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Activation of Dendritic Cells Alters the Mechanism of MHC Class II Antigen Presentation to CD4 T Cells

Kyung-Jin Cho, Satoshi Ishido, Laurence C. Eisenlohr and Paul A. Roche
J Immunol January 29, 2020, ji1901234; DOI: https://doi.org/10.4049/jimmunol.1901234
Kyung-Jin Cho
*Experimental Immunology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892;
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Satoshi Ishido
†Department of Microbiology, Hyogo College of Medicine, Nishinomiya, 663-8501 Japan;
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Laurence C. Eisenlohr
‡The Children’s Hospital of Philadelphia Research Institute, Philadelphia, PA 19104; and
§Perelman School of Medicine at The University of Pennsylvania, Philadelphia, PA 19104
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Paul A. Roche
*Experimental Immunology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892;
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Key Points

  • MHC-II recycling through early endosomes in mature DCs is regulated by Rab11a.

  • MHC-II synthesis enhances presentation of late endosome Ags by immature DCs.

  • MHC-II recycling enhances presentation of early endosome Ags by mature DCs.

Abstract

Both immature and mature dendritic cells (DCs) can process and present foreign Ags to CD4 T cells; however, the mechanism by which MHC class II (MHC-II) in mature DCs acquires antigenic peptides remains unknown. To address this, we have studied Ag processing and presentation of two distinct CD4 T cell epitopes of the influenza virus hemagglutinin coat protein by both immature and mature mouse DCs. We find that immature DCs almost exclusively use newly synthesized MHC-II targeted to DM+ late endosomes for presentation to influenza virus–specific CD4 T cells. By contrast, mature DCs exclusively use recycling MHC-II that traffics to both early and late endosomes for antigenic peptide binding. Rab11a knockdown partially inhibits recycling of MHC-II in mature DCs and selectively inhibits presentation of an influenza virus hemagglutinin CD4 T cell epitope generated in early endosomes. These studies highlight a “division of labor” in MHC-II peptide binding, in which immature DCs preferentially present Ags acquired in Rab11a− DM+ late endosomes, whereas mature DCs use recycling MHC-II to present antigenic peptides acquired in both Rab11a+ early endosomes and Rab11a− endosomes for CD4 T cell activation.

Footnotes

  • This work was supported by a National Institutes of Health grant (to L.C.E.) and the Intramural Research Program of the National Institutes of Health (to P.A.R.).

  • The online version of this article contains supplemental material.

  • Received October 23, 2019.
  • Accepted December 31, 2019.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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Activation of Dendritic Cells Alters the Mechanism of MHC Class II Antigen Presentation to CD4 T Cells
Kyung-Jin Cho, Satoshi Ishido, Laurence C. Eisenlohr, Paul A. Roche
The Journal of Immunology January 29, 2020, ji1901234; DOI: 10.4049/jimmunol.1901234

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Activation of Dendritic Cells Alters the Mechanism of MHC Class II Antigen Presentation to CD4 T Cells
Kyung-Jin Cho, Satoshi Ishido, Laurence C. Eisenlohr, Paul A. Roche
The Journal of Immunology January 29, 2020, ji1901234; DOI: 10.4049/jimmunol.1901234
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Print ISSN 0022-1767        Online ISSN 1550-6606