Cellular and molecular aspects of oocyte maturation and fertilization: a perspective from the actin cytoskeleton

Abstract

Much of the scientific knowledge on oocyte maturation, fertilization, and embryonic development has come from the experiments using gametes of marine organisms that reproduce by external fertilization. In particular, echinoderm eggs have enabled the study of structural and biochemical changes related to meiotic maturation and fertilization owing to the abundant availability of large and transparent oocytes and eggs. Thus, in vitro studies of oocyte maturation and sperm-induced egg activation in starfish are carried out under experimental conditions that resemble those occurring in nature. During the maturation process, immature oocytes of starfish are released from the prophase of the first meiotic division, and acquire the competence to be fertilized through a highly programmed sequence of morphological and physiological changes at the oocyte surface. In addition, the changes in the cortical and nuclear regions are essential for normal and monospermic fertilization. This review summarizes the current state of research on the cortical actin cytoskeleton in mediating structural and physiological changes during oocyte maturation and sperm and egg activation in starfish and sea urchin. The common denominator in these studies with echinoderms is that exquisite rearrangements of the egg cortical actin filaments play pivotal roles in gamete interactions, Ca 2+ signaling, exocytosis of cortical granules, and control of monospermic fertilization. In this review, we also compare findings from studies using invertebrate eggs with what is known about the contributions made by the actin cytoskeleton in mammalian eggs. Since the cortical actin cytoskeleton affects microvillar morphology, movement, and positioning of organelles and vesicles, and the topography of the egg surface, these changes have impacts on the fertilization process, as has been suggested by recent morphological studies on starfish oocytes and eggs using scanning electron microscopy. Drawing the parallelism between vitelline layer of echinoderm eggs and the zona pellucida of mammalian eggs, we also discuss the importance of the egg surface in mediating monospermic fertilization.

Rocking the Boat: The Decisive Roles of Rho Kinases During Oocyte, Blastocyst, and Stem Cell Development

“…Through this process, the oocyte maintains a haploid chromosome number, as the other three genome copies are deposited into the polar bodies. These processes rely heavily on actin organization ( Liu et al, 2018 ; Roeles and Tsiavaliaris, 2019 ; Santella et al, 2020 ).…”

“…Through this process, the oocyte maintains a haploid chromosome number, as the other three genome copies are deposited into the polar bodies. These processes rely heavily on actin organization (Liu et al, 2018;Roeles and Tsiavaliaris, 2019;Santella et al, 2020). Various factors that promote actin filament formation, migration, and assembly during the entire process of oocyte maturation have been exhaustively studied (Namgoong and Kim, 2016;Roeles and Tsiavaliaris, 2019).…”

A condensate dynamic instability orchestrates oocyte actomyosin cortex activation

“…Improper cortical organization leads to an impairment of key cellular and developmental processes from as early as meiosis in oocytes to every subsequent cell division 3 . During meiotic maturation of oocytes, the actomyosin cortex transitions from inactive and non-contractile to active and tension-generating 4,5 .…”

Signaling Enzymes and Ion Channels Being Modulated by the Actin Cytoskeleton at the Plasma Membrane

“…On the other hand, in neuronal growth cones, polymerization dynamics of actin filaments underneath the plasma membrane contributes to the neurite's pathfinding [6]. The enormous plasticity of cell surface topography due to the actin-mediated membrane protrusion and retraction is also manifested by phagocytic immune cells and fertilized eggs [7,8]. The rapid reorganization of the subplasmalemmal actin cytoskeleton in these cells assists in engulfing the foreign objects and fertilizing sperm, respectively.…”