Calcium signaling differentiation during Xenopus oocyte maturation

Abstract

Ca2+ is the universal signal for egg activation at fertilization in all sexually reproducing species. The Ca2+ signal at fertilization is necessary for egg activation and exhibits specialized spatial and temporal dynamics. Eggs acquire the ability to produce the fertilization-specific Ca2+ signal during oocyte maturation. However, the mechanisms regulating Ca2+ signaling differentiation during oocyte maturation remain largely unknown. At fertilization, Xenopus eggs produce a cytoplasmic Ca2+ (Ca2+cyt) rise that lasts for several minutes, and is required for egg activation. Here, we show that during oocyte maturation Ca2+ transport effectors are tightly modulated. The plasma membrane Ca2+ ATPase (PMCA) is completely internalized during maturation, and is therefore unable to extrude Ca2+ out of the cell. Furthermore, IP3-dependent Ca2+ release is required for the sustained Ca2+cyt rise in eggs, showing that Ca2+ that is pumped into the ER leaks back out through IP3 receptors. This apparent futile cycle allows eggs to maintain elevated cytoplasmic Ca2+ despite the limited available Ca2+ in intracellular stores. Therefore, Ca2+ signaling differentiates in a highly orchestrated fashion during Xenopus oocyte maturation endowing the egg with the capacity to produce a sustained Ca2+cyt transient at fertilization, which defines the egg's competence to activate and initiate embryonic development.