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ICOS-Deficient Regulatory T Cells Can Prevent Spontaneous Autoimmunity but Are Impaired in Controlling Acute Inflammation

Jinsam Chang, Antoine Bouchard, Yasser Bouklouch, Vincent Panneton, Joanna Li, Nikoletta Diamantopoulos, Saba Mohammaei, Roman Istomine, Fernando Alvarez, Ciriaco A. Piccirillo and Woong-Kyung Suh
J Immunol June 27, 2022, ji2100897; DOI: https://doi.org/10.4049/jimmunol.2100897
Jinsam Chang
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
†Molecular Biology Program, University of Montreal, Montreal, Quebec, Canada;
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Antoine Bouchard
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
†Molecular Biology Program, University of Montreal, Montreal, Quebec, Canada;
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Yasser Bouklouch
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
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Vincent Panneton
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
‡Department of Microbiology, Infectiology and Immunology, University of Montreal, Montreal, Quebec, Canada;
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Joanna Li
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
§Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada; and
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Nikoletta Diamantopoulos
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
§Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada; and
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Saba Mohammaei
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
¶Division of Experimental Medicine, McGill University, Montreal, Quebec, Canada
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Roman Istomine
§Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada; and
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Fernando Alvarez
§Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada; and
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Ciriaco A. Piccirillo
§Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada; and
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Woong-Kyung Suh
*Institut de Recherches Cliniques de Montréal, Montreal, QC, Canada;
†Molecular Biology Program, University of Montreal, Montreal, Quebec, Canada;
‡Department of Microbiology, Infectiology and Immunology, University of Montreal, Montreal, Quebec, Canada;
§Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada; and
¶Division of Experimental Medicine, McGill University, Montreal, Quebec, Canada
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Key Points

  • ICOS-deficient Treg cells can suppress spontaneous autoimmunity.

  • ICOS-deficient Treg cells show impaired differentiation of Th1-Treg cells.

Abstract

ICOS is induced in activated T cells and its main role is to boost differentiation and function of effector T cells. ICOS is also constitutively expressed in a subpopulation of Foxp3+ regulatory T cells under steady-state condition. Studies using ICOS germline knockout mice or ICOS-blocking reagents suggested that ICOS has supportive roles in regulatory T (Treg) cell homeostasis, migration, and function. To avoid any compounding effects that may arise from ICOS-deficient non–Treg cells, we generated a conditional knockout system in which ICOS expression is selectively abrogated in Foxp3-expressing cells (ICOS FC mice). Compared to Foxp3-Cre control mice, ICOS FC mice showed a minor numerical deficit of steady-state Treg cells but did not show any signs of spontaneous autoimmunity, indicating that tissue-protective Treg populations do not heavily rely on ICOS costimulation. However, ICOS FC mice showed more severe inflammation in oxazolone-induced contact hypersensitivity, a model of atopic dermatitis. This correlated with elevated numbers of inflammatory T cells expressing IFN-γ and/or TNF-α in ICOS FC mice compared with the control group. In contrast, elimination of ICOS in all T cell compartments negated the differences, confirming that ICOS has a dual positive role in effector and Treg cells. Single-cell transcriptome analysis suggested that ICOS-deficient Treg cells fail to mature into T-bet+CXCR3+ “Th1-Treg” cells in the draining lymph node. Our results suggest that regimens that preferentially stimulate ICOS pathways in Treg cells might be beneficial for the treatment of Th1-driven inflammation.

Footnotes

  • ↵1 J.C. and A.B. contributed equally to this work.

  • This work was supported by Canadian Institutes of Health Research Grants PJT-159526 (to W.-K.S.) and PJT-148821 (to C.A.P.).

  • The online version of this article contains supplemental material.

  • Received September 13, 2021.
  • Accepted May 2, 2022.
  • Copyright © 2022 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 209 (4)
The Journal of Immunology
Vol. 209, Issue 4
15 Aug 2022
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ICOS-Deficient Regulatory T Cells Can Prevent Spontaneous Autoimmunity but Are Impaired in Controlling Acute Inflammation
Jinsam Chang, Antoine Bouchard, Yasser Bouklouch, Vincent Panneton, Joanna Li, Nikoletta Diamantopoulos, Saba Mohammaei, Roman Istomine, Fernando Alvarez, Ciriaco A. Piccirillo, Woong-Kyung Suh
The Journal of Immunology June 27, 2022, ji2100897; DOI: 10.4049/jimmunol.2100897

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ICOS-Deficient Regulatory T Cells Can Prevent Spontaneous Autoimmunity but Are Impaired in Controlling Acute Inflammation
Jinsam Chang, Antoine Bouchard, Yasser Bouklouch, Vincent Panneton, Joanna Li, Nikoletta Diamantopoulos, Saba Mohammaei, Roman Istomine, Fernando Alvarez, Ciriaco A. Piccirillo, Woong-Kyung Suh
The Journal of Immunology June 27, 2022, ji2100897; DOI: 10.4049/jimmunol.2100897
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Print ISSN 0022-1767        Online ISSN 1550-6606