Molecular Human Reproduction

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Molecular Human Reproduction, Vol. 5, No. 3, 189-192, March 1999
© 1999 European Society of Human Reproduction and Embryology

Sperm-induced calcium oscillations

Isolation of the Ca²⁺ releasing component(s) of mammalian sperm extracts: the search continues

Rafael A. Fissore¹, Marcos M. Reis² and Gianpiero D. Palermo^2,3

¹ Department of Veterinary and Animal Sciences, University of Massachusetts, Amherst, USA, and ² The Center for Reproductive Medicine, The New York Hospital–Cornell Medical Center, 505 East 70th Street, HT-336, New York, NY 10021–4872, USA

	Introduction

Top Introduction Oscillin/glucosamine phosphate... Desirable functional features of... Possible mechanism(s) through... IP3 receptor system is... Conclusions References

 
During fertilization, mammalian oocytes of all the species studied to date exhibit a series of intracellular calcium ([Ca²⁺]_i) elevations which are responsible for triggering the activation of metaphase II (MII) oocytes (Miyazaki et al., 1993). In the oviduct, MII oocytes age rapidly and signs of spontaneous resumption of meiosis appear at ~4 h post-ovulation, as demonstrated by a 20–25% decrease in histone H1 and mitogen-activated protein kinases (Xu et al., 1997). Thus, the spermatozoa must rapidly meet, penetrate, and activate recently ovulated oocytes which cannot be easily activated by common parthenogenetic agents, e.g. ethanol or ionophores, and that induce a single Ca²⁺ response (Ozil, 1990; Vitullo and Ozil, 1992; Wu et al., 1998a). The spermatozoa, however, relying on the ability to generate oscillations, are able to initiate full activation in these oocytes. The molecular targets of these oscillations have not been wholly identified, but since low kinase levels are critical for the resumption/completion of meiosis and initiation of DNA synthesis, down-regulation and preservation of low histone H1 kinase, maturation promoting kinase (MPF) activity and mitogen-associated kinase activities (MAPK) are probably important (Collas et al., 1993).

Despite the significance of [Ca²⁺]_i oscillations in the initiation of mammalian development, the signalling mechanism(s) utilized by spermatozoa to initiate and perpetuate these responses, and the channels through which Ca²⁺ is released, have not been established. Two theories have been proposed: (i) the fusion theory (Dale et al., 1985) and (ii) the receptor theory (Kline et al., 1988). The reader is referred to recent reviews for supporting data for each theory (Miyazaki et al., 1993; Whitaker and Swann, 1993; Schultz and Kopf, 1995; Swann and Lai, 1997). The fusion theory, which suggests the presence of active Ca²⁺-releasing component(s) in the sperm cytosol, finds experimental support from the observation that injections of spermatozoa or sperm-derived cytosolic fractions elicit [Ca²⁺]_i oscillations similar to those observed during fertilization (Swann, 1990; Homa and Swann, 1994; Tesarik and Souza, 1994; Palermo et al., 1997; Wu et al., 1997). The fact that, during intracytoplasmic sperm injection (ICSI), the spermatozoon is injected directly into the cytoplasm of the oocyte, seems consistent with a cytosolic Ca²⁺-releasing compound coming from the spermatozoon. That spermatozoa can activate oocytes without interacting with the oolemma is further supported by the results of ICSI on mouse oocytes (Kimura and Yanagimachi, 1995; Nakano et al., 1997). Moreover, the egg activation observed with ICSI does not appear to be an artefact caused by the injection procedure itself (Tesarik et al., 1994; Dozortsev et al., 1995), since injection of dead spermatozoa does not activate eggs (Dozortsev et al., 1995). Moreover, the onset of Ca²⁺ oscillations is delayed after ICSI, suggesting that the same Ca²⁺ mobilizing factor demonstrated with sperm extract injection, may be involved (Tesarik et al., 1994). The improved rate of activation observed after slightly deforming the tail to immobilize the spermatozoa prior to injection was attributed to facilitation of the release of the `activating factor' (Palermo et al., 1996). This was confirmed by transmission electron microspcopy (TEM) observation of membrane damage in samples fixed immediately following the immobilization (G.D.Palermo, personal communication). Also, cytosolic extract of normal human spermatozoa can activate human oocytes that failed to fertilize after the injection of spermatozoa or immature germ cells (Palermo et al., 1997). Thus, evidence that a sperm `factor' stimulates Ca²⁺ release is substantial. Nevertheless, irrefutable evidence that a sperm protein elicits Ca²⁺ oscillations can only be obtained after injection of this putative protein(s) into mammalian eggs at concentrations similar to those found in a single spermatozoon.

