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      Macrophages transfer antigens to dendritic cells by releasing exosomes containing dead‐cell‐associated antigens partially through a ceramide‐dependent pathway to enhance CD4 + T‐cell responses

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          Summary

          Defects in rapid clearance of apoptotic cells lead to an accumulation of dead cells (late apoptotic or secondary necrotic cells), which results in an aberrant immune response. However, little is known about whether and how macrophages (M φs) cooperate with dendritic cells ( DCs) in the presentation of dead‐cell‐associated antigens in this process. By transferring high numbers of dead cells to mimic a failure of apoptotic cell clearance in vivo, we found that M φs and neutrophils were the predominant phagocytes in the uptake of dead cells in the spleen. Moreover, both M φs and DCs were required for an optimal CD4 + T‐cell response triggered by dead‐cell‐associated antigens. Importantly, although M φs alone had a poor capacity for antigen presentation, they could transfer phagocytosed antigens to DCs for potent antigen presentation to enhance T‐cell responses. Finally, we found that exosomes released from M φs acted as a transmitter to convey antigens to DCs partially in a ceramide‐dependent manner, since treatment with the neutral sphingomyelinase inhibitor GW4869 and spiroepoxide resulted in a significant reduction of T‐cell proliferation in vitro and in vivo. These findings point to a novel pathway of cross‐talk between M φs and DCs, which will be helpful to explain possible mechanisms for autoimmune diseases characterized by increased rates of apoptosis.

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          Author and article information

          Journal
          Immunology
          Immunology
          10.1111/(ISSN)1365-2567
          IMM
          Immunology
          John Wiley and Sons Inc. (Hoboken )
          0019-2805
          1365-2567
          30 July 2016
          October 2016
          : 149
          : 2 ( doiID: 10.1111/imm.2016.149.issue-2 )
          : 157-171
          Affiliations
          [ 1 ] Institute of Immunology Taishan Medical University Taian China
          Author notes
          [*] [* ] Correspondence: Hua Tang, Institute of Immunology, Taishan Medical University, Taian 271000, China. Email: Tanghuazhang218@ 123456163.com

          and

          Wengang Song, Department of Immunology, Taishan Medical University, Taian 271000, China. E‐mail: s.com@ 123456163.com

          Senior author: Hua Tang

          Article
          PMC5011679 PMC5011679 5011679 IMM12630
          10.1111/imm.12630
          5011679
          27278624
          b6fc8e86-b756-487a-afc1-41b162d4448e
          © 2016 John Wiley & Sons Ltd
          History
          : 22 October 2015
          : 26 May 2016
          : 03 June 2016
          Page count
          Pages: 15
          Funding
          Funded by: National Natural Science Foundation of China
          Award ID: 81302603
          Award ID: 81471553
          Award ID: 81172882
          Award ID: 81272315
          Award ID: 81172791
          Award ID: 81202308
          Award ID: 81273212
          Funded by: National Basic Research Programme of China
          Award ID: 2015CB943203
          Funded by: National Science and Technology Major Projects
          Award ID: 2014ZX09508003
          Funded by: National Science Foundation of Shandong Provice, China
          Award ID: ZR2011CM037
          Award ID: J13LK01
          Categories
          Original Article
          Original Articles
          Custom metadata
          2.0
          imm12630
          October 2016
          Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:06.09.2016

          macrophages,antigen transfer,dead‐cell‐associated antigen,dendritic cells,exosomes

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