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RESEARCH |
Laboratory of Biotechnology and Animal Reproduction, BioRep, Federal University of Santa Maria, 97105-900 Santa Maria, RS, Brazil
Correspondence should be addressed to P B D Gonçalves who is now at Departamento de Clínica de Grandes Animais, Hospital Veterinário, Universidade Federal de Santa Maria, 97105-900 Santa Maria, RS, Brazil; Email: bayard{at}biorep.ufsm.br
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Abstract |
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 Top Abstract IntroductionResultsDiscussionMaterials and MethodsDeclaration of interestAcknowledgementsReferences |
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or AngII was present in the co-culture system with follicular cells (PGE2 77.4%, PGF2 70.0%, and AngII 75.0% MI). In conclusion, our results provide strong evidence that AngII mediates the resumption of meiosis induced by an LH surge in bovine oocytes and that this event is dependent on PGE2 or PGF2 produced by follicular cells. |
Introduction |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestAcknowledgementsReferences |
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AngII is the active octapeptide hormone product of the renin enzymatic cascade, and two receptor subtypes of AngII have been identified (Bottari et al. 1993, De Gasparo et al. 1995, Gallinat et al. 2000). The classic effects of AngII regarding the muscular contraction, aldosterone secretion, and sanguineous pressure regulation are mediated by the AngII receptor type 1. In fact, the AngII receptor type 2 has been demonstrated to be the mediator of several reproductive functions including steroidogenesis, oocyte maturation, and ovulation (Kuji et al. 1996, Yoshimura et al. 1996, Ferreira et al. 2007). In cows, the AngII receptor type 2 is present in the dominant follicle (Schauser et al. 2001), and its mRNA expression was positively correlated with estradiol production (Portela et al. 2006). In perfused rabbit ovaries, the ovulation and the meiosis resumption induced by hCG are blocked by saralasin (1-sarcosine-8-alanine-5-isoleucine-AngII, a competitive AngII antagonist; Yoshimura et al. 1992). In contrast, Kuo et al. (1991) reported that saralasin inhibited ovulation without affecting oocyte nuclear maturation in rabbits. Recently, our group demonstrated that intrafollicular injection of saralasin in follicles larger than 12 mm, before the LH surge, inhibits ovulation in cows (Ferreira et al. 2007). These results suggest that AngII can act as an intrafollicular mediator of LH actions during the periovulatory period. However, the specific role of AngII in the regulatory mechanism of ovulation and oocyte nuclear maturation is unknown.
AngII stimulates PG-endoperoxide synthase 2 (PTGS2) and PG synthesis in the vascular endothelium (Gimbrone & Wayne 1975), renal tissue (Hernández et al. 2002), and human monocytes (Kim et al. 2005). In rabbit ovaries perfused in vitro, AngII was found to stimulate PGE2 and PGF2 production in the absence of gonadotropins (Yoshimura et al. 1993). Recently, our group demonstrated that AngII stimulates the expression of PTGS2 mRNA in cultured bovine granulosa cells, which was potentiated by LH (Portela et al. 2008). The involvement of the PTGS2 pathway in oocyte nuclear maturation has been previously demonstrated in sheep (Murdoch 1988, 1996), cattle (Nuttinck et al. 2002, Calder et al. 2005), mice (Takahashi et al. 2006), humans (Ben-Ami et al. 2006), and horses (Dell'Aquila et al. 2004). In sheep, the systemic administration of indomethacin (nonselective PTGS inhibitor) resulted in suppression of the cumulus cell expansion and oocyte nuclear maturation, which were reversed by PGE2 intrafollicular injection (Murdoch 1988, 1996). In PTGS2 knockout mice, ovulation and oocyte maturation did not occur normally (Lim et al. 1997).
In spite of reports that AngII induces meiotic resumption in oocytes co-cultured with follicular cells (Giometti et al. 2005, Stefanello et al. 2006), there is no information available regarding the requirement of AngII for oocyte resumption of meiosis after the LH surge. Consequently, our hypotheses were that AngII is essential for meiotic resumption after the LH surge and that it acts through PTGS2-mediated PG synthesis. Therefore, the aim of this study was to verify whether AngII is required for meiotic resumption after the LH surge induced by GnRH agonist and to test the hypothesis that the PGE2 and F2 mediate this process.
