Regulation of dynamic events by microfilaments during oocyte maturation and fertilization

Abstract

Actin filaments (microfilaments) regulate various dynamic events during oocyte meiotic maturation and fertilization. In most species, microfilaments are not required for germinal vesicle breakdown and meiotic spindle formation, but they mediate peripheral nucleus (chromosome) migration, cortical spindle anchorage, homologous chromosome separation, cortex development/maintenance, polarity establishment, and first polar body emission during oocyte maturation. Peripheral cortical granule migration is controlled by microfilaments, while mitochondria movement is mediated by microtubules. During fertilization, microfilaments are involved in sperm incorporation, spindle rotation (mouse), cortical granule exocytosis, second polar body emission and cleavage ring formation, but are not required for pronuclear apposition (except for the mouse). Many of the events are driven by the dynamic interactions between myosin and actin filaments whose polymerization is regulated by RhoA, Cdc42, Arp2/3 and other signaling molecules. Studies have also shown that oocyte cortex organization and polarity formation mediated by actin filaments are regulated by mitogen-activated protein kinase, myosin light-chain kinase, protein kinase C and its substrate p-MARKS as well as PAR proteins. The completion of several dynamic events, including homologous chromosome separation, spindle anchorage, spindle rotation, vesicle organelle transport and pronuclear apposition (mouse), requires interactions between microfilaments and microtubules, but determination of how the two systems of the cytoskeleton precisely cross-link, and which proteins link microfilaments to microtubules to perform functions in eggs, requires further studies. Finally, the meaning of microfilament-mediated oocyte polarity versus embryo polarity and embryo development in different species (Drosophila, Xenopus and mouse) is discussed.

Pins homolog LGN regulates meiotic spindle organization in mouse oocytes

“…The cortex of mouse oocytes has no apparent polarity at the GV stage, but undergoes local reorganization and polarization during meiotic spindle migration to the cortex [1,3,4]. In this study, we found that cortical LGN was also polarized during this process.…”

“…In mouse oocytes, LGN cortical localization may also be mediated by interaction with the cortical heterotrimeric G protein α-subunits. Interestingly, the polarization pattern of cortical LGN is distinct from several identified polarity proteins (such as conserved polarity mediators Par3 and Par6, and the small GTPases Rac and Cdc42), which are concentrated at the actin cap region [7][8][9][10], whereas it is similar to those of cortical granules and microvilli [1,4]. The specific function of cortical polarized LGN has not been elucidated, In Drosophila neuroblasts and C. elegans one-cell embryos, Pins or its counterparts regulate spindle orientation and positioning and thus asymmetric cell division, but do not affect spindle organization [11].…”

“…When the spindle reaches the cortex, the metaphase to anaphase transition is triggered and the first polar body is extruded. Subsequently, metaphase II (MII) spindles form and are located under the actin cap with the long axis approximately parallel to the cortex [1,4]. The molecular details of oocyte cortical polarization and meiotic spindle organization are only beginning to emerge.…”

Expression and localization of nitric oxide synthase isoforms during porcine oocyte growth and acquisition of meiotic competence

“…The presence of iNOS on the periphery of oocytes is not surprising with regard to the well-known association of iNOS with sub-membranous cortical actin cytoskeleton in somatic cells (Webb et al, 2001) and the presence of cortical actin cytoskeleton in oocytes (Sun and Schatten, 2006). This peripheral localization is probably important for the propagation of NO-signalling in somatic cells (Webb et al, 2001), and we cannot exclude that it is also important for oocytes.…”

RhoA-mediated MLC2 regulates actin dynamics for cytokinesis in meiosis

“…27 During mouse oocyte meiotic maturation, actin was required for the chromosome migration, 9,28 cortical spindle anchorage, 29,30 cortex development and polarity establishment 2,31 and first polar body extrusion. 6,27 Additionally, some actin nucleation factors such as Arp2/3 complex, 6 Formin2 7,29 and Spire1/2 32 were involved in the actin organization during mouse oocyte maturation. Previous work showed that myosin II was activated by phosphorylation of its regulatory MLC at Ser19/Thr18, and the phosphorylation at MLC Ser19 was critical for actin assembly.…”