Molecular Human Reproduction, Vol. 5, No. 6, 527-533,
June 1999
© 1999 European Society of Human Reproduction and Embryology
Male accessory sex gland secretions affect oocyte Ca2+ oscillations during in-vitro fertilization in golden hamsters
1 Department of Anatomy, Faculty of Medicine, The University of Hong Kong, 5 Sassoon Road, Hong Kong and 2 Department of Anatomy, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China
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Abstract |
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To evaluate the effect of male accessory sex gland secretions on Ca2+ oscillations of oocytes, epididymal or ejaculated spermatozoa recovered from uteri were used to inseminate oocytes. Ca2+ oscillations were measured by Fura 2 fluorescence imaging (F340/F380). We showed that although Ca2+ oscillations induced by ejaculated spermatozoa had a pattern similar to those induced by epididymal spermatozoa, the amplitude of the first Ca2+ transient in the former group was significantly higher (P < 0.05) and the duration was significantly longer (P < 0.01). Oocytes inseminated with ejaculated spermatozoa recovered from uteri from males had ampullary glands or ventral prostates removed showed significantly lower Ca2+ oscillations compared to the controls (P < 0.05, P < 0.01 respectively). Moreover, the relative area of the first Ca2+ transient in treatment groups was significantly smaller than the control. In addition, a significantly higher percentage of oocytes (52%) inseminated by spermatozoa from males with all accessory sex glands removed showed non-oscillatory Ca2+ transients, compared to the controls (5%, P < 0.05). These results indicate that accessory sex gland secretions can affect Ca2+ oscillations. The differences between Ca2+ oscillations induced by epididymal and uterine spermatozoa from males with all accessory sex glands removed suggest that uterine factors may also influence this process.
Ca2+ oscillations/golden hamster/in-vitro fertilization/male accessory sex glands/oocyte
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Introduction |
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Male accessory sex gland secretions make up most of the volume and chemical components such as zinc, fructose and acid phosphatase and some proteins, of seminal plasma. Although several of these chemical components can be used to indicate the function of the male accessory sex glands, very little is known about the role of these components in promoting the fertilizing capacity of spermatozoa (Setchell et al., 1994
). In mammals, a spermatozoon acquires fertilizing ability in the epididymis, but the degree to which male accessory sex gland secretions affect male fertility is controversial (Henault et al., 1995). In vivo it is very difficult to show whether male accessory sex gland secretions affect fertility in humans. In the rodent model, removal of some or all of the male accessory sex glands reduces fertility in the mouse (Pang et al., 1979; Peitz et al., 1986), rat (Queen et al., 1981) and hamster (Chow et al., 1986), even though fertilization rate is not affected (Chow et al., 1994; Ying et al., 1998).
In-vitro studies show that the fertilization rate of epididymal spermatozoa from rats (Shalgi et al., 1981), cats (Niwa et al., 1985) and pigs (Nagai et al., 1984) is higher than that of ejaculated spermatozoa. Antifertility factors from seminal plasma have been described for several species including human (Baas et al., 1983; Iwamonto and Gagnon, 1988; Iwamonto et al., 1992). These factors are believed to inhibit sperm motility, capacitation and acrosome reaction, and eventually to interfere with fertilization (Van Der Ven et al., 1982; Audhya et al., 1987; Robert and Gagnon, 1996). On the other hand, there are also reports which show that some proteins which bind with sperm plasma membrane during ejaculation are beneficial to fertility (Miller et al., 1990; Killian et al., 1993). Recent studies show that prostate secretions in some species including rabbit, rat and human contain a fertilization-promoting peptide (FPP) (Cockle et al., 1989; Green et al., 1996). FPP can significantly promote the capacitation of epididymal mouse spermatozoa and human ejaculated spermatozoa and increase the percentage of fertilized oocytes in vitro but not acrosome reaction. Thus it is believed that FPP could stimulate male fertility (Green et al., 1994, 1996).
In many studies, effects of male accessory sex gland secretions on male fertility are mainly focused on the function of spermatozoa, or the ability of spermatozoa to fertilize oocytes and the ability of the zygotes to continue to develop into offspring in vivo or blastocysts in vitro. Relatively little is known about the effect of ASG secretions on the subtle events during oocyte activation. Sometimes spermatozoa may penetrate oocytes and form normal-appearing zygotes but fail to initiate subsequent embryonic development properly (Chow et al., 1994; Ying et al., 1998). This has been illustrated by in-vitro and in-vivo studies in which male accessory sex glands have been shown to affect DNA replication of zygotes in the first cell cycle (Eid et al., 1994; Ying et al., 1998).
