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RESEARCH |
Laboratory for Animal Reproduction and Embryology, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai-an City 271018, Shandong Province, People's Republic of China
Correspondence should be addressed to J-H Tan; Email: tanjh{at}sdau.edu.cn
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Abstract |
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 Top Abstract IntroductionResultsDiscussionMaterials and MethodsDeclaration of interestReferences |
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Introduction |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestReferences |
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Oocyte maturation involves both nuclear and cytoplasmic events. While nuclear maturation includes the resumption of the first meiotic division and the progression of meiosis to the metaphase II stage, cytoplasmic maturation includes a series of processes that are necessary for the oocyte to acquire the capacity to support male pronucleus formation, monospermic fertilization, and early embryonic development (Eppig et al. 1996). The completion of nuclear maturation in vitro does not assure the completion of normal cytoplasmic maturation. Thus, although spontaneous nuclear maturation of oocytes appears to occur normally in vitro, the functionality of the oocytes for post-fertilization development is apparently not completely normal because development of the in vitro matured bovine oocytes to the preimplantation stages following IVF is less successful than that of oocytes matured in vivo (Leibfried-Rutledge et al. 1987, Eppig 1996, Van de Leemput et al. 1999). Chromosomal spindle exchange experiments between metaphase II oocytes showed that in vitro maturation (Liu et al. 2003a) and post-ovulatory aging processes (Bai et al. 2006) reduced the developmental potential of mouse oocytes by affecting the cytoplasmic components rather than the nuclear components. However, whether heat stress during oocyte maturation affects the nuclear or cytoplasmic component is unclear. In addition, reports on the effect of hyperthermia on the maturing mouse oocytes are few (Fiorenza & Mangia 1992), and the effect of heat stress during in vitro maturation on the developmental potential of mouse oocytes has not been reported, to our knowledge.
The objectives of the present study were to investigate the effect of heat stress during in vitro maturation on the developmental potential of mouse oocytes and to determine whether the detrimental effect is on the nuclear or cytoplasmic component. The critical hyperthermal temperature for in vitro maturation of mouse oocytes was first determined by observing nuclear maturation to metaphase II and preimplantation development after oocytes were matured in vitro under different culture temperatures. The effect of heat stress on oocyte nuclear or cytoplasmic component was then differentiated by observing development following chromosome spindle exchange between the heat stressed and unstressed metaphase II oocytes. Finally, cytoplasmic changes were examined after oocytes were matured under heat stress. The results indicated that 1) oocyte cytoplasmic maturation is more susceptible to heat stress than nuclear maturation to metaphase II and 2) cytoplasmic rather than nuclear components determine the pre-implantation developmental capacity of an oocyte.
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Results |
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-tubulin staining, oocytes were classified into those with tine-pole spindles (Fig. 1E) and those with even-pole spindles (Fig. 1F) under a laser confocal microscope. After MAD2 labeling, some of the oocytes were MAD2 positive with labeling concentrated around the chromosomes (Fig. 1I) while others were MAD2 negative (Fig. 1J) when observed under a laser confocal microscope. Percentages of oocytes with tine-pole spindles did not differ between 37 and 40 °C, and no oocytes matured under these two temperatures were found MAD2-positive (Table 5). However, the percentage of oocytes with tine-pole spindles decreased significantly and over 20% of the oocytes became MAD2-positive after maturation at 40.7 °C. Furthermore, over 60% of the oocytes matured at 40.7 °C displayed scattered microtubule asters in the ooplasm (Fig. 1G). The results indicated that the damaging effect of heat stress on microtubule organization of mouse oocytes did not occur until the temperature increased to 40.7 °C.
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Discussion |
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The present results showed that blastocyst formation was normal when spindles matured at 40.7 °C were transplanted into in vivo matured ooplasts, although spindle assembling was obviously affected and MAD2 was activated in oocytes matured at 40.7 °C. However, when the in vivo matured spindles were transferred into ooplasts matured at 40 °C, no blastocyst formation was observed in reconstructed oocytes, apparently due to the impaired cytoplasmic maturation. This indicates that it is the cytoplasmic components but not the nuclear components that determine the pre-implantation developmental competence of an oocyte. Similarly, while transfer of the spindle apparatus from in vitro-grown and -matured mouse oocytes (that developed poorly when fertilized in vitro) to the in vivo matured ooplasts resulted in a high rate of blastocyst development, transfer of the spindle apparatus from in vivo-matured oocytes into the in vitro-grown and -matured ooplasts produced poor quality embryos with a low rate of blastocyst formation (Liu et al. 2003a). Furthermore, while mouse oocytes reconstructed from fresh spindle apparatus and aged cytoplasm developed to blastocyst at a low rate following fertilization or parthenogenetic activation, blastocyst formation rate of reconstructed oocytes from aged spindle apparatus and fresh cytoplasm was high (Bai et al. 2006). Taken together, the results substantiate the notion that while the nuclear (chromosomal or genetic) constitution determines the viability and morbidity of the late-stage fetus and offspring, the cytoplasmic constitution of the oocyte determines fertilization and the early development capacity of the embryo (Moor et al. 1998).
