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Gamete cells are electrogenic, i.e. capable of responding to electrical stimuli and modifying their electrical proper-
ties during the crucial periods of maturation and fertilization. Ion channels have been widely demonstrated on the
Human Reproduction Update Vol. 10 No. 1 ã European Society of Human Reproduction and Embryology 2004; all rights reserved 53
E.Tosti and R.Boni
concentration externally, whereas there is a great variation in the The patch-clamp technique, ®rst described by Neher and
anions present inside the cell. These intracellular anions include Sakmann (1976), is the most popular technique used to study
negative charges provided by several constituents that carry cell currents; the basic con®gurations of this technique involve
phosphate and carboxyl groups. The different distribution of whole cell or single channel recordings. The former measures
electrical charges inside and outside the cell creates an electrical currents from an entire cell under voltage clamp and this is
gradient across the membrane, known as voltage, and this is normally obtained after seal and destruction of the patched
measured in Volts. The voltage difference across the cell membrane. The single channel con®guration records a channel
membrane creates a store of potential energy in the form of an activity inside the intact patched membrane. The application of
ion gradient, giving rise to a transmembrane potential known as Giga-seal resistance and different con®gurations of the patch-
resting potential (RP). This parameter changes in relation to ion clamp technique literally revolutionized the study of membrane
distribution and membrane permeability. electrophysiology, and allowed access to new information about
In the majority of cells studied, the RP is negative, in a range of cell function (for review see: Neher, 1988, 1992; Neher and
±10 to ±100 mV (Hagiwara and Jaffe, 1979). Potassium is Sakmann, 1992; Levis and Rae, 1998). Figure 1 lists a glossary of
electively stored inside the cell, and it is the ion that contributes the main electrophysiological parameters described above.
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 speci®c transport proteins Electrical properties of the gamete plasma membrane
and ion channels in the plasma membrane. The transport proteins
(ion pumps) maintain the concentration gradients that determine The oocyte
54
Ion channels in gametes
current component has a role in regulating cytosolic calcium units occurs spontaneously in the mature oocyte, but during
during early developmental processes. immature stages there is an intimate interaction between the
Schlichter (1989a) has provided an excellent overview on ion oocyte and the cumulus cells, and this is maintained by
channels in amphibian oocytes; a role for Cl± currents emerges in intercellular communications such as gap junctions (Gilula et al.,
both immature and mature oocytes in all the species studied. In the 1978; Canipari, 2000). Notwithstanding this interaction, cumulus
European frog Rana esculenta, changes in membrane permeability cells and oocytes do maintain different membrane potentials
occur during maturation; in particular, K+ and Cl± voltage-gated (Emery et al., 2001). The signi®cance of this ®nding is still
currents present in the immature oocytes disappear in mature unclear, especially if it is related to the high level of electrical
oocytes, replaced by a Na+ current (Taglietti et al., 1984). A Ca2+- coupling found between these two cell types and to the presence of
dependent Cl± current has been shown in Xenopus immature low resistance channels such as gap junctions (Furshpan and
oocytes (Barish, 1983), and Na+ currents similar to those of Potter, 1959). The cumulus cells are devoted to transmitting
neuronal cells, as well as other non-speci®c ion currents, have also stimuli to the oocyte, such as those involved in maintaining (Aktas
been described (Bourinet et al., 1992; Weber, 1999). The same et al., 1995) or removing (Batta and Knudsen, 1980; Mattioli et al.,
currents are present in immature metaphase I oocytes of R. pipiens, 1990) meiotic arrest. In the former case, the oocyte RP is
each contributing differently to subsequent fertilization potential maintained under hyperpolarizing conditions, whereas in the latter
(Schlichter, 1989b); in particular, Cl± is lost as the oocyte case a depolarization occurs as consequence of the action of
undergoes maturation (Schlichter, 1983). A noticeable voltage- gonadotrophins on the cumulus cells (Mattioli et al., 1990, 1991),
dependent hydrogen current was ®rst demonstrated in the axolotl leading to progression of meiosis. Membrane properties of
Ambistoma oocytes (Barish and Baud, 1984). cumulus cells may play an interesting role in follicle and oocyte
In addition to the above species, ion currents that play a possible growth and maturation (Mattioli et al., 1993). Depolarization of
role in the mechanism of maturation and fertilization have been granulosa cells was, in fact, addressed as an essential feature of
observed in other non-mammalian species such as molluscs follicular maturation; this hypothesis is supported by the ®nding
(Moreau et al., 1996; Ouadid-Ahidouch, 1998; Gould et al., 2001; that differential granulosa cell proliferation, steroidogenic cap-
E.Tosti, unpublished data), and marine polychaetes (Gunning, ability and apoptosis can be in¯uenced by selective antagonism of
1983; Fox and Krasne, 1984). granulosa cell K+ channels with distinct molecular correlates,
In mammals, separating the oocyte from the cumulus invest- electrophysiological properties, and expression patterns
ment makes the measurement of electrical parameters technically (Manikkam et al., 2002).
