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FoxP3+RORγt+ T Helper Intermediates Display Suppressive Function against Autoimmune Diabetes

Danielle M. Tartar, Amie M. VanMorlan, Xiaoxiao Wan, F. Betul Guloglu, Renu Jain, Cara L. Haymaker, Jason S. Ellis, Christine M. Hoeman, Jason A. Cascio, Mermagya Dhakal, Mohamed Oukka and Habib Zaghouani
J Immunol April 1, 2010, 184 (7) 3377-3385; DOI: https://doi.org/10.4049/jimmunol.0903324
Danielle M. Tartar
*Department of Molecular Microbiology and Immunology and
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Amie M. VanMorlan
†Department of Child Health, University of Missouri School of Medicine, Columbia, MO 65212; and
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Xiaoxiao Wan
*Department of Molecular Microbiology and Immunology and
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F. Betul Guloglu
*Department of Molecular Microbiology and Immunology and
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Renu Jain
*Department of Molecular Microbiology and Immunology and
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Cara L. Haymaker
*Department of Molecular Microbiology and Immunology and
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Jason S. Ellis
*Department of Molecular Microbiology and Immunology and
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Christine M. Hoeman
*Department of Molecular Microbiology and Immunology and
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Jason A. Cascio
*Department of Molecular Microbiology and Immunology and
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Mermagya Dhakal
*Department of Molecular Microbiology and Immunology and
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Mohamed Oukka
‡Center for Neurologic Diseases, Harvard University, Boston, MA 02115
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Habib Zaghouani
*Department of Molecular Microbiology and Immunology and
†Department of Child Health, University of Missouri School of Medicine, Columbia, MO 65212; and
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Abstract

Recently, traces of double-positive FoxP3+RORγt+ T cells were identified and viewed as dual programming differentiation intermediates geared toward development into T regulatory or Th17 cells. In this study, we report that FoxP3+RORγt+ intermediates arise in the NOD mouse T cell repertoire prior to inflammation and can be expanded with tolerogen without further differentiation. Furthermore, FoxP3+RORγt+ cells express both CD62L and membrane-bound TGFβ and use the former to traffic to the pancreas and the latter to suppress effector T cells both in vitro and in vivo. The cells perform these functions as FoxP3+RORγt+ intermediates, despite being able to terminally differentiate into either FoxP3+RORγt− T regulatory or FoxP3−RORγt+ Th17 cells on polarization. These previously unrecognized observations extend plasticity to both differentiation and function and indicate that the intermediates are poised to traffic to sites of inflammation and target diverse pathogenic T cells, likely without prior conditioning by effector T cells, thus broadening efficacy against autoimmunity.

Footnotes

  • This work was supported by National Institutes of Health Grants RO1DK65748 and R21AI68746 (to H.Z.). D.M.T. and J.A.C. were supported by Life Sciences Fellowships from the University of Missouri, Columbia. C.M.H. was supported by National Institute of General Medical Sciences training Grant GM008396.

  • The online version of this article contains supplemental material.

  • Abbreviations used in this paper:

    GAD
    glutamic acid decarboxylase
    hi
    high
    int
    intermediate
    mTGFβ
    membrane-bound active TGFβ
    RQ
    relative quantity
    TID
    type I diabetes
    Tregs
    T regulatory cells.

  • Received October 13, 2009.
  • Accepted January 21, 2010.
  • Copyright © 2010 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 184 (7)
The Journal of Immunology
Vol. 184, Issue 7
1 Apr 2010
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FoxP3+RORγt+ T Helper Intermediates Display Suppressive Function against Autoimmune Diabetes
Danielle M. Tartar, Amie M. VanMorlan, Xiaoxiao Wan, F. Betul Guloglu, Renu Jain, Cara L. Haymaker, Jason S. Ellis, Christine M. Hoeman, Jason A. Cascio, Mermagya Dhakal, Mohamed Oukka, Habib Zaghouani
The Journal of Immunology April 1, 2010, 184 (7) 3377-3385; DOI: 10.4049/jimmunol.0903324

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FoxP3+RORγt+ T Helper Intermediates Display Suppressive Function against Autoimmune Diabetes
Danielle M. Tartar, Amie M. VanMorlan, Xiaoxiao Wan, F. Betul Guloglu, Renu Jain, Cara L. Haymaker, Jason S. Ellis, Christine M. Hoeman, Jason A. Cascio, Mermagya Dhakal, Mohamed Oukka, Habib Zaghouani
The Journal of Immunology April 1, 2010, 184 (7) 3377-3385; DOI: 10.4049/jimmunol.0903324
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