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陕西福彩快乐十分任5:Ultrastructural organization of NompC in the mechanoreceptive organelle of Drosophila campaniform mechanoreceptors
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Mechanosensory cells convert environmental mechanical stimuli into intracellular signals. This process, termed mechanotransduction, occurs in specialized mechanoreceptive organelles. Using electron tomography we discovered that the mechanoreceptive organelle in fly campaniform mechanoreceptors contains thousands of force-sensitive ion channels that are arranged in a regular pattern, aligned to the intracellular microtubule cytoskeleton. A mechanical model suggests that the pattern is structurally and functionally optimized, because more force-sensitive channels are located at regions that are subject to larger activating forces. We propose that such a pattern enhances the sensitivity and broadens the dynamic range of mechanosensation in this type of mechanoreceptor.
Mechanoreceptive organelles (MOs) are specialized subcellular entities in mechanoreceptors that transform extracellular mechanical stimuli into intracellular signals. Their ultrastructures are key to understanding the molecular nature and mechanics of mechanotransduction. Campaniform sensilla detect cuticular strain caused by muscular activities or external stimuli in Drosophila. Each campaniform sensillum has an MO located at the distal tip of its dendrite. Here we analyzed the molecular architecture of the MOs in fly campaniform mechanoreceptors using electron microscopic tomography. We focused on the ultrastructural organization of NompC (a force-sensitive channel) that is linked to the array of microtubules in these MOs via membrane-microtubule connectors (MMCs). We found that NompC channels are arranged in a regular pattern, with their number increasing from the distal to the proximal end of the MO. Double-length MMCs in nompC29+29ARs confirm the ankyrin-repeat domain of NompC (NompC-AR) as a structural component of MMCs. The unexpected finding of regularly spaced NompC-independent linkers in nompC3 suggests that MMCs may contain non-NompC components. Localized laser ablation experiments on mechanoreceptor arrays in halteres suggest that MMCs bear tension, providing a possible mechanism for why the MMCs are longer when NompC-AR is duplicated or absent in mutants. Finally, mechanical modeling shows that upon cuticular deformation, sensillar architecture imposes a rotational activating force, with the proximal end of the MO, where more NOMPC channels are located, being subject to larger forces than the distal end. Our analysis reveals an ultrastructural pattern of NompC that is structurally and mechanically optimized for the sensory functions of campaniform mechanoreceptors.
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Author contributions: B.L., X.F. and X.L. designed research; L.S., Y.G., L.C., J.M., B.L., and X.L. performed research; J.-M.V. contributed new reagents/analytic tools; L.S., Y.G., J.H., B.L., X.F., and X.L. analyzed data; and L.S. and X.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. M.B.G. is a guest editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1819371116/-/DCSupplemental.
Published under the PNAS license.