Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans

Abstract

The diversity of sensory cilia on Caenorhabditis elegans neurons allows the animal to detect a variety of sensory stimuli. Sensory cilia are assembled by intraflagellar transport (IFT) kinesins, which transport ciliary precursors, bound to IFT particles, along the ciliary axoneme for incorporation into ciliary structures. Using fluorescence microscopy of living animals and serial section electron microscopy of high pressure–frozen, freeze-substituted IFT motor mutants, we found that two IFT kinesins, homodimeric OSM-3 kinesin and heterotrimeric kinesin II, function in a partially redundant manner to build full-length amphid channel cilia but are completely redundant for building full-length amphid wing (AWC) cilia. This difference reflects cilia-specific differences in OSM-3 activity, which serves to extend distal singlets in channel cilia but not in AWC cilia, which lack such singlets. Moreover, AWC-specific chemotaxis assays reveal novel sensory functions for kinesin II in these wing cilia. We propose that kinesin II is a “canonical” IFT motor, whereas OSM-3 is an “accessory” IFT motor, and that subtle changes in the deployment or actions of these IFT kinesins can contribute to differences in cilia morphology, cilia function, and sensory perception.

Kinesin-2 family in vertebrate ciliogenesis

“…A limited role for kif17 in zebrafish ciliogenesis, especially in double mutants with kif3b, is surprising, given the prominent function of this kinesin in C. elegans cilia (31,36). In vertebrates, the function of kif17 has been studied in tissue culture as well as in mouse and zebrafish models.…”

IFT‐81 and IFT‐74 are required for intraflagellar transport in C. elegans

“…Here, we used a model organism, C. elegans. In C. elegans, 60 of the 302 neurons of the hermaphrodite are ciliated sensory neurons, and several works have demonstrated that the mutants of IFT-related genes show defects in sensory functions (Cole et al 1998;Signor et al 1999;Qin et al 2001;Haycraft et al 2003;Schafer et al 2003;Blacque et al 2004;Scholey et al 2004;Snow et al 2004;Ou et al 2005;Bell et al 2006;Evans et al 2006). In the present work, we identified nematode IFT-81 and IFT-74, whose C. reinhardtii orthologues were recently shown to form core complex in subcomplex B (Lucker et al 2005), and attempted to elucidate their physiological roles in C. elegans.…”

Assembly of primary cilia

“…This homodimeric kinesin-2 motor was first characterized in C. elegans where it is known as OSM-3 (Shakir et al, 1993;Signor et al, 1999b), and it has subsequently been identified in cilia of Tetrahymena and some vertebrate cell types, where it is named Kin5 and KIF17, respectively (Awan et al, 2004;Setou et al, 2000). Genetic and motility studies in C. elegans have suggested that OSM-3 functions as an accessory anterograde IFT motor involved in the assembly or function of specific subsets of sensory cilia, thereby contributing to the generation of ciliary structural and functional diversity (Evans et al, 2006;Mukhopadhyay et al, 2007). For example, in the C. elegans amphid channel cilia, OSM-3 appears to cooperate with kinesin-II to drive anterograde IFT along the middle segment of the cilia, where the axoneme consists of doublet MTs; OSM-3 alone mediates anterograde transport along the distal segment, which contains singlet MTs (Snow et al, 2004).…”