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      Infection with Salmonella enterica Serovar Typhimurium Leads to Increased Proportions of F4/80 + Red Pulp Macrophages and Decreased Proportions of B and T Lymphocytes in the Spleen

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          Abstract

          Infection of mice with Salmonella enterica serovar Typhimurium ( Salmonella) causes systemic inflammatory disease and enlargement of the spleen (splenomegaly). Splenomegaly has been attributed to a general increase in the numbers of phagocytes, lymphocytes, as well as to the expansion of immature CD71 +Ter119 + reticulocytes. The spleen is important for recycling senescent red blood cells (RBCs) and for the capture and eradication of blood-borne pathogens. Conservation of splenic tissue architecture, comprised of the white pulp (WP), marginal zone (MZ), and red pulp (RP) is essential for initiation of adaptive immune responses to captured pathogens. Using flow cytometry and four color immunofluorescence microscopy (IFM), we show that Salmonella-induced splenomegaly is characterized by drastic alterations of the splenic tissue architecture and cell population proportions, as well as in situ cell distributions. A major cause of splenomegaly appears to be the significant increase in immature RBC precursors and F4/80 + macrophages that are important for recycling of heme-associated iron. In contrast, the proportions of B220 +, CD4 + and CD8 + lymphocytes, as well as MZ MOMA + macrophages decrease significantly as infection progresses. Spleen tissue sections show visible tears and significantly altered tissue architecture with F4/80 + macrophages and RBCs expanding beyond the RP and taking over most of the spleen tissue. Additionally, F4/80 + macrophages actively phagocytose not only RBCs, but also lymphocytes, indicating that they may contribute to declining lymphocyte proportions during Salmonella infection. Understanding how these alterations of spleen microarchitecture impact the generation of adaptive immune responses to Salmonella has implications for understanding Salmonella pathogenesis and for the design of more effective Salmonella-based vaccines.

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          Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation.

          A defining feature of inflammation is the accumulation of innate immune cells in the tissue that are thought to be recruited from the blood. We reveal that a distinct process exists in which tissue macrophages undergo rapid in situ proliferation in order to increase population density. This inflammatory mechanism occurred during T helper 2 (T(H)2)-related pathologies under the control of the archetypal T(H)2 cytokine interleukin-4 (IL-4) and was a fundamental component of T(H)2 inflammation because exogenous IL-4 was sufficient to drive accumulation of tissue macrophages through self-renewal. Thus, expansion of innate cells necessary for pathogen control or wound repair can occur without recruitment of potentially tissue-destructive inflammatory cells.
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            Macrophage receptors and immune recognition.

            Macrophages express a broad range of plasma membrane receptors that mediate their interactions with natural and altered-self components of the host as well as a range of microorganisms. Recognition is followed by surface changes, uptake, signaling, and altered gene expression, contributing to homeostasis, host defense, innate effector mechanisms, and the induction of acquired immunity. This review covers recent studies of selected families of structurally defined molecules, studies that have improved understanding of ligand discrimination in the absence of opsonins and differential responses by macrophages and related myeloid cells.
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              Normal structure, function, and histology of the spleen.

              Mark Cesta (2005)
              The spleen is the largest secondary immune organ in the body and is responsible for initiating immune reactions to blood-borne antigens and for filtering the blood of foreign material and old or damaged red blood cells. These functions are carried out by the 2 main compartments of the spleen, the white pulp (including the marginal zone) and the red pulp, which are vastly different in their architecture, vascular organization, and cellular composition. The morphology of these compartments is described and, to a lesser extent, their functions are discussed. The variation between species and effects of aging and genetics on splenic morphology are also discussed.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                12 June 2015
                2015
                : 10
                : 6
                : e0130092
                Affiliations
                [1 ]Department of Microbiology, Southern Illinois University, Carbondale, Illinois, United States of America
                [2 ]Department of Plant Biology, Southern Illinois University, Carbondale, Illinois, United States of America
                Université Libre de Bruxelles, BELGIUM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: VK. Performed the experiments: KLR, ATA, JNK, BTP, VK. Analyzed the data: KLR, JNK. Contributed reagents/materials/analysis tools: VK. Wrote the paper: VK.

                Article
                PONE-D-14-35985
                10.1371/journal.pone.0130092
                4466801
                26068006
                ea04e073-d82f-4efd-bc99-62c13bff9ce4
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 10 August 2014
                : 15 May 2015
                Page count
                Figures: 10, Tables: 0, Pages: 20
                Funding
                This work was funded by start-up funds provided to VK by Southern Illinois University.
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                Research Article
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                All data are included in the paper.

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