhimurium (S. Typhimurium) of poultry origin on cells of the chicken innate immune system is not well known. In this study, S. Typhimurium OMVs were first isolated from three different poultry strains of Salmonella, Salmonella 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-Salmonella 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-Salmonella by HD11 cells and chicken spleen mononuclear cells and reduced the secretion of IL-1β, LITAF, and IL-6 cytokines. These results demonstrated that Salmonella OMVs activated chicken macrophages and spleen mononuclear cells and the activation was achieved mainly through lipopolysaccharides and membrane proteins.

Extracellular vesicle-mediated regulation of macrophage polarization in bacterial infections

“…All these changes in macrophage iron homeostasis are reported to be IFN-γ-mediated. Similar results are found in the treatment of Salmonella MVs on chicken macrophages (Cui et al, 2022 ). Therefore, MVs released from Salmonella , like those from Mtb, can carry virulence factors that induce macrophages to polarize toward type M1 and exert the ability to eliminate bacteria.…”

“…Bacteria are major pathogens that develop resistance and cause distinct types of infectious diseases such as tuberculosis, legionnaires' disease, and acute fibrinopurulent pneumonia (Livermore, 2004 ; Kiszewski et al, 2006 ; Schwechheimer and Kuehn, 2015 ; Jung et al, 2016 ). Independent of the location, microbes have developed many tools to facilitate microbe–microbe, microbe–host, and microbe–environment interactions (Kaparakis et al, 2010 ; Furuyama and Sircili, 2021 ; Cui et al, 2022 ). One strategy is through the classical secretion system types (1~7), which have been widely studied and characterized (El Qaidi et al, 2017 ; Hui et al, 2018 ; Grigoryeva et al, 2021 ; Hardy et al, 2022 ).…”

“…Previous reports have shown that SecA and Esx protein secretion systems are important for mycobacterial virulence effectors' delivery into the cytosol of the host (Feltcher and Braunstein, 2012 ; Gröschel et al, 2016 ). More recently, evolving evidence suggests that Mtb MVs transport various effectors including cell membranes, cell walls, and extracellular proteins into the recipient cells, particularly macrophages, to regulate the host immune response depending on but not limited to nutrient uptake, oxidative stress, envelope stress, and antimicrobial peptides (Jurkoshek et al, 2016 ; Palacios et al, 2021 ; Cui et al, 2022 ).…”

Using ScRNA-seq to Reveal Lymphocyte Responses to ALV-J in Bone Marrow Microenvironment

“…However, studies on the role of bone marrow in resistance to pathogenic infections have mainly focused on myeloid cells. For example, Salmonella outer membrane vesicles promote the development of monocytes into macrophages in the bone marrow [32], and infectious bronchitis virus inhibits antigen presentation by bone marrow dendritic cells [33]. In the current study, 10x scRNA-seq was used to characterize the composition of chicken bone marrow lymphocytes in different levels of ALV-J infection, the response of bone marrow lymphocytes to ALV-J infection, and the differences between virus-infected and non-virus-infected lymphocytes.…”

Mycoplasma synoviae lipid-associated membrane proteins identification and expression changes when exposed to chicken cells

“…Bacterial outer membrane vesicles (OMVs) can activate macrophages and splenic mononuclear cells from chickens, primarily through the effects of membrane proteins and lipopolysaccharides (2). Mycoplasma infection necessitates the initial adhesion and colonization of epithelial sites, and lipid-associated membrane proteins (LAMPs) are required for this adhesion (3), promoting inflammation through the binding of host receptor proteins (4).…”