In fact, a mammalian sperm factor has been shown to induce Ca²⁺ oscillations, once injected into hepatocytes (Berrie et al., 1996), and Ca²⁺-dependent electrical pulses developed after its injection into dorsal root ganglion neurons (Currie et al., 1992). The oscillations seen in hepatocytes are of large amplitude and low frequency, resembling the fertilization response in mammalian eggs. Moreover, some pharmacological compounds have been able to reproduce sperm-induced [Ca²⁺]_i oscillations. One, thimerosal, was indicated as a consistent initiator of Ca²⁺ oscillations in human oocytes (Tesarik et al., 1995). More recently Ca²⁺ oscillations, similar to those observed at fertilization and lasting at least 3 h, were produced in mouse oocytes by a single injection of adenophostin B isolated from fungal products, a novel non-metabolizable agonist of the inositol 1,4,5-trisphosphate receptor (IP₃ receptor) (Sato et al., 1998).

	Oscillin/glucosamine phosphate deaminase (gpd) is not the active Ca2+ release component(s) of mammalian sperm fractions

Top Introduction Oscillin/glucosamine phosphate... Desirable functional features of... Possible mechanism(s) through... IP3 receptor system is... Conclusions References

 
Oscillin/gpd was reported to be the sperm Ca²⁺-activating component, as its presence was correlated (using chromatographic procedures) with sperm fractions that exhibited maximal Ca²⁺ releasing activity (Parrington et al., 1996). Additionally, its localization to the equatorial segment of the sperm head, further supported its possible involvement in the early events of fertilization. The possibility that an enzyme involved in carbohydrate metabolism may be involved in Ca²⁺ release suggested a novel pathway. This could have spurred research into a new area of Ca²⁺ release regulation. However, this idea was quickly challenged, in that the recombinant form of the protein, or the native affinity-purified oscillin/gpd from hamster spermatozoa proved to lack Ca²⁺-releasing activity (Wolosker et al., 1998), as did the human homologue of glucosamine phosphate isomerase (GPI), exposed as a recombinant protein in prokaryotic cells (Wolny et al., 1999). In the latter study, two antibodies were raised against peptides of GPI, one from a highly conserved region (GM) and the other from the carboxy-terminal end (GK). However, following immunoblot analysis, only GK was used for further studies. To determine whether the GK polyclonal antibody had neutralizing properties, sperm cytosolic factor was incubated with GK, but this failed to block Ca²⁺ oscillations (Wolny et al., 1999).

This observation is important because, while Wolosker et al. (1998) demonstrated that oscillin/gpd does not trigger Ca²⁺ release, it might be a crucial component in a Ca²⁺-releasing complex. This question was recently answered by a combination of chromatographic procedures in which fractions enriched in oscillin/gpd lacked Ca²⁺ activity and, conversely, fractions with no oscillin/gpd had maximal Ca²⁺ activity (Wu et al., 1998b) conclusively demonstrating that oscillin/gpd is completely separated from Ca²⁺-active fractions. This conclusion is further supported by immunodepletion experiments in which the Ca²⁺-releasing activity of fractions depleted of oscillin/gpd was compared with fractions with a full complement of oscillin/gpd (Wolny et al., 1999). Truncated c-kit, which has been recently suggested as a possible candidate for the sperm Ca²⁺-activating molecule (Sette et al., 1997), was not detected by Western blotting in the Ca²⁺ active fractions of porcine sperm extracts (Wu et al., 1998b). Together, the data show that oscillin/gpd is not the mammalian sperm Ca²⁺ oscillogen, but strongly suggests the presence of a powerful Ca²⁺-release agonist in cytosolic fractions of mammalian spermatozoa. This finding supports the effort, as expressed by Tesarik (1998), to continue the search for the true sperm Ca²⁺ oscillogen.