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Results |
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Experiment II: effect of saralasin on oocyte nuclear maturation in the presence of follicular cells
This experiment was performed to evaluate the potential deleterious effect of saralasin on oocyte and follicular cell function. The ability of follicular cells to inhibit meiosis was maintained after treating follicular hemisections with 10 µM saralasin for 15 h (21.4 and 13.3% MI in the saralasin and negative control groups respectively; P>0.1; Fig. 1). Similarly, the follicular cell function was assessed using 100 pM AngII. In oocytes cultured with follicular hemisections, the resumption of meiosis was induced by AngII (80.0% MI), results that did not differ from the positive control group without follicular cells (86.7% MI) in 15 h of culture. The oocytes previously co-cultured for 15 h in the presence of follicular hemisections and saralasin resumed meiosis after co-culture with follicular cells and AngII for an additional 15 h (83.9% MII, P<0.001; Fig. 2). Also, the MII rate observed in oocytes cultured with follicular hemisections and AngII (77.4%) was not different from those cultured in the positive control group (86.7%). Even culturing for 15 h+15 h with (Sar 15 h+ Sar 15 h group; 21.9% MII) or without saralasin (negative control group; 19.4% MII), the oocyte nuclear maturation was inhibited by follicular cells, showing that saralasin did not affect the cell function.
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Experiment IV: effect of PTGS on AngII-induced meiotic resumption
This experiment was conducted to assess whether AngII-induced oocyte meiotic resumption is mediated by PTGS. The AngII effect in follicular cells was inhibited by indomethacin (10 µM; nonselective PTGS inhibitor). Oocytes cultured for 15 h with AngII and indomethacin reached 13.4% MI while those cultured with AngII but not indomethacin achieved 77.5% MI (P<0.001; Fig. 3) when follicular cells were present. The inhibition of meiotic resumption rate did not differ between groups of oocytes cultured with or without indomethacin when AngII was absent and follicular cells were present (26.6% MI without indomethacin versus 13% MI with indomethacin). Indomethacin did not affect the meiotic resumption rate (80.7% MI) without follicular hemisections when compared with the positive control group (78.1% MI) and the AngII treated group (77.5% MI; P>0.1).
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on bovine oocyte meiosis resumption (76.1%) did not differ from those cultured with AngII (80.4%) when follicular cells were in the system (Fig. 4).
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Discussion |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestAcknowledgementsReferences |
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into an in vitro co-culture system of oocytes and follicular cells resulted in the same pattern of meiotic resumption induced by AngII. Resumption of meiosis in fully grown follicles is triggered by a preovulatory surge of LH (Ayalon et al. 1972, Dekel et al. 1979), and herein we report the inhibition of these events by a competitive AngII antagonist. These results are complementary to previous findings of our group regarding oocyte meiotic resumption (Giometti et al. 2005, Stefanello et al. 2006) and ovulation, an event closely related to oocyte maturation (Ferreira et al. 2007). Together, these results suggest that AngII is an important intrafollicular mediator of the LH surge to induce meiotic resumption in bovine oocytes. In this study, an intrafollicular injection was performed when follicles reached a minimal diameter of 12 mm to obtain an efficient response to the GnRH challenge (Sartori et al. 2001). The saline intrafollicular injection did not affect meiotic resumption after the GnRH challenge (30.8% GV breakdown (GVBD) and 69.2% MI). These results validate the intrafollicular injection model as a useful tool to study bovine follicular development, ovulation, and oocyte nuclear maturation. Likewise, the intrafollicular injection procedure did not affect the final follicular development and ovulation in previous investigations (Kot et al. 1995, Ginther et al. 2004, Ferreira et al. 2007).
Saralasin was used as a potent AngII antagonist to block all the receptor subtypes (Kuji et al. 1996, Yoshimura et al. 1996). A saralasin concentration of 10 µM has been used as an effective inhibitor of AngII action (Kuji et al. 1996). In experiment II, it was demonstrated that saralasin had no detrimental effects on follicular cells. The follicular cells cultured with saralasin for 15 h responded to AngII, showing that the cell function of inducing the resumption of meiosis was maintained. In vitro oocyte maturation in the presence of 10 µM saralasin did not impair the early embryo development and hatching rates (experiment III). The results of experiment II and III together strongly suggest that saralasin has no toxic effect on oocyte nuclear and cytoplasmatic maturation. Furthermore, this peptide has been widely used to block the effects of the RAS with high specificity for the AngII receptors (Kuji et al. 1996, Yoshimura et al. 1996, Camargo & Saad 1999, Ferreira et al. 2007). The high rate of embryo development demonstrates that saralasin did not change the kinetics of oocyte nuclear and cytoplasmatic maturation. These results show that saralasin does not have a direct effect on bovine oocyte, which are in agreement with those reported previously (Giometti et al. 2005, Stefanello et al. 2006).
