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The C. elegans Tubby homolog dynamically modulates olfactory cilia membrane morphogenesis and phospholipid composition

  1. Danielle DiTirro
  2. Alison Philbrook
  3. Kendrick Rubino
  4. Piali Sengupta  Is a corresponding author
  1. Brandeis University, United States
Research Article
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Cite this article as: eLife 2019;8:e48789 doi: 10.7554/eLife.48789

Abstract

Plasticity in sensory signaling is partly mediated via regulated trafficking of signaling molecules to and from primary cilia. Tubby-related proteins regulate ciliary protein transport; however, their roles in remodeling cilia properties are not fully understood. We find that the C. elegans TUB-1 Tubby homolog regulates membrane morphogenesis and signaling protein transport in specialized sensory cilia. In particular, TUB-1 is essential for sensory signaling-dependent reshaping of olfactory cilia morphology. We show that compromised sensory signaling alters cilia membrane phosphoinositide composition via TUB-1-dependent trafficking of a PIP5 kinase. TUB-1 regulates localization of this lipid kinase at the cilia base in part via localization of the AP-2 adaptor complex subunit DPY-23. Our results describe new functions for Tubby proteins in the dynamic regulation of cilia membrane lipid composition, morphology, and signaling protein content, and suggest that this conserved family of proteins plays a critical role in mediating cilia structural and functional plasticity.

Article and author information

Author details

  1. Danielle DiTirro

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  2. Alison Philbrook

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  3. Kendrick Rubino

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
  4. Piali Sengupta

    Department of Biology, Brandeis University, Waltham, United States
    For correspondence
    sengupta@brandeis.edu
    Competing interests
    Piali Sengupta, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7468-0035

Funding

National Institute of General Medical Sciences (R35 GM122463)

  • Piali Sengupta

National Institute of Neurological Disorders and Stroke (T32 NS007292)

  • Alison Philbrook

National Institute of General Medical Sciences (T32 GM007122)

  • Danielle DiTirro

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

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Publication history

  1. Received: May 24, 2019
  2. Accepted: June 21, 2019
  3. Accepted Manuscript published: July 1, 2019 (version 1)
  4. Version of Record published: July 11, 2019 (version 2)

Copyright

© 2019, DiTirro 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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