Calcium signals and oocyte maturation in marine invertebrates

Abstract

In various oocytes and eggs of animals, transient elevations in cytoplasmic calcium ion concentrations are known to regulate key processes during fertilization and the completion of meiosis. However, whether or not calcium transients also help to reinitiate meiotic progression at the onset of oocyte maturation remains controversial. This article summarizes reports of calcium signals playing essential roles during maturation onset (=germinal vesicle breakdown, GVBD) in several kinds of marine invertebrate oocytes. Conversely, other data from the literature, as well as previously unpublished findings for jellyfish oocytes, fail to support the view that calcium signals are required for GVBD. In addition to assessing the effects of calcium transients on GVBD in marine invertebrate oocytes, the ability of maturing oocytes to enhance their calcium-releasing capabilities after GVBD is also reviewed. Furthermore, possible explanations are proposed for the contradictory results that have been obtained regarding calcium signals during oocyte maturation in marine invertebrates.

Cellular and molecular aspects of oocyte maturation and fertilization: a perspective from the actin cytoskeleton

“…The role of a Ca 2+ influx from external seawater [163] has been neglected for decades as the eggs could be activated in seawater containing low Ca 2+ [164], or even in Ca 2+ free seawater by acrosome-reacted sperm [134]. Investigations aimed at understanding how fertilization activates Ca 2+ release in echinoderm eggs have pointed to the exclusive role of IP 3 as the messenger that initiates the increase and spreading of Ca 2+ . This possibility emerged from experiments in which the measurement of phosphoinositide turnover and IP 3 generation were found to coincide with the sperm-elicited Ca 2+ wave [87], and by the finding of the blockade of the Ca 2+ increase by chemical inhibitors of PLC [165,166].…”

“…These Ca 2+ signals regard only the Ca 2+ wave taking place at fertilization, and not the initial cortical Ca 2+ influx. They were nevertheless used to propose an exclusive coupling mechanism between IP 3 and RyRs in shaping the Ca 2+ signaling at fertilization of sea urchin eggs [169,170]. However, the finding that cADPr and its upstream modulator cGMP were increased prior to the generation of the Ca 2+ transient cast doubt on the notion that IP 3 alone initiates Ca 2+ release at fertilization [171].…”

“…It was later shown that this abnormal fertilization response was the consequence of the alteration of the structural organization of the cortical actin cytoskeleton [104]. The F-actin-linked morphological changes of the egg cortex induced by heparin favoured polyspermic fertilization and inhibited CG exocytosis not only at fertilization, but also in response to the Ca 2+ releases triggered by uncaging of IP 3 and cADPr [80,104]. Thus, at variance with previous reports that cytoplasmic Ca 2+ [178] is sufficient for CG exocytosis [179], our results have shown that the integrity of the actin cytoskeleton of the starfish egg cortex is also essential for successful CG exocytosis.…”

“…Eggs of nemerteans, ascidians, some annelids, and molluscs are blocked at the metaphase of the first meiotic division until fertilization triggers the completion of meiosis. The eggs of frogs and mammals are arrested and fertilized at metaphase II, i.e., after the second maturation spindle has formed and one polar body has been extruded [1][2][3][4]. Thus, as highlighted by Ernest Everett Just, "the fertilizability of all animal eggs hangs together with some condition in the cytoplasm of the egg and is independent of its nuclear state, as germinal vesicle, as first or second maturation-nucleus or as a completely matured nucleus" ( [5], page 185), and may be related to the structural organization of the cortex of the female gametes.…”

Kisspeptin/Kisspeptin Receptor System in the Ovary

“…LH induces a rapid rise of intracellular Ca 2+ that is released from Ca 2+ stores in the cumulus layers, and subsequently an increased Ca 2+ efflux into the oocyte ( 95 ). The increase of Ca 2+ in the oocyte is thought to play a role in controlling either spontaneous or gonadotropin-induced oocyte maturation, possibly by modulating the intracytoplasmic cAMP concentrations via a Ca 2+ -sensitive adenylate cyclase ( 96 , 97 ).…”