Patterned by Smell

Science Signaling  20 May 2008:
Vol. 1, Issue 20, pp. ec187
DOI: 10.1126/stke.120ec187

Olfactory and visual signals are transduced through nonmotile cilia, some of which have elaborate structural modifications. Mukhopadhyay et al. report that the architecture of one such sensory neuron’s cilia are shaped by the sensory input the cell receives. The AWB neuron in the nematode Caenorhabditis elegans is a chemosensory neuron that detects repulsive cues from bacteria through long, branched cilia. The AWB of worms raised without bacteria in the culture medium had cilia with short, wide branches with increased membrane surface area. This phenotype was also observed in worms that lacked any one of several proteins required in AWB for sensory signaling, including two cyclic nucleotide-gated channel subunits, a guanylyl cyclase, and a G protein-coupled receptor kinase. Cilium remodeling also required the second messengers Ca2+ and guanosine 3',5'-monophosphate (cGMP), as well as proteins required for ciliary biogenesis such as Kinesin-II and RAB8. The signaling requirement for proper morphology was cell-autonomous, because transgenically providing these proteins to only the AWB neuron restored wild-type morphology. TAX-2, a subunit of cyclic nucleotide-gated ion channel predicted to be permeable to Ca2+, was specifically required during late larval development to maintain wild-type ciliary structure, because inactivation of tax-2 during this time period using temperature-sensitive alleles produced cilia with altered morphology. Therefore, the ciliary architecture of the AWB neuron was affected by sensory input only during a defined developmental window. These findings identify a cell-autonomous requirement for sensory input in shaping the structure of the sensory cilia and suggest that plasticity in ciliary architecture could provide a means for increasing the sensory surface area (and therefore increasing sensitivity) to olfactory signals as an adaptation to sensory deprivation experienced during a critical developmental time period.

S. Mukhopadhyay, Y. Lu, S. Shaham, P. Sengupta, Sensory signaling-dependent remodeling of olfactory cilia architecture in C. elegans. Dev. Cell 14, 762-774 (2008). [PubMed]

J. F. Reiter, A cilium is not a cilium is not a cilium: Signaling contributes to ciliary morphological diversity. Dev. Cell 14, 635-636 (2008). [PubMed]