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SUMOylation of DDX39A Alters Binding and Export of Antiviral Transcripts to Control Innate Immunity

Peidian Shi, Yanyu Guo, Yanxin Su, Min Zhu, Yali Fu, Heng Chi, Jiaqi Wu and Jinhai Huang
J Immunol May 11, 2020, ji2000053; DOI: https://doi.org/10.4049/jimmunol.2000053
Peidian Shi
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Yanyu Guo
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Yanxin Su
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Min Zhu
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Yali Fu
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Heng Chi
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Jiaqi Wu
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Jinhai Huang
School of Life Sciences, Tianjin University, Tianjin 300072, China
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Key Points

  • DDX39A impairs IFN-β production by preferentially binding to antiviral transcripts.

  • SUMO1 modification of DDX39A alters binding of antiviral transcripts.

  • RanBP2 mediates SUMO1 modification of DDX39A.

Abstract

The RNA helicase DDX39A plays an important role in the RNA splicing/export process. In our study, human DDX39A facilitated RNA virus escape from innate immunity to promote virus proliferation by trapping TRAF3, TRAF6, and MAVS mRNAs in the HEK293T cell nucleus. DDX39A was a target for SUMOylation. SUMO1, 2, and 3 modifications were found on immunoprecipitated DDX39A. However, only the SUMO1 modification decreased in vesicular stomatitis virus–infected HEK293T cells. Further studies have found that viral infection reduced SUMO1 modification of DDX39A and enhanced its ability to bind innate immunity–associated mRNAs by regulating the abundance of RanBP2 with SUMO1 E3 ligase activity. RanBP2 acted as an E3 SUMO ligase of DDX39A, which enhanced SUMO1 modification of DDX39A and attenuated its ability to bind RNA. This work described that specific mRNAs encoding antiviral signaling components were bound and sequestered in the nucleus by DDX39A to limit their expression, which proposed a new protein SUMOylation model to regulate innate immunity in viral infection.

Footnotes

  • This work was supported by the National Key Research and Development Program of China (2018YFD0500500) and the National Natural Science Foundation of China (31272540).

  • The online version of this article contains supplemental material.

  • Received January 21, 2020.
  • Accepted April 21, 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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SUMOylation of DDX39A Alters Binding and Export of Antiviral Transcripts to Control Innate Immunity
Peidian Shi, Yanyu Guo, Yanxin Su, Min Zhu, Yali Fu, Heng Chi, Jiaqi Wu, Jinhai Huang
The Journal of Immunology May 11, 2020, ji2000053; DOI: 10.4049/jimmunol.2000053

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SUMOylation of DDX39A Alters Binding and Export of Antiviral Transcripts to Control Innate Immunity
Peidian Shi, Yanyu Guo, Yanxin Su, Min Zhu, Yali Fu, Heng Chi, Jiaqi Wu, Jinhai Huang
The Journal of Immunology May 11, 2020, ji2000053; DOI: 10.4049/jimmunol.2000053
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Print ISSN 0022-1767        Online ISSN 1550-6606