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

Elife. 2019 Jul 1;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.

Keywords: C. elegans; PI(4,5)P2; PIP 5 kinase; cell biology; cilia; sensory signaling; tub-1 tubby.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Protein Complex 2 / genetics*
  • Animals
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans / physiology
  • Caenorhabditis elegans Proteins / genetics*
  • Cilia / genetics
  • Cilia / metabolism
  • Lipids / genetics
  • Morphogenesis / genetics
  • Olfactory Receptor Neurons / metabolism*
  • Olfactory Receptor Neurons / physiology
  • Protein Transport / genetics
  • Signal Transduction / genetics

Substances

  • Adaptor Protein Complex 2
  • Caenorhabditis elegans Proteins
  • Dpy-23 protein, C elegans
  • Lipids
  • tub-1 protein, C elegans