The AngII signaling pathway on follicular cells to promote the meiotic resumption is unknown. In this study, it was demonstrated (experiment IV) that a nonspecific PTGS inhibitor (indomethacin) suppressed meiotic resumption induced by AngII. Murdoch (1988) demonstrated that systemic administration of indomethacin in ewes inhibited the oocyte nuclear maturation and cumulus cell expansion. Impairment of ovulatory process and oocyte maturation has been observed in PTGS2 knockout mice females (Lim et al. 1997). These results indicate the importance of PTGS2 in oocyte meiotic resumption in different species. The cumulus cells of bovine oocytes express PTGS2 mRNA during in vitro maturation (Nuttinck et al. 2002, Calder et al. 2005). However, indomethacin did not affect oocyte nuclear maturation when the follicular hemisections were absent, suggesting that the effect of PTGS and AngII is through follicular cells. Additionally, our laboratory recently demonstrated that AngII stimulated PTGS2 expression in bovine granulosa cells (Portela et al. 2008).
In experiment V, PGE2 and PGF2 induced meiotic resumption in the same way as AngII. In ewes, the intrafollicular injection of PGE2 was found to reverse the negative effect on oocyte nuclear maturation and cumulus cell expansion caused by systemic administration of indomethacin (Murdoch 1988). In the case of PTGS2 knockout mice, PGE2 modulated oocyte nuclear maturation and granulosa cell expansion, differentially regulating the intracellular signaling pathways related to MAP kinase, cAMP-dependent protein kinase, phosphatidylinositol 3-kinase/Akt, and nuclear factor kappa B (Takahashi et al. 2006). Furthermore, intrafollicular injection of indomethacin decreased PGE2 secretion in bovine follicular fluid induced by LH (Li et al. 2006). Together, these results supply evidence that meiotic resumption induced by AngII is modulated by the PGE2 and F2. However, the signaling pathway of PGs in the induction of meiotic resumption needs further investigation. Li et al. (2006) demonstrated that indomethacin inhibited the effect of the LH surge on the expression of an enzyme that degrades the preovulatory extracellular matrix in cows, providing evidence for the involvement of the PTGS pathway in the extracellular matrix remodeling of follicular cells during the periovulatory period. Similarly, AngII inhibited the expression of protease nexin-1 in bovine granulosa cells (Portela et al. 2006). These results together provide evidence that the signaling pathway of AngII, through PGE2 and F2, to induce the meiotic resumption in bovine oocytes involves extracellular matrix remodeling factors. In conclusion, we have demonstrated the involvement of AngII and PGE2 and F2 in bovine oocyte meiotic resumption induced by LH.
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Materials and Methods |
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; Sincrocio, Ouro Fino, Ribeirão Preto, Brazil; 250 µg; s.c.) was administered and the follicle-stimulating hormone (FSH) treatment was initiated (Pluset, Hertape Calier Saúde Animal, Juatuba, Brazil). Each cow received 437.5 IU FSH, divided into 11 decreasing doses (from 87.5 to 12.5 IU; i.m.) each given 12 h apart. The progesterone intravaginal device was maintained for 10 days.
Ultrasound-guided intrafollicular injection procedure
The intrafollicular injections were guided by ultrasound equipped with a 7.5 MHz vaginal probe (Pie Medical Scanner 200, Maastricht, The Netherlands). A system with two sterile needles was used as previously described by Ferreira et al. (2007). Briefly, the double-channeled needle system consisted of an inner sterile 25-gauge needle attached to a 35 cm long cannula and an outer 20-gauge needle coupled to a needle guide. To the opposite end of the cannula, a Hamilton syringe was attached. Epidural anesthesia was administered and perineal cleaning was performed before injections. The transducer was coupled to a biopsy guide (Pie Medical Equipment BV), coated with lubricant, and placed in the vaginal fornix. The course of the echogenic needle was observed on the ultrasound display, which allowed us to reach the follicle of interest. The ovary was manipulated so that the needle entered the follicle via penetration of the ovarian stroma at the base of the follicle. The needle path to the injected follicle contained ovarian stroma and no additional follicle or corpus luteum.
When the ovary and follicle of interest were in position, the outer needle was advanced until the image of its tip became visible on the screen, 
3–5 mm from the follicle. At this moment, a second operator pushed the inner needle forward until the image of the needle tip was visible within the follicle. Treatments were then injected into the follicle. Swirling of the fluid entering the follicle indicated that the injection was successful. The amount of AngII receptor antagonist for the injection was calculated based on the volume of follicular fluid, to obtain an adequate final concentration inside the follicle. The follicular fluid volume was estimated by the linear regression equation V=685.1+120.7D (P=0.0001), as described by Ferreira et al. (2007), where V corresponds to the estimated follicular volume and D to the diameter of the follicle to be injected. The probe and needles were withdrawn immediately after injection to minimize pressure on the newly punctured follicle. Follicular diameter was measured again 2 h after intrafollicular injection. Follicles were excluded from the experiment if the reduction in the follicular diameter was greater than 2 mm.
