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• W2006296781 abstract "Mukhopadhyay and colleagues reveal in this issue of Developmental Cell that signaling mediated by a specialized neuronal cilium in C. elegans affects its structure. The finding that this cilium is modified in response to the cues it transduces suggests that cilia may not be static antennae, but organelles whose functions are shaped by their signaling activities. Mukhopadhyay and colleagues reveal in this issue of Developmental Cell that signaling mediated by a specialized neuronal cilium in C. elegans affects its structure. The finding that this cilium is modified in response to the cues it transduces suggests that cilia may not be static antennae, but organelles whose functions are shaped by their signaling activities. Cilia and flagella are appendages of many different cell types of many different organisms, from Chlamydomonas to C. elegans to mammals. Introductory biology courses usually mention the presence of two types of cilia defined by distinct microtubule arrangements, described as 9+2 and 9+0. Generally, multiciliated cells possess motile 9+2 cilia, and uniciliated cells possess immotile 9+0 cilia. However, these rules have exceptions, evidenced by nodal cells that possess single, motile 9+0 cilia, and olfactory neurons that possess many immotile 9+0 cilia. These exceptions begin to suggest that there may be many different types of cilia and, at the extreme, as many types of cilia as there are ciliated cell types. Perhaps retinal photoreceptor cells are the most radical example of this structural specialization; each vertebrate rod and cone cell possesses an immotile 9+0 cilium (the connecting cilium) with a greatly expanded tip containing the photoreceptors (the outer segment). Although C. elegans only possesses cilia on 60 of its neurons, these cilia also display widely distinct morphologies. The amphids are the main sensory organs of C. elegans, and contain neurons that have sensory cilia on dendritic endings (Figure 1A). Amphid neurons that sense aqueous odorants possess fairly simple “channel” cilia, consisting of one or two rod-like branches. Other neurons involved in sensing volatile odorants have more elaborate “wing” cilia. Of these, the AWA neuron has a highly branched cilium, the AWC neuron has a fan-shaped cilium, and the AWB neuron has a cilium with two unequal branches that sometimes are adorned with fans. How is this structural diversity generated? One mechanism is via ciliary modulators present specifically in distinct cell types. For example, in C. elegans, a HEAT repeat protein is expressed in only a subset of amphid neuron cilia where it helps generate the distal cilium (Bacaj et al., 2008Bacaj T. Lu Y. Shaham S. Genetics. 2008; 178: 989-1002Crossref PubMed Scopus (26) Google Scholar), and the AWB neuron uniquely expresses a forkhead transcription factor that regulates genes involved in ciliary morphogenesis (Mukhopadhyay et al., 2007Mukhopadhyay S. Lu Y. Qin H. Lanjuin A. Shaham S. Sengupta P. EMBO J. 2007; 26: 2966-2980Crossref PubMed Scopus (69) Google Scholar). Similarly, in mouse, a forkhead transcription factor is essential for the generation specifically of 9+2 cilia (Brody et al., 2000Brody S.L. Yan X.H. Wuerffel M.K. Song S.K. Shapiro S.D. Am. J. Respir. Cell Mol. Biol. 2000; 23: 45-51Crossref PubMed Scopus (258) Google Scholar, Chen et al., 1998Chen J. Knowles H.J. Hebert J.L. Hackett B.P. J. Clin. Invest. 1998; 102: 1077-1082Crossref PubMed Scopus (316) Google Scholar). Another mechanism by which ciliary and flagellar diversity arises is through responses to extracellular cues, including cues mediated by cilia and flagella themselves. For example, Chlamydomonas gametes extend the tips of their flagella upon activation of the fertilization signaling pathway (Mesland et al., 1980Mesland D.A. Hoffman J.L. Caligor E. Goodenough U.W. J. Cell Biol. 1980; 84: 599-617Crossref PubMed Scopus (81) Google Scholar). In this issue of Developmental Cell, Mukhopadhyay et al. reveal that the unique morphology of the C. elegans AWB cilium is also shaped by sensory signaling (Mukhopadhyay et al., 2008Mukhopadhyay S. Lu Y. Shaham S. Sengupta P. Dev. Cell. 2008; 14 (this issue): 762-774Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar). AWB neurons sense repulsive odorants produced by pathogenic bacteria (Pradel et al., 2007Pradel E. Zhang Y. Pujol N. Matsuyama T. Bargmann C.I. Ewbank J.J. Proc. Natl. Acad. Sci. USA. 2007; 104: 2295-2300Crossref PubMed Scopus (224) Google Scholar). Interestingly, depriving C. elegans of these cues by feeding them only chemically defined food increases the proportion of AWB cilia with fans and shortens the length of the ciliary branches (Figure 