Sensory signaling-dependent remodeling of olfactory cilia architecture in C. elegans

Dev Cell. 2008 May;14(5):762-74. doi: 10.1016/j.devcel.2008.03.002.

Abstract

Nonmotile primary cilia are sensory organelles composed of a microtubular axoneme and a surrounding membrane sheath that houses signaling molecules. Optimal cellular function requires the precise regulation of axoneme assembly, membrane biogenesis, and signaling protein targeting and localization via as yet poorly understood mechanisms. Here, we show that sensory signaling is required to maintain the architecture of the specialized AWB olfactory neuron cilia in C. elegans. Decreased sensory signaling results in alteration of axoneme length and expansion of a membraneous structure, thereby altering the topological distribution of a subset of ciliary transmembrane signaling molecules. Signaling-regulated alteration of ciliary structures can be bypassed by modulation of intracellular cGMP or calcium levels and requires kinesin-II-driven intraflagellar transport (IFT), as well as BBS- and RAB8-related proteins. Our results suggest that compensatory mechanisms in response to altered levels of sensory activity modulate AWB cilia architecture, revealing remarkable plasticity in the regulation of cilia structure.

Publication types

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

MeSH terms

  • Animals
  • Bacteria
  • Biological Transport
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans / ultrastructure*
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism
  • Cell Membrane / metabolism
  • Cilia / ultrastructure*
  • Cyclic GMP / metabolism
  • Embryonic Development
  • Ion Channels / metabolism
  • Kinesin / metabolism
  • Larva
  • Mutation / genetics
  • Olfactory Receptor Neurons / cytology*
  • Olfactory Receptor Neurons / ultrastructure*
  • Phenotype
  • Protein Binding
  • Signal Transduction*

Substances

  • Caenorhabditis elegans Proteins
  • Ion Channels
  • tax-2 protein, C elegans
  • kinesin-II
  • Kinesin
  • Cyclic GMP
  • Calcium