dif®cult, and therefore there are very few papers that discuss This coupling decreases at the end of maturation, along with
electrical properties of the mammalian oocyte plasma membrane cumulus expansion and the breaking of heterologous gap junction
during maturation. A functional separation between these two communications (Gilula et al., 1978; Suzuki et al., 2000).
55
E.Tosti and R.Boni
However, this is not accompanied by a simultaneous decrease in these studies, a large variability was found in mitochondrial
electrical coupling (Racowsky and Satterlie, 1985, 1987). The membrane potential, and this has been considered as a discrim-
expansion of cumulus in the mature oocyte causes a depolarization inating parameter for evaluating oocyte quality (Van Blerkom
of the resting potential which reaches the same value as that et al., 2002; Wilding et al., 2003).
obtained in immature oocytes after cumulus removal (Emery et al., The role played by membrane potential modi®cations in oocyte
2001). The arti®cial separation of these two integrated components maturation is still unclear. The change in current amplitude,
may therefore generate artefacts. On the other hand, the mainten- density and membrane capacitance in the oocytes of all animals
ance of the cumulus±oocyte complex prevents advanced investi- described appears to be related to progression of meiotic
gation of the plasma membrane, which can only be performed after maturation and to the preparation of the oocyte for fertilization.
cumulus removal. In our experience with bovine oocytes, we did In fact, most of the oocytes studied to date show a clear change in
not ®nd signi®cant differences between immature (GV stage) and their electrical properties upon fertilization. The oocyte hyperpo-
in vitro matured (MII stage) oocytes with regards to the RP values; larization occurring at the beginning of the maturation process is
this could be attributed to cumulus removal. However, RP due to a selective permeability to K+ ions (Powers and Tupper,
variations were found during meiosis progression (Tosti et al., 1977). However, maturation is arrested by the K+-selective
2000). In addition, the removal of cumulus cells allowed us to ionophore, valinomycin (Powers and Biggers, 1976). In addition,
appreciate large variations in plasma membrane ion channels, the depolarization of immature oocytes following LH exposure
related both to conductance as well as to Ca2+ stores (Boni et al., (Dawson and Conrad, 1972; Georgiou et al., 1984; Kline, 1988)
2002; Tosti et al., 2002). follows granulosa cell depolarization and may, hence, represent a
A wide range of modi®cations were found on the oocyte plasma consequence rather than a cause of the meiotic block removal.
56
Ion channels in gametes
Caenorhabditis elegans by Machaca et al. (1996); in this study a membrane which in turn elevates cAMP. A cascade of cAMP-
new inwardly rectifying Cl± channel was characterized and put dependent kinases may then activate sperm motility (Izumi et al.,
forward as a candidate factor in spermatid differentiation. 1999). Moreover, T- type Ca2+ channels were found to be related
In mouse spermatogenetic cells (Santi et al., 1998), a pH- to the elevation of cAMP (Yoshida et al., 1994), suggesting a role
dependent Ca2+ permeability factor and a series of K+-selective for Ca2+ in ascidian sperm chemotaxis. In contrast to these
currents have been correlated with the state and function of mature ®ndings, recent evidence showed that ¯agellar movements in
sperm. In particular, Ca2+ in¯ux is required for initiating the ascidian sperm are regulated by a capacitative and not a voltage-
acrosome reaction in mature sperm, whereas K+ seems to gated Ca2+ entry (Yoshida et al., 2003).