	Desirable functional features of sperm Ca2+ oscillogen

Top Introduction Oscillin/glucosamine phosphate... Desirable functional features of... Possible mechanism(s) through... IP3 receptor system is... Conclusions References

 
While the nature of the sperm Ca²⁺-activating component(s) has not been elucidated, we can speculate about the features it should possess. Firstly, it must be able to induce signalling amplification upon interaction with potential target(s) in the MII oocyte cytosol. Therefore, although the concentration of this protein in the spermatozoa may be high, it is unlikely that this in itself could trigger a rapid and widespread Ca²⁺ release without amplification. There is considerable evidence that MII oocytes contain signalling pathways that can amplify Ca²⁺ responses, including those involving phospholipase C, ß and g, which are usually linked to G-protein and tyrosine kinase-mediated responses (for review, see Schultz and Kopf, 1995, and for additional information see Dupont et al., 1996; Williams et al., 1998). Moreover, the need for an amplification step was suggested by exposing sperm extracts to different fractions of sea urchin egg homogenates. The Ca²⁺ release induced by sperm extracts was substantially reduced in latency and greatly increased in magnitude when the sperm extracts interacted with unknown soluble components present in the sea urchin egg homogenate (Galione et al., 1997).

The second important characteristic of the sperm Ca²⁺-releasing compound(s) is that it must be able to stimulate Ca²⁺-induced further Ca²⁺ release (CICR). CICR can be repeatedly elicited in fertilized MII oocytes by injection of small amounts of CaCl₂ which trigger, in these oocytes, a large, enhanced and repetitive intracellular Ca²⁺ release (Igusa and Miyazaki, 1983; Fissore and Robl, 1994; Ozil and Swann, 1995). When this occurs, it is said that CICR is sensitized. Conversely, in unfertilized oocytes, CICR can be elicited by injecting increasing and larger amounts of CaCl₂, but no enhancement of Ca²⁺ release is observed after subsequent Ca²⁺ injections (Igusa and Miyazaki, 1983, Fissore and Robl, 1993). In fertilized oocytes, the ability to trigger CICR diminishes, and then disappears, in the advanced stages of pronucleus formation (Fissore et al., 1994), with [Ca²⁺]_i oscillations being absent during the pronuclear stage (Jones et al., 1995). Injections of sperm fractions have been shown to sensitize CICR in unfertilized mouse oocytes (Swann, 1994), further suggesting that the active component(s) present in sperm fractions use similar pathway(s) to those stimulated by the spermatozoa.

	Possible mechanism(s) through which the sperm factor may function

Top Introduction Oscillin/glucosamine phosphate... Desirable functional features of... Possible mechanism(s) through... IP3 receptor system is... Conclusions References

 
Natural entry of a spermatozoon and injection of sperm fractions may sensitize CICR by several mechanisms. Firstly, they may stimulate Ca²⁺ influx from the extracellular medium and this, in turn, may trigger additional Ca²⁺ release. Secondly, they may act directly on the Ca²⁺ release systems by either stimulating the production of a Ca²⁺-releasing agonist, i.e. IP₃ or cyclic ADP ribose, or by directly modifying the Ca²⁺ receptors/channels, i.e. IP₃ receptor or ryanodine receptor. Although the first possibility, Ca²⁺ influx, undoubtedly plays a role in the persistence of [Ca²⁺]_i oscillations, since [Ca²⁺]_i oscillations cease in Ca²⁺-free medium (Igusa and Miyazaki, 1983; Swann, 1994), is unlikely to be the sensitizing stimulus since in unfertilized oocytes CICR is not enhanced by repeated injections of CaCl₂ (Igusa and Miyazaki, 1983).

The second possibility, stimulation of the production of a specific Ca²⁺-releasing agonist, is supported by the finding that IP₃ injection/production elicits Ca²⁺ release in MII oocytes of all species tested to date (for review, see Miyazaki et al., 1993). Moreover, increased intracellular levels of IP₃ may facilitate CICR, a finding which has been demonstrated for the IP₃ receptor (Iino, 1990; Missiaen et al., 1997). Repeated CICR events, via the IP₃ receptor, may drive the generation of [Ca²⁺]_i oscillations during fertilization, as suggested by Miyazaki et al. (1992). Alternatively, CICR during fertilization may be mediated by a different agonist or channel, such as cyclic ADP ribose acting on the ryanodine receptor. However, such a mechanism has not yet been reported in mammalian fertilization. Finally, the sperm factor may sensitize CICR by acting directly on the Ca²⁺ channels through a mechanism similar to that operating in the case of thimerosal, an oxidizing agent known to trigger Ca²⁺ release (Swann, 1991). It is important to emphasize that, even if the sperm Ca²⁺ oscillogen acts in this manner, it would still need amplification, given the large number of Ca²⁺ channels required to be stimulated to produce a Ca²⁺ wave. In addition, thimerosal-induced [Ca²⁺]_i oscillations are blocked by the addition of dithiothreitol (DTT), a reducing agent (Swann, 1991); although fertilization and sperm factor-induced oscillations are not blocked by DTT (Cheek et al., 1993). Thus, if the active sperm factor acts directly on Ca²⁺ channels, this is likely to involve a mechanism(s) other than simple reduction/oxidization.

