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Ubc9 Interacts with and SUMOylates the TCR Adaptor SLP-76 for NFAT Transcription in T Cells

Yiwei Xiong, Yulan Yi, Yan Wang, Naiqi Yang, Christopher E. Rudd and Hebin Liu
J Immunol December 1, 2019, 203 (11) 3023-3036; DOI: https://doi.org/10.4049/jimmunol.1900556
Yiwei Xiong
Department of Biological Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, Jiangsu Province 215123, China;
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  • ORCID record for Yiwei Xiong
Yulan Yi
Department of Biological Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, Jiangsu Province 215123, China;
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Yan Wang
Department of Biological Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, Jiangsu Province 215123, China;
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Naiqi Yang
Department of Biological Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, Jiangsu Province 215123, China;
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Christopher E. Rudd
Division of Immunology-Oncology Research Center, Maisonneuve-Rosemont Hospital, Montreal, Quebec H1T 2M4, Canada; andDépartement de Medicine, Université de Montréal, Montreal, Quebec H3C 3J7, Canada
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Hebin Liu
Department of Biological Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, Jiangsu Province 215123, China;
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Key Points

  • Ubc9 interacts with and SUMOylates the immune adaptor SLP-76 in T cells.

  • Synergy of SLP-76–Ubc9 on IL-2 transcription is SLP-76 SUMOylation dependent.

  • SLP-76 SUMOylation is required for Ubc9-NFAT complex assembly for IL-2 transcription.

Visual Abstract

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Abstract

Although the immune adaptor SH2 domain containing leukocyte phosphoprotein of 76 kDa (SLP-76) integrates and propagates the TCR signaling, the regulation of SLP-76 during the TCR signaling is incompletely studied. In this article, we report that SLP-76 interacts with the small ubiquitin-like modifier (SUMO) E2 conjugase Ubc9 and is a substrate for Ubc9-mediated SUMOylation in human and mouse T cells. TCR stimulation promotes SLP-76–Ubc9 binding, accompanied by an increase in SLP-76 SUMOylation. Ubc9 binds to the extreme C terminus of SLP-76 spanning residues 516–533 and SUMOylates SLP-76 at two conserved residues K266 and K284. In addition, SLP-76 and Ubc9 synergizes to augment the TCR-mediated IL-2 transcription by NFAT in a manner dependent of SUMOylation of SLP-76. Moreover, although not affecting the TCR proximal signaling events, the Ubc9-mediated SUMOylation of SLP-76 is required for TCR-induced assembly of Ubc9-NFAT complex for IL-2 transcription. Together, these results suggest that Ubc9 modulates the function of SLP-76 in T cell activation both by direct interaction and by SUMOylation of SLP-76 and that the Ubc9–SLP-76 module acts as a novel regulatory complex in the control of T cell activation.

Footnotes

  • This work was supported by grants from the National Natural Science Foundation of China (31470840 to H.L.) and the Suzhou Key Program Special Fund (KSF-E-30 to H.L.).

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    ADAP
    adhesion and degranulation-promoting adapter protein
    ChIP
    chromatin immunoprecipitation
    GADS
    Grb2-related adaptor downstream of Shc
    HA
    hemagglutinin
    LC-MS/MS
    liquid chromatography–tandem mass spectrometry
    PLCγ1
    phospholipase Cγ1
    PRR
    proline-rich region
    RanGAP1
    Ran GTPase activating protein 1
    SKAP1
    src kinase associated phosphoprotein 1
    SLP-76
    SH2 domain containing leukocyte phosphoprotein of 76 kDa
    SUMO
    small ubiquitin-like modifier
    WT
    wild type.

  • Received May 14, 2019.
  • Accepted September 30, 2019.
  • Copyright © 2019 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 203 (11)
The Journal of Immunology
Vol. 203, Issue 11
1 Dec 2019
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Ubc9 Interacts with and SUMOylates the TCR Adaptor SLP-76 for NFAT Transcription in T Cells
Yiwei Xiong, Yulan Yi, Yan Wang, Naiqi Yang, Christopher E. Rudd, Hebin Liu
The Journal of Immunology December 1, 2019, 203 (11) 3023-3036; DOI: 10.4049/jimmunol.1900556

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Ubc9 Interacts with and SUMOylates the TCR Adaptor SLP-76 for NFAT Transcription in T Cells
Yiwei Xiong, Yulan Yi, Yan Wang, Naiqi Yang, Christopher E. Rudd, Hebin Liu
The Journal of Immunology December 1, 2019, 203 (11) 3023-3036; DOI: 10.4049/jimmunol.1900556
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