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Klar ensures thermal robustness of oskar localization by restraining RNP motility
Communication usually applies feedback loop–based filters and amplifiers to ensure undistorted delivery of messages. Such an amplifier acts during Drosophila melanogaster midoogenesis, when oskar messenger ribonucleic acid (mRNA) anchoring depends on its own locally translated protein product. We fi...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The Rockefeller University Press
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4107779/ https://www.ncbi.nlm.nih.gov/pubmed/25049271 http://dx.doi.org/10.1083/jcb.201310010 |
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author | Gaspar, Imre Yu, Yanxun V. Cotton, Sean L. Kim, Dae-Hwan Ephrussi, Anne Welte, Michael A. |
author_facet | Gaspar, Imre Yu, Yanxun V. Cotton, Sean L. Kim, Dae-Hwan Ephrussi, Anne Welte, Michael A. |
author_sort | Gaspar, Imre |
collection | PubMed |
description | Communication usually applies feedback loop–based filters and amplifiers to ensure undistorted delivery of messages. Such an amplifier acts during Drosophila melanogaster midoogenesis, when oskar messenger ribonucleic acid (mRNA) anchoring depends on its own locally translated protein product. We find that the motor regulator Klar β mediates a gain-control process that prevents saturation-based distortions in this positive feedback loop. We demonstrate that, like oskar mRNA, Klar β localizes to the posterior pole of oocytes in a kinesin-1–dependent manner. By live imaging and semiquantitative fluorescent in situ hybridization, we show that Klar β restrains oskar ribonucleoprotein motility and decreases the posterior-ward translocation of oskar mRNA, thereby adapting the rate of oskar delivery to the output of the anchoring machinery. This negative regulatory effect of Klar is particularly important for overriding temperature-induced changes in motility. We conclude that by preventing defects in oskar anchoring, this mechanism contributes to the developmental robustness of a poikilothermic organism living in a variable temperature environment. |
format | Online Article Text |
id | pubmed-4107779 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | The Rockefeller University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-41077792015-01-21 Klar ensures thermal robustness of oskar localization by restraining RNP motility Gaspar, Imre Yu, Yanxun V. Cotton, Sean L. Kim, Dae-Hwan Ephrussi, Anne Welte, Michael A. J Cell Biol Research Articles Communication usually applies feedback loop–based filters and amplifiers to ensure undistorted delivery of messages. Such an amplifier acts during Drosophila melanogaster midoogenesis, when oskar messenger ribonucleic acid (mRNA) anchoring depends on its own locally translated protein product. We find that the motor regulator Klar β mediates a gain-control process that prevents saturation-based distortions in this positive feedback loop. We demonstrate that, like oskar mRNA, Klar β localizes to the posterior pole of oocytes in a kinesin-1–dependent manner. By live imaging and semiquantitative fluorescent in situ hybridization, we show that Klar β restrains oskar ribonucleoprotein motility and decreases the posterior-ward translocation of oskar mRNA, thereby adapting the rate of oskar delivery to the output of the anchoring machinery. This negative regulatory effect of Klar is particularly important for overriding temperature-induced changes in motility. We conclude that by preventing defects in oskar anchoring, this mechanism contributes to the developmental robustness of a poikilothermic organism living in a variable temperature environment. The Rockefeller University Press 2014-07-21 /pmc/articles/PMC4107779/ /pubmed/25049271 http://dx.doi.org/10.1083/jcb.201310010 Text en © 2014 Gaspar et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/). |
spellingShingle | Research Articles Gaspar, Imre Yu, Yanxun V. Cotton, Sean L. Kim, Dae-Hwan Ephrussi, Anne Welte, Michael A. Klar ensures thermal robustness of oskar localization by restraining RNP motility |
title | Klar ensures thermal robustness of oskar localization by restraining RNP motility |
title_full | Klar ensures thermal robustness of oskar localization by restraining RNP motility |
title_fullStr | Klar ensures thermal robustness of oskar localization by restraining RNP motility |
title_full_unstemmed | Klar ensures thermal robustness of oskar localization by restraining RNP motility |
title_short | Klar ensures thermal robustness of oskar localization by restraining RNP motility |
title_sort | klar ensures thermal robustness of oskar localization by restraining rnp motility |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4107779/ https://www.ncbi.nlm.nih.gov/pubmed/25049271 http://dx.doi.org/10.1083/jcb.201310010 |
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