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      Intracellular Trafficking Pathways of Edwardsiella tarda: From Clathrin- and Caveolin-Mediated Endocytosis to Endosome and Lysosome


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          Edwardsiella tarda is a Gram-negative bacterium that can infect a broad range of hosts including humans and fish. Accumulating evidences have indicated that E. tarda is able to survive and replicate in host phagocytes. However, the pathways involved in the intracellular infection of E. tarda are unclear. In this study, we examined the entry and endocytic trafficking of E. tarda in the mouse macrophage cell line RAW264.7. We found that E. tarda entered RAW264.7 and multiplied intracellularly in a robust manner. Cellular invasion of E. tarda was significantly impaired by inhibition of clathrin- and caveolin-mediated endocytic pathways and by inhibition of endosome acidification, but not by inhibition of macropinocytosis. Consistently, RAW264.7-infecting E. tarda was co-localized with clathrin, caveolin, and hallmarks of early and late endosomes, and intracellular E. tarda was found to exist in acid organelles. In addition, E. tarda in RAW264.7 was associated with actin and microtubule, and blocking of the functions of these cytoskeletons by inhibitors significantly decreased E. tarda infection. Furthermore, formaldehyde-killed E. tarda exhibited routes of cellular uptake and intracellular trafficking similar to that of live E. tarda. Together these results provide the first evidence that entry of live E. tarda into macrophages is probably a passive, virulence-independent process of phagocytosis effected by clathrin- and caveolin-mediated endocytosis and cytoskeletons, and that the intracellular traffic of E. tarda involves endosomes and endolysosomes.

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          The plasma membrane is the interface between cells and their harsh environment. Uptake of nutrients and all communication among cells and between cells and their environment occurs through this interface. 'Endocytosis' encompasses several diverse mechanisms by which cells internalize macromolecules and particles into transport vesicles derived from the plasma membrane. It controls entry into the cell and has a crucial role in development, the immune response, neurotransmission, intercellular communication, signal transduction, and cellular and organismal homeostasis. As the complexity of molecular interactions governing endocytosis are revealed, it has become increasingly clear that it is tightly coordinated and coupled with overall cell physiology and thus, must be viewed in a broader context than simple vesicular trafficking.
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              The inflammatory process is usually tightly regulated, involving both signals that initiate and maintain inflammation and signals that shut the process down. An imbalance between the two signals leaves inflammation unchecked, resulting in cellular and tissue damage. Macrophages are a major component of the mononuclear phagocyte system that consists of closely related cells of bone marrow origin, including blood monocytes, and tissue macrophages. From the blood, monocytes migrate into various tissues and transform macrophages. In inflammation, macrophages have three major function; antigen presentation, phagocytosis, and immunomodulation through production of various cytokines and growth factors. Macrophages play a critical role in the initiation, maintenance, and resolution of inflammation. They are activated and deactivated in the inflammatory process. Activation signals include cytokines (interferon gamma, granulocyte-monocyte colony stimulating factor, and tumor necrosis factor alpha), bacterial lipopolysaccharide, extracellular matrix proteins, and other chemical mediators. Inhibition of inflammation by removal or deactivation of mediators and inflammatory effector cells permits the host to repair damages tissues. Activated macrophages are deactivated by anti-inflammatory cytokines (interleukin 10 and transforming growth factor beta) and cytokine antagonists that are mainly produced by macrophages. Macrophages participate in the autoregulatory loop in the inflammatory process. Because macrophages produce a wide range of biologically active molecules participated in both beneficial and detrimental outcomes in inflammation, therapeutic interventions targeted macrophages and their products may open new avenues for controlling inflammatory diseases.

                Author and article information

                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                06 September 2017
                : 7
                [1] 1Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences Qingdao, China
                [2] 2Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology Qingdao, China
                [3] 3University of Chinese Academy of Sciences Beijing, China
                [4] 4State Key Laboratory of Electroanalytical Chemistry, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences Changchun, China
                Author notes

                Edited by: Rey Carabeo, Washington State University, United States

                Reviewed by: Charles Lawrence Larson, Rocky Mountain Laboratory, United States; Stefania Spano, University of Aberdeen, United Kingdom

                *Correspondence: Li Sun lsun@ 123456qdio.ac.cn
                Copyright © 2017 Sui, Xu, Wang, Jiang, Chi and Sun.

                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.

                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 47, Pages: 10, Words: 5932
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31330081
                Original Research

                Infectious disease & Microbiology

                edwardsiella tarda, endocytosis, endosome, lysosome, cytoskeleton


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