Oocyte recovery and nuclear maturation
Bovine ovaries at different stages of the estrous cycle were obtained from an abattoir and transported to the laboratory in saline solution (0.9% NaCl) at 30 °C containing 100 IU/ml penicillin and 50 µg/ml streptomycin sulfate (All chemicals used were purchased from Sigma Chemical Company, unless otherwise indicated in the text). COCs were aspirated from follicles 3 to 8 mm in diameter. The COCs were recovered under a stereomicroscope and selected according to Leibfried & First (1979). Grade 1 and 2 COCs (n=10–30) were randomly distributed into 200 µl maturation medium and cultured in an incubator at 39 °C in a saturated humidity atmosphere containing 5% CO2 and 95% air, for either 15 or 24 h depending on the experiment. The maturation medium used was TCM 199 containing Earle's salts and L-glutamine (Gibco Labs) supplemented with 25 mM HEPES, 0.2 mM pyruvic acid, 2.2 mg/ml sodium bicarbonate, 5.0 µg/ml LH (Lutropin-V, Bioniche, Ontario, CA, USA), 0.5 µg/ml FSH (Folltropin-V, Bioniche), 0.4% fatty acid-free BSA, 100 IU/ml penicillin, and 50 µg/ml streptomycin sulfate.
At the end of the maturation period, the cumulus cells were removed by vortexing. The oocytes were fixed in glacial acetic acid:methanol (1:3) solution (Merck KG) for 4 h and then stained with 1% lacmoid in 45% glacial acetic acid in PBS. Oocytes were analyzed under a phase contrast microscope (1000x) and classified according to the nuclear maturation stage as germinal vesicle (GV), GVBD, metaphase I (MI), anaphase I (AI), telophase I (TI), and metaphase II (MII).
Sperm preparation, in vitro fertilization, and embryo culture
A tested frozen semen pool of a single batch from two sires (Jersey and Holstein) was used in all experiments. Semen was fractionated on discontinuous Percoll (Amersham Biosciences AB) gradients as described previously (Parrish et al. 1986). Briefly, 2.7 ml Percoll was mixed with 300 µl 10x sperm-TALP medium (modified Tyrode with albumin, lactate, and pyruvate), yielding a 90% Percoll solution. A 45% Percoll solution was obtained by 1:1 dilution in 1x sperm-TALP medium. A gradient column overlaying 45 and 90% Percoll solutions was then prepared to separate live sperm by centrifugation at 700 g for 30 min. The sperm were diluted to a final concentration of 2x106 spermatozoa/ml in 250 µl Fert-TALP medium containing 10 mg/ml heparin (Parrish et al. 1988). In vitro fertilization was carried out in drops by co-culture of sperm and oocytes for 18 h in an incubator (same atmospheric conditions as those used for maturation). After gamete co-incubation, cumulus cells were removed by vortexing. Presumptive zygotes and embryos were washed thrice and then cultured at 39 °C in a saturated humidity atmosphere containing 5% CO2, 5% O2, and 90% N2 for 9 days in 200 µl synthetic oviduct fluid medium as previously described by Holm et al. (1999).
Preparation of follicular hemisections
Follicles were isolated from the ovaries and dissected free of stromal tissue (Richard & Sirard 1996). Transparent follicles measuring 2–5 mm in diameter were selected. The follicles were sectioned into equal halves with a scalpel and the oocytes were removed and discarded. Next, the follicular hemisections were washed ten times in TCM 199 containing 0.4% BSA and incubated for 2 h before adding the COCs. The dissection and follicle culture procedures have been previously conducted in our laboratory and validated by measuring the progesterone and estradiol ratio and by histological analysis (Giometti et al. 2005, Stefanello et al. 2006).
Experiment I: effect of competitive AngII antagonist on LH-induced meiotic resumption
As described above, seven cows were submitted to the superovulation protocol. On day 9 of the progesterone treatment, the number of follicles in the ovary was evaluated by ultrasound scanning and all follicles with size from 5 to 11 mm were aspirated using a vacuum pump, remaining only the two to four largest follicles in each ovary. In the afternoon of day 10, after the intravaginal device had been removed, an ultrasound image of each ovary was processed to produce a map of the follicles in the ovary and all follicles greater than 12 mm in diameter were intrafollicularly injected. The follicles of the right ovaries were treated with 10 µM saralasin (saralasin group; n=17) and those of the left ovaries were treated with 0.9% saline (control group; n=17). Immediately after the intrafollicular injections, the cows received 100 µg gonadorelin acetate intramuscularly (GnRH agonist; Profertil, Tortuga, Santo Amaro, Brazil). Fifteen hours after challenging with the GnRH agonist, the animals were ovariectomized for recovery of the oocytes. The oocytes were immediately denuded, fixed, stained, evaluated as described above and classified according to the nuclear maturation stage as GV, GVBD, or MI.
