Calcium wave pacemakers in eggs

Abstract

During the past 25 years, the characterization of sperm-triggered calcium signals in eggs has progressed from the discovery of a single calcium increase at fertilization in the medaka fish to the observation of repetitive calcium waves initiated by multiple meiotic calcium wave pacemakers in the ascidian. In eggs of all animal species, sperm-triggered inositol (1,4,5)-trisphosphate[Ins(1,4,5)P3] production regulates the vast array of calcium wave patterns observed in the different species. The spatial organization of calcium waves is driven either by the intracellular distribution of the calcium release machinery or by the localized and dynamic production of calcium-releasing second messengers. In the highly polarized egg cell, cortical endoplasmic reticulum (ER)-rich clusters act as pacemaker sites dedicated to the initiation of global calcium waves. The extensive ER network made of interconnected ER-rich domains supports calcium wave propagation throughout the egg. Fertilization triggers two types of calcium wave pacemakers depending on the species: in mice, the pacemaker site in the vegetal cortex of the egg is probably a site that has enhanced sensitivity to Ins(1,4,5)P3; in ascidians, the calcium wave pacemaker may rely on a local source of Ins(1,4,5)P3 production apposed to a cluster of ER in the vegetal cortex.

Fertilisation calcium signals in the ascidian egg

“…Albrieux et al, 1998;Albrieux et al, 2000;Dumollard et al, 2002; Table 1). In the ascidian genome only one IP3 receptor type corresponding to type I can be found but the three types of ryanodine receptors are present.…”

“…The ascidian zygote was the first example of a non-excitable cell where two physiological Ca 2+ wave pacemakers exist successively; this phenomenon has now also been observed during mammalian fertilisation (Deguchi et al, 2000). A third artificial pacemaker can be induced in ascidian eggs and it can compete with the natural pacemakers induced by fertilisation (Dumollard and Sardet, 2001;Dumollard et al, 2003). The occurrence in the same cell of two distinct pacemakers both regulated by IP3 raises the question of how a highly diffusible second messenger like IP3 can give rise to distinct Ca 2+ wave pacemakers with distinct spatio-temporal characteristics in a cell.…”

“…In most species, sperm entry is accompanied by an increase in the Ca 2+ concentration ([Ca 2+ ] c ) that invades the whole egg and activates the development of the egg. In ascidians, as in nemerteans, some molluscs and mammals, the fertilisation Ca 2+ wave is followed by a series of repetitive Ca 2+ waves driving the destruction of maturation promoting factor (MPF) and completion of meiosis before the pronuclei can form (McDougall and Levasseur, 1998;Stricker, 1999;Nixon et al, 2000;Carroll, 2001;Dumollard et al, 2002). Eggs of mammals are arrested in metaphase II and a minimum number of Ca 2+ transients is necessary for establishment of a block to polyspermy, recruitment of maternal RNAs and entry into first interphase (Ducibella et al, 2002).…”

“…The ascidian egg possesses a complex Ca 2+ signalling machinery hosted by the plasma membrane, the endoplasmic reticulum (ER) and mitochondria. The interior of the mature, metaphase I-arrested egg is organised into cortical and cytoplasmic domains made of different concentrations of intracellular organelles (the three main ones being ER, mitochondria and yolk platelets, Speksnijder et al, 1993;Roegiers et al, 1999;Dumollard and Sardet 2001). The Ca 2+ waves are initiated in the cortex and they spread through the subcortex and the deeper cytoplasm of the egg.…”

“…The fertilisation Ca 2+ wave triggers an actomyosin-driven contraction that reorganises the cortex and subcortex of the egg to form a vegetal constriction called the contraction pole, a specialised domain dedicated to the initiation of meiotic Ca 2+ waves (Speksnijder et al, 1993;McDougall and Sardet, 1995;Roegiers et al, 1995;Roegiers et al, 1999;Dumollard et al, 2002). A first Ca 2+ wave pacemaker functions during this cortical contraction and it is translocated towards the vegetal pole of the egg.…”