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

Phuong Anh T Nguyen, Willisa Liou, David H. Hall, Michel R. Leroux

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)5317-5330
Number of pages14
JournalJournal of Cell Science
Volume127
Issue number24
DOIs
StatePublished - 2014

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Neurons
Cyclic GMP
Mammals
Proteins
Bardet-Biedl Syndrome
Cilia
Guanylate Cyclase
Caenorhabditis elegans
Sensory Receptor Cells
Microvilli
Dendrites
Ion Channels
Signal Transduction
Lipids
Membranes
Ciliopathies
Bardet-Biedl Syndrome 8
Meckel syndrome type 1

Keywords

  • cGMP signaling
  • Compartmentalization
  • Primary cilia
  • Sensory neuron
  • Thermotaxis
  • Transition zone

ASJC Scopus subject areas

  • Cell Biology

Cite this

Ciliopathy proteins establish a bipartite signaling compartment in a C. elegans thermosensory neuron. / Nguyen, Phuong Anh T; Liou, Willisa; Hall, David H.; Leroux, Michel R.

In: Journal of Cell Science, Vol. 127, No. 24, 2014, p. 5317-5330.

Research output: Contribution to journalArticle

Nguyen, Phuong Anh T ; Liou, Willisa ; Hall, David H. ; Leroux, Michel R. / Ciliopathy proteins establish a bipartite signaling compartment in a C. elegans thermosensory neuron. In: Journal of Cell Science. 2014 ; Vol. 127, No. 24. pp. 5317-5330.
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