Uni-directional ciliary membrane protein trafficking by a cytoplasmic retrograde IFT motor and ciliary ectosome shedding

  1. Muqing Cao
  2. Jue Ning
  3. Carmen I Hernandez-Lara
  4. Olivier Belzile
  5. Qian Wang
  6. Susan K Dutcher
  7. Yanjie Liu
  8. William J Snell  Is a corresponding author
  1. University of Texas Southwestern Medical Center, United States
  2. Washington University, United States

Abstract

The role of the primary cilium in key signaling pathways depends on dynamic regulation of ciliary membrane protein composition, yet we know little about the motors or membrane events that regulate ciliary membrane protein trafficking in existing organelles. Recently, we showed that cilium-generated signaling in Chlamydomonas induced rapid, anterograde IFT-independent, cytoplasmic microtubule-dependent redistribution of the membrane polypeptide, SAG1-C65, from the plasma membrane to the periciliary region and the ciliary membrane. Here, we report that the retrograde IFT motor, cytoplasmic dynein 1b, is required in the cytoplasm for this rapid redistribution. Furthermore, signaling-induced trafficking of SAG1-C65 into cilia is unidirectional and the entire complement of cellular SAG1-C65 is shed during signaling and can be recovered in the form of ciliary ectosomes that retain signal-inducing activity. Thus, during signaling, cells regulate ciliary membrane protein composition through cytoplasmic action of the retrograde IFT motor and shedding of ciliary ectosomes.

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Author details

  1. Muqing Cao

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jue Ning

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Carmen I Hernandez-Lara

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Olivier Belzile

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Qian Wang

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Susan K Dutcher

    Department of Genetics, Washington University, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Yanjie Liu

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. William J Snell

    Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, United States
    For correspondence
    william.snell@utsouthwestern.edu
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, Cao 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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  1. Muqing Cao
  2. Jue Ning
  3. Carmen I Hernandez-Lara
  4. Olivier Belzile
  5. Qian Wang
  6. Susan K Dutcher
  7. Yanjie Liu
  8. William J Snell
(2015)
Uni-directional ciliary membrane protein trafficking by a cytoplasmic retrograde IFT motor and ciliary ectosome shedding
eLife 4:e05242.
https://doi.org/10.7554/eLife.05242

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https://doi.org/10.7554/eLife.05242