contribute to the hyperpolarization and regulation of sperm Osmolarity is one the main parameters that regulate sperm
fertilizing capability (Munoz-Garay et al., 2001; Felix et al., motility in ®shes. In particular, a change in external osmolarity
2002). Recently, biomolecular studies provided evidence for the seems to be converted into a change in intracellular K+ concen-
regulation of T-type Ca2+ channel expression during mouse tration. Subsequently, a K+ ef¯ux and intracellular Ca2+ rise has
spermatogenesis (Son et al., 2002) and suggested that these been shown to act as a trigger that initiates sperm motility in
sperm channels are implicated in the fertility block caused by marine and freshwater teleosts, salmonid and rainbow trout
contraceptive substances (Bai and Shi, 2002a). (Tanimoto and Morisawa, 1988; Oda and Morisawa, 1993;
The above literature indicates a clear involvement of ion Tanimoto et al., 1994; Takai and Morisawa, 1995).
channels in spermatogenesis and in the functionality of the mature In mammals, the role of follicular factors causing chemotactic
spermatozoon. More information is available on the electrical sperm attraction has only recently been highlighted (Eisenbach,
properties of the spermatozoon immediately after ejaculation, 1999). However, the molecular mechanism underlying the process
57
E.Tosti and R.Boni
Ca2+ channels and their synergistic action in inducing AR has been voltage-gated Ca2+ channels has been demonstrated in human
reported by Guerrero and Darszon (1989). The Na+/H+ exchange sperm (Linares-HernaÂndez et al., 1998), their function in the
and pH rise is induced by mobilization of K+ channels that results induction of the AR has not yet been elucidated (for review see
in a fast and transient hyperpolarization followed by a Ca2+- Jagannathan et al., 2002). A capacitating Ca2+ entry mechanism
mediated depolarization (LieÁvano et al., 1985; GonzaÁlez-MartõÁnez has been proposed as a possible mechanism for gating plasma
and Darszon, 1987; GonzaÁlez-MartõÁnez et al., 1992). Cl±-selective membrane Ca2+ channels. In mouse sperm, the existence of a Ca2+
anion channels have also been identi®ed in sea urchin sperm in¯ux dependent on depletion of Ca2+ stores has recently been
plasma membrane; they may have a role in the AR, in¯uencing the shown (O'Toole et al., 2000). Rossato et al. (2001) have proposed
RP of the gamete (Morales et al., 1993). an interesting model to explain a possible mechanism for the AR in
Mammalian sperm acquire the ability to fertilize at the end of a human sperm. They demonstrated the existence of Ca2+ stores
process called `capacitation' (for review, see Yanagimachi, 1994). whose depletion activates a double process: (i) gating of Ca2+-
This enables the spermatozoon to induce its AR, in response to the activated K+ channels, with K+ ef¯ux causing a hyperpolarization,
zona pellucida (ZP) or to agents such as progesterone (Osman and (ii) the capacitative gating of voltage-gated Ca2+ channels,
et al., 1989). As in invertebrates, the contact of the sperm receptor with a subsequent depolarization of the plasma membrane.
with the oocyte envelope (ZP in mammals) or AR inducers causes Anions have also been implicated in the mammalian AR
elevation of intracellular Ca2+, pH increase and a change in the RP (Morales et al., 1993). This hypothesis was recently supported by
(Arnoult et al., 1999; Florman et al., 1998; Patrat et al., 2000; electrophysiological studies that found different types of Cl±
Darszon et al., 2001). channels with different conductance on the sperm head (Bai and
Ion channels on the head of the mammalian spermatozoa that Shi, 2001). A Cl± ef¯ux is feasible for inducing a depolarization of
are responsible for Ca2+ entry and intracellular Ca2+ rise include: the RP since it has been shown that sperm contain a high amount of
(i) low and high voltage-activated channels, (ii) receptor-operated Cl± ions internally (Sato et al., 2000). Moreover, a Cl± ef¯ux seems
Ca2+ channels and (iii) store-operated Ca2+ channels (Benoff, to be induced by progesterone (Meizel, 1997).
1998). T-type voltage-gated Ca2+ channels have a pivotal role in Although the role of Ca2+ in inducing the AR is well
mediating the AR (Florman et al., 1998; Darszon et al., 1999). The demonstrated, and Ca2+ elevation has been shown to be mediated
gating of these channels has been demonstrated in mammalian by ion channels, the mechanism by which the ZP or other agents
(Arnoult et al., 1996; Publicover and Barratt, 1999) and in human are able to gate the channels is not yet understood. Figure 2
sperm by AR inducers such as progesterone (Garcia and Meizel, (bottom) demonstrates a schematic representation of the sperm
1999) and mannose±bovine serum albumin (Blackmore and plasma membrane ion channel activity during the processes of
Eisoldt, 1999; Son et al., 2000). Although the existence of chemotaxis and AR.
