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Bardet-Biedl Syndrome 3 protein promotes ciliary exit of the signaling protein phospholipase D via the BBSome

  1. Yan-Xia Liu
  2. Bin Xue
  3. Wei-Yue Sun
  4. Jenna L Wingfield
  5. Jun Sun
  6. Mingfu Wu
  7. Karl F Lechtreck
  8. Zhenlong Wu
  9. Zhen-Chuan Fan  Is a corresponding author
  1. Tianjin University of Science and Technology, China
  2. University of Georgia, United States
  3. Albany Medical College, United States
  4. China Agricultural University, China
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Cite this article as: eLife 2021;10:e59119 doi: 10.7554/eLife.59119

Abstract

Certain ciliary signaling proteins couple with the BBSome, a conserved complex of Bardet-Biedl syndrome (BBS) proteins, to load onto retrograde intraflagellar transport (IFT) trains for their removal out of cilia in Chlamydomonas reinhardtii. Here, we show that loss of the Arf-like 6 (ARL6) GTPase BBS3 causes the signaling protein phospholipase D (PLD) to accumulate in cilia. Upon targeting to the basal body, BBSomes enter and cycle through cilia via IFT, while BBS3 in a GTP-bound state separates from BBSomes, associates with the membrane, and translocates from the basal body to cilia by diffusion. Upon arriving at the ciliary tip, GTP-bound BBS3 binds and recruits BBSomes to the ciliary membrane for interacting with PLD, thus making the PLD-laden BBSomes available to load onto retrograde IFT trains for ciliary exit. Therefore, BBS3 promotes PLD exit from cilia via the BBSome providing a regulatory mechanism for ciliary signaling protein removal out of cilia.

Article and author information

Author details

  1. Yan-Xia Liu

    Institute of Health Biotechnology, Tianjin University of Science and Technology, Tianjin, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Bin Xue

    Institute of Health Biotechnology, Tianjin University of Science and Technology, Tianjin, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Wei-Yue Sun

    Institute of Health Biotechnology, Tianjin University of Science and Technology, Tianjin, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Jenna L Wingfield

    Department of Cellular Biology, University of Georgia, Athens, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jun Sun

    Institute of Health Biotechnology, Tianjin University of Science and Technology, Tianjin, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Mingfu Wu

    Department of Molecular and Cellular Physiology, Albany Medical College, Albany, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Karl F Lechtreck

    Department of Cellular Biology, University of Georgia, Athens, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Zhenlong Wu

    State Key Laboratory of Animal Nutrition, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Zhen-Chuan Fan

    Institute of Health Biotechnology, Tianjin University of Science and Technology, Tianjin, China
    For correspondence
    fanzhen@tust.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3007-4281

Funding

International Center for Genetic Engineering and Biotechnology (CRP/CHN15-01)

  • Zhen-Chuan Fan

National Natural Science Foundation of China (41876134)

  • Jun Sun

National Institutes of Health (GM110413)

  • Karl F Lechtreck

National Natural Science Foundation of China (32070698)

  • Zhen-Chuan Fan

Tianjin Municipal Science and Technology Bureau (19PTSYJC00050)

  • Zhen-Chuan Fan

Tianjin Municipal Science and Technology Bureau (18JCZDJC34100)

  • Zhen-Chuan Fan

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

Reviewing Editor

  1. Junmin Pan, Tsinghua University, China

Publication history

  1. Received: May 20, 2020
  2. Accepted: February 13, 2021
  3. Accepted Manuscript published: February 15, 2021 (version 1)

Copyright

© 2021, 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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