Abstract
Egg activation is a series of highly coordinated processes that prepare the mature oocyte for embryogenesis. Typically associated with fertilization, egg activation results in many downstream outcomes, including the resumption of the meiotic cell cycle, translation of maternal mRNAs and cross-linking of the vitelline membrane. While some aspects of egg activation, such as initiation factors in mammals and environmental cues in sea animals, have been well-documented, the mechanics of egg activation in insects are less well-understood. For many insects, egg activation can be triggered independently of fertilization. In Drosophila melanogaster, egg activation occurs in the oviduct resulting in a single calcium wave propagating from the posterior pole of the oocyte. Here we use physical manipulations, genetics and live imaging to demonstrate the requirement of a volume increase for calcium entry at egg activation in ex vivo mature Drosophila oocytes. The addition of water, modified with sucrose to a specific osmolarity, is sufficient to trigger the calcium wave in the mature oocyte and the downstream events associated with egg activation. We show that the swelling process is regulated by the conserved osmoregulatory channels, aquaporins and DEGenerin/Epithelial Na+ channels. Furthermore, through pharmacological and genetic disruption, we reveal a concentration-dependent requirement of transient receptor potential M channels to transport calcium, most probably from the perivitelline space, across the plasma membrane into the mature oocyte. Our data establish osmotic pressure as a mechanism that initiates egg activation in Drosophila and are consistent with previous work from evolutionarily distant insects, including dragonflies and mosquitos, and show remarkable similarities to the mechanism of egg activation in some plants.
Highlights
Egg activation is a conserved process that prepares a mature oocyte for embryogenesis
The likely initiation cues for the calcium wave at Drosophila egg activation include physical pressure applied on the posterior pole by the oviduct or the uptake of the fluid by the mature oocyte from the oviduct [8,15]
To test if this swelling is required for the initiation and propagation of the calcium wave, we blocked the ability of the egg to swell by placing the anterior pole in a plastic capillary with the posterior pole being exposed to oil
Summary
Egg activation is a conserved process that prepares a mature oocyte for embryogenesis It actuates many essential cellular processes including the resumption of meiosis, modification of the outer membrane, post-transcriptional regulation of maternal mRNAs and broad changes in the cytoskeletal environment [1,2,3]. This process requires a transient increase of intracellular calcium, often referred to as a calcium wave(s), with multiple waves observed in mammals and ascidians, compared to a single wave in Xenopus laevis, Danio rerio and Drosophila melanogaster [4,5,6]. In the stick insect Catrausius morosus, exposure of the oocyte to oxygen in the air results in the resumption of meiosis [12]
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