It is well known that gamete fusion initiates a cascade of events in the oocyte, termed oocyte activation, which blocks polyspermic fertilization and launches the fertilized oocyte onto a path leading to DNA synthesis and further embryonic development (Whitaker and Patel, 1990; Kline and Kline, 1992). It is also generally accepted that the fusion of the oocyte with the fertilizing spermatozoa is the physiological trigger of oocyte activation. However, the mechanism by which spermatozoa activate the oocyte is still a matter of controversy. Ca2+ is the major intracellular signalling molecule in somatic cells. Intracellular Ca2+ oscillations play a central role in oocyte activation (Fissore et al., 1992; Xu et al., 1994). Some studies have indicated that a non-oscillatory Ca2+ increase, such as during parthenogenetic activation, often leads to an early embryonic developmental arrest (Sun et al., 1992), whereas repetitive Ca2+ oscillations result in a viable embryo (Kline and Kline, 1992).
Using the golden hamster as a model, we have demonstrated that the ampullary gland and ventral prostate may play an important role in the regulation of male fertility (O et al., 1988; Chow et al., 1994). Male hamsters with either ampullary glands or ventral prostates removed had reduced fertility, which was found to be related to retarded embryonic development and lower implantation rate (O et al., 1988; Chow et al., 1994). Recently we reported that the removal of male ampullary glands or ventral prostates delayed zygotic DNA replication in the first cell cycle during in-vivo fertilization (IVF) (Ying et al., 1998). We postulate that the modification of the sperm plasma membrane by male accessory sex gland secretions might affect the initiation of embryonic development by interfering with signal transduction at the time of oocyte activation. The objective of this paper is to study the patterns of intracellular Ca2+ oscillations in oocytes activated by spermatozoa ejaculated from males whose accessory sex glands had been totally or partially removed.
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Materials and methods |
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Animals
Randomly bred golden hamsters (Mesocricetus auratus) were fed with standard food and tapwater ad libitum, and maintained in the Laboratory Animal Unit, Faculty of Medicine, The University of Hong Kong, under a 14 h light/10 h dark regime (light 11:00–01:00). Female hamsters, aged 10 weeks, were checked daily for vaginal secretion for at least two consecutive normal oestrous cycles before mating.
Reagents
Unless otherwise stated, all inorganic and organic chemicals were purchased from Sigma Chemical Company (St Louis, MO, USA).
Media
Tyrode's albumin–lactate pyruvate medium (TALP) was used for collection and manipulation of oocytes and for IVF. The composition of TALP medium was: 114.0 mM NaCl, 3.2 mM KCl, 2.0 mM CaCl2, 0.5 mM MgCl2, 25.0 mM NaHCO3, 0.4 mM NaH2PO4, 5.0 mM glucose, 10.0 mM sodium lactate, 0.1 mM sodium pyruvate, 0.35 mg/ml gentamicin sulphate and 3 mg/ml bovine serum albumin BSA. For capacitation of hamster spermatozoa, modified TALP (m-TALP: TALP supplemented with 0.5 mM taurine, 0.05 mM adrenaline and 15 mg/ml BSA) was used.
Surgery
Male accessory sex glands were removed from 7–8 week old male hamsters following established methods (Chow et al., 1986) to give the following four groups: SH, sham-operated controls; AGX, bilateral excision of the ampullary glands; VPX, bilateral excision of the ventral prostates; TX, bilateral excision of the ampullary glands, ventral prostates, dorsolateral prostates, coagulating glands and seminal vesicles. The operated males were used for mating 4 weeks after surgery and the success of the operation was checked at the end of the experiments. Each female hamster was mated with one surgically treated male on the day of oestrus for 15 min. Seven or eight operated males were used for each experimental group.
Collection of oocytes
Naturally ovulating female hamsters were killed by chloroform inhalation on the day of oestrus. About 10–12 oocytes were flushed from oviducts of one female with 0.05 mg/ml hyaluronidase in BSA-free TALP pre-equilibrated with 5% CO2 at 37°C and then treated with 0.05 mg/ml trypsin in BSA-free TALP to remove zona pellucida. The zona-free oocytes were loaded with 3.3 µM Fura 2-AM (diluted from a 330 µM Fura 2 stock solution in dimethylsulphoxide) in TALP which contained the detergent pluronic F-127 (0.04%) for 30 min before insemination. These Fura 2-loaded oocytes were immediately used for the detection of Ca2+ oscillations.
