Centrioles initiate cilia assembly but are dispensable for maturation and maintenance in C. elegans

J Cell Biol. 2017 Jun 5;216(6):1659-1671. doi: 10.1083/jcb.201610070. Epub 2017 Apr 14.

Abstract

Cilia are cellular projections that assemble on centriole-derived basal bodies. While cilia assembly is absolutely dependent on centrioles, it is not known to what extent they contribute to downstream events. The nematode C. elegans provides a unique opportunity to address this question, as centrioles do not persist at the base of mature cilia. Using fluorescence microscopy and electron tomography, we find that centrioles degenerate early during ciliogenesis. The transition zone and axoneme are not completely formed at this time, indicating that cilia maturation does not depend on intact centrioles. The hydrolethalus syndrome protein HYLS-1 is the only centriolar protein known to remain at the base of mature cilia and is required for intraflagellar transport trafficking. Surprisingly, targeted degradation of HYLS-1 after initiation of ciliogenesis does not affect ciliary structures. Taken together, our results indicate that while centrioles are essential to initiate cilia formation, they are dispensable for cilia maturation and maintenance.

Publication types

  • Video-Audio Media
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Axoneme / physiology
  • Basal Bodies / metabolism
  • Basal Bodies / physiology*
  • Basal Bodies / ultrastructure
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans / ultrastructure
  • Caenorhabditis elegans Proteins / metabolism
  • Centrioles / metabolism
  • Centrioles / physiology*
  • Centrioles / ultrastructure
  • Cilia / physiology
  • Electron Microscope Tomography
  • Microscopy, Fluorescence
  • Microscopy, Video
  • Neurogenesis*
  • Proteolysis
  • Sensory Receptor Cells / metabolism
  • Sensory Receptor Cells / physiology*
  • Sensory Receptor Cells / ultrastructure
  • Time Factors
  • Time-Lapse Imaging

Substances

  • Caenorhabditis elegans Proteins
  • HYLS-1 protein, C elegans