Ciliopathy proteins establish a bipartite signaling compartment in a C. elegans thermosensory neuron

J Cell Sci. 2014 Dec 15;127(Pt 24):5317-30. doi: 10.1242/jcs.157610. Epub 2014 Oct 21.


How signaling domains form is an important, yet largely unexplored question. Here, we show that ciliary proteins help establish two contiguous, yet distinct cyclic GMP (cGMP) signaling compartments in Caenorhabditis elegans thermosensory AFD neurons. One compartment, a bona fide cilium, is delineated by proteins associated with Bardet-Biedl syndrome (BBS), Meckel syndrome and nephronophthisis at its base, and requires NPHP-2 (known as inversin in mammals) to anchor a cGMP-gated ion channel within the proximal ciliary region. The other, a subcompartment with profuse microvilli and a different lipid environment, is separated from the dendrite by a cellular junction and requires BBS-8 and DAF-25 (known as Ankmy2 in mammals) for correct localization of guanylyl cyclases needed for thermosensation. Consistent with a requirement for a membrane diffusion barrier at the subcompartment base, we reveal the unexpected presence of ciliary transition zone proteins where no canonical transition zone ultrastructure exists. We propose that differential compartmentalization of signal transduction components by ciliary proteins is important for the functions of ciliated sensory neurons.

Keywords: Compartmentalization; Primary cilia; Sensory neuron; Thermotaxis; Transition zone; cGMP signaling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Animals
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Compartmentation*
  • Cilia / metabolism*
  • Cyclic GMP / metabolism
  • Dendrites / metabolism
  • Guanylate Cyclase / metabolism
  • Intercellular Junctions / metabolism
  • Intermediate Filaments / metabolism
  • Lipids / chemistry
  • Models, Biological
  • Mutation / genetics
  • Protein Transport
  • Sensory Receptor Cells / cytology*
  • Sensory Receptor Cells / metabolism*
  • Signal Transduction*
  • Temperature*
  • Tomography


  • Actins
  • Caenorhabditis elegans Proteins
  • Lipids
  • Guanylate Cyclase
  • Cyclic GMP