Human Reproduction Update, Vol.10, No.1 pp.53-65, 2004
© European Society of Human Reproduction and Embryology 2004; all rights reserved
Electrical events during gamete maturation and fertilization in animals and humans
1 Laboratory of Cell Biology, Stazione Zoologica, Villa Comunale, 80121 Naples and 2 Department of Animal Science, University of Basilicata, Potenza, Italy 3 To whom correspondence should be addressed: e-mail: tosti{at}szn.it
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Abstract |
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Gamete cells are electrogenic, i.e. capable of responding to electrical stimuli and modifying their electrical properties during the crucial periods of maturation and fertilization. Ion channels have been widely demonstrated on the plasma membrane of the oocyte and spermatozoon in all animals studied, and electrical modifications in gametes are due to ion currents that are modulated via these ion channels. The modification of intracellular calcium levels in gametes has been extensively studied, and these modifications are recognized to be a second messenger system for gamete maturation and fertilization. Other ions also move through the plasma membrane, either in association with or independent of calcium, and these generate typical features such as fertilization currents and oscillation of resting potential. These modifications were first studied in marine invertebrates, and the observations subsequently compared with mammalian systems, including human. The precise role played by these currents in the processes of maturation and fertilization is still poorly understood; however, recent research opens new frontiers for their clinical and technological application.
Key words: electrophysiology/fertilization/gamete maturation/ion channels/ion currents
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Introduction |
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TOPAbstractIntroductionElectrophysiology of the cellElectrical properties of the...Electrical events at...Concluding remarksAcknowledgementsReferences |
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The growth of germinal cells follows unique rhythms and dynamics that differ from those of somatic cells. A preliminary long-lasting quiescent phase allows the proper development of cellular growth and differentiation, and mechanisms of gamete maturation then follow at a tumultuous cascading speed. Gamete metabolism is then newly modified during the process of fertilization, and the success of the process relies upon a reciprocal activation of the male and female cells. Specifically, sperm competence for activation and fusion is triggered by the external investments of the oocyte, and the activated spermatozoon then drives the oocyte into metabolic activation. Electrical modifications of the plasma membrane underlie both of these processes.
Electrical events are one of the first indications that gametes are undergoing activation steps during maturation and fertilization (Moreau et al., 1985
; Dale, 1994; Darszon et al., 1999). This is due to activation of ion channels located on the plasma membrane. An exchange of ions between the internal and the external compartments of the cell generates an electrical current, and this modifies the electrical steady state of the cell. Fertilization is the best example of the link between a transient electrical modification and a new metabolic condition within a cell. A species-dependent fertilization current and a large hyperpolarization or depolarization of membrane potential occur in the oocyte shortly after sperm entry. These events coincide with the initiation of embryo development.
In this review, we focus on the electrical properties of the plasma membrane of animal germ cells, i.e. the oocyte and the spermatozoon, throughout their maturation and following their union to form a new individual. After a preliminary description of the main parameters used for electrophysiological study of the cell plasma membrane, we report information on the properties and changes in intracellular ions, ion channels and ion currents that occur during gamete maturation and fertilization.
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Electrophysiology of the cell |
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TOPAbstractIntroductionElectrophysiology of the cellElectrical properties of the...Electrical events at...Concluding remarksAcknowledgementsReferences |
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The plasma membrane marks the border between the internal and external compartments of a cell. The fluids in these compartments consist of saline solutions of differing compositions. The intracellular fluid contains organelles bathed in a matrix whose ion content differs from that of the external compartment. This compartmentalization must be maintained, and is essential for cell activity as well as for cell viability; it is regulated by specific dynamics that are modulated by complex mechanisms, as described below.
Potassium cations (K+) are the most significant intracellular ions, whereas sodium (Na+) and calcium (Ca2+) cations are significant extracellularly. Chloride anion (Cl–) is present at higher concentration externally, whereas there is a great variation in the anions present inside the cell. These intracellular anions include negative charges provided by several constituents that carry phosphate and carboxyl groups. The different distribution of electrical charges inside and outside the cell creates an electrical gradient across the membrane, known as voltage, and this is measured in Volts. The voltage difference across the cell membrane creates a store of potential energy in the form of an ion gradient, giving rise to a transmembrane potential known as resting potential (RP). This parameter changes in relation to ion distribution and membrane permeability.
In the majority of cells studied, the RP is negative, in a range of –10 to –100 mV (Hagiwara and Jaffe, 1979). Potassium is electively stored inside the cell, and it is the ion that contributes mainly to determining and regulating the resting potential (De Felice, 1997). The K+ gradient and differences in membrane ion permeability are, in turn, determined by specific transport proteins and ion channels in the plasma membrane. The transport proteins (ion pumps) maintain the concentration gradients that determine resting potential (e.g. Na+/K+ pump) and the general homeostasis of the cell. Ion channels are characterized by their specificity, gating, conductance and sensitivity to drugs, and these act as gated ion-selective pores that allow ions to move down their concentration gradients. An ion channel is specific if it allows the passage of one ion species predominantly. Ion channel opening is triggered in response to (i) a ligand (second messenger-operated channels) (Sutcliffe et al., 1998), (ii) a change in voltage (voltage-operated channels) (Terlau and Stuhmer, 1998) or (iii) a mechanical stimulus (stretch-activated channels) (Hamill and McBride, 1996; Saitou et al., 2000). Moreover, each channel has a proper conductance, which is measured in Siemens (S). A specific ion channel shows a mean conductance between 5 and 10 pS; however, some highly specific channels, such as Ca2+ channels, may have a conductance that is <1 pS. Non-specific channels show higher conductance measurements. The passage of ions across membrane ion channels determines an electrical flux which is called an ion current; this is measured in Amperes (A). Normally, the ion current is associated with a change in RP, since the concentration of ions inside the cell is transiently modified. In particular, depolarization of the plasma membrane causes a shift of RP towards more positive values, whereas hyperpolarization modifies the RP towards more negative values. The type and the number of channels within a cell depends on several parameters which determine the grade of cell excitability. Electrical excitability is an essential property of neurons, and this involves characteristic sets of voltage-dependent ion channels. Muscle cells (Katz, 1966), germ cells (Chambers, 1989a), many endocrine cells (Ozawa and Sand, 1986) and even so-called non-excitable cells, such as glial cells (Barres et al., 1990), express voltage-dependent ion channels at a certain stage of cellular differentiation. Hence, electrical properties characterize individual cells in relation to their function and differentiation (for review see Takahashi and Okamura, 1998).
