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Dendritic Cell Migration and Antigen Presentation Are Coordinated by the Opposing Functions of the Tetraspanins CD82 and CD37

Eleanor L. Jones, Janet L. Wee, Maria C. Demaria, Jessica Blakeley, Po Ki Ho, Javier Vega-Ramos, Jose A. Villadangos, Annemiek B. van Spriel, Michael J. Hickey, Günther J. Hämmerling and Mark D. Wright
J Immunol January 4, 2016, 1500357; DOI: https://doi.org/10.4049/jimmunol.1500357
Eleanor L. Jones
*Department of Immunology and Pathology, Monash University, Melbourne, Victoria 3004, Australia;
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Janet L. Wee
*Department of Immunology and Pathology, Monash University, Melbourne, Victoria 3004, Australia;
†Department of Medicine, Centre for Inflammatory Diseases, Monash University, Clayton, Victoria 3168, Australia;
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Maria C. Demaria
*Department of Immunology and Pathology, Monash University, Melbourne, Victoria 3004, Australia;
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Jessica Blakeley
*Department of Immunology and Pathology, Monash University, Melbourne, Victoria 3004, Australia;
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Po Ki Ho
*Department of Immunology and Pathology, Monash University, Melbourne, Victoria 3004, Australia;
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Javier Vega-Ramos
‡Department of Microbiology and Immunology, University of Melbourne, Melbourne 3010, Australia;
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Jose A. Villadangos
‡Department of Microbiology and Immunology, University of Melbourne, Melbourne 3010, Australia;
§Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Melbourne 3010, Australia;
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Annemiek B. van Spriel
¶Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, G525 GA Nijmegen, the Netherlands; and
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Michael J. Hickey
†Department of Medicine, Centre for Inflammatory Diseases, Monash University, Clayton, Victoria 3168, Australia;
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Günther J. Hämmerling
‖Molecular Immunology, German Cancer Research Center, 69120 Heidelberg, Germany
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Mark D. Wright
*Department of Immunology and Pathology, Monash University, Melbourne, Victoria 3004, Australia;
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Abstract

This study supports a new concept where the opposing functions of the tetraspanins CD37 and CD82 may coordinate changes in migration and Ag presentation during dendritic cell (DC) activation. We have previously published that CD37 is downregulated upon monocyte-derived DC activation, promotes migration of both skin and bone marrow–derived dendritic cells (BMDCs), and restrains Ag presentation in splenic and BMDCs. In this article, we show that CD82, the closest phylogenetic relative to CD37, appears to have opposing functions. CD82 is upregulated upon activation of BMDCs and monocyte-derived DCs, restrains migration of skin and BMDCs, supports MHC class II maturation, and promotes stable interactions between T cells and splenic DCs or BMDCs. The underlying mechanism involves the rearrangement of the cytoskeleton via a differential activation of small GTPases. Both CD37−/− and CD82−/− BMDCs lack cellular projections, but where CD37−/− BMDCs spread poorly on fibronectin, CD82−/− BMDCs are large and spread to a greater extent than wild-type BMDCs. At the molecular level, CD82 is a negative regulator of RhoA, whereas CD37 promotes activation of Rac-1; both tetraspanins negatively regulate Cdc42. Thus, this study identifies a key aspect of DC biology: an unactivated BMDC is CD37hiCD82lo, resulting in a highly motile cell with a limited ability to activate naive T cells. By contrast, a late activated BMDC is CD37loCD82hi, and thus has modified its migratory, cytoskeletal, and Ag presentation machinery to become a cell superbly adapted to activating naive T cells.

Footnotes

  • This work was supported by grants from the Australian National Health and Medical Research Council and the Netherlands Organization for Scientific Research (NWO-Vidi Grant 864.11.006 to A.B.v.S.).

  • The online version of this article contains supplemental material.

  • Received February 12, 2015.
  • Accepted December 1, 2015.
  • Copyright © 2016 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 209 (3)
The Journal of Immunology
Vol. 209, Issue 3
1 Aug 2022
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Dendritic Cell Migration and Antigen Presentation Are Coordinated by the Opposing Functions of the Tetraspanins CD82 and CD37
Eleanor L. Jones, Janet L. Wee, Maria C. Demaria, Jessica Blakeley, Po Ki Ho, Javier Vega-Ramos, Jose A. Villadangos, Annemiek B. van Spriel, Michael J. Hickey, Günther J. Hämmerling, Mark D. Wright
The Journal of Immunology January 4, 2016, 1500357; DOI: 10.4049/jimmunol.1500357

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Dendritic Cell Migration and Antigen Presentation Are Coordinated by the Opposing Functions of the Tetraspanins CD82 and CD37
Eleanor L. Jones, Janet L. Wee, Maria C. Demaria, Jessica Blakeley, Po Ki Ho, Javier Vega-Ramos, Jose A. Villadangos, Annemiek B. van Spriel, Michael J. Hickey, Günther J. Hämmerling, Mark D. Wright
The Journal of Immunology January 4, 2016, 1500357; DOI: 10.4049/jimmunol.1500357
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