Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos

Abstract

Background: The magnitude of the inner mitochondrial membrane potential (Δψm) appears to influence the level of certain mitochondrial activities including regulation of ionic fluxes and ATP liberation, activities that are often compartmentalized or location dependent in cells. Recent evidence suggests that within cells, mitochondria can be heterogeneous with respect to Δψm, and that high-polarized mitochondria (high Δψm) may occur in the subplasmalemmal cytoplasm where intercellular contact is absent. Here, we investigated whether Δψm in oocytes and preimplantation embryos was heterogeneous and cell contact-associated. Methods: Mouse and human oocytes and preimplantation stage embryos stained with mitochondria-specific probes rhodamine 123, MitoTracker Orange, and the Δψm-sensitive probe JC-1, (5,5′,6,6′-tetrachloro-1,1,3,3′-tetraethylbenzimidazoylcarbocy anine iodide), were examined by epifluorescence, scanning laser confocal, and transmission electron microscopy. The possibility that intercellular contact and Δψm are associated was examined for oocytes, where transzonal coronal cell contacts were terminated naturally or experimentally, and for intact, disaggregated, and reconstructed cleavage stage mouse embryos. Results: For both oocytes and embryos, clusters of apparently high-polarized mitochondria occur in the pericortical cytoplasm in regions free from intercellular contact. Conclusions: The findings suggest that mitochondria in oocytes and preimplantation embryos may be heterogeneous with respect to Δψm. We propose that high-polarized pericortical mitochondria may have a role in the acquisition of oocyte competence and the regulation of early developmental processes that may be associated with elevated metabolism or intracellular signalling through calcium-induced calcium release pathways.