Capacitance is another example of an electrophysiological parameter which every cell has by virtue of the membrane lipid bilayer. This is well described in the sea urchin (McCulloh and Chambers, 1992) and is also reported in mouse oocytes (Lee et al., 2001), where an increase in plasma membrane capacitance as well as cortical granule exocytosis follows sperm–oocyte fusion.
The patch-clamp technique, first described by Neher and Sakmann (1976), is the most popular technique used to study cell currents; the basic configurations of this technique involve whole cell or single channel recordings. The former measures currents from an entire cell under voltage clamp and this is normally obtained after seal and destruction of the patched membrane. The single channel configuration records a channel activity inside the intact patched membrane. The application of Giga-seal resistance and different configurations of the patch-clamp technique literally revolutionized the study of membrane electrophysiology, and allowed access to new information about cell function (for review see: Neher, 1988, 1992; Neher and Sakmann, 1992; Levis and Rae, 1998). Figure 1 lists a glossary of the main electrophysiological parameters described above.
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Electrical properties of the gamete plasma membrane |
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The oocyte
Oocytes are electrogenic cells that block their development during different species-specific stages of the meiotic cycle. Early studies on the role of ions in oocyte physiology date back to 1946, when Edward Chambers started to investigate Na+ and K+ exchange during fertilization in the sea urchin (for review see Chambers, 1989a).
Different species of echinoderms, i.e. starfish and sea urchin, have been used extensively to study the electrophysiological properties of the oocyte plasma membrane. In starfish, immature oocytes exhibit three types of voltage-dependent currents: an inward Ca2+, a fast transient K+ and an inwardly rectifying K+ current (Moody and Lansman, 1983). During hormone-induced in vitro maturation, a gradual change in the amplitude of all three currents is seen: the Ca2+ current becomes larger whereas both K+ currents become smaller (Moody and Lansman, 1983). These changes are also associated with a decrease in membrane conductance and a depolarization of RP during maturation due to changes in Na+ and K+ conductance (Miyazaki et al., 1975a,b; Moreau and Cheval, 1976). The sea urchin is the species that has been most extensively studied for mechanisms of fertilization (for review see Monroy, 1986). However, the electrical properties of its plasma membrane have not been clearly elucidated, possibly due to the fact that patching the oocyte plasma membrane in this species is technically difficult to accomplish. Earlier studies on sea urchin oocyte RP suggested that the membrane has a high permeability to K+ and a lower permeability to Na+ and Cl– (Steinhardt et al., 1971; Jaffe and Robinson, 1978). The presence of Ca2+ channels was first demonstrated in a comparative study by Okamoto et al. (1977). Electrical studies of oocytes during the germinal vesicle breakdown (GVBD) stage suggest that immature oocytes have a high K+ permeability which is lost during maturation (Dale and De Santis, 1981).
Another marine invertebrate, the ascidian, has also been used to study gamete biology. In oocytes of Boltenia villosa, Block and Moody (1987) described three principal voltage-dependent currents as follows: (i) a transient inward Na+ current, (ii) a transient inward Ca2+ current, and (iii) an inwardly rectifying K+ current. A more accurate characterization of Ca2+ channel sub-types performed in Ciona intestinalis oocytes showed the presence of L-type Ca2+ currents (Dale et al., 1991), suggesting that this calcium current component has a role in regulating cytosolic calcium during early developmental processes.
Schlichter (1989a) has provided an excellent overview on ion channels in amphibian oocytes; a role for Cl– currents emerges in both immature and mature oocytes in all the species studied. In the European frog Rana esculenta, changes in membrane permeability occur during maturation; in particular, K+ and Cl– voltage-gated currents present in the immature oocytes disappear in mature oocytes, replaced by a Na+ current (Taglietti et al., 1984). A Ca2+-dependent Cl– current has been shown in Xenopus immature oocytes (Barish, 1983), and Na+ currents similar to those of neuronal cells, as well as other non-specific ion currents, have also been described (Bourinet et al., 1992; Weber, 1999). The same currents are present in immature metaphase I oocytes of R. pipiens, each contributing differently to subsequent fertilization potential (Schlichter, 1989b); in particular, Cl– is lost as the oocyte undergoes maturation (Schlichter, 1983). A noticeable voltage-dependent hydrogen current was first demonstrated in the axolotl Ambistoma oocytes (Barish and Baud, 1984).
