Calcium ion currents mediating oocyte maturation events

Abstract

During maturation, the last phase of oogenesis, the oocyte undergoes several changes which prepare it to be ovulated and fertilized. Immature oocytes are arrested in the first meiotic process prophase, that is morphologically identified by a germinal vesicle. The removal of the first meiotic block marks the initiation of maturation. Although a large number of molecules are involved in complex sequences of events, there is evidence that a calcium increase plays a pivotal role in meiosis re-initiation. It is well established that, during this process, calcium is released from the intracellular stores, whereas less is known on the role of external calcium entering the cell through the plasma membrane ion channels. This review is focused on the functional role of calcium currents during oocyte maturation in all the species, from invertebrates to mammals. The emerging role of specific L-type calcium channels will be discussed. Review Oocyte maturationOogenesis is characterized by a unique process of cell division occurring only in gametes, called meiosis; whose goal is the production of haploid cells highly specialized for fertilization. In the majority of species the oocyte arrests in different stages of meiotic division, in particular, the block occurring in the first meiotic prophase (PI) marks the state of immature oocyte characterized by a prominent nucleus called the germinal vesicle (GV), which contains de-condensed transcriptionally active chromatin [[1] for a review]. As a general scheme, in response to a stimulus, meiosis is resumed and manifested by a germinal vesicle breakdown (GVBD), it then progresses to metaphase I (MI) or II (MII) where it undergoes a second arrest that is removed after successful fertilization.Oocyte maturation is usually defined as the period of progression from the first to the second meiotic arrest and involves coordinated nuclear and cytoplasmic modifications [2]. These are highly complex processes and their interplay is regulated by a series of sequential molecular events. Nuclear maturation starts with the GVBD, ends at the meiosis exit, and is marked by the presence of the two polar bodies. Cytoplasmic maturation is a more obscure process and involves both morphological and functional alterations related to: i) changes in the expression profile of cell cycle control proteins responsible for driving the oocyte towards developmental competencies [3][4][5]; ii) relocation of organelles [6][7][8]; iii) transcriptional modifications of mRNA [9], modification of the plasma membrane permeability [10,11]; iv) the differentiation of the calcium signalling machinery [12].Although the arrest at the PI stage seems to be strictly correlated with the oocyte growth, the meiotic stage correlated with fertilizable oocyte is species-specific. In some animals, oocytes are fertilized at the PI stage

Molecular and functional characterization of Anopheles gambiae inward rectifier potassium (Kir1) channels: A novel role in egg production

“…Moreover, ion channel currents (e.g. calcium currents) are involved in oocyte maturation and fertilization in vertebrate and invertebrate animals (Tosti, 2006; Tosti and Boni, 2004). Therefore, given that AgKir1 expression is enriched in the ovaries and that AgKir1 gene silencing reduces fecundity, it is possible that AgKir1 may participate in the regulation of mosquito oocyte maturation by modulating membrane excitability in these tissues.…”

T-Type Ca2+ Current Activity during Oocyte Growth and Maturation in the Ascidian Styela plicata

“…The influence of Ca 2+ entry through plasma membrane channels during oocyte maturation has been described only in few mammalian species [38]–[40]and mollusks [9], [11], [41]–[46]. In the majority of cases, the currents responsible for Ca 2+ influx have been shown to be L-type Ca 2+ currents [10], [17]–[19].…”

“…The role of ion currents in the gametes physiology has been well described in many animal species [7], [11], [13]–[16]. A pivotal role in gamete physiology is played by different types of voltage dependent Ca 2+ currents; in particular, it has been shown that the high threshold L-type Ca 2+ currents are either expressed in the immature oocytes and modulate oocyte growth, cytoplasmic maturation and early embryo development in a variety of organisms [9], [10], [17]–[20].…”

Store-Operated Calcium Entry in Human Oocytes and Sensitivity to Oxidative Stress1

“…However, little is known about the precise molecular mechanism of this Ca 2þ influx at fertilization and the nature of the Ca 2þ channels or transporters involved in this event. In this regard, a recent review highlights the involvement of voltage-operated calcium channels (VOCs) during oocyte maturation from germinal vesicle to metaphase II (MII) oocytes [13], although the relative contribution of a broad range of plasma membrane calcium channels during early signaling in mammalian fertilized oocytes remains unclear. In other somatic cell types, such as neurons, smooth muscle cells, and a variety of endocrine cells, it is well established that calcium waves triggered by diverse stimuli are dependent on the process of calcium entry through plasma membrane in order to replenish calcium levels in Ca 2þ stores to maintain the rapid rate of cytosolic Ca 2þ spiking.…”