For IVF, adult female golden hamsters were superovulated with 40 IU pregnant mare's serum gonadotrophin on the day of oestrus followed by 30 IU human chorionic gonadotrophin (HCG) 55 h later. Oocytes were collected 16 h after HCG.
Preparation of spermatozoa
Collection of epididymal spermatozoa
The epididymis was removed from 10–14 week old male hamsters and cleared of blood and connective tissues. A small cut was made on the tubules of the cauda epididymis to release spermatozoa. About 20–30 µl of this dense sperm mass was transferred to the bottom of a test tube (12 mmx55 mm) and 2 ml of m-TALP medium was gently added. The test tube was allowed to stand for 5 min at 37°C. The upper 1 ml of sperm suspension was transferred to a culture dish (10 mmx35 mm) and the concentration of spermatozoa was adjusted to 3x105/ml. Spermatozoa were incubated under mineral oil in 5% CO2 and 95% O2 at 37°C for 4–5 h for capacitation.
Collection of ejaculated spermatozoa from uteri
About 20–30 µl of sperm mass was collected from uterine horns of 8–12 week old female hamsters 30 min after mating with operated males. Spermatozoa were processed and incubated for capacitation as in previous section.
In-vitro fertilization
Cumulus–oocyte complexes were collected from oviducts of superovulated females and transferred to 1 ml of TALP medium. Oocytes were coincubated with capacitated spermatozoa (3.0x105 spermatozoa/ml) under mineral oil for 4–5 h. They were then transferred to new medium and cultured for another 15 h. The oocytes were examined for fertilization with a phase contrast microscope. An oocyte was recorded as being fertilized when both male and female pronuclei had formed.
Insemination and measurement of Ca2+ oscillations
Ca2+ oscillations of oocytes were measured according to previously reported methods (Ben-Yosef et al., 1993; Maleszewski et al., 1995) with modifications. Briefly the Fura 2-loaded oocytes were transferred to 100 µl of BSA-free TALP buffered with HEPES covered with mineral oil on a glass coverslip (~20 mm diameter) which had been pretreated with polylysine (0.5 mg/ml) to make oocytes adherent. The glass coverslip was fitted into a stainless steel-welled chamber, mounted on a Zeiss inverted epifluorescence microscope and heated to 37°C by a thermostatically controlled hot plate. To prevent polyspermic penetration, only a small amount of sperm suspension (2–3 µl) was introduced to the surface of the oocyte.
A Metafluor Imaging System (Universal Corporation, USA) was used for fluorescence recordings. Fluorescence signal was displayed as the ratio of fluorescence intensity for 340:380 nm excitation wavelengths after background subtraction. Emitted fluorescence was recorded at each excitation wavelength and the ratio calculated once every 2 s. Three or four oocytes were monitored simultaneously in each experiment and each oocyte was examined individually for the Ca2+ oscillations. Once Ca2+ transient was detected the oocyte was monitored continuously. To avoid the variations of Ca2+ oscillations amongst the experimental groups from day to day, Ca2+ oscillations of oocytes were measured from each group on alternate days. After this, the oocytes were labelled with 10 µg/ml Hoechst 33342 to confirm sperm fusion.
Statistical analyses
The following sets of data were collected from each treatment group and analysed: the percentage of IVF; the percentage of eggs showing Ca2+ oscillations; the number of sperm fused in each oocyte; the first peak ratio amplitude in Ca2+ transients; the first peak duration in Ca2+ transients; the first peak area of Ca2+ transients and duration of peak intervals between Ca2+ transients. ANOVA or 
2-test was used for statistical analysis, P < 0.05 was considered as significant.
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Results |
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In-vitro fertilization and polyspermy
In order to find out if the secretions of male accessory sex glands affected IVF, cumulus-intact superovulated eggs were inseminated with ejaculated spermatozoa collected from female uteri 30 min after mating with various operated males. About 60% of eggs were found fertilized (Table I
). No significant difference was found between SH control and other treatment groups in terms of fertilization rate.
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Polyspermic fertilization, which will affect Ca2+ oscillations of oocytes, is a common phenomenon in zona-free hamster oocytes. To prevent polyspermic fertilization, a very small amount of sperm suspension was introduced to inseminate oocytes. No significant difference was found in terms of the mean number of sperm fusions in each oocyte amongst the experimental groups (Table II
).