	IP3 receptor system is likely to be a Ca2+ release channel stimulated during the generation of oscillations by fertilization or injection of sperm fractions

Top Introduction Oscillin/glucosamine phosphate... Desirable functional features of... Possible mechanism(s) through... IP3 receptor system is... Conclusions References

 
The specific intracellular Ca²⁺ receptor(s) that mediates Ca²⁺ release during fertilization or injection of sperm fractions has not been fully elucidated. Moreover, functional and molecular evidence for the presence of IP₃ receptor and ryanodine receptor in mammalian MII oocytes abounds in the literature (Fissore et al., 1992; Miyazaki et al., 1992; Swann, 1992; Ayabe et al., 1995; Yue et al., 1995; Souza et al., 1996; He et al., 1997; Machaty et al., 1997). Two recent findings, however, suggest a predominant role for the IP₃ receptor system. Firstly, the IP₃ receptor type 1 isoform is abundant in mammalian MII oocytes; only 15 mouse oocytes and 10 bovine oocytes are required to detect its presence by conventional Western blotting (He et al., 1997; Fissore et al., 1999). Conversely, >1000 mouse or >400 bovine oocytes are required to detect the ryanodine receptor (Ayabe et al., 1995; He et al., 1997).

Secondly, the spatial distribution of IP₃ receptor type 1, from cortex to cortex and deep in the cytoplasm (Fissore et al., 1999), offers the only possible pathway by which the Ca²⁺ wave can propagate across the oocyte, given the poor diffusion rate of Ca²⁺ (Clapham, 1995). It is important to point out that fertilization-induced [Ca²⁺]_i oscillations in hamster MII oocytes are blocked by injection of an antibody against the type 1 IP₃ receptor (Miyazaki et al., 1992).

Similarly, sperm factor-induced oscillations are blocked by pre-injection of heparin, an IP₃ receptor competitive antagonist (Wu et al., 1997). The reported spatial distribution of the ryanodine receptor, that locates the receptor to an exclusively cortical distribution, considerably lessens its role in whole-cell Ca²⁺ release (Ayabe et al., 1995; Yue et al., 1998). Whether this spatial distribution is not completely accurate, due to unknown technical limitations, is not known and further experiments are required to clarify this issue. Together, these data suggest that the role of the ryanodine receptor during fertilization/sperm factor injections is likely to be complementary, one of additional amplification rather than of initiation and propagation. The fact that Xenopus oocytes, that do not contain ryanodine receptor (Parys et al., 1992), can initiate whole-egg [Ca²⁺]_i rises and mount oscillations (Lechleiter, 1992), supports the contention that the IP₃ receptor system is the main mediator of [Ca²⁺]_i oscillations in oocytes.

	Conclusions

Top Introduction Oscillin/glucosamine phosphate... Desirable functional features of... Possible mechanism(s) through... IP3 receptor system is... Conclusions References

 
The presence of a potent Ca²⁺-releasing agonist in mammalian sperm fractions has been reported by numerous laboratories. However, neither the nature nor the mode of action of this factor have been definitively identified, and this requires further research. Although recent data indicate that oscillin/gpd is not the long-awaited triggering molecule, other proteins have appeared as interesting candidates (Wu et al., 1998b). Identification of the trigger may offer insights into the regulation of Ca²⁺ release in oocytes and in other systems, and may also have immediate practical applications in assisted reproductive procedures and cloning techniques.

	Acknowledgments

 
We thank Professor J.Michael Bedford for his critical review of the manuscript, and Queenie Neri for editorial assistance.