In addition to the above species, ion currents that play a possible role in the mechanism of maturation and fertilization have been observed in other non-mammalian species such as molluscs (Moreau et al., 1996; Ouadid-Ahidouch, 1998; Gould et al., 2001; E.Tosti, unpublished data), and marine polychaetes (Gunning, 1983; Fox and Krasne, 1984).
In mammals, separating the oocyte from the cumulus investment makes the measurement of electrical parameters technically difficult, and therefore there are very few papers that discuss electrical properties of the mammalian oocyte plasma membrane during maturation. A functional separation between these two units occurs spontaneously in the mature oocyte, but during immature stages there is an intimate interaction between the oocyte and the cumulus cells, and this is maintained by intercellular communications such as gap junctions (Gilula et al., 1978; Canipari, 2000). Notwithstanding this interaction, cumulus cells and oocytes do maintain different membrane potentials (Emery et al., 2001). The significance of this finding is still unclear, especially if it is related to the high level of electrical coupling found between these two cell types and to the presence of low resistance channels such as gap junctions (Furshpan and Potter, 1959). The cumulus cells are devoted to transmitting stimuli to the oocyte, such as those involved in maintaining (Aktas et al., 1995) or removing (Batta and Knudsen, 1980; Mattioli et al., 1990) meiotic arrest. In the former case, the oocyte RP is maintained under hyperpolarizing conditions, whereas in the latter case a depolarization occurs as consequence of the action of gonadotrophins on the cumulus cells (Mattioli et al., 1990, 1991), leading to progression of meiosis. Membrane properties of cumulus cells may play an interesting role in follicle and oocyte growth and maturation (Mattioli et al., 1993). Depolarization of granulosa cells was, in fact, addressed as an essential feature of follicular maturation; this hypothesis is supported by the finding that differential granulosa cell proliferation, steroidogenic capability and apoptosis can be influenced by selective antagonism of granulosa cell K+ channels with distinct molecular correlates, electrophysiological properties, and expression patterns (Manikkam et al., 2002).
This coupling decreases at the end of maturation, along with cumulus expansion and the breaking of heterologous gap junction communications (Gilula et al., 1978; Suzuki et al., 2000). However, this is not accompanied by a simultaneous decrease in electrical coupling (Racowsky and Satterlie, 1985, 1987). The expansion of cumulus in the mature oocyte causes a depolarization of the resting potential which reaches the same value as that obtained in immature oocytes after cumulus removal (Emery et al., 2001). The artificial separation of these two integrated components may therefore generate artefacts. On the other hand, the maintenance of the cumulus–oocyte complex prevents advanced investigation of the plasma membrane, which can only be performed after cumulus removal. In our experience with bovine oocytes, we did not find significant differences between immature (GV stage) and in vitro matured (MII stage) oocytes with regards to the RP values; this could be attributed to cumulus removal. However, RP variations were found during meiosis progression (Tosti et al., 2000). In addition, the removal of cumulus cells allowed us to appreciate large variations in plasma membrane ion channels, related both to conductance as well as to Ca2+ stores (Boni et al., 2002; Tosti et al., 2002).
A wide range of modifications were found on the oocyte plasma membrane in association with rapid modifications of the intracellular environment, such as changes in free Ca2+ concentration. These modifications occur both on resumption of meiotic arrest due to hormonal signals (Eppig et al, 1984) and on sperm entry (Miyazaki and Igusa, 1981b). In the immature oocyte, plasma membrane properties vary according to meiosis progression (McCulloh and Levitan, 1987; Tosti et al., 2000) as well as according to developmental competence (Murnane and De Felice, 1993; Boni et al., 2002). In particular, in bovine oocytes the RP depolarizes during meiosis progression, after a preliminary hyperpolarization at GVBD stage (Tosti et al., 2000). The opposite pattern has also been recorded in relation to plasma membrane permeability (Murnane and De Felice, 1993; Tosti et al., 2000). Biophysical and pharmacological evidence strongly suggests that these electrical currents on the oocyte plasma membrane represent L-type Ca2+ channels. These channels have been demonstrated to underlie meiosis resumption in ascidian (Dale et al., 1991), mussel (Tomkoviak et al, 1997), Pleurodeles (Ouadid-Ahidouch, 1998) and mouse (Murnane et al., 1988) oocytes. In bovine oocytes, the activity of the L-type Ca2+ channels decreases throughout meiosis progression (Tosti et al., 2000). Since Ca2+ is necessary for meiosis progression (Homa, 1991, 1995; He et al., 1997), this pattern may support the cytosolic Ca2+ rise in GV following LH and/or growth factor exposure (Mattioli et al., 1998; Hill et al., 1999). This highlights the additional role of external Ca2+ in mobilization of intracellular Ca2+ during oocyte activation and fertilization in this species.
In humans, the first studies on membrane potential were performed by measuring intracellular electrical recordings in immature oocytes collected by ovariectomy (Eusebi et al., 1984; Dolci et al., 1985). Using the same electrophysiological technique, Feichtinger et al. (1988) tested membrane potential variations in oocytes collected at different stages of maturation by ultrasound-guided retrieval. De Felice et al. (1988) first applied patch-clamp and whole cell recordings to immature and mature oocytes. The most frequently observed channel in mature oocytes was a 60 pS non-inactivating, K+-selective pore, which was activated by depolarization. Recently, the recording of membrane potential has been extended to oocyte mitochondrial membranes by using fluorescent probes combined with image analysis techniques. In these studies, a large variability was found in mitochondrial membrane potential, and this has been considered as a discriminating parameter for evaluating oocyte quality (Van Blerkom et al., 2002; Wilding et al., 2003).
