Comparative Biology of Calcium Signaling during Fertilization and Egg Activation in Animals

Abstract

During animal fertilizations, each oocyte or egg must produce a proper intracellular calcium signal for development to proceed normally. As a supplement to recent synopses of fertilization-induced calcium responses in mammals, this paper reviews the spatiotemporal properties of calcium signaling during fertilization and egg activation in marine invertebrates and compares these patterns with what has been reported for other animals. Based on the current database, fertilization causes most oocytes or eggs to generate multiple wavelike calcium oscillations that arise at least in part from the release of internal calcium stores sensitive to inositol 1,4,5-trisphosphate (IP3). Such calcium waves are modulated by upstream pathways involving oolemmal receptors and/or soluble sperm factors and in turn regulate calcium-sensitive targets required for subsequent development. Both "protostome" animals (e.g., mollusks, annelids, and arthropods) and "deuterostomes" (e.g., echinoderms and chordates) display fertilization-induced calcium waves, IP3-mediated calcium signaling, and the ability to use a combination of external calcium influx and internal calcium release. Such findings fail to support the dichotomy in calcium signaling modes that had previously been proposed for protostomes vs deuterostomes and instead suggest that various features of fertilization-induced calcium signals are widely shared throughout the animal kingdom.

Calcium wave pacemakers in eggs

“…Conversely, eggs of nemerteans, some molluscs, annelids, ascidians and mammals display repetitive Ca 2+ waves. In most of these eggs, the oscillations following the fertilization Ca 2+ wave all emanate from cortical sites distinct from the initial sperm entry site (Eckberg and Miller, 1995;Kline et al, 1999;Deguchi et al, 2000) (reviewed in Sardet, 1998;Stricker, 1999). Perhaps the most elaborate of these examples is the egg of ascidians (urochordates at the base of the vertebrate line).…”

“…In some species, external Ca 2+ is also used for the fertilization wave [in molluscs (Deguchi et al, 1996) (reviewed in Sardet et al, 1998)] or contributes to the maintenance of the repetitive Ca 2+ waves [in mice (McGuiness et al, 1996) (reviewed in Stricker, 1999)]. In many species, voltage-operated Ca 2+ channels [VOCC (Arnoult and Villaz, 1994;Leclerc et al, 2000)] and Ca 2+ -release-activated Ca 2+ (CRAC) channels that mediate so-called 'capacitative Ca 2+ entry' (Arnoult et al, 1996;Jaconi et al, 1997;Csutora et al, 1999;Machaca et al, 2000;Putney et al, 2001) are also present, but their role at fertilization is still ill defined.…”

“…In eggs, Ca 2+ waves triggered by sperm entry result mainly from the release of Ca 2+ from intracellular stores by inositol 1,4,5 trisphosphate [Ins(1,4,5)P 3]-induced Ca 2+ release (IICR) (reviewed in Miyazaki et al, 1993;Stricker, 1999;McDougall et al, 2000). The mechanism underlying Ins(1,4,5)P 3 production in eggs at the time of fertilization is still intensely debated.…”

“…The mechanism underlying Ins(1,4,5)P 3 production in eggs at the time of fertilization is still intensely debated. Similarly, the nature of the sperm factor(s) inducing Ca 2+ release at fertilization remains elusive, although several competing groups agree that it must be a protein, possibly a form of phospholipase C or an activator of it (see Stricker, 1999;Swann and Parrington, 1999;Parrington et al, 2000;McDougall et al, 2000;Nixon et al, 2000;Runft and Jaffe, 2000;Mehlmann et al, 2001;Jaffe et al, 2001;Carroll, 2001;Runft et al, 2002). Very recently, a mammalian sperm factor was characterized and found to be a new form of PLC [PLCζ (Saunders et al, 2002)].…”

A new approach to the molecular analysis of docking, priming, and regulated membrane fusion

“…Shearing yields cell surface complexes (CSC)-plasma membrane (PM) sheets with docked, fusion-ready cortical vesicles (CV), from which high purity CV are isolated [29,31,85,96]. Unlike mammalian secretory vesicles, CV retain Ca 2+ sensitivity and fusion competence in vitro hours after isolationwashed free of soluble components, CV are 'locked' in the docked, fusion-ready state, requiring only an increase in [Ca 2+ ] free to trigger fusion [30,57,75,80,90]. Being amenable to biochemical manipulations, CSC and CV have proven invaluable in dissecting molecular mechanisms underlying docking, Ca 2+ -triggering, and membrane fusion; comparable quantitative manipulations are unfeasible in other secretory systems [30,76,97].…”