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Ca2+ oscillations induced by epididymal or ejaculated spermatozoa
The addition of spermatozoa to zona-free naturally ovulated oocytes resulted in a microscopically visible sperm attachment. Immediately following sperm attachment, oocytes were continuously monitored. Ca2+ oscillations of oocytes induced by epididymal spermatozoa in golden hamster have been described elsewhere (Swann, 1990
; Miyazaki et al., 1992; Maleszewski et al., 1997). In the present study, epididymal spermatozoa induced Ca2+ oscillations in 65.4% (17 of 26) of the oocytes (Table II
). The first Ca2+ transient varied from almost immediately (8 s) to as long as 10 min following the addition of spermatozoa. The first Ca2+ transient varied in both intensity and duration (0.95 ± 0.41 and 40.9 ± 10.0 s, respectively, n = 17, Table II). This elevation was followed by subsequent regular Ca2+ transients at intervals of 1–3 min. Characteristically, the first Ca2+ transient in each oocyte was of larger amplitude than later ones (Figure 1A). Ca2+ oscillations usually subsided in 30–50 min, during which the baseline gradually drifted upward due to Fura 2 dye bleaching.
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Spermatozoa (recovered from uteri) from sham-operated males induced Ca2+ oscillations in 86.4% (19 of 22) of the oocytes (Table II
). This was slightly higher, but not statistically significant compared with that induced by epididymal spermatozoa. Ca2+ oscillations induced by uterine spermatozoa (Figure 1B) had a pattern similar to those induced by epididymal spermatozoa (Figure 1A). However, the amplitude of the first Ca2+ transient was significantly higher (P < 0.05), while the duration was longer (P < 0.01) compared with those induced by epididymal spermatozoa (Table II).
Effects of male accessory sex gland secretions on Ca2+ oscillations
Table II summarizes changes of Ca2+ oscillations of oocytes induced by uterine spermatozoa from males in the different treatment groups. In the four different experiments, a total of 99 oocytes were examined. About 83% of them showed Ca2+ oscillations after insemination. No significant differences were observed in the percentage of oocytes exhibiting Ca2+ oscillations among these groups. However, when the first Ca2+ transient was analysed, differences between SH and the treatment groups were noted. The first peak ratio amplitude in AGX and VPX groups was significantly lower than that of SH (Table II, P < 0.05 and P < 0.01). The relative area of the first peak in AGX, VPX and TX were all significantly smaller than that of SH (Figure 2). Although variability in both amplitude and duration of the oscillations were observed in oocytes inseminated with uterine spermatozoa from AGX and VPX males, the basic pattern of Ca2+ oscillations was similar in most of the oocytes. An exception to this was the TX group, in which 52% of oocytes (13 of 25) showed only one or two and very small Ca2+ transients (Figure 3A), and was significantly higher than that in the SH group (5% or one of 19, P < 0.05, Figure 3B).
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Discussion |
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In the present study, we focused on Ca2+ oscillation changes in oocytes inseminated by epididymal and uterine spermatozoa from males with some or all of the accessory sex glands removed. Our results show that male accessory sex gland secretions affect Ca2+ oscillations, shown by the amplitude and duration of the first Ca2+ transient, even though the rate of IVF was not affected (Table I
). Furthermore, to the best of our knowledge, this is the first demonstration that Ca2+ oscillations in hamster oocytes inseminated by epididymal and ejaculated spermatozoa recovered from the uterus are different.
In hamsters, the first Ca2+ transient of oocyte after insemination was always higher in amplitude and longer in duration than subsequent ones (Swann, 1990; Miyazaki et al., 1992; Maleszewski et al., 1997). Despite the fact that the pattern of Ca2+ oscillations and frequency was similar in oocytes inseminated with epididymal or uterine spermatozoa (Figure 1A,B), the duration of the first transient in the former group (Table II) was much shorter than those induced by uterine spermatozoa, which suggests that male accessory sex gland secretions have an effect on Ca2+ oscillations. This conclusion is further substantiated by the differences observed between the sham control and treatment groups (Table II). In hamster oocytes a single spermatozoon induces Ca2+ oscillations over a period of 1 h (Miyazaki et al., 1992). In our model, Ca2+ oscillations in most of the oocytes stopped after 30–50 min. This relatively short duration may be due to the bleaching of Fura 2 and/or the absence of protein in the medium.
