Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Gaspar, Imre, Yu, Yanxun V., Cotton, Sean L., Kim, Dae-Hwan, Ephrussi, Anne, Welte, Michael A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2014
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
_version_ 1782327648427442176
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
work_keys_str_mv AT gasparimre klarensuresthermalrobustnessofoskarlocalizationbyrestrainingrnpmotility
AT yuyanxunv klarensuresthermalrobustnessofoskarlocalizationbyrestrainingrnpmotility
AT cottonseanl klarensuresthermalrobustnessofoskarlocalizationbyrestrainingrnpmotility
AT kimdaehwan klarensuresthermalrobustnessofoskarlocalizationbyrestrainingrnpmotility
AT ephrussianne klarensuresthermalrobustnessofoskarlocalizationbyrestrainingrnpmotility
AT weltemichaela klarensuresthermalrobustnessofoskarlocalizationbyrestrainingrnpmotility