Abstract
BackgroundA characteristic feature of frog reproduction is external fertilization accomplished outside the female's body. Mature fertilization-competent frog eggs are arrested at the meiotic metaphase II with high activity of the key meiotic regulators, maturation promoting factor (MPF) and cytostatic factor (CSF), awaiting fertilization. If the eggs are not fertilized within several hours of ovulation, they deteriorate and ultimately die by as yet unknown mechanism.ResultsHere, we report that the vast majority of naturally laid unfertilized eggs of the African clawed frog Xenopus laevis spontaneously exit metaphase arrest under various environmental conditions and degrade by a well-defined apoptotic process within 48 hours after ovulation. The main features of this process include cytochrome c release, caspase activation, ATP depletion, increase of ADP/ATP ratio, apoptotic nuclear morphology, progressive intracellular acidification, and egg swelling. Meiotic exit seems to be a prerequisite for execution of the apoptotic program, since (i) it precedes apoptosis, (ii) apoptotic events cannot be observed in the eggs maintaining high activity of MPF and CSF, and (iii) apoptosis in unfertilized frog eggs is accelerated upon early meiotic exit. The apoptotic features cannot be observed in the immature prophase-arrested oocytes, however, the maturation-inducing hormone progesterone renders oocytes susceptible to apoptosis.ConclusionsThe study reveals that naturally laid intact frog eggs die by apoptosis if they are not fertilized. A maternal apoptotic program is evoked in frog oocytes upon maturation and executed after meiotic exit in unfertilized eggs. The meiotic exit is required for execution of the apoptotic program in eggs. The emerging anti-apoptotic role of meiotic metaphase arrest needs further investigation.
Highlights
A characteristic feature of frog reproduction is external fertilization accomplished outside the female’s body
Eggs and early embryos have been widely used in cell cycle studies, which provided a basis for the current understanding of meiotic and mitotic transition
The eggs are arrested in metaphase, as it can be judged by the presence of cyclin B and phosphorylated mitogen-activated protein kinase (MAPK) (Figure 1i, j)
Summary
A characteristic feature of frog reproduction is external fertilization accomplished outside the female’s body. Eggs and early embryos have been widely used in cell cycle studies, which provided a basis for the current understanding of meiotic and mitotic transition. Calcium-dependent degradation of mitotic cyclins and Mos occurs, resulting in the inactivation of CSF and MPF, meiotic exit, and entry into the mitotic cell cycle. Ovulated unfertilized eggs undergo a time-dependent quality loss, the process known as postovulatory oocyte deterioration [7,8]. Spontaneous activation of ovulated mammalian eggs has been implicated as a likely biochemical basis for the time-dependent decrease of the fertilization rate [13]. The rapid loss of fertilization capacity of fish eggs during spawning has been linked to their spontaneous activation in aquatic environment [14]
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