Epididymal secretory products are known to be essential for mammalian sperm maturation, and evidence indicates that specific proteins become associated with spermatozoa during epididymal transit (Cornwall et al., 1990; Boue et al., 1995, 1996). After epididymal transit, spermatozoa undergo other surface transformations when they encounter male accessory sex gland secretions during ejaculation. Modifications of sperm plasma membrane during ejaculation have been poorly defined, and their physiological significance varies from one species to another (Henault et al., 1995). Recent studies suggest that the lower fertilization and pregnancy rates for ICSI with epididymal and/or testicular spermatozoa may be related to a physiological difference in sperm membrane characteristics (Eddy and O'Brien, 1994; Palermo et al., 1996). It may be inferred that mature spermatozoa require some modification so as to promote membrane permeabilization and permit cytosolic sperm factors to find access to the oocyte and produce its activation (Dozortsev et al., 1995; Palermo et al., 1996). In the golden hamster, it has been shown that secretions from ventral prostates and ampullary glands modify sperm plasma membrane proteins, especially glycoproteins (Cheng et al., 1995; Chow et al., 1995). These modifications may later affect Ca2+ oscillations during or after fusion of the sperm and oocyte plasma membrane. The mechanism of oocyte Ca2+ oscillations at fertilization is not fully understood. There are two main hypotheses which explain how the spermatozoon induces Ca2+ oscillations in the oocyte. One is that spermatozoa act via the oocyte plasma membrane receptor to produce inositol 1,4,5-trisphosphate (IP3), which releases Ca2+ from the endoplasmic reticulum and leads to Ca2+ oscillations (Shilling et al., 1994; Swann et al., 1998), although such sperm receptors have not yet been fully identified (Tesarik et al., 1994). The other hypothesis is that Ca2+ oscillations are induced by a sperm-derived factor that diffuses into oocytes after the sperm–oocyte membrane fusion (Parrington et al., 1996; Swann et al., 1998). The recent trigger/oscillator hypothesis unifies the oocyte plasma membrane receptor and the sperm factor hypotheses (Tesarik, 1998a). According to this hypothesis, the first Ca2+ transient in the oocyte is induced by the action of the fertilizing spermatozoa at the oocyte plasma membrane just before or during their fusion, whereas the subsequent Ca2+ oscillations are facilitated by a change in the respective sensibilities of the IP3 and ryanodine recepors, which result from both the first Ca2+ transient and the subsequent action of a soluble spermatozoa cytosolic factor released into the oocyte (Tesarik, 1998b). Based on our present results, we speculate that male accessory sex gland secretions may first affect spermatozoa trigger activity by the modification of sperm plasma membrane and then further influencing subsequent Ca2+ oscillations.
In this study, we also found that Ca2+ oscillations in oocytes induced by epididymal spermatozoa and TX ejaculated spermatozoa was quite different, suggesting that uterine factors also affect this process. Physiological modifications of spermatozoa within the female reproductive tract have been extensively studied (Yanagimachi, 1994). These mainly focused on the effects of oviductal secretions on sperm capacitation, motility and acrosome reaction (Bastias et al., 1993; Zhu et al., 1994; Abe et al., 1995). Little is known about uterine factors on sperm function. During normal fertilization, components from male accessory sex gland secretions such as glycoproteins and fibronectin-like proteins are coated on to the spermatozoa (Koehler et al., 1980; Oliphant et al., 1985). These coated components may prevent spermatozoa from being exposed to uterine secretions. Removal of male accessory sex glands allows uterine factors to act upon spermatozoa. This may partly account for the difference in Ca2+ oscillations of oocytes induced by epididymal spermatozoa and TX ejaculated spermatozoa.
It is well established that Ca2+ oscillations play a central role in the oocyte activation (Kline and Kline, 1994; Bos-Mikich et al., 1995; Maleszewski et al., 1997). In our present study, two different patterns of Ca2+ oscillations induced by uterine sperms are noted, one is oscillatory (Figure 1B) and the other non-oscillatory (Figure 3A). Removal of either ampullary glands or ventral prostates increased the percentage of oocytes with the non-oscillatory pattern, albeit not statistically significantly different compared with the sham control group. After removal of all male accessory sex glands, 52% of oocytes showed the non-oscillatory pattern (Figure 3A). Non-oscillatory Ca2+ increases have been associated with parthenogenetic activation followed by early developmental arrest, whereas oscillatory Ca2+ increases, as in normal fertilization, lead to a viable embryo (Sun et al., 1992; Kline and Kline, 1992). Agents that induce oscillatory Ca2+ increases similar to that triggered by the fertilizing spermatozoa prolong greatly the development of the activated oocytes (Ozil, 1990). It may be reasonable to assume that even though those oocytes showing non-oscillatory Ca2+ increases can form normal-looking pronuclei, development may be arrested at the time of the maternal–embryonic transition which is a particularly vulnerable period in preimplantation development. In human embryos, it takes place between the 4-cell and 8-cell stage (Braude et al., 1988; Tesarik et al., 1994). This may also be true in the hamster, because we previously found that removal of some or all male accessory sex glands increased the percentage of abnormally developed embryos, which could be detected ultrastructurally at the 4-cell stage (Chow et al., 1994). At the 8-cell stage, the cell number of viable embryos was considerably decreased (O et al., 1988).