The role played by membrane potential modifications in oocyte maturation is still unclear. The change in current amplitude, density and membrane capacitance in the oocytes of all animals described appears to be related to progression of meiotic maturation and to the preparation of the oocyte for fertilization. In fact, most of the oocytes studied to date show a clear change in their electrical properties upon fertilization. The oocyte hyperpolarization occurring at the beginning of the maturation process is due to a selective permeability to K+ ions (Powers and Tupper, 1977). However, maturation is arrested by the K+-selective ionophore, valinomycin (Powers and Biggers, 1976). In addition, the depolarization of immature oocytes following LH exposure (Dawson and Conrad, 1972; Georgiou et al., 1984; Kline, 1988) follows granulosa cell depolarization and may, hence, represent a consequence rather than a cause of the meiotic block removal.
The spermatozoon
The role of the fertilizing spermatozoon is to transport the male genome into the oocyte and to trigger the oocyte into metabolic activation. In order to become competent for oocyte activation, the spermatozoon must first undergo a series of modifications induced by contact with components of the external layers of the oocyte. Many of these processes involve a change in the electrical properties of the plasma membrane. During the past decade, an improvement in techniques of investigation such as voltage- and ion-sensitive fluorescent indicators, immunocytochemistry, pharmacology and DNA recombinant technology has led to an accumulation of evidence that increasingly implies a role for ion channels in sperm physiology (Darszon et al., 1999; 2001, 2002). The application of the patch-clamp technique to monolayers generated from a mixture of lipid vesicles and isolated sperm membranes had a significant technological impact on our understanding of the electrophysiology of the sperm cell. Single channel recording from sea urchin sperm plasma membrane identified the presence of K+ and Cl– channel activity (Lièvano et al., 1985). Subsequently, this was extended to a series of animal models revealing the presence of several types of ion channels on the sperm plasma membrane, including cation (K+ and Ca2+) and anion (Cl–) channels (Chan et al., 1997). However, the molecular mechanisms that link the action of ion channels to gamete physiology are yet to be clarified.
Immature germ cells offer a technical advantage, in that their size and immobility allow the patch-clamp technique to be easily applied. Although only a few studies have so far been conducted on the role of ion channels in immature male germ cells, they have supplied useful information about the role of ion channels in sperm physiology. These may only be extrapolated to mature sperm if it is assumed that immature germ cells express the same proteins that are present on the sperm plasma membrane.
The presence of K+ and Ca2+ currents in rat spermatogenetic cells was first demonstrated by Hagiwara and Kawa (1984). Subsequently, a more accurate analysis showed that rat spermatids exhibited a negative RP, determined by Cl– and K+ conductance with a minor contribution of Na+ conductance (Reyes et al., 1994). A role for Cl– conductance in spermatogenesis was later shown in Caenorhabditis elegans by Machaca et al. (1996); in this study a new inwardly rectifying Cl– channel was characterized and put forward as a candidate factor in spermatid differentiation.
In mouse spermatogenetic cells (Santi et al., 1998), a pH-dependent Ca2+ permeability factor and a series of K+-selective currents have been correlated with the state and function of mature sperm. In particular, Ca2+ influx is required for initiating the acrosome reaction in mature sperm, whereas K+ seems to contribute to the hyperpolarization and regulation of sperm fertilizing capability (Munoz-Garay et al., 2001; Felix et al., 2002). Recently, biomolecular studies provided evidence for the regulation of T-type Ca2+ channel expression during mouse spermatogenesis (Son et al., 2002) and suggested that these sperm channels are implicated in the fertility block caused by contraceptive substances (Bai and Shi, 2002a).
The above literature indicates a clear involvement of ion channels in spermatogenesis and in the functionality of the mature spermatozoon. More information is available on the electrical properties of the spermatozoon immediately after ejaculation, when it is not yet competent for fertilization. Fertilizing ability relies on a final maturation process known as sperm activation (or capacitation in mammals), a process that may be divided into two main events: chemotaxis (and hyperactivated motility) and the acrosome reaction.
Chemotaxis
Chemotaxis is described by the activation of sperm motility and the attraction of activated sperm towards the oocyte. The communication of pre-contact gametes by means of chemotaxis is well documented in species with external fertilization (for review see Tosti, 1994). Rothschild (1948) demonstrated that extreme conditions of K+ concentration, pH and oxygen tension maintain sea urchin sperm quiescent in the testis. After spawning, a change in these physical parameters induced sperm to swim, by acting on the tail axonema. Subsequent studies demonstrated that sperm motility is triggered by environmental cues, including diffusible compounds from the outer layer of oocytes, through transduction events involving sperm ion channels (Morisawa, 1994). In particular, many small peptides on the external envelope of echinoderm oocytes can induce ion fluxes causing a mobilization of second messengers. All of these peptides have a similar function in inducing sperm motility; they essentially use K+ channel modulation as the first response to their binding with a receptor on the sperm plasma membrane (Lièvano et al., 1985; Lee and Garbers, 1986). At spawning, K+ efflux through this channel causes a cascade of consecutive electrical events that can be summarized as follows: hyperpolarization of the RP, Na+/H+ exchange, pH rise, increase in cyclic nucleotides, Na+ influx, depolarization of RP and Ca2+ efflux (for review see Darszon et al., 2001). In addition, the hyperpolarization is also strictly related to a cation channel which has been found mainly in the flagellum and whose function may be involved in flagellar beating (Gauss, 1998).