1B). These results suggest that the structure of the AWB cilium is not static, but is refined in response to extracellular signals. Mukhopadhyay et al. further show that disabling genes involved in transducing odorant cues, including genes encoding a GPCR kinase, the ODR-1 guanylyl cyclase, and two cyclic nucleotide gated channel subunits, causes changes in AWB ciliary structure similar to those that result from limiting exposure to bacteria. Gating of the odorant-responsive channels by cGMP is thought to result in Ca2+ flux. Either treatment with a cGMP analog or elevation of Ca2+ signaling partially suppresses the ciliary defects of odr-1 mutants. Together, these results suggest that it is the signaling pathway itself, and not some additional function of these proteins, that alters the morphology of AWB cilia. Why would a signaling pathway modify the organelle that transduces it? One possibility, suggested by Mukhopadhyay et al., is that regulation of ciliary structure is homeostatic. There is precedence for homeostatic mechanisms operating within cilia; if you turn down the lights, your ability to still read these words depends on Arrestin leaving your rod outer segments and Transducin entering. Perhaps if C. elegans fails to smell malodorous bacteria during larval stages, it expands the AWB ciliary membrane to form a fan and increase sensitivity. It would be interesting to test this possibility by assessing whether increasing ciliary membrane area through an independent means (such as mutation of arl-3, a gene encoding a G protein that represses fan formation) increases responsiveness to bacterial odorants. Another possibility is raised by experiments in which Mukhopadhyay et al. take advantage of a temperature-sensitive allele of one of the odorant-responsive channels to demonstrate that the morphology of the AWB cilium depends on the activity of this signaling pathway specifically during a critical period of larval development. Thus, AWB ciliary morphology is not changing constantly in response to signaling but, rather, morphology is defined by the activity of the pathway during a developmental window of time. Perhaps alterations in ciliary morphology are one mechanism by which cells retain a memory of prior signals. It remains unclear whether signal-dependent changes in ciliary architecture are found in cell types beyond AWB. Given that pathways similar to those operating in AWB can also affect AWC cilium morphology and protein composition, it will be exciting to find out whether the morphology of this cilium is sensitive to AWC cues such as temperature (Kuhara et al., 2008Kuhara A. Okumura M. Kimata T. Tanizawa Y. Takano R. Kimura K.D. Inada H. Matsumoto K. Mori I. Science. 2008; (in press. Published online April 10, 2008)https://doi.org/10.1126/science.1148922Crossref PubMed Scopus (123) Google Scholar, Lans and Jansen, 2006Lans H. Jansen G. Genetics. 2006; 173: 1287-1299Crossref PubMed Scopus (8) Google Scholar, Mukhopadhyay et al., 2008Mukhopadhyay S. Lu Y. Shaham S. Sengupta P. Dev. Cell. 2008; 14 (this issue): 762-774Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar). The conservation of ciliary sensory functions from C. elegans to mammals raises the possibility that mammalian cells may also share the ability to modify the structure of their cilia in response to signaling. In support of this proposition, expanded fan-like tips have occasionally been observed on mammalian cilia (Del Brio et al., 1991Del Brio M.A. Riera P. Garcia J.M. Alvarez-Uria M. J. Submicrosc. Cytol. Pathol. 1991; 23: 147-157PubMed Google Scholar). Defects in mammalian cilia are implicated in a diverse category of human diseases called ciliopathies. Do these emerging abilities of cilia to refine their architectures reveal anything about the pathogenesis of ciliopathies? Perhaps certain ciliopathies result not from isolated defects in structure or signal transduction, but from defects in the ciliary structural response to those signals. Indeed, disruption of the homeostatic mechanisms in photoreceptor cell cilia may be one mechanism leading to retinal degeneration. The recent surge of interest in cilia suggests that this question, and many others regarding these mysterious organelles, will be unraveled in the near future. Sensory Signaling-Dependent Remodeling of Olfactory Cilia Architecture in C. elegansMukhopadhyay et al.Developmental CellMay 13, 2008In BriefNonmotile 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. Full-Text PDF Open Archive" @default.
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• W2006296781 title "A Cilium Is Not a Cilium Is Not a Cilium: Signaling Contributes to Ciliary Morphological Diversity" @default.
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