The significance of amplitude and duration of Ca2+ transients in the oocyte activation and subsequent embryonic development has not been established. In our present study, we found that some oocytes inseminated by epididymal spermatozoa or uterine spermatozoa from AGX and VPX males showed smaller Ca2+ oscillation amplitude (Table II). Previously we observed that removal of ventral prostates resulted in delayed DNA synthesis in 30–40% of hamster zygotes (Ying et al., 1998); this figure cannot be accounted for entirely by oocytes showing non-oscillatory Ca2+ increases (Figure 3B). We suggest that these attenuated Ca2+ transients may also affect oocyte activation. Sire effects on the Ca2+ transients of oocyte may also explain our other observations of paternal effects on the delayed resumption of meiosis and inactivation of MPF in hamster oocytes during in-vivo fertilization (Ying et al., 1999).
In conclusion, the present findings demonstrate that Ca2+ oscillations of oocytes inseminated by epididymal and uterine spermatozoa are different. Male accessory sex gland secretions affect the amplitude and relative area of the first Ca2+ transient during fertilization. Differences of Ca2+ oscillations induced by epididymal spermatozoa and uterine spermatozoa from males with all accessory sex glands removed suggest that uterine factors may also influence this process. Furthermore, we have demonstrated that ASG has no effect on percentage of zygotes showing two pronuclei (Chow et al., 1994; Ying et al., 1998; Table I), but the fact that Ca2+ oscillations in oocyte activation is abnormal may mean that fertility is compromised.
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Acknowledgments |
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This research was supported by Research Grant Council, Hong Kong 338/031/016 and Committee on Research and Conference Grant, The University of Hong Kong 337/031/0033. We would like to thank the Department of Obstetrics and Gynecology, Faculty of Medicine, The University of Hong Kong, for the kind permission for the use of the Metafluor Imaging System, and Dr W.S.B.Yeung and Mr T.M.Cheung for their advice and technical assistance.
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3 To whom correspondence should be addressed
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References |
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Abe, H., Sendai, Y., Satoh, T. et al. (1995) Secretory products of bovine oviductal epithelial cells support the viability and mobility of bovine spermatozoa in culture in vitro. J. Exp. Zool., 272, 54–61.
Audhya, T., Reddy, J. and Zaneveld, L.J.D. (1987) Purification and partial chemical characterization of a glycoprotein with antifertility activity from human seminal plasma. Biol. Reprod., 36, 511–521.
Baas, J.W., Molan, P.C. and Shannon, P. (1983) Factors in seminal plasma of bulls that affect the viability and motility of spermatozoa. J. Reprod. Fertil., 68, 275–280.
Bastias, M.C., Kamijo, H. and Osteen, K.G. (1993) Assessment of human sperm functional changes after in-vitro coincubation with cells retrieved from the human female reproductive tract. Hum. Reprod., 8, 1670–1677.
Ben-Yosef, D., Oron, Y. and Shalgi, R. (1993) Prolonged, repetitive calcium transients in rat oocytes fertilized in vitro and in vivo. FEBS Lett., 331, 239–242.
Bos-Mikich, A., Swann, K. and Whittingham, D.G. (1995) Calcium oscillations and protein synthesis inhibition synergistically activate mouse oocytes. Mol. Reprod. Dev., 41, 84–90.
Boue, F., Blais, J. and Sullivan, R. (1996) Surface localization of P34H, an epididymal protein, during maturation, capacitation, and acrosome reaction of human spermatozoa. Biol. Reprod., 54, 1009–1017.
Boue, F., Duquenne, C., Lasalle, B. et al. (1995) FLB1, a human protein of epididymal origin that is involved in the sperm oocyte recognition process. Biol. Reprod., 52, 267–278.
Braude, P., Bolton, V. and Moore, S. (1988) Human gene expression first occurs between the four- and eight-cells stages of preimplantation development. Nature, 332, 459–461.
Cheng, L.Y.L., Yuen, A.C.Y. and Chow, P.H. (1995) Electrophoretic study of modification of sperm plasma membrane by ventral prostate secretion in golden hamsters. Archiv. Androl., 35, 13–20.
