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IFN-λ Enhances Constitutive Expression of MHC Class I Molecules on Thymic Epithelial Cells

Mohamed Benhammadi, Justine Mathé, Maude Dumont-Lagacé, Koichi S. Kobayashi, Louis Gaboury, Sylvie Brochu and Claude Perreault
J Immunol July 20, 2020, ji2000225; DOI: https://doi.org/10.4049/jimmunol.2000225
Mohamed Benhammadi
*Institute for Research in Immunology and Cancer, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
†Department of Medicine, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
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Justine Mathé
*Institute for Research in Immunology and Cancer, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
†Department of Medicine, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
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Maude Dumont-Lagacé
*Institute for Research in Immunology and Cancer, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
†Department of Medicine, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
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Koichi S. Kobayashi
‡Department of Microbial Pathogenesis and Immunology, Texas A&M Health Science Center, College Station, TX 77843;
§Department of Immunology, Hokkaido University Graduate School of Medicine, Sapporo, Hokkaido 060-8638, Japan; and
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Louis Gaboury
¶Department of Pathology and Cell Biology, University of Montreal, Montreal, Quebec H3T 1J4, Canada
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Sylvie Brochu
*Institute for Research in Immunology and Cancer, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
†Department of Medicine, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
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Claude Perreault
*Institute for Research in Immunology and Cancer, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
†Department of Medicine, University of Montreal, Montreal, Quebec H3C 3J7, Canada;
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Key Points

  • Thymic ECs express more MHC I molecules than extrathymic ECs.

  • Aire, Nlrc5, Stat1, and IFN-λ enhance constitutive MHC I expression in thymic ECs.

Abstract

Regulation of MHC class I (MHC I) expression has been studied almost exclusively in hematolymphoid cells. We report that thymic epithelial cells (TECs), particularly the medullary TECs, constitutively express up to 100-fold more cell surface MHC I proteins than epithelial cells (ECs) from the skin, colon, and lung. Differential abundance of cell surface MHC I in primary ECs is regulated via transcription of MHC I and of genes implicated in the generation of MHC I–binding peptides. Superior MHC I expression in TECs is unaffected by deletion of Ifnar1 or Ifngr1, but is lessened by deletion of Aire, Ifnlr1, Stat1, or Nlrc5, and is driven mainly by type III IFN produced by medullary TECs. Ifnlr1−/− mice show impaired negative selection of CD8 thymocytes and, at 9 mo of age, present autoimmune manifestations. Our study shows unanticipated variation in MHC I expression by ECs from various sites and provides compelling evidence that superior expression of MHC I in TECs is crucial for proper thymocyte education.

Footnotes

  • This work was supported by Canadian Institutes of Health Research Grant FDN-148400 (to C.P.). The CD1d–α-GalCer tetramers were obtained through the National Institutes of Health Tetramer Core Facility.

  • The RNA-sequencing data reported in this article have been submitted to the Gene Expression Omnibus database (http://www.ncbi.nlm.nih.gov/geo/) under accession number GSE144722.

  • The online version of this article contains supplemental material.

  • Received February 28, 2020.
  • Accepted June 24, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 206 (2)
The Journal of Immunology
Vol. 206, Issue 2
15 Jan 2021
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IFN-λ Enhances Constitutive Expression of MHC Class I Molecules on Thymic Epithelial Cells
Mohamed Benhammadi, Justine Mathé, Maude Dumont-Lagacé, Koichi S. Kobayashi, Louis Gaboury, Sylvie Brochu, Claude Perreault
The Journal of Immunology July 20, 2020, ji2000225; DOI: 10.4049/jimmunol.2000225

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IFN-λ Enhances Constitutive Expression of MHC Class I Molecules on Thymic Epithelial Cells
Mohamed Benhammadi, Justine Mathé, Maude Dumont-Lagacé, Koichi S. Kobayashi, Louis Gaboury, Sylvie Brochu, Claude Perreault
The Journal of Immunology July 20, 2020, ji2000225; DOI: 10.4049/jimmunol.2000225
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Print ISSN 0022-1767        Online ISSN 1550-6606