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The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors
In mechanoreceptors, mechanical stimulation by external forces leads to the rapid opening of transduction channels followed by an electrical response. Despite intensive studies in various model systems, the molecular pathway by which forces are transmitted to the transduction channels remains elusiv...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The Biophysical Society
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4269791/ https://www.ncbi.nlm.nih.gov/pubmed/25517144 http://dx.doi.org/10.1016/j.bpj.2014.10.052 |
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author | Liang, Xin Madrid, Johnson Howard, Jonathon |
author_facet | Liang, Xin Madrid, Johnson Howard, Jonathon |
author_sort | Liang, Xin |
collection | PubMed |
description | In mechanoreceptors, mechanical stimulation by external forces leads to the rapid opening of transduction channels followed by an electrical response. Despite intensive studies in various model systems, the molecular pathway by which forces are transmitted to the transduction channels remains elusive. In fly campaniform mechanoreceptors, the mechanotransduction channels are gated by compressive forces conveyed via two rows of microtubules that are hypothesized to be mechanically reinforced by an intervening electron-dense material (EDM). In this study, we tested this hypothesis by studying a mutant fly in which the EDM was nearly absent, whereas the other ultrastructural elements in the mechanosensitive organelle were still present at 50% (or greater) of normal levels. We found that the mechanosensory response in this mutant was reduced by 90% and the sensitivity by at least 80%. To test whether loss of the EDM could lead to such a reduction in response, we performed a mechanical analysis and estimated that the loss of the EDM is expected to greatly decrease the overall rigidity, leading to a marked reduction in the gating force conveyed to the channel. We argue that this reduction in force, rather than the reduction in the number of transduction channels, is primarily responsible for the nearly complete loss of mechanosensory response observed in the mutant fly. Based on these experiments and analysis, we conclude that the microtubule-based cytoskeleton (i.e., microtubules and EDM) is an essential component of the mechanical signaling pathway in fly campaniform mechanoreceptor. |
format | Online Article Text |
id | pubmed-4269791 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | The Biophysical Society |
record_format | MEDLINE/PubMed |
spelling | pubmed-42697912015-12-16 The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors Liang, Xin Madrid, Johnson Howard, Jonathon Biophys J Cell Biophysics In mechanoreceptors, mechanical stimulation by external forces leads to the rapid opening of transduction channels followed by an electrical response. Despite intensive studies in various model systems, the molecular pathway by which forces are transmitted to the transduction channels remains elusive. In fly campaniform mechanoreceptors, the mechanotransduction channels are gated by compressive forces conveyed via two rows of microtubules that are hypothesized to be mechanically reinforced by an intervening electron-dense material (EDM). In this study, we tested this hypothesis by studying a mutant fly in which the EDM was nearly absent, whereas the other ultrastructural elements in the mechanosensitive organelle were still present at 50% (or greater) of normal levels. We found that the mechanosensory response in this mutant was reduced by 90% and the sensitivity by at least 80%. To test whether loss of the EDM could lead to such a reduction in response, we performed a mechanical analysis and estimated that the loss of the EDM is expected to greatly decrease the overall rigidity, leading to a marked reduction in the gating force conveyed to the channel. We argue that this reduction in force, rather than the reduction in the number of transduction channels, is primarily responsible for the nearly complete loss of mechanosensory response observed in the mutant fly. Based on these experiments and analysis, we conclude that the microtubule-based cytoskeleton (i.e., microtubules and EDM) is an essential component of the mechanical signaling pathway in fly campaniform mechanoreceptor. The Biophysical Society 2014-12-16 2014-12-16 /pmc/articles/PMC4269791/ /pubmed/25517144 http://dx.doi.org/10.1016/j.bpj.2014.10.052 Text en © 2014 The Authors http://creativecommons.org/licenses/by-nc-nd/3.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). |
spellingShingle | Cell Biophysics Liang, Xin Madrid, Johnson Howard, Jonathon The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors |
title | The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors |
title_full | The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors |
title_fullStr | The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors |
title_full_unstemmed | The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors |
title_short | The Microtubule-Based Cytoskeleton Is a Component of a Mechanical Signaling Pathway in Fly Campaniform Receptors |
title_sort | microtubule-based cytoskeleton is a component of a mechanical signaling pathway in fly campaniform receptors |
topic | Cell Biophysics |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4269791/ https://www.ncbi.nlm.nih.gov/pubmed/25517144 http://dx.doi.org/10.1016/j.bpj.2014.10.052 |
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