A single and rapid calcium wave at egg activation in Drosophila
Activation is an essential process that accompanies fertilisation in all animals and heralds major cellular changes, most notably, resumption of the cell cycle. While activation involves wave-like oscillations in intracellular Ca<sup>2+</sup> concentration in mammals, ascidians and polyc...
Main Authors: | , , , , , |
---|---|
Format: | Journal article |
Language: | English |
Published: |
Company of Biologists
2015
|
_version_ | 1797053807472934912 |
---|---|
author | York-Andersen, A Parton, R Bi, C Bromley, C Davis, I Weil, T |
author_facet | York-Andersen, A Parton, R Bi, C Bromley, C Davis, I Weil, T |
author_sort | York-Andersen, A |
collection | OXFORD |
description | Activation is an essential process that accompanies fertilisation in all animals and heralds major cellular changes, most notably, resumption of the cell cycle. While activation involves wave-like oscillations in intracellular Ca<sup>2+</sup> concentration in mammals, ascidians and polychaete worms and a single Ca<sup>2+</sup> peak in fish and frogs, in insects, such as <em>Drosophila</em>, to date, it has not been shown what changes in intracellular Ca<sup>2+</sup> levels occur. Here, we utilise ratiometric imaging of Ca<sup>2+</sup> indicator dyes and genetically encoded Ca<sup>2+</sup> indicator proteins to identify and characterise a single, rapid, transient wave of Ca<sup>2+</sup> in the <em>Drosophila</em> egg at activation. Using genetic tools, physical manipulation and pharmacological treatments we demonstrate that the propagation of the Ca<sup>2+</sup> wave requires an intact actin cytoskeleton and an increase in intracellular Ca<sup>2+</sup> can be uncoupled from egg swelling, but not from progression of the cell cycle. We further show that mechanical pressure alone is not sufficient to initiate a Ca<sup>2+</sup> wave. We also find that processing bodies, sites of mRNA decay and translational regulation, become dispersed following the Ca<sup>2+</sup> transient. Based on this data we propose the following model for egg activation in <em>Drosophila</em>: exposure to lateral oviduct fluid initiates an increase in intracellular Ca<sup>2+</sup> at the egg posterior via osmotic swelling, possibly through mechano-sensitive Ca<sup>2+</sup> channels; a single Ca<sup>2+</sup> wave then propagates in an actin dependent manner; this Ca<sup>2+</sup> wave co-ordinates key developmental events including resumption of the cell cycle and initiation of translation of mRNAs such as <em>bicoid</em>. |
first_indexed | 2024-03-06T18:48:45Z |
format | Journal article |
id | oxford-uuid:0f734397-bf12-4fbb-b7d5-69bacda46bd0 |
institution | University of Oxford |
language | English |
last_indexed | 2024-03-06T18:48:45Z |
publishDate | 2015 |
publisher | Company of Biologists |
record_format | dspace |
spelling | oxford-uuid:0f734397-bf12-4fbb-b7d5-69bacda46bd02022-03-26T09:51:16ZA single and rapid calcium wave at egg activation in DrosophilaJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:0f734397-bf12-4fbb-b7d5-69bacda46bd0EnglishORA DepositCompany of Biologists2015York-Andersen, AParton, RBi, CBromley, CDavis, IWeil, TActivation is an essential process that accompanies fertilisation in all animals and heralds major cellular changes, most notably, resumption of the cell cycle. While activation involves wave-like oscillations in intracellular Ca<sup>2+</sup> concentration in mammals, ascidians and polychaete worms and a single Ca<sup>2+</sup> peak in fish and frogs, in insects, such as <em>Drosophila</em>, to date, it has not been shown what changes in intracellular Ca<sup>2+</sup> levels occur. Here, we utilise ratiometric imaging of Ca<sup>2+</sup> indicator dyes and genetically encoded Ca<sup>2+</sup> indicator proteins to identify and characterise a single, rapid, transient wave of Ca<sup>2+</sup> in the <em>Drosophila</em> egg at activation. Using genetic tools, physical manipulation and pharmacological treatments we demonstrate that the propagation of the Ca<sup>2+</sup> wave requires an intact actin cytoskeleton and an increase in intracellular Ca<sup>2+</sup> can be uncoupled from egg swelling, but not from progression of the cell cycle. We further show that mechanical pressure alone is not sufficient to initiate a Ca<sup>2+</sup> wave. We also find that processing bodies, sites of mRNA decay and translational regulation, become dispersed following the Ca<sup>2+</sup> transient. Based on this data we propose the following model for egg activation in <em>Drosophila</em>: exposure to lateral oviduct fluid initiates an increase in intracellular Ca<sup>2+</sup> at the egg posterior via osmotic swelling, possibly through mechano-sensitive Ca<sup>2+</sup> channels; a single Ca<sup>2+</sup> wave then propagates in an actin dependent manner; this Ca<sup>2+</sup> wave co-ordinates key developmental events including resumption of the cell cycle and initiation of translation of mRNAs such as <em>bicoid</em>. |
spellingShingle | York-Andersen, A Parton, R Bi, C Bromley, C Davis, I Weil, T A single and rapid calcium wave at egg activation in Drosophila |
title | A single and rapid calcium wave at egg activation in Drosophila |
title_full | A single and rapid calcium wave at egg activation in Drosophila |
title_fullStr | A single and rapid calcium wave at egg activation in Drosophila |
title_full_unstemmed | A single and rapid calcium wave at egg activation in Drosophila |
title_short | A single and rapid calcium wave at egg activation in Drosophila |
title_sort | single and rapid calcium wave at egg activation in drosophila |
work_keys_str_mv | AT yorkandersena asingleandrapidcalciumwaveateggactivationindrosophila AT partonr asingleandrapidcalciumwaveateggactivationindrosophila AT bic asingleandrapidcalciumwaveateggactivationindrosophila AT bromleyc asingleandrapidcalciumwaveateggactivationindrosophila AT davisi asingleandrapidcalciumwaveateggactivationindrosophila AT weilt asingleandrapidcalciumwaveateggactivationindrosophila AT yorkandersena singleandrapidcalciumwaveateggactivationindrosophila AT partonr singleandrapidcalciumwaveateggactivationindrosophila AT bic singleandrapidcalciumwaveateggactivationindrosophila AT bromleyc singleandrapidcalciumwaveateggactivationindrosophila AT davisi singleandrapidcalciumwaveateggactivationindrosophila AT weilt singleandrapidcalciumwaveateggactivationindrosophila |