58
Ion channels in gametes
59
E.Tosti and R.Boni
Table I. Type of ion channels involved in oocyte and sperm activation and membrane potential modi®cations at oocyte activation/fertilization
Sea urchin Non-speci®c, Na+, Ca2+ Depolarization, +17 mV Dale et al., 1978; De Simone et al., 1998
Na+, H+, Ca2+, K+ GonzaÁlez-MartõÁnez et al., 1992
Ascidians Non-speci®c Depolarization, +60 mV Dale et al., 1983; Dale and De Felice, 1984
Amphibians Cl±, K+, Na+; Ca2+- Depolarization, +22 mV Webb and Nuccitelli, 1985a,b;
activated Cl± Glahn and Nuccitelli, 2003
Mouse Ca2+-activated K+ Hyperpolarization, ±22 mV Igusa et al., 1983
T-type Ca2+ Arnoult et al., 1996
Hamster Ca2+-activated K+ Hyperpolarization, ±42 mV Miyazaki and Igusa, 1981b
Bovine Ca2+-activated K+ Hyperpolarization, ±32 mV Tosti et al., 2002
Human Ca2+-activated K+ Hyperpolarization, ±40 mV Gianaroli et al., 1994; Dale et al., 1996
T-type Ca2+, Ca2+- Garcia and Meizel, 1999; Sato et al., 2000;
activated, K+, Cl± Bai and Shi, 2001; Rossato et al., 2001
60
Ion channels in gametes
membrane Ca2+ channels have an increased role in replenishing many years the most feasible hypothesis has been that the
stores for the continuation of Ca2+ oscillations (Stricker, 1999). In electrical change in oocytes at fertilization was devoted to a rapid
hamster, external Ca2+ is required for oocyte activation (Igusa and block to polyspermy. However, recent studies reported in this
Miyazaki, 1983). review shed new light on the role of ion currents in many processes
It can be seen that the dynamics of RP modi®cations at of gamete biology. A tremendous potential of knowledge is now
fertilization change in relation to the phyla and species. In the emerging from studies on ion channels in sperm physiology. The
ascidian C. intestinalis, fertilization channels are not activated by molecular cloning of an ion channel speci®c for mouse and human
Ca2+ (Dale, 1987). In sea urchin and frog oocytes, Ca2+ entry testis and sperm (Quill et al., 2001; Ren et al., 2001) has clearly
causes a long-lasting phase of depolarization (Whitaker and shown that sperm ion currents are involved in male fertility.
Steinhardt, 1982; Busa, 1990), which can be detected as a wave Ion channels can be used to elucidate ion current signalling
moving across the oocyte surface in relation to the Ca2+ wave patterns, and may provide new potential tools to help clarify the
(Kline and Nuccitelli, 1985). In hamster, repetitive hyperpolariza- mechanism of fertilization and to improve both assisted repro-
tion pulses following fertilization are related to repetitive Ca2+ ductive and contraceptive technologies.
rises due to Ca2+-activated K+ channels (Miyazaki and Igusa,
1981b, 1982). This reveals a clear dependence between membrane
Acknowledgements
potential activity and Ca2+ modi®cations. In the bovine, a clear
relationship between electrical properties of the oocyte plasma We thank Dr K.Elder and Dr L.J.De Felice for their helpful comments
membrane and intracellular calcium modi®cations has also been and Mr G.Gargiulo for ®gure preparation. This work was supported by
recorded following fertilization, as well as following chemical the Italian Ministry of University and Research (M.I.U.R.), COFIN
61
E.Tosti and R.Boni
oocytes is related to cumulus-oocyte complex (COC) grade, calcium Dawson JE and Conrad JT (1972) The effect of human chorionic
current activity and calcium stores. Biol Reprod 66,836±842. gonadotrophin and luteinizing hormone upon the membrane potential of
Bourinet E, Nargeot J and Charnet P (1992) Electrophysiological unovulated frog oocytes. Biol Reprod 6,58±66.
characterization of a TTX-sensitive sodium current in native Xenopus De Felice LJ (1997) Electrical Properties of Cells, Patch Clamp for Biologists.
oocytes. Proc R Soc Lond Biol Sci 250,127±132. Plenum Press, New York, chap 2, pp 49±122.
