Stereotypical interciliary contacts in a C. elegans sense organ

Abstract

Physical interactions among cells and their processes are critical for intercellular communication and the generation of ordered tissue patterns. Primary cilia projecting from the cell surface have recently been shown to form contacts with the processes of diverse cell types, as well as with other cilia, in the brain and other organs. Whether these ciliary contacts are established in an instructive manner or are formed passively due to physical proximity is unclear. Ultrastructural analyses previously showed that the cilia of a subset of sensory neurons in the head amphid organs of C. elegans exhibit interciliary contacts within a glia-defined channel. Here we show that these ciliary contact patterns are stereotyped and can be established in the absence of neighboring cilia, indicating that these associations may not simply reflect relative positioning within the amphid channel. We show that mutations in genes implicated in ciliary protein trafficking, ciliary membrane phospholipid composition, and cilia-cell interactions disrupt cilia structure and/or interciliary contacts, and that in a subset of mutants, cilia with altered morphologies can nevertheless establish correct contacts. Together, our findings suggest that cilia-cilia interactions within a sense organ are established via instructive mechanisms, and raise the possibility that cellular functions may be modulated by cilia-mediated intercellular communication. Summary This work investigates how primary cilia, structures that detect and transmit signals, form contacts with one another in a head sensory organ of the nematode Caenorhabditis elegans. The authors found that these contacts follow consistent patterns and can form even when neighboring cilia are absent, suggesting they are actively established rather than occurring due to physical proximity. The authors identified mutations in genes that regulate cilia protein content, membrane composition, and cellular adhesion that disrupt cilia structure or contacts. These findings suggest that cilia-cilia interactions are regulated, raising the possibility that they play important roles in cell communication.