Chow, P.H., Pang, S.F., Ng, K.W. et al. (1986) Fertility, sex ratio and the accessory sex glands in male golden hamsters. Int. J. Androl., 9, 312–320.
Chow, P.H., Dochery, P., Cheung, M.P.L. et al. (1994) Effects of male accessory sex glands on fertilization, polyspermy, and morphometry of early embryos in the golden hamster. Int. J. Androl., 17, 107–112.
Chow, P.H., Yuen, A.C.Y. and Cheng, L.Y. L. (1995) Quantitative electrophoretic study of the modification of sperm plasma membrane by the ampullary glands in the golden hamster. Archiv. Androl., 34, 53–61.
Cockle, S.M., Aitken, A., Beg, F. et al. (1989) A novel peptide, pyroglutamylprolineamide in the rabbit prostate complex, structurally related to TRH. J. Biol. Chem., 264, 7788–7791.
Cornwall, G.A., Vreeburg, J.T., Holland, M.K. et al. (1990). Interactions of labelled epididymal secretory proteins with spermatozoa after injection of 35S-methionine in the mouse. Biol. Reprod., 43, 121–129.
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.
Eddy, E.M. and O'Brien, D.A. (1994) The spermatozoon. In Knobil, E. and Neill, J.D. (eds), The Physiology of Reproduction. Raven Press, New York, pp. 29–78.
Eid, L.N., Lorton, S.P. and Parrish, J.J. (1994) Paternal influence on S-phase in the first cell cycle of the bovine embryo. Biol. Reprod., 51, 1232–1237.
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.
Green, C.M., Cockle, S.M., Watson, P.F. et al. (1994) Stimulating effect of pyroglutamylglutamylprolineamide, a prostatic, TRH-related tripeptide, on mouse sperm capacitation and fertilizing ability in vitro. Mol. Reprod. Dev., 38, 215–221.
Green, C.M., Cockle, S.M., Watson, P.F. et al. (1996) Fertilization promoting peptide, a tripeptide similar to thyrotrophin-releasing hormone, stimulates the capacitation and fertilizing ability of human spermatozoa in vitro. Hum. Reprod., 11, 830–836.
Henault, M.A., Killian, G.J., Kavanaugh, J. et al. (1995) Effects of accessory sex gland fluid from bulls of differing fertility on the ability of cauda epididymal sperm to penetrate zona-free bovine oocytes. Biol. Reprod., 52, 390–397.
Iwamonto, T. and Gagnon, C. (1988) Purification and characterization of a sperm motility inhibitor in human seminal plasma. J. Androl., 9, 377–383.
Iwamonto, T., Tsang, T., Luterman, M. et al. (1992) Purification and characterization of a sperm motility-dynein ATPase inhibitor from boar seminal plasma. Mol. Reprod. Dev. 31, 55–62.
Killian, G.J., Chapman, D.A. and Rogowski, L.A. (1993) Fertility-associated proteins in Holstein bull seminal plasma. Biol. Reprod., 49, 1202–1208.
Kline, D. and Kline, J.T. (1992) Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol., 149, 80–89.
Kline, J.T. and Kline, D. (1994) Regulation of intracellular calcium in the mouse egg: evidence from inositol triphosphate-induced calcium release, but not calcium-induced calcium release. Biol. Reprod., 50, 193–203.
Koehler, J.K., Nudelman, E.D. and Hakomori, S. (1980) A collagen-binding protein of the surface of ejaculated rabbit spermatozoa. J. Cell. Biol., 86, 529–536.
Maleszewski, M., Kline, D. and Yanagimachi, R. (1997) Activation of hamster zona-free oocytes by homologous and heterologous spermatozoa. J. Reprod. Fertil., 105, 99–107.
Miller, D.J., Winer, M.A. and Ax, R.L. (1990) Heparin-binding proteins from seminal plasma bind to bovine spermatozoa and modulate capacitation by heparin. Biol. Reprod., 42, 899–915.
Miyazaki, S., Yuzaki, M., Nakada, K. et al. (1992) Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science, 257, 251–255.
Nagai, T., Niwa, K. and Iritani, A. (1984) Effect of sperm concentration during preincubation in a defined medium on fertilization in vitro of pig follicular oocytes. J. Reprod. Fertil., 70, 271–275.
Niwa, K., Ohara, K., Hosoe, Y. et al. (1985) Early events of in vitro fertilization of cat eggs by epididymal spermatozoa. J. Reprod. Fertil., 74, 657–660.
