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Plasmacytoid Dendritic Cells: Neglected Regulators of the Immune Response to Staphylococcus aureus

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      Abstract

      Plasmacytoid dendritic cells (pDC) are a rare subset of leukocytes equipped with Fcγ and Fcε receptors, which exert contrary effects on sensing of microbial nucleic acids by endosomal Toll-like receptors. In this article, we explain how pDC contribute to the immune response to Staphylococcus aureus. Under normal circumstances the pDC participates in the memory response to the pathogen: pDC activation is initiated by uptake of staphylococcal immune complexes with IgG or IgE. However, protein A-expressing S. aureus strains additionally trigger pDC activation in the absence of immunoglobulin. In this context, staphylococci exploit the pDC to induce antigen-independent differentiation of IL-10 producing plasmablasts, an elegant means to propagate immune evasion. We further discuss the role of type I interferons in infection with S. aureus and the implications of these findings for the development of immune based therapies and vaccination.

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      Most cited references 148

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      Cryopyrin activates the inflammasome in response to toxins and ATP.

      A crucial part of the innate immune response is the assembly of the inflammasome, a cytosolic complex of proteins that activates caspase-1 to process the proinflammatory cytokines interleukin (IL)-1beta and IL-18. The adaptor protein ASC is essential for inflammasome function, binding directly to caspase-1 (refs 3, 4), but the triggers of this interaction are less clear. ASC also interacts with the adaptor cryopyrin (also known as NALP3 or CIAS1). Activating mutations in cryopyrin are associated with familial cold autoinflammatory syndrome, Muckle-Wells syndrome and neonatal onset multisystem inflammatory disease, diseases that are characterized by excessive production of IL-1beta. Here we show that cryopyrin-deficient macrophages cannot activate caspase-1 in response to Toll-like receptor agonists plus ATP, the latter activating the P2X7 receptor to decrease intracellular K+ levels. The release of IL-1beta in response to nigericin, a potassium ionophore, and maitotoxin, a potent marine toxin, was also found to be dependent on cryopyrin. In contrast to Asc-/- macrophages, cells deficient in the gene encoding cryopyrin (Cias1-/-) activated caspase-1 and secreted normal levels of IL-1beta and IL-18 when infected with Gram-negative Salmonella typhimurium or Francisella tularensis. Macrophages exposed to Gram-positive Staphylococcus aureus or Listeria monocytogenes, however, required both ASC and cryopyrin to activate caspase-1 and secrete IL-1beta. Therefore, cryopyrin is essential for inflammasome activation in response to signalling pathways triggered specifically by ATP, nigericin, maitotoxin, S. aureus or L. monocytogenes.
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        Plasmacytoid dendritic cells in immunity.

        Human and mouse plasmacytoid dendritic cells have been shown to correspond to a specialized cell population that produces large amounts of type I interferons in response to viruses, the so-called natural interferon-producing cells. As a result, intensive investigation is now focused on the potential functions of plasmacytoid dendritic cells in both innate and adaptive immunity. Here we review recent progress on the characterization of plasmacytoid dendritic cell origin, development, migration and function in immunity and tolerance, as well as their effect on human diseases.
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          IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors.

           Yong-feng Liu (2004)
          Type 1 interferon-(alpha, beta, omega)-producing cells (IPCs), also known as plasmacytoid dendritic cell precursors (pDCs), represent 0.2%-0.8% of peripheral blood mononuclear cells in both humans and mice. IPCs display plasma cell morphology, selectively express Toll-like receptor (TLR)-7 and TLR9, and are specialized in rapidly secreting massive amounts of type 1 interferon following viral stimulation. IPCs can promote the function of natural killer cells, B cells, T cells, and myeloid DCs through type 1 interferons during an antiviral immune response. At a later stage of viral infection, IPCs differentiate into a unique type of mature dendritic cell, which directly regulates the function of T cells and thus links innate and adaptive immune responses. After more than two decades of effort by researchers, IPCs finally claim their place in the hematopoietic chart as the most important cell type in antiviral innate immunity. Understanding IPC biology holds future promise for developing cures for infectious diseases, cancer, and autoimmune diseases.
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            Author and article information

            Affiliations
            1Institute for Microbiology, Immunology and Parasitology, University Hospital Bonn , Bonn, Germany
            2Department of Pediatrics, University Hospital Heidelberg , Heidelberg, Germany
            3Department of Infectious Diseases, Medical Microbiology and Hygiene, University Hospital Heidelberg , Heidelberg, Germany
            Author notes

            Edited by: Fabio Bagnoli, Novartis Vaccines, Italy

            Reviewed by: Eliana Marina Coccia, Istituto Superiore di Sanità, Italy; Elisabetta Adelaide Pia Soldaini, Novartis Vaccines, Italy

            *Correspondence: Isabelle Bekeredjian-Ding, Institute for Microbiology, Immunology and Parasitology, University Hospital Bonn, Sigmund-Freud-Strasse 25, D-53105 Bonn, Germany e-mail: bekeredjian-ding@ 123456uni-bonn.de

            This article was submitted to Microbial Immunology, a section of the journal Frontiers in Immunology.

            Contributors
            URI : http://frontiersin.org/people/u/28149
            Journal
            Front Immunol
            Front Immunol
            Front. Immunol.
            Frontiers in Immunology
            Frontiers Media S.A.
            1664-3224
            23 May 2014
            2014
            : 5
            4033153
            10.3389/fimmu.2014.00238
            Copyright © 2014 Bekeredjian-Ding, Greil, Ammann and Parcina.

            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) or licensor 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.

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            Figures: 2, Tables: 0, Equations: 0, References: 148, Pages: 10, Words: 8615
            Categories
            Immunology
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