1. Biochemistry and Chemical Biology
  2. Cell Biology
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Phospholipase D activity couples plasma membrane endocytosis with retromer dependent recycling

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Cite this article as: eLife 2016;5:e18515 doi: 10.7554/eLife.18515

Abstract

During illumination, the light sensitive plasma membrane (rhabdomere) of Drosophila photoreceptors undergoes turnover with consequent changes in size and composition. However the mechanism by which illumination is coupled to rhabdomere turnover remains unclear. We find that photoreceptors contain a light-dependent phospholipase D (PLD) activity. During illumination, loss of PLD resulted in an enhanced reduction in rhabdomere size, accumulation of Rab7 positive, rhodopsin1-containing vesicles (RLVs) in the cell body and reduced rhodopsin protein. These phenotypes were associated with reduced levels of phosphatidic acid, the product of PLD activity and were rescued by reconstitution with catalytically active PLD. In wild type photoreceptors, during illumination, enhanced PLD activity was sufficient to clear RLVs from the cell body by a process dependent on Arf1-GTP levels and retromer complex function. Thus, during illumination, PLD activity couples endocytosis of RLVs with their recycling to the plasma membrane thus maintaining plasma membrane size and composition.

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Author details

  1. Rajan Thakur

    National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9511-5729
  2. Aniruddha Panda

    National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  3. Elise Coessens

    Inositide Laboratory, Babraham Institute, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Nikita Raj

    National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  5. Shweta Yadav

    National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  6. Sruthi Balakrishnan

    National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  7. Qifeng Zhang

    Inositide Laboratory, Babraham Institute, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Plamen Georgiev

    Inositide Laboratory, Babraham Institute, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Bishal Basak

    National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  10. Renu Pasricha

    National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  11. Michael JO Wakelam

    Inositide Laboratory, Babraham Institute, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Nicholas T Ktistakis

    Inositide Laboratory, Babraham Institute, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9397-2914
  13. Raghu Padinjat

    National Centre for Biological Sciences, Bangalore, India
    For correspondence
    praghu@ncbs.res.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3578-6413

Funding

Wellcome Trust DBT India Alliance (IA/S/14/2/501540)

  • Rajan Thakur
  • Nikita Raj
  • Shweta Yadav
  • Sruthi Balakrishnan
  • Bishal Basak
  • Raghu Padinjat

National Centre for Biological Sciences (core)

  • Rajan Thakur
  • Aniruddha Panda
  • Nikita Raj
  • Shweta Yadav
  • Sruthi Balakrishnan
  • Bishal Basak
  • Renu Pasricha
  • Raghu Padinjat

Department of Biotechnology , Ministry of Science and Technology (BT/PR4833/MED/30/744/2012)

  • Rajan Thakur
  • Aniruddha Panda
  • Nikita Raj
  • Shweta Yadav
  • Sruthi Balakrishnan
  • Bishal Basak
  • Renu Pasricha
  • Raghu Padinjat

Biotechnology and Biological Sciences Research Council (core)

  • Elise Coessens
  • Qifeng Zhang
  • Plamen Georgiev
  • Michael JO Wakelam
  • Nicholas T Ktistakis

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

Reviewing Editor

  1. Randy Schekman, Howard Hughes Medical Institute, University of California, Berkeley, United States

Publication history

  1. Received: June 5, 2016
  2. Accepted: November 14, 2016
  3. Accepted Manuscript published: November 16, 2016 (version 1)
  4. Version of Record published: November 28, 2016 (version 2)

Copyright

© 2016, Thakur 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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