	Notes

 
³ To whom correspondence should be addressed

	References

Top Introduction Oscillin/glucosamine phosphate... Desirable functional features of... Possible mechanism(s) through... IP3 receptor system is... Conclusions References

 
Ayabe, T., Kopf, G.S. and Schultz, R.M. (1995) Regulation of mouse egg activation: presence of ryanodine receptors and effect of microinjected ryanodine and cyclic ADP ribose on uninseminated and inseminated eggs. Development, 121, 2233–2244.[Abstract]

Berrie, C.P., Cuthbertson, K.S.R., Parrington, J. et al. (1996) A cytosolic sperm factor triggers calcium oscillations in rat hepatocytes. Biochem. J., 313, 369–372.

Cheek, T.R., McGuiness, O.M., Vincent, C. et al. (1993) Fertilization and thimerosal stimulate calcium spiking patterns in mouse oocytes by separate mechanisms. Development, 119, 179–189.[Abstract]

Clapham, D.E. (1995) Calcium signaling. Cell, 80, 259–268.[ISI][Medline]

Currie, K.P.M., Swann, K., Galione, A. and Scott, R.H. (1992) Activation of Ca -dependent currents in cultured dorsal root ganglion neurons by a sperm factor and cyclic-ADP ribose. Mol. Biol. Cell, 3, 1415–1425.[Abstract]

Collas, P., Sullivan, E.J. and Barnes, F.L. (1993) Histone H1 kinase activity in bovine oocytes following calcium stimulation. Mol. Reprod. Dev., 34, 224–231.[ISI][Medline]

Dale, B., DeFelice, L.J. and Ehrenstein, G. (1985) Injection of a soluble sperm extract into sea urchin eggs triggers the cortical reaction. Experientia, 41, 1068–1070.[ISI][Medline]

Dozortsev, D., Rybouchkin, A., De Sutter, P. et al. (1995) Human oocyte activation following intracytoplasmic injection: the role of the sperm cell. Hum. Reprod., 10, 403–407.[Abstract/Free Full Text]

Dupont, G., McGuinness, O.M., Johnson, M.H. et al. (1996) Phospholipase C in mouse oocytes: characterization of B and Y isoforms and their possible involvement in sperm-induced Ca²⁺ spiking. Biochem. J., 316, 583–591.

Fissore, R.A., Dobrinsky, J.R., Balise, J.J. et al (1992) Patterns of intracellular Ca²⁺ concentrations in fertilized bovine eggs. Biol. Reprod., 47, 960–969.[Abstract]

Fissore, R.A. and Robl, J.M. (1993) Sperm, inositol trisphosphate, and thimerosal-induced intracellular Ca²⁺ elevations in rabbit eggs. Dev. Biol., 159, 122–130.[ISI][Medline]

Fissore, R.A. and Robl, J.M. (1994) Mechanism of calcium oscillations in fertilized rabbit eggs. Dev. Biol., 166, 634–642.[ISI][Medline]

Fissore, R.A., Longo, F.J., Anderson, E. et al. (1999) Differential distribution of inositol triphosphate receptor isoforms in mouse oocytes. Biol. Reprod., 60, 49–57.[Abstract/Free Full Text]

Galione, A., Jones, K.T., Lai, A.F. and Swann, K. (1997) A cytosolic sperm protein factor mobilizes Ca²⁺ from intracellular stores by activating multiple Ca²⁺ release mechanisms independently of low molecular weight messengers. J. Biol. Chem., 272, 28901–28905.[Abstract/Free Full Text]

He, C.L., Damiani, P., Parys, J.B. and Fissore, R.A. (1997) Calcium, calcium release receptors, and meiotic resumption in bovine oocytes. Biol. Reprod., 57, 1245–1255.[Abstract]

Homa, S.T. and Swann, K. (1994) A cytosolic sperm factor triggers calcium oscillations and membrane hyperpolarizations in human oocytes. Hum. Reprod., 9, 2356–2361.[Abstract/Free Full Text]

Igusa, Y. and Miyazaki, S. (1983) Effects of altered extracellular and intracellular calcium concentration on hyperpolarizing responses of the hamster egg. J. Physiol., 340, 611–632.[Abstract/Free Full Text]

Iino, M. (1990) Biphasic Ca²⁺ dependence of inositol 1,4,5-trphosphate-induced Ca release in smooth muscle cells of the guinea pig Taenia. Caeci J. Gen. Physiol., 95, 1103–1122.

