Calcium waves occur as Drosophila oocytes activate

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-01, Vol.112 (3), p.791-796
• Main Authors: Kaneuchi, Taro, Sartain, Caroline V, Takeo, Satomi, Horner, Vanessa L, Buehner, Norene A, Aigaki, Toshiro, Wolfner, Mariana F
• Format: Article
• Language: English
• Subjects: Animals; Arthropoda; Biological Sciences; Calcium; Calcium - metabolism; Drosophila; Drosophila - cytology; Drosophila - metabolism; Inositol 1,4,5-Trisphosphate - metabolism; Insects; Ion Transport; Molecules; Oocytes - metabolism
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1420589112

Egg activation is the process by which a mature oocyte becomes capable of supporting embryo development. In vertebrates and echinoderms, activation is induced by fertilization. Molecules introduced into the egg by the sperm trigger progressive release of intracellular calcium stores in the oocyte. Calcium wave(s) spread through the oocyte and induce completion of meiosis, new macromolecular synthesis, and modification of the vitelline envelope to prevent polyspermy. However, arthropod eggs activate without fertilization: in the insects examined, eggs activate as they move through the female’s reproductive tract. Here, we show that a calcium wave is, nevertheless, characteristic of egg activation in Drosophila . This calcium rise requires influx of calcium from the external environment and is induced as the egg is ovulated. Pressure on the oocyte (or swelling by the oocyte) can induce a calcium rise through the action of mechanosensitive ion channels. Visualization of calcium fluxes in activating eggs in oviducts shows a wave of increased calcium initiating at one or both oocyte poles and spreading across the oocyte. In vitro, waves also spread inward from oocyte pole(s). Wave propagation requires the IP3 system. Thus, although a fertilizing sperm is not necessary for egg activation in Drosophila , the characteristic of increased cytosolic calcium levels spreading through the egg is conserved. Because many downstream signaling effectors are conserved in Drosophila , this system offers the unique perspective of egg activation events due solely to maternal components. Significance This paper reports the first visualization of calcium dynamics in Drosophila eggs in vivo and in vitro, demonstrating that a calcium wave is a conserved feature of egg activation (the process by which a mature egg becomes able to initiate embryo development). In vertebrates and echinoderms, the fertilizing sperm triggers egg activation by inducing calcium release from the egg’s internal stores, causing wave(s) of increased calcium to sweep across the egg. However, insect eggs activate without fertilization. We show that a wave of increased calcium occurs during activation of Drosophila eggs. The wave is induced during ovulation by influx of calcium into the egg through mechanosensitive ion channels. Release of calcium from intracellular stores is required for wave propagation.