Chemotaxis in ascidians has been well described for some time (Miller, 1975); however, the involvement of ion channels in this process has been highlighted only recently by Morisawa’s team (Izumi et al., 1999), who proposed a mechanism similar to that described above. In brief, an increase in K+ permeability occurs at the point of contact of the sperm with the oocyte investment, and this induces –50 mV hyperpolarization of the sperm plasma membrane which in turn elevates cAMP. A cascade of cAMP-dependent kinases may then activate sperm motility (Izumi et al., 1999). Moreover, T- type Ca2+ channels were found to be related to the elevation of cAMP (Yoshida et al., 1994), suggesting a role for Ca2+ in ascidian sperm chemotaxis. In contrast to these findings, recent evidence showed that flagellar movements in ascidian sperm are regulated by a capacitative and not a voltage-gated Ca2+ entry (Yoshida et al., 2003).
Osmolarity is one the main parameters that regulate sperm motility in fishes. In particular, a change in external osmolarity seems to be converted into a change in intracellular K+ concentration. Subsequently, a K+ efflux and intracellular Ca2+ rise has been shown to act as a trigger that initiates sperm motility in marine and freshwater teleosts, salmonid and rainbow trout (Tanimoto and Morisawa, 1988; Oda and Morisawa, 1993; Tanimoto et al., 1994; Takai and Morisawa, 1995).
In mammals, the role of follicular factors causing chemotactic sperm attraction has only recently been highlighted (Eisenbach, 1999). However, the molecular mechanism underlying the process is still poorly understood. Whereas the role of ion channels has been clearly demonstrated in chemotaxis in invertebrates, in mammals there is some evidence to indicate that intracellular Ca2+ release from stores in the mid-piece is involved. The Ca2+ increase seems to mediate flagellar beating and, hence, chemotactic response (Cook et al., 1994; Ho and Suarez, 2001; Suarez and Ho, 2003).
Acrosome reaction
The acrosome reaction (AR) is the last activating event in the spermatozoon as it becomes competent for fertilization. The exocytosis of the acrosome and the consequent release of its contained enzymes allows the spermatozoon to penetrate the extracellular oocyte investments (Garbers, 1989). As with chemotaxis, AR is induced at the contact with the outer layer of the oocyte. Different compounds have been shown to be responsible for AR induction.
In echinoderms, sea urchin and starfish, substances on the oocyte jelly, such as fucose sulphate polymers (Alves et al., 1998), sulphated fucose, galactose, xylose and the acrosome reaction-inducing substance (ARIS), are involved in AR induction (Ikadai and Hoshi, 1981; Alves et al., 1997; Koyota et al., 1997). The AR takes place after binding between these substances and a specific receptor on the sperm plasma membrane. The AR is recognized to be an ion channel-regulated event; in fact, ion channels on the sperm plasma membrane are mobilized within a few seconds of sperm binding. Ca2+ influx is an absolute requirement for AR in the sperm of all species (Darszon et al., 1999), since it seems to be involved in the dehiscence of the acrosomal vesicle and in membrane fusion (Darszon et al., 2001). Along with Ca2+, K+ also plays a role in the AR; this is supported by experimental evidence: (i) K+ and Ca2+ channel inhibitors block the AR (Kazazoglou et al., 1985; Yanagimachi, 1994) and (ii) specific Ca2+ and K+ ionophores trigger the AR (Collins and Epel, 1977; Schackmann et al., 1978; Yanagimachi, 1994). In sea urchin the electrical events underlying the AR after contact of oocyte jelly with a sperm receptor result in an immediate Na+ and Ca2+ influx and H+ and K+ efflux. These events also result in a change in RP, an increase in pH due to a Na+/H+ exchange and the intracellular Ca2+ rise (Darszon et al., 1999). Evidence for the presence of two different Ca2+ channels and their synergistic action in inducing AR has been reported by Guerrero and Darszon (1989). The Na+/H+ exchange and pH rise is induced by mobilization of K+ channels that results in a fast and transient hyperpolarization followed by a Ca2+-mediated depolarization (Lièvano et al., 1985; Gonzàlez-Martìnez and Darszon, 1987; Gonzàlez-Martìnez et al., 1992). Cl–-selective anion channels have also been identified in sea urchin sperm plasma membrane; they may have a role in the AR, influencing the RP of the gamete (Morales et al., 1993).
Mammalian sperm acquire the ability to fertilize at the end of a process called ‘capacitation’ (for review, see Yanagimachi, 1994). This enables the spermatozoon to induce its AR, in response to the zona pellucida (ZP) or to agents such as progesterone (Osman et al., 1989). As in invertebrates, the contact of the sperm receptor with the oocyte envelope (ZP in mammals) or AR inducers causes elevation of intracellular Ca2+, pH increase and a change in the RP (Arnoult et al., 1999; Florman et al., 1998; Patrat et al., 2000; Darszon et al., 2001).