Jones, K.T., Carroll, J., Merriman, J.A. et al. (1995) Repetitive sperm-induced Ca²⁺ transients in mouse oocytes are cell cycle dependent. Development, 121, 3259–3266.[Abstract]

Kline, D., Simoncini, L., Mandel, G. et al. (1988) Fertilization events induced by neurotransmitters after injection of mRNA in Xenopus eggs. Science, 241, 464–467.[Abstract/Free Full Text]

Kimura, Y. and Yanagimachi, R. (1995) Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development, 121, 2397–2405.[Abstract]

Lechleiter, J.D. and Clapham, D.E. (1992) Molecular mechanisms of intracellular calcium excitability in X.laevis oocytes. Cell, 69, 283–294.[ISI][Medline]

Machaty, Z., Funahashi, H., Day, B.N. and Prather, R.S. (1997) Developmental changes in the intracellular Ca²⁺ release mechanisms in porcine oocytes. Biol. Reprod., 56, 921–930.[Abstract]

Missiaen, L., De Smedt, H., Parys, J.B. and Casteels, R. (1997) Effect of a cytosolic Ca²⁺ concentration ramp on the InsP₃-induced Ca²⁺ release in A7r5 smooth-muscle cells and in EBTr cells from tracheal mucosa. Biochem. Biophys. Res. Comm., 237, 354–358.[ISI][Medline]

Miyazaki, S., Yuzaki, Nakada, K. et al. (1992) Block of the Ca²⁺ wave and Ca²⁺ oscillation by antibody to the inositol 1,4,5-triphosphate receptor in fertilized hamster eggs. Science, 257, 251–255.[Abstract/Free Full Text]

Miyazaki, S., Shirakawa, H., Nakada, K. and Honda, Y. (1993) Essential role of the inositol 1,4,5 trisphosphate receptor/ Ca²⁺ release channel in Ca²⁺ waves and Ca²⁺ oscillations at fertilization of mammalian oocytes. Dev. Biol., 158, 62–78.[ISI][Medline]

Nakano, Y., Shirakawa, H., Mitsuhashi, N. et al. (1997) Spatiotemporal dynamics of intracellular calcium in the mouse egg injected with a spermatozoon. Mol. Hum. Reprod., 3, 1087–1093.[Abstract/Free Full Text]

Ozil, J.P. (1990) The parthenogenetic development of rabbit oocytes after repetitive pulsatile electrical stimulation. Development, 109, 117–127.[Abstract]

Ozil, J.P. and Swann, K. (1995) Stimulation of repetitive calcium transients in mouse eggs. J. Physiol., 483, 331–346.[ISI][Medline]

Palermo, G.D., Schlegel, P.N., Colombero, L.T. et al. (1996) Aggressive sperm immobilization prior to intracytoplasmic sperm injection with immature spermatozoa improves fertilization and pregnancy rates. Hum. Reprod., 11, 1023–1029.[Abstract/Free Full Text]

Palermo, G.D., Avrech, O.M., Colombero, L.T. et al. (1997) Human sperm cytosolic factor triggers Ca²⁺ oscillations and overcomes activation failure of mammalian oocytes. Mol. Hum. Reprod., 3, 367–374.[Abstract/Free Full Text]

Parrington, J., Swann, K., Shevchenko, V.I. et al. (1996) Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature, 379, 364–368.[Medline]

Parys, J.B., Sernett, S.W., DeLisle, S. et al. (1992) Isolation, characterization, and localization of the inositol l,4,5-triphosphate receptor protein in Xenopus laevis oocytes. J. Biol. Chem., 268, 25206–25212.[Abstract/Free Full Text]

Sato, Y., Miyazaki, S., Shikano, T. et al. (1998) Adenophostin, a potent agonist of the inositol 1,4,5-trisphosphate receptor, is useful for fertilization of mouse oocytes injected with round spermatids leading to normal offspring. Biol. Reprod., 58, 867–873.[Abstract/Free Full Text]

Schultz, R.M. and Kopf, G.S. (1995) Molecular basis of mammalian egg activation. Curr. Topics Dev. Biol., 30, 21–62.[ISI][Medline]

Sette, C., Bevilacqua, A., Bianchini, A. and Manglia (1997) Parthenogenetic activation of mouse eggs by microinjection of truncated c-kit tyrosine kinase present in spermatozoa. Development, 124, 2267–2274.[Abstract]

Souza, M., Barros, A. and Tesarik, J. (1996) The role of ryanodine-sensitive Ca²⁺ stores in the Ca²⁺ oscillation machine of human oocytes. Mol. Hum. Reprod., 2, 265–272.[Abstract/Free Full Text]

Swann, K. (1990) A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development, 110, 1295–1302.[Abstract/Free Full Text]

Swann, K. (1991) Thimerosal causes calcium oscillations and sensitizes calcium-induced calcium release in unfertilized hamster eggs. FEBS Letts., 278, 175–178.[ISI][Medline]

Swann, K. (1992) Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem J., 287, 79–84.