O, W.S., Chen, H.Q. and Chow, P.H. (1988) Effects of male accessory sex gland secretions on early embryonic development in the golden hamster. J. Reprod. Fertil., 84, 341–344.
Oliphant, G., Reynolds, A.B. and Thomas, T.S. (1985) Sperm surface components involved in the control of the acrosome reaction. Am. J. Anat., 174, 269–283.
Ozil, J.P. (1990) The parthenogenetic development of rabbit oocytes after repetitive pulsatile electrical stimulation. Development, 109, 117–127.
Palermo, G.D., Schligel, 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, 1023–1023.
Pang, S.F., Chow, P.H. and Wong, T.M. (1979) The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice. J. Reprod. Fertil., 56, 129–132.
Parrington, J., Swann, K., Shevchenlo, V.I. et al. (1996) Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature, 379, 364–368.
Peitz, B. and Olds-Clarke, P. (1986) Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol. Reprod., 35, 608–617.
Queen, K., Dhabuwala, C.B. and Pierrepoint, C.G. (1981) The effect of the removal of the various accessory sex glands on the fertility of male rats. J. Reprod. Fertil., 62, 423–426.
Robert, M. and Gagnon, C. (1996) Purification and characterization of the active precursor of a human sperm motility inhibitor secreted by the seminal vesicles: identity with semenogelin. Biol. Reprod., 55, 813–821.
Setchell, B.P., Maddocks, S. and Brooks, D.E. (1994) Anatomy, vasculature, innervation, and fluids of male reproductive tract. In Knobil, E. and Neil, J.D. (eds), The Physiology of Reproduction. Raven Press, New York, pp. 1063–1175.
Shalgi, R., Kaplan, R., Nebel, L. et al. (1981) The male factor in fertilization of rat eggs in vitro. J. Exp. Zool., 217, 399–402.
Shilling, F.M., Carroll, D.J., Muslin, A.J. et al. (1994) Evidence for both tyrosine kinase and G-protein coupled pathways leading to starfish egg activation. Dev. Biol., 162, 590–599.
Sun, F.Z., Hoyland, J., Haung, X. et al. (1992) A comparison of intracellular Ca2+ changes in porcine eggs after fertilization and electroactivation. Development, 115, 947–956.
Swann, K. (1990) A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development, 110, 1259–1302.
Swann, K., Parrington, J. and Jones, K.T. (1998) On the search for the sperm oscillogen. Mol. Hum. Reprod., 4, 1010–1012.
Tesarik, J. (1998a) Oocyte activation after intracytoplasmic injection of mature and immature sperm cells. Hum. Reprod., 13 (Suppl. 1), 117–127.
Tesarik, J. (1998b) Sperm-induced calcium oscillations oscillin-reopening the hunting season. Mol. Hum. Reprod., 11, 1007–1012.
Tesarik, J., Sousa, M. and Testart, J. (1994) Human oocyte activation after intracytoplasmic sperm injection. Hum. Reprod., 9, 511–518.
Van Der Ven, H., Bhattacharyya, A.K., Binor, Z. et al. (1982) Inhibition of human sperm capacitation by a high-molecular-weight factor from human seminal plasma. Fertil. Steril., 38, 753–755.
Whitaker, M. and Patel, R. (1990) Calcium and cell cycle control. Development, 108, 525–542.
Xu, Z., Kopt, G.S. and Schultz, R.M. (1994) Involvement of inositol 1,4,5-trisphophate mediated Ca2+ release in early and late events of mouse egg activation. Development, 120, 1851–1859.
Yanagimachi, R. (1994) Mammalian fertilization. In Knobil, E.and Neil, J.D. (eds), The Physiology of Reproduction. Raven Press, New York, pp. 189–317.
Ying, Y., Cheung, M.P.L., Chow, P.H. et al. (1999) Effects of male accessory sex glands on sperm decondensation and oocyte activation during in vivo fertilization in golden hamsters. Int. J. Androl., 22, In press.
Ying, Y., Chow, P.H. and O, W.S. (1998) Effects of male accessory sex glands on deoxyribonucleic acid synthesis in the first cell cycle of golden hamster embryos. Biol. Reprod., 58, 659–663.
Zhu, J., Barratt, C.L., Lippes, J. et al. (1994) The sequential effects of human cervical mucus, oviductal fluid, and follicular fluid on sperm function. Fertil. Steril., 61, 1129–1135.
Submitted on August 10, 1998; accepted on February 9, 1999.
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