Experiment II: effect of saralasin on oocyte nuclear maturation in the presence of follicular cells
COCs (n=270) derived from abattoir ovaries were used to evaluate the saralasin effect on oocyte nuclear maturation with follicular cells. COCs were cultured with follicular hemisections treated with 100 pM AngII (AngII group; n=60) or 10 µM saralasin (saralasin group; n=90). As control groups, COCs cultured with (negative control group; n=60) or without follicular hemisections (positive control group; n=60) were used. After in vitro maturation for 15 h, 30 oocytes of each group were denuded, fixed and then stained for evaluation of nuclear maturation. The remaining oocytes and the follicular hemisections were transferred to other culture dishes with the same maturation medium for each group. However, the oocytes that were cultured with saralasin (n=60) were divided into two subgroups with follicular hemisections treated with 10 µM saralasin (Sar 15 h+ Sar 15 h group; n=30) or 100 pM AngII (Sar 15 h+ AngII 15 h group; n=30). The oocytes were cultured for an additional period of 15 h (totaling 30 h) after changing the medium, excepting those cultured without follicular hemisections, for which the culture period was 22 h. At the end of the maturation period, the oocytes of all groups were denuded, fixed, and then stained for evaluation of meiotic resumption.
Experiment III: effect of saralasin on bovine oocyte maturation and subsequent blastocyst production
This experiment was designed to evaluate possible detrimental effects of saralasin on the capacity of oocytes to support embryo development. COCs were cultured with (saralasin group; 10 µM; n=45) or without saralasin (control group; n=43) with no follicular cells for 24 h. After the maturation period, oocytes were fertilized and the embryos cultured for 7 days to determine the blastocyst rate per oocyte. The hatching blastocyst rate was evaluated on day 9 and calculated as the number of hatching blastocysts divided by the total number of blastocysts in each group.
Experiment IV: effect of PTGS on AngII-induced meiotic resumption
To evaluate whether AngII action on oocyte nuclear maturation is mediated by PTGS from follicular cells, COCs were cultured with follicular hemisections treated with 100 pM AngII (n=89), 100 pM AngII, and 10 µM indomethacin (a PTGS nonselective inhibitor; n=97) or 10 µM indomethacin (n=100). The COCs in the control groups were cultured with (negative control group; n=94) or without follicular hemisections (positive control group; n=96). Eighty-eight COCs were cultured with 10 µM indomethacin without follicular hemisections to evaluate deleterious effects of indomethacin on bovine oocytes. After 15 h of in vitro culture, oocytes of all groups were denuded, fixed, stained, and evaluated for nuclear status.
Experiment V: effect of PGE2 and F2 on nuclear maturation
This experiment was designed to assess the role of PGE2 and F2 on AngII-induced meiotic resumption. COCs were co-incubated with follicular hemisections treated with 100 pM AngII (n=92), 100 pM AngII and 10 µM indomethacin (n=92), and 1 µM PGE2 (n=92) or 1 µM PGF2 (n=92). The COCs in the negative control group (n=95) were cultured with non-treated follicular hemisections. After 15 h of in vitro culture, oocytes of all groups were denuded, fixed, stained, and evaluated for nuclear status.
Statistical analysis
In experiment I, the mean initial follicle diameters of the two groups were compared by ANOVA to validate the results. The progression of nuclear maturation was used as the variable response, grouped into classes (GV, GVBD, and MI), and normalized by PROC RANK. The percentage of meiotic progression among groups was compared by ANOVA (PROC GLM). The results of the experiments II, III, IV, and V were analyzed using the ANOVA test in a statistical model for categorical data, using the PROC CATMOD (Categorical Data Analysis Procedures). All in vitro experiments were performed in triplicate. On detecting statistical differences, the independent variables were compared using the contrast test. All the data were analyzed using the statistical analysis software (SAS; SAS Institute Inc., Cary, NC, USA).
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Declaration of interest |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestAcknowledgementsReferences |
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Funding |
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Acknowledgements |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestAcknowledgementsReferences |
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Received June 13, 2008
First decision August 6, 2008
Accepted September 3, 2008
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References |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestAcknowledgementsReferences |
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