Comparative biology of sperm factors and fertilization‐induced calcium signals across the animal kingdom

Abstract

SUMMARYFertilization causes mature oocytes or eggs to increase their concentrations of intracellular calcium ions (Ca 2þ ) in all animals that have been examined, and such Ca 2þ elevations, in turn, provide key activating signals that are required for non-parthenogenetic development. Several lines of evidence indicate that the Ca 2þ transients produced during fertilization in mammals and other taxa are triggered by soluble factors that sperm deliver into oocytes after gamete fusion. Thus, for a broad-based analysis of Ca 2þ dynamics during fertilization in animals, this article begins by summarizing data on soluble sperm factors in non-mammalian species, and subsequently reviews various topics related to a sperm-specific phospholipase C, called PLCz, which is believed to be the predominant activator of mammalian oocytes. After characterizing initiation processes that involve sperm factors or alternative triggering mechanisms, the spatiotemporal patterns of Ca 2þ signals in fertilized oocytes or eggs are compared in a taxon-by-taxon manner, and broadly classified as either a single major transient or a series of repetitive oscillations. Both solitary and oscillatory types of fertilization-induced Ca 2þ signals are typically propagated as global waves that depend on Ca 2þ release from the endoplasmic reticulum in response to increased concentrations of inositol 1,4,5-trisphosphate (IP 3 ). Thus, for taxa where relevant data are available, upstream pathways that elevate intraoocytic IP 3 levels during fertilization are described, while other less-common modes of producing Ca 2þ transients are also examined. In addition, the importance of fertilization-induced Ca 2þ signals for activating development is underscored by noting some major downstream effects of these signals in various animals.Mol. Reprod. Dev. 80: 787À815,

Single Ca2+ transients vs oscillatory Ca2+ signaling for assisted oocyte activation: limitations and benefits

“…It has been well documented that oocyte activation initiates when sperm delivers a specific soluble factor to the ooplasm upon gamete fusion in all mammalian species studied to date (reviewed by Kashir et al 2013, Swann & Lai 2013. Phospholipase C ζ was identified as the sperm-borne soluble factor that triggers oocyte activation (Cox et al 2002, Saunders et al 2002.…”

Calcium signals and oocyte maturation in marine invertebrates

“…During such fertilizations, prophase-arrested oocytes exhibit a Ca 2+ rise that comprises an initial peak (cortical flash) and a subsequent elevated plateau lasting for several minutes (Deguchi and Osanai, 1994;Deguchi and Morisawa, 2003). Several lines of evidence suggest that the sperm-induced Ca 2+ rise in these bivalves strictly depends on the influx of external Ca 2+ (see Kashir et al, 2013, for a recent review) and GVBD can be triggered only when Ca 2+ influx and the resultant intraoocytic Ca 2+ rise continue for at least a few minutes (Deguchi and Osanai, 1994).…”

“…In any case, although the underlying regulatory mechanisms of GVBD have yet to be fully elucidated, many molluscan oocytes are known to enhance their abilities to generate proper fertilizationinduced Ca 2+ responses during maturation from prophase I to metaphase I, with optimal responses generated during fertilization typically taking the form of repetitive Ca 2+ oscillations in bivalves versus a single but prolonged Ca 2+ rise in limpets (Kashir et al, 2013). Moreover, fertilization-induced Ca 2+ signals are necessary and sufficient for these oocytes to be released from a metaphase I arrest (Kashir et al, 2013), whereas an additional pH elevation is not required for such cell cycle progression (Deguchi and Osanai, 1995).…”

“…Moreover, fertilization-induced Ca 2+ signals are necessary and sufficient for these oocytes to be released from a metaphase I arrest (Kashir et al, 2013), whereas an additional pH elevation is not required for such cell cycle progression (Deguchi and Osanai, 1995).…”

“…Urechis) or at metaphase I (e.g. Chaetopterus, Arenicola, and Pseudopotamilla) (Meijer, 1979;Stephano and Gould, 1997;Kashir et al, 2013), and in either case, fully-grown oocytes arrested at prophase I accumulate in the coelom after having already been freed from follicle cells. As in molluscs, the connection between a Ca 2+ rise and subsequent meiotic progression is well documented for annelid oocytes that are normally fertilized at prophase I (Fig.…”