Busa WB (1990) Involvement of calcium and inositol phosphates in De Felice LJ and Dale B (1979) Voltage response to fertilization and
amphibian egg activation. J Reprod Fertil 90 (Suppl 42),155±161. polyspermy in sea urchin eggs and oocytes. Dev Biol 72,327±341.
Busa WB and Nuccitelli R (1985) An elevated free cytosolic Ca2+ wave De Felice LJ and Kell MJ (1987) Sperm-activated currents in ascidian oocytes.
follows fertilization in eggs of the frog, Xenopus laevis. J Cell Biol Dev Biol 119,123±128.
100,1325±1329. De Felice LJ, Mazzanti M, Murnane J and Cohen J (1988) Patch-clamp and
Canipari R (2000) Oocyte±granulosa cell interactions. Hum Reprod Update whole-cell recording from human oocytes. Biophys J 53,547a (abstract).
6,279±289. DeSimone ML, Grumetto L, Tosti E, Wilding M and Dale B (1998) Non-
Carroll J and Swann K (1992) Spontaneous cytosolic calcium oscillations speci®c currents at fertilisation in sea urchin oocytes. Zygote 6,11±15.
driven by inositol trisphosphate occur during in vitro maturation of mouse Digonnet C, Aldon D, Leduc N, Dumas C and Rougier M (1997) First
oocytes. J Biol Chem 267,11196±11201. evidence of a calcium transient in ¯owering plants at fertilization.
Chambers EL (1989a) An autobiographical sketch. In Nuccitelli R, Cherr G Development 124,2867±2874.
and Clark WH Jr (eds) Mechanism of egg activation. Plenum Press, New Dolci S, Eusebi F and Siracusa G (1985) Gamma-Amino butyric-N-acid
York, pp XV±XXVIII. sensitivity of mouse and human oocytes. Dev Biol 109,242±246.
Chambers EL (1989b) Fertilization in voltage clamped sea urchin eggs. In Dube F (1988) The relationships between early ionic events, the pattern of
Nuccitelli R, Cherr G and Clark WH Jr (eds) Mechanism of egg protein synthesis, and oocyte activation in the surf clam, Spisula
activation. Plenum Press, New York, pp 1±18. solidissima. Dev Biol 126,233±241.
Chan HC, Zhou TS, Fu WO, Wang WP, Shi YL and Wong PY (1997) Cation Eckberg WR and Miller AL (1995) Propagated and non propagated calcium
and anion channels in rat and human spermatozoa. Biochim Biophys Acta transients during egg activation in the annelid Chaetopterus. Dev Biol
1323,117±129. 172,654±664.
62
Ion channels in gametes
Gilula NB, Epstein ML and Beers WH (1978) Cell-to-cell communication and Jaffe LA and Schlichter LC (1985) Fertilization-induced ionic conductances in
ovulation. A study of the cumulus±oocyte complex. J Cell Biol 78,58±75. eggs of the frog, Rana pipiens. J Physiol (Lond) 358,299±319.
Glahn D and Nuccitelli R (2003) Voltage-clamp study of the activation Jaffe LA, Sharp AP and Wolf DP (1983) The role of calcium explosions,
currents and fast block to polyspermy in the egg of Xenopus laevis. Dev waves and pulses in activating eggs. In Metz CB and Monroy A (eds)
Growth Differ 45,187±197. Biology of Fertilization, vol 3. Academic Press, Orlando, Florida, pp 127±
Goudeau M and Goudeau H (1993) In the egg of acidian Phallusia 165.
mammillata, removal of external Ca2+ modi®es the fertilization Jones KT, Carroll J and Whittingham DG (1995) Ionomycin, thapsigargin,
potential, induces polyspermy, and blocks the resumption of meiosis. ryanodine and sperm induced Ca2+ release increase during meiotic
Dev Biol 160,165±177. maturation of mouse oocytes. J Biol Chem 270,6671±6677.