Ion channels on the head of the mammalian spermatozoa that are responsible for Ca2+ entry and intracellular Ca2+ rise include: (i) low and high voltage-activated channels, (ii) receptor-operated Ca2+ channels and (iii) store-operated Ca2+ channels (Benoff, 1998). T-type voltage-gated Ca2+ channels have a pivotal role in mediating the AR (Florman et al., 1998; Darszon et al., 1999). The gating of these channels has been demonstrated in mammalian (Arnoult et al., 1996; Publicover and Barratt, 1999) and in human sperm by AR inducers such as progesterone (Garcia and Meizel, 1999) and mannose–bovine serum albumin (Blackmore and Eisoldt, 1999; Son et al., 2000). Although the existence of voltage-gated Ca2+ channels has been demonstrated in human sperm (Linares-Hernández et al., 1998), their function in the induction of the AR has not yet been elucidated (for review see Jagannathan et al., 2002). A capacitating Ca2+ entry mechanism has been proposed as a possible mechanism for gating plasma membrane Ca2+ channels. In mouse sperm, the existence of a Ca2+ influx dependent on depletion of Ca2+ stores has recently been shown (O’Toole et al., 2000). Rossato et al. (2001) have proposed an interesting model to explain a possible mechanism for the AR in human sperm. They demonstrated the existence of Ca2+ stores whose depletion activates a double process: (i) gating of Ca2+-activated K+ channels, with K+ efflux causing a hyperpolarization, and (ii) the capacitative gating of voltage-gated Ca2+ channels, with a subsequent depolarization of the plasma membrane.
Anions have also been implicated in the mammalian AR (Morales et al., 1993). This hypothesis was recently supported by electrophysiological studies that found different types of Cl– channels with different conductance on the sperm head (Bai and Shi, 2001). A Cl– efflux is feasible for inducing a depolarization of the RP since it has been shown that sperm contain a high amount of Cl– ions internally (Sato et al., 2000). Moreover, a Cl– efflux seems to be induced by progesterone (Meizel, 1997).
Although the role of Ca2+ in inducing the AR is well demonstrated, and Ca2+ elevation has been shown to be mediated by ion channels, the mechanism by which the ZP or other agents are able to gate the channels is not yet understood. Figure 2 (bottom) demonstrates a schematic representation of the sperm plasma membrane ion channel activity during the processes of chemotaxis and AR.
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Electrical events at fertilization |
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TOPAbstractIntroductionElectrophysiology of the cellElectrical properties of the...Electrical events at...Concluding remarksAcknowledgementsReferences |
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Fertilization is a highly specialized process of cell–cell interaction that marks the creation of a new and unique individual. It is a complex multi-step process involving many events, including gamete recognition, binding and fusion. Reciprocal activation of the two gametes is a crucial element of these events; signals from the oocyte investments induce dramatic changes in form and function of the spermatozoon, and the spermatozoon triggers the quiescent oocyte into metabolic activation (for review see Yanagimachi, 1994
). Oocyte activation is a dynamic mechanism, and its progress is characterized by early and late events (Xu et al., 1994). Cortical granule exocytosis is an early activation event, and resumption of meiosis is a late activation event.
The first described metabolic findings associated with oocyte activation were described in the sea urchin, an increase in O2 consumption and activation of NAD kinase (Epel, 1978). At fertilization, an increase in internal pH occurs in sea urchin oocytes is required for the initiation of development (Johnson et al., 1976). This is not the case for mammalian oocytes, where no detectable change in pH occurs after fertilization (Baltz et al., 1995).
However, the first well-recognized event driving oocyte activation is a sperm-induced Ca2+ release (for review see Swann and Jones, 2002). An increase in intracellular Ca2+ at fertilization was observed for the first time in the oocytes of the medaka fish (Ridgway et al., 1977). This mechanism was subsequently universally recognized, in both animal and vegetable kingdoms (Roberts et al., 1994; Digonnet et al., 1997). Ca2+ is therefore considered to be the major second messenger during oocyte activation (Whittingham, 1980; Whitaker and Steinhardt, 1982; Jaffe et al., 1983; Kline, 1988; Kline and Kline, 1992; Swann and Ozil, 1994; Lawrence et al., 1997). However, the mechanism by which sperm can evoke this event is not yet characterized. Three theories are currently under investigation, named by Jaffe (1991) as ‘conduit, contact and content’ models (for review see Nixon et al., 2000). In the ‘conduit’ model the sperm acts as a conduit for Ca2+ entry from the extracellular medium (Creton and Jaffe, 1995). The ‘contact’ model assumes the activation of an oocyte phospholipase C following sperm–oocyte interaction (Foltz and Shilling, 1993; Evans and Kopf, 1998). The ‘content’ model proposes that a soluble sperm factor is released into the oocyte following gamete fusion (Dale et al., 1985; Swann, 1990). Regardless of the mechanism, it is certain that sperm acts as a preliminary stimulus for oocyte activation. The activation signal from the site of sperm entry is transmitted to the entire oocyte, mediated by an increase in intracellular Ca2+ that quickly returns to baseline. This calcium wave represents a single event in some species, such as medaka fish (Ridgway et al., 1977), sea urchin (Steinhardt et al., 1977) and frog (Busa and Nuccitelli, 1985). In other species, such as mammals and ascidians, the wave is followed by a long-lasting series of Ca2+ oscillations (Miyazaki and Igusa, 1981b; Cuthbertson and Cobbold, 1985). The mechanism of propagation, amplification and regeneration of this Ca2+ signal is mediated by Ca2+-specific receptors (Fujiwara et al., 1990; Carroll and Swann, 1992; Swann, 1992; Whitaker and Swann, 1993; Miyazaki et al., 1993; Yue et al., 1995; Galione et al., 2000). Among these, ryanodine receptors are considered to be involved in Ca2+-induced Ca2+ release (CICR), a plausible mechanism for the regenerative Ca2+ waves during fertilization (Eisen et al., 1984; Swann and Whitaker, 1986).
