External Ca2+ is predominantly used for cytoplasmic and nuclear Ca2+ increases in fertilized oocytes of the marine bivalveMactra chinensis

Abstract

IntroductionFully-grown oocytes arrested at the first meiotic prophase (prophase I, PI) in ovaries progress oocyte maturation, when exposed to hormones or released from inhibitory substances, to acquire the ability for fertilization in most animal species. These oocytes are again arrested at species-specific stages including the first metaphase (metaphase I, MI), second metaphase (metaphase II, MII), and pronuclear stage (PN), until fertilization (Masui, 1985). In the bivalves such as Mytilus and Ruditapes, the second arrest of meiosis occurs at MI prior to fertilization (MI-type) (Masui, 1985;Osanai and Kuraishi, 1988). In contrast, there are some bivalve species (e.g. Spisula and Mactra) in which meiosis reinitiation from PI is physiologically triggered concomitantly with fertilization without a process of oocyte maturation (PI-type) (Masui, 1985;Deguchi and Osanai, 1994b). Regardless of the stages of fertilization, single or multiple increases in intracellular Ca 2+ in fertilized oocytes or eggs have been detected in all animal species investigated so far (reviewed by Jaffe, 1985;Miyazaki et al., 1993;Stricker, 1999). The Ca 2+ increases are recognized as essential for the oocytes or eggs to be released from the cell cycle arrest (for a review, see Whitaker and Patel, 1990).As for MI-type bivalves, temporal patterns of Ca 2+ increases at fertilization have been analyzed in five different species: Mytilus, Crassostrea, Ruditapes, Limaria and Hiatella. When the Ca 2+ indicator Fluo-3 is introduced as AM ester, only a single blunt Ca 2+ increase, which persists for several minutes, is observed in fertilized oocytes of Mytilus (Abdelmajid et al., 1993) and Ruditapes (Leclerc et al., 2000). In the oocytes injected with Ca 2+ indicators such as Fura-2 and Calcium Green-1, however, Ca 2+ response at fertilization comprises an initial sharp Ca 2+ transient and subsequent repetitive Ca 2+ spikes (Ca 2+ oscillations) in all of the five species, including Mytilus and Ruditapes (Deguchi and Osanai, 1994a;Deguchi and Morisawa, 1997). In Mytilus, the initial Ca 2+ transient at fertilization arises almost synchronously in the oocyte without forming a point-source Ca 2+ wave (Deguchi and Osanai, 1994a). A more recent analysis revealed that the increased Ca 2+ 367Oocytes of the marine bivalve Mactra chinensis are spawned and arrested at the germinal vesicle stage (first meiotic prophase) until fertilization, without undergoing a process called oocyte maturation. As is the case of other animals, a fertilized oocyte of the bivalve displays increases in intracellular free Ca 2+ . We have clarified here the spatiotemporal patterns and sources of the intracellular Ca 2+ changes at fertilization. Shortly after insemination, increased Ca 2+ simultaneously appeared at the whole cortical region of the oocyte and spread inwardly to the center, attaining the maximal Ca 2+ levels throughout the oocyte, including the cytoplasm and nucleus. The initial maximal Ca 2+ peak was followed by a submaximal plateau phase of cytoplasmic and nuclear...

Transitioning from egg to embryo: Triggers and mechanisms of egg activation

“…Each arrest-point class generally conforms to a set of Ca 2ϩ "rules": upon fertilization in prophase I arrested oocytes, a single Ca 2ϩ increase starts at the cortex (cortical flash), but then spreads to the center of the egg to become an elevated plateau of internal Ca 2ϩ . External Ca 2ϩ is necessary for these events (Stricker, 1996;Stephano and Gould, 1997;Deguchi and Morisawa, 2003). Alternatively, upon fertilization in metaphase I arrested mollusks there is a cortical flash, but instead of an elevated plateau of Ca 2ϩ a series of secondary Ca 2ϩ oscillations occurs.…”

NAADP and InsP3 play distinct roles at fertilization in starfish oocytes

“…Nevertheless, in prophase I-arrested oocytes, the FP-dependent Ca 2+ influx may Developmental Biology 294 (2006) 24 -38 www.elsevier.com/locate/ydbio participate in oocyte activation . Consistently, in molluscs and echiurans, the cortical flash spreads centripetally without recruiting either InsP 3 receptors (InsP 3 Rs) or RyRs (Deguchi and Morisawa, 2003;Stephano and Gould, 1997). Moreover, in annelids, the sperm-promoted membrane depolarization initiates the Ca 2+ spiking that activates the eggs (Eckberg and Miller, 1995).…”

Role of Mos/MEK/ERK cascade and Cdk1 in Ca2+ oscillations in fertilized ascidian eggs

“…[Ca 2 þ ] i transients in the eggs of most animals are mediated by the inositol 1,4,5-trisphosphate (IP 3 ) receptor (IP 3 R) (Deguchi and Morisawa, 2003;Stricker, 1999), and activation of either MPF or MAPK sensitizes IP 3 -dependent Ca 2 þ release, possibly through direct phosphorylation of the IP 3 R (Sun et al, 2009). Thus, the Cdk1 and ERK activities and [Ca 2 þ ] i oscillations in the egg regulate each other.…”