Goudeau H, Depresle Y, Rosa A and Goudeau M (1994) Evidence by a Johnson JD, Paul M and Epel D (1976) Intracellular pH and activation of sea
voltage-clamp study of an electrically mediated block to polyspermy in urchin eggs after fertilization. Nature 262,661±664.
the egg of the ascidian Phallusia mammillata. Dev Biol 166,489±501. Katz B (1966) Nerve, Muscle, and Synapse. McGraw-Hill, New York.
GonzaÁlez-MartõÁnez MT and Darszon A (1987) A fast transient Kazazoglou T, Schackmann RW, Fossett M and Shapiro BM (1985) Calcium
hyperpolarization occurs during the sea urchin sperm acrosome reaction channel antagonists inhibit the acrosome reaction and bind to plasma
induced by egg jelly. FEBS Lett 218,247±250. membranes of sea urchin sperm. Proc Natl Acad Sci USA 82,1460±1464.
GonzaÁlez-MartõÁnez MT, Guerrero A, Morales E, De La Torre L and Darszon Kline D (1988) Ca2+-dependent events at fertilization in frog egg: injection of
A (1992) A depolarization can trigger Ca2+ uptake and the acrosome a Ca2+ buffer blocks ion channel opening, exocytosis and formation of
reaction when preceded by a hyperpolarization in L pictus sea urchin pronuclei. Dev Biol 126,346±361.
sperm. Dev Biol 150,193±202. Kline D and Kline JT (1992) Repetitive calcium transients and the role of
Gould MC, Stephano JL, Ortiz-Barron BJ and Perez-Quezada I (2001) calcium in exocytosis and cell cycle activation in the mouse egg. Dev
Maturation and fertilization in Lottia gigantea oocytes: intracellular pH, Biol 149,80±89.
Ca(2+), and electrophysiology. J Exp Zool 290,411±420. Kline D and Nuccitelli R (1985) The wave of activation current in the
Guerrero A and Darszon A (1989) Evidence for the activation of two different Xenopus egg. Dev Biol 111,471±487.
Ca2+ channels during the egg jelly-induced acrosome reaction of sea Koyota S, Wimalasiri KM and Hoshi M (1997) Structure of the main
63
E.Tosti and R.Boni
facilitates sperm entry, large fertilization cone formation, and prolonged initiation of sperm motility by hyperosmolality in marine teleosts. Cell
current responses in sea urchin oocytes. Dev Biol 124,177±190. Motil Cytoskel 25,171±178.
Meizel S (1997) Amino acid neurotransmitter receptor/chloride channels of Okamoto H, Takahashi K, Yamashita N (1977) Ionic currents through the
mammalian sperm and the acrosome reaction. Biol Reprod 56,569±574. membrane of the mammalian oocyte and their comparison with those in
Miller RL (1975) Chemotaxis of the spermatozoa of Ciona intestinalis. Nature the tunicate and sea urchin. J Physiol (Lond) 267,465±495.
(Lond) 254,244±245. Osman RA, Andria ML, Jones AD and Meizel S (1989) Steroid induced
Miyazaki S (1988) Fertilization potential and calcium transient in mammalian exocytosis: the human sperm acrosome reaction. Biochem Biophys Res
eggs. Dev Growth Differ 30,603±610. Commun 160,828±833.
Miyazaki S (1989) Signal transduction of sperm±egg interaction causing O'Toole CM, Arnoult C, Darszon A, Steinhardt RA and Florman HM (2000)
periodic calcium transient in hamster eggs. In Nuccitelli R, Cherr GN and Ca(2+) entry through store-operated channels in mouse sperm is initiated
Clark WH Jr (eds) Mechanism of Egg Activation. Plenum Press, New by egg ZP3 and drives the acrosome reaction. Mol Biol Cell 11,1571±
York, pp 231±246. 1584.
Miyazaki S and Igusa Y (1981a) Fertilization potential in golden hamster eggs Ouadid-Ahidouch H (1998) Voltage-gated calcium channels in Pleurodeles
consists of recurring hyperpolarization. Nature (Lond) 290,702±704. oocytes: classi®cation, modulation and functional roles. Zygote 6,85±95.
Miyazaki S and Igusa Y (1981b) Ca2+-dependent action potential and Ca2+- Ozawa S and Sand O (1986) Electrophysiology of excitable endocrine cells.
induced fertilization potential in golden hamster eggs. In Ohnishi ST and Physiol Rev 66,887±952.