Electrical changes of the oocyte plasma membrane represent the other crucial event of oocyte activation, along with the rise in intracellular Ca2+. The relationship between these two events varies among species, and is not yet clear. Hagiwara and Jaffe (1979) have demonstrated that an oocyte is not activated by electrical modifications alone, and that intracellular calcium modifications are not strictly dependent on electrical changes. However, these two events occur almost simultaneously, with similar dynamics, and they are linked by common mechanisms. A clear example of the linkage between these two events is given by calcium-activated K+ channels in mammalian oocyte activation. In other species, the linkage between electrical changes and calcium rise varies from a strict dependence as in annelids (Eckberg and Miller, 1995) to completely separate pathways as in ascidian (Dale, 1987).
A role for K+ ion fluxes through the plasma membrane in the process of oocyte activation was first described in pioneering studies on marine animals (Tyler et al., 1956; Hiramoto, 1958). The spermatozoon generates a transient change of the RP in the oocyte, described as the fertilization potential (FP). However, the biophysical origin of this voltage modification was not elucidated. Using the voltage-clamp technique, it was later demonstrated that the FP results from an ion flux (the fertilization current: FC) across the plasma membrane. Further characterization demonstrated that this current is due to the gating of novel plasma membrane ion channels in the newly fertilized oocyte (for reviews see Miyazaki, 1988; Dale and De Felice, 1984, 1990). Pharmacological agents generated similar ion activation currents in oocytes mimicking the form and the effects of the sperm-induced ion current, resulting in the early development of parthenogenetic embryos (Boni et al., 2002; Tosti et al., 2002).
During the 1950s, electrical parameters and ion contents were shown to change at fertilization in echinoderm oocytes (Monroy-Oddo and Esposito, 1951; Hiramoto, 1959). In starfish oocytes, a FP is the first electrical event of fertilization (Dale et al., 1981), and an inward ion current underlies the FP (Lansman, 1983). In sea urchin oocytes, Dale et al. (1978) characterized a typical FP as a depolarization, preceded by a depolarizing-like step; these events were accompanied by an increase in voltage noise and a decrease in membrane resistance (Figure 3). The FP form was attributed to the activation of a transient voltage-dependent inward current, due to the increase in intracellular Ca2+ concentration occurring at fertilization (David et al., 1988). Initial characterization of ion channels responsible for the FC demonstrated that non-specific ion 70 pS single channel conductance (Dale et al., 1978) and voltage-gated Na+ and Ca2+ channels (Chambers, 1989b) are involved. More recently, De Simone et al. (1998) recorded an inward Ca2+-dependent FC in whole cell voltage-clamped sea urchin oocytes, demonstrating that this current is driven by non-specific ion channels.
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In the oocytes of Ciona intestinalis, the spermatozoon induces an inward FC via a new population of channels that appears in the membrane a few seconds after insemination (Dale and De Felice, 1984
). Gating of these channels is accompanied by a small step-like depolarization followed by a larger overshooting depolarization (Dale et al., 1983). These fertilization channels have been characterized as large and non-specific, with a single conductance of 400 pS (Dale and De Felice, 1984; De Felice and Kell, 1987). Recently, Tosti et al. (2003) have demonstrated a role for FC in triggering normal embryo development in C. intestinalis. A different pattern of voltage-gated channels was described in Phallusia mammillata after fertilization, where voltage-gated Ca2+ channels play a role (Goudeau and Goudeau, 1993) and an inward rectifying Cl– current appears after fertilization in Boltenia villosa (Coombs et al., 1992). A summary of RP modifications and the major channels involved in oocyte activation and fertilization are reported in Table I.
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Oocyte Cl– channels are responsible for the FP in several amphibian species. In Xenopus laevis, a membrane depolarization at fertilization is influenced by the external Cl– concentration (Webb and Nuccitelli, 1985a
,b); this is a consequence of Cl– ion efflux (Cross and Elinson, 1980). Similarly, a positive shift in FP was shown in R. pipiens associated with an increase of either K+ or Cl– and a decrease in Na+ conductance (Jaffe and Schlichter, 1985; Schlichter, 1989b). Membrane potential changes in R. cameranoi oocytes are also based on K+ as well as on Cl– conductance (Erdogan et al., 1996), with a different function for these two ions. Cl– ions are apparently responsible for the first depolarization phase evoked by sperm, whereas K+ contributes to the repolarizing phase. The role of Ca2+ channels in amphibian FP is less clear. Although no significant role for external Ca2+ has been shown in R. cameranoi (Erdogan et al., 1996), there is clear evidence that intracellular Ca2+ contributes to gating the Cl– channels (Barish, 1983). Recently, Glahn and Nuccitelli (2003) recorded the FC in Xenopus oocytes for the first time; this FC resembles that of marine invertebrates, but it is generated by Ca2+-activated Cl– channels. Studies in hamster oocyte demonstrated a series of hyperpolarizations following fertilization, the first marked difference shown between mammalian and non-mammalian electrical responses (Miyazaki and Igusa, 1981a). Similar FC have subsequently been recorded in other mammalian species, such as mouse (Igusa et al., 1983; Jaffe et al., 1983), human (Gianaroli et al., 1994) and bovine (Tosti et al., 2002). The pattern in rabbit oocytes is different, in that a preliminary depolarization is followed by a repeated diphasic (hyperpolarization/depolarization) pattern of membrane modifications (McCulloh et al., 1983). As in the marine models, these electrical modifications of the plasma membrane following fertilization in mammals are due to ion passage. However, in contrast to the marine species, where FC is apparently directly gated by the spermatozoon, in mammals Ca2+-activated K+ channels are gated by an initial calcium release (Miyazaki and Igusa, 1981b; Dale et al., 1996; Tosti et al., 2002). A dependence between calcium modification and plasma membrane potential was argued by Miyazaki (1989) based on biophysical evidence together with the fact that: (i) loading the oocyte with EGTA prevents hyperpolarization oocyte and (ii) Ca2+ injection into the oocyte triggers a similar hyperpolarization. The hyperpolarization that follows fertilization is the first of a series of electrical oscillations of the membrane potential, in accordance with Ca2+ oscillations (for review see Miyazaki, 1989) that continue up to pronuclear formation (Jones et al., 1995). These oscillations decrease in frequency and amplitude during their progression. The oscillations are large in hamster (Miyazaki and Igusa, 1983) and smaller in mouse (Igusa et al., 1983; Jaffe et al., 1983) and rabbit (McCulloh et al., 1983) oocytes. After oocyte activation, plasma membrane Ca2+ channels have an increased role in replenishing stores for the continuation of Ca2+ oscillations (Stricker, 1999). In hamster, external Ca2+ is required for oocyte activation (Igusa and Miyazaki, 1983).