Swann, K. (1994) Ca²⁺ oscillations and sensitization of Ca²⁺ release in unfertilized mouse eggs injected with a sperm factor. Cell Calcium, 15, 331–339.[ISI][Medline]

Swann, K. and Lai, F.A. (1997) A novel signaling mechanisms for generating calcium oscillations at fertilization in mammals. Bio Essays, 19, 371–378.[ISI][Medline]

Tesarik, J. (1998) Sperm-induced calcium oscillations. Oscillin – reopening the hunting season. Mol. Hum. Reprod., 4, 1007–1012.[Free Full Text]

Tesarik, J. and Sousa, M. (1994) Comparison of Ca²⁺ responses in human oocytes fertilized by subzonal insemination and by intracytoplasmic sperm injection. Fertil. Steril., 62, 1197–1204.[ISI][Medline]

Tesarik, J., Sousa, M. and Testart, J. (1994) Human oocyte activation after intracytoplasmic sperm injection. Hum. Reprod., 9, 511–518.[Abstract/Free Full Text]

Tesarik, J., Sousa, M. and Mendoza, C. (1995) Sperm induced calcium oscillations of human oocytes show distinct features in oocyte center and periphery. Mol. Reprod. Dev., 41, 257–263.[ISI][Medline]

Vitullo, A.D. and Ozil, J.P. (1992) Repetitive calcium stimuli drive meiotic resumption and pronuclear development during mouse oocyte activation. Dev. Biol., 151, 128–136.[ISI][Medline]

Williams, C.J., Mehlmann, L.M., Jaffe, L.A. et al. (1998) Evidence that G_q family proteins do not function in mouse egg activation at fertilization. Dev. Biol., 198, 116–127.[ISI][Medline]

Whitaker, M.J. and Swann, K. (1993) Lighting the fuse at fertilization. Development, 117, 1–12.[Abstract]

Wolosker, H., Kline, D., Bian, Y. et al. (1998) Molecularly cloned mammalian glucosamine-6-phosphate deaminase localizes to transporting epithelium and lacks oscillin activity. FASEB J., 12, 91–99.[Abstract/Free Full Text]

Wolny, Y.M., Fissore, R.A., Wu, H. et al. (1999) Human glucosamine-6-phosphate isomerase (GPI), a homologue of hamster oscillin, does not appear to be involved in Ca²⁺ release in mammalian oocytes. Mol. Reprod. Dev., 52, 277–287.[ISI][Medline]

Wu, H., He, C.L. and Fissore, R.A. (1997) Injection of a porcine sperm factor triggers calcium oscillations in mouse oocytes and bovine eggs. Mol. Reprod. Dev., 46, 176–189.[ISI][Medline]

Wu, H., He, C.L. and Fissore, R.A. (1998a) Injection of a sperm fraction induces activation of mouse eggs. Mol. Reprod. Dev., 49, 37–47.[ISI][Medline]

Wu, H., He, C.L., Jehn, B. et al. (1998b) Partial characterization of the Calcium-releasing activity of porcine sperm cytosolic extracts. Dev. Biol., 203, 369–381.[ISI][Medline]

Yue, C., White, K.L., Reed, W.A. and Bunch, T.D. (1995) The existence of 1,4,5-triphosphate and 333 ryanodine receptors in mature bovine eggs. Development, 121, 2645–2654.[Abstract]

Yue, C., White, K.L., Reed, W.A. and King, E. (1998) Localization and regulation of ryanodine receptor in bovine oocytes. Biol. Reprod., 58, 608–614.[Abstract/Free Full Text]

Xu, Z., Abbott, A., Kopf, G.S. et al. (1997) Spontaneous activation of ovulated mouse eggs: time dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger RNA recruitment and inositol 1,4,5-trisphosphate sensitivity. Biol. Reprod., 57, 743–750.[Abstract]

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