Endo M (eds) The Mechanism of Gated Calcium Transport Across Patrat C, Serres C and Jouannet P (2000) Induction of a sodium ion in¯ux by
Biological Membranes, Accademic Press, New York, pp 305±311. progesterone in human spermatozoa. Biol Reprod 62,1380±1386.
Miyazaki S and Igusa Y (1982) Ca2+-mediated activation of a K+ current at Powers RD and Biggers JD (1976) Inhibition of mouse oocyte maturation by
fertilization of golden hamster eggs. Proc Natl Acad Sci USA 79,931± cell membrane potential hyperpolarization. J Cell Biol 70,352a (abstract).
935. Powers RD and Tupper JT (1977) Developmental changes in membrane
Miyazaki S and Igusa Y (1983) Effects of altered extracellular and transport and permeability in the early mouse embryo. Dev Biol 56,306±
intracellular calcium concentration on hyperpolarizing responses of the 315.
hamster egg. J Physiol 340,611±632. Publicover SJ and Barratt CL (1999) Voltage-operated Ca2+ channels and the
64
Ion channels in gametes
spermatozoa is mainly mediated by alpha 1H T-type calcium channels. oocytes involves L-type voltage gated calcium channels. J Cell Biochem
Mol Hum Reprod 6,893±897. 64,152±160.
Son WY, Han CT, Lee JH, Jung KY, Lee HM and Choo YK (2002) Tosti E (1994) Sperm activation in species with external fertilization. Zygote
Developmental expression patterns of alpha1H T-type Ca2+ channels 2,359±361.
during spermatogenesis and organogenesis in mice. Dev Growth Differ Tosti E, Boni R and Cuomo A (2000) Ca2+ current activity decreases during
44,181±190. meiotic progression in bovine oocytes. Am J Physiol, Cell Physiol
Steinhardt RA, Lundin L and Mazia D (1971) Bioelectric responses of the 279,C1795±C1800.
echinoderm egg to fertilization. Proc Natl Acad Sci USA 68,2426±2430. Tosti E, Boni R and Cuomo A (2002) Fertilization and activation currents in
Steinhardt RA, Zucker R and Schatten G (1977) Intracellular calcium release bovine oocytes. Reproduction 124,835±846.
at fertilization in the sea urchin egg. Dev Biol 58,185±196. Tosti E, Romano G, Buttino I, Cuomo A, Ianora A and Miralto A (2003)
Stricker SA (1999) Comparative biology of calcium signalling during Bioactive aldehydes from diatoms block the fertilization current in
fertilization and egg activation in animals. Dev Biol 211,157±176. ascidian oocytes. Mol Reprod Dev 66,72±80.
Suarez SS and Ho HC (2003) Hyperactivated motility in sperm. Reprod Dom Tyler A, Monroy A, Kao C and Grundfest H (1956) Membrane potential and
Anim 38,119±124. resistance of the star®sh egg before and after fertilisation. Biol Bull
Sutcliffe MJ, Smeeton AH, Wo ZG and Oswald RE (1998) Molecular 111,153±177.
modelling of ligand-gated ion channels. In Conn M (ed) Methods in VanBlerkom J, Davis P, Vicky Mathwig V and Alexander S (2002) Domains
Enzymology, 293, Ion Channels, part B. Academic Press, New York, pp of high-polarized and low-polarized mitochondria may occur in mouse
589±620. and human oocytes and early embryos. Hum Reprod 17,393±406.
Suzuki H, Jeong BS and Yang X (2000) Dynamic change of cumulus±oocyte Webb DJ and Nuccitelli R (1985a) A comparative study of the membrane
cell communication during in vitro maturation of porcine oocytes. Biol potential from before fertilization through early cleavage in two frogs,
Reprod 63,723±729. Rana pipiens and Xenopus laevis. Comp Biochem Physiol A 82,35±42.
Swann K (1990) A cytosolic sperm factor stimulates repetitive calcium Webb DJ and Nuccitelli R (1985b) Fertilization potential and electrical
increases and mimics fertilization in hamster eggs. Development properties of the Xenopus laevis egg. Dev Biol 107,395±406.
110,1295±1302. Weber WM (1999) Endogenous ion channels in oocytes of Xenopus laevis:
65