It can be seen that the dynamics of RP modifications at fertilization change in relation to the phyla and species. In the ascidian C. intestinalis, fertilization channels are not activated by Ca2+ (Dale, 1987). In sea urchin and frog oocytes, Ca2+ entry causes a long-lasting phase of depolarization (Whitaker and Steinhardt, 1982; Busa, 1990), which can be detected as a wave moving across the oocyte surface in relation to the Ca2+ wave (Kline and Nuccitelli, 1985). In hamster, repetitive hyperpolarization pulses following fertilization are related to repetitive Ca2+ rises due to Ca2+-activated K+ channels (Miyazaki and Igusa, 1981b, 1982). This reveals a clear dependence between membrane potential activity and Ca2+ modifications. In the bovine, a clear relationship between electrical properties of the oocyte plasma membrane and intracellular calcium modifications has also been recorded following fertilization, as well as following chemical oocyte activation or after exposure to specific Ca2+ releasers (Tosti et al., 2002). A schematic representation of the bovine oocyte plasma membrane ion channel activity along maturation and fertilization processes is illustrated in Figure 2 (top).
In the human oocyte, Gianaroli et al. (1994) described a bell-shaped outward FC accompanied by a long hyperpolarization of the plasma membrane. Homa and Swann (1994) observed Ca2+-activated outward activation currents, following cytosolic sperm factor injection that was proposed as a signal of oocyte activation. Similar activation currents were also found following Ca2+ ionophore exposure (Dale et al., 1996). Further characterization of ion channels in the human revealed that, similar to other mammalian species, the initial activation response of the oocyte is related to the gating of Ca2+-activated K+ channels (Dale et al., 1996).
The significance of the change in resting potential at fertilization is still unclear in the majority of cases. Membrane depolarization represents a key stimulus for activation in invertebrate oocytes (Dube, 1988). In addition, electrical modifications have been proposed as a mechanism for preventing polyspermy in sea urchin (Jaffe, 1976), ascidian (Goudeau at al., 1994) and Xenopus (Glahn and Nuccitelli, 2003) oocytes. However, this hypothesis remains controversial, since different authors have proposed contrasting findings (De Felice and Dale, 1979; McCulloh et al., 1987). In addition, there is no evidence for an electrical block to polyspermy in mammalian oocytes (Miyazaki and Igusa, 1982; Jaffe et al., 1983; McCulloh et al., 1983). Hence, a clear role for the electrical events has not yet been demonstrated, apart from their linkage with an increase in intracellular free Ca2+ concentration. Recent studies in mouse, however, hint that a food contaminant (the cotton seed gossypol, with anti-fertility properties) may have a direct effect on sperm fertilizing capability by elective inhibition of T-type Ca2+ channels (Bai and Shi, 2002b).
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Concluding remarks |
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TOPAbstractIntroductionElectrophysiology of the cellElectrical properties of the...Electrical events at...Concluding remarksAcknowledgementsReferences |
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The presence of ion currents in gamete plasma membranes and their modification during the maturation and fertilization processes are described from marine invertebrates to humans. Nonetheless, their role in gamete biology is not completely understood. For many years the most feasible hypothesis has been that the electrical change in oocytes at fertilization was devoted to a rapid block to polyspermy. However, recent studies reported in this review shed new light on the role of ion currents in many processes of gamete biology. A tremendous potential of knowledge is now emerging from studies on ion channels in sperm physiology. The molecular cloning of an ion channel specific for mouse and human testis and sperm (Quill et al., 2001
; Ren et al., 2001) has clearly shown that sperm ion currents are involved in male fertility. Ion channels can be used to elucidate ion current signalling patterns, and may provide new potential tools to help clarify the mechanism of fertilization and to improve both assisted reproductive and contraceptive technologies.
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Acknowledgements |
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TOPAbstractIntroductionElectrophysiology of the cellElectrical properties of the...Electrical events at...Concluding remarksAcknowledgementsReferences |
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We thank Dr K.Elder and Dr L.J.De Felice for their helpful comments and Mr G.Gargiulo for figure preparation. This work was supported by the Italian Ministry of University and Research (M.I.U.R.), COFIN 2002 project.
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References |
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