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The exon junction complex regulates the splicing of cell polarity gene dlg1 to control Wingless signaling in development

  1. Min Liu
  2. Yajuan Li
  3. Aiguo Liu
  4. Ruifeng Li
  5. Ying Su
  6. Juan Du
  7. Cheng Li
  8. Alan Jian Zhu  Is a corresponding author
  1. Peking University, China
  2. Ocean University of China, China
Research Article
  • Cited 6
  • Views 1,813
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Cite this article as: eLife 2016;5:e17200 doi: 10.7554/eLife.17200

Abstract

Wingless (Wg)/Wnt signaling is conserved in all metazoan animals and plays critical roles in development. The Wg/Wnt morphogen reception is essential for signal activation, whose activity is mediated through the receptor complex and a scaffold protein Dishevelled (Dsh). We report here that the exon junction complex (EJC) activity is indispensable for Wg signaling by maintaining an appropriate level of Dsh protein for Wg ligand reception in Drosophila. Transcriptome analyses in Drosophila wing imaginal discs indicate that the EJC controls the splicing of the cell polarity gene discs large 1 (dlg1), whose coding prote¬in directly interacts with Dsh. Genetic and biochemical experiments demonstrate that Dlg1 protein acts independently from its role in cell polarity to protect Dsh protein from lysosomal degradation. More importantly, human orthologous Dlg protein is sufficient to promote Dvl protein stabilization and Wnt signaling activity, thus revealing a conserved regulatory mechanism of Wg/Wnt signaling by Dlg and EJC.

Article and author information

Author details

  1. Min Liu

    State Key Laboratory of Membrane Biology, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Yajuan Li

    State Key Laboratory of Membrane Biology, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Aiguo Liu

    State Key Laboratory of Membrane Biology, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Ruifeng Li

    Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ying Su

    Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Juan Du

    State Key Laboratory of Membrane Biology, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Cheng Li

    Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Alan Jian Zhu

    State Key Laboratory of Membrane Biology, Peking University, Beijing, China
    For correspondence
    zhua@pku.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8208-1729

Funding

State Key Laboratory of Membrane Biology of the People's Republic of China (Grant)

  • Alan Jian Zhu

Peking-Tsinghua Center for Life Sciences (Grant)

  • Cheng Li
  • Alan Jian Zhu

Ministry of Science and Technology of the People's Republic of China (2014CB942804)

  • Alan Jian Zhu

National Science Foundation of the People's Republic of China (31371410)

  • Alan Jian Zhu

National Science Foundation of the People's Republic of China (31401241)

  • Min Liu

China Postdoctoral Science Foundation (Postdoctoral Fellowship, 2014M550556)

  • Min Liu

Peking-Tsinghua Center for Life Sciences (Postdoctoral Fellowship)

  • Min Liu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Duojia Pan, UT Southwestern Medical Center, United States

Publication history

  1. Received: April 24, 2016
  2. Accepted: August 14, 2016
  3. Accepted Manuscript published: August 18, 2016 (version 1)
  4. Version of Record published: September 1, 2016 (version 2)

Copyright

© 2016, Liu et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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