Our immunofluorescence microscopy revealed that hyperthermia during in vitro maturation impaired migration of both cortical granules and mitochondria of mouse oocytes. Previous studies have shown that migration of cortical granules to the egg cortex in the mouse was a continuous process regardless of germinal vesicle breakdown and it was normally completed before or soon after germinal vesicle breakdown (Ducibella & Buetow 1994, Liu et al. 2003b, 2005). Nishi et al. (2003) found that the rate of mitochondrial congregation was significantly higher in the in vivo than in vitro matured mouse oocytes. Miki et al. (2006) and Ge et al. (2008) reported that mouse oocytes matured under optimized conditions essentially resembled in vivo matured oocytes in mitochondrial distribution. According to Sun & Schatten (2006), while peripheral cortical granule migration in oocytes is controlled by microfilaments, mitochondria movement is mediated by microtubules. Therefore, it is suggested that the incomplete congregation of mitochondrial distribution observed in the heat-stressed mouse oocytes could have resulted from a poor mediation of mitochondrial translocation by the microtubules, because both the present study and others (Ju et al. 2005, Roth & Hansen 2005) have observed disturbed microtubule assembly following hyperthermia during in vitro maturation. The incomplete migration of cortical granules in heat stressed oocytes could have been due to a poor mediation by microfilaments, because alterations in microfilament structures were observed following heat stress of matured porcine oocytes (Ju & Tseng 2004). However, we were unable to find any difference in microfilament distribution between mouse oocytes matured at 37 and 40 °C following staining with Phalloidin-TRITC (data not shown).
The present results indicated that heat shock during in vitro maturation decreased the GSH/GSSG ratio of mouse oocytes, although the total GSH level was similar between the heat stressed oocytes and unstressed controls. A positive effect of GSH concentration on oocyte developmental competence has been demonstrated, and therefore the intracellular GSH level is used as a marker for oocyte cytoplasmic maturation (de Matos et al. 1995, 2002, Abeydeera et al. 1998, Gasparrini et al. 2003). Hyperthermia-induced oxidative stress has been suggested as one of the mechanisms by which heat stress disrupts reproductive performance. For example, exposing zygotes to heat shock has resulted in early embryonic loss, in association with increased hydrogen peroxide concentrations and reduced levels of GSH within the embryos (Ozawa et al. 2002). Hyperthermia enhances the production of ROS in the mouse liver (Ozawa et al. 2004) and oviduct (Matsuzuka et al. 2005), shifting the redox status toward oxidative stress. In addition, in vitro supplementation of GSH or GSH ester reduced the effect of heat shock on viability of mouse embryos (Aréchiga et al. 1995), while inhibition of GSH synthesis aggravated the deleterious effect of heat stress on the oocyte developmental capacity (Edwards & Hansen 1997). Furthermore, treatment of buffalo–cows or supplementation with antioxidants before the beginning of months of heat-stress and during the stress period corrected the infertility due to heat-stress through the decrease in cortisol secretion and a decrease in the oxidative stress (Megahed et al. 2008). Similarly, pretreatment of female mice with antioxidants alleviated the negative effect of hyperthermia on developmental competence of oocytes and improve embryonic development (Roth et al. 2008).
In this study, while the percentage of oocytes with tine-pole spindles did not differ from 37 to 40 °C, it decreased significantly in oocytes matured at 40.7 °C. The barrel-shaped spindle has been considered less normal than the tine-pole spindle and it occurred more frequently in the in vitro matured than in vivo matured oocytes (Sanfins et al. 2003). Ge et al. (2008) found that while the percentage of oocytes with tine-pole spindles was lower, that of oocytes with even-pole spindles was higher significantly following maturation with cumulus denuded than with cumulus intact. Roth & Hansen (2005) noticed that a subset of bovine oocytes possessed misshapen metaphase-I spindles with disorganized microtubules and unaligned chromosomes after heat-shock during in vitro maturation. Ju et al. (2005) found that the metaphase spindle became elongated or aberrant and smaller following post-maturation heat shock of bovine oocytes. In addition, we observed microtubule organizing center-like structures in some of the oocytes matured at 40.7 °C, but not in oocytes matured at 37 or 40 °C. Ju & Tseng (2004) also showed that the spindle microtubules of porcine oocytes were completely depolymerized or formed as microtubule arrays following post-maturation heat stress. Furthermore, our recent observations indicated that while freshly ovulated oocytes did not, 80% of the aged mouse oocytes formed cytoplasmic asters of microtubules (data to be published). The results that heat stress during in vitro maturation impaired microtubule organization were further substantiated by our observation that spindle assembly checkpoint protein (MAD2) was activated in some of the mouse oocytes matured at 40.7 °C. Zhang et al. (2004) found that MAD2 was at the kinetochores in rat oocytes at germinal vesicle and pro-metaphase I stages, but disappeared once the oocytes reached the metaphase I or metaphase II stage. Similarly, while no MAD2 was observed in freshly ovulated mouse oocytes in this study, a MAD2 concentration around chromosomes was obvious in heat-stressed mouse oocytes. However, when rat oocytes at metaphase II stage were treated by nocodazole, spindles were destroyed and MAD2 reappeared (Zhang et al. 2004). This suggests that heat stress destroyed the spindles and thereby activated MAD2 of mouse oocytes.
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Materials and Methods |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestReferences |
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Animals and oocyte recovery
Animals
Mice of the Kunming breed were kept in a room with 14h light:10h darkness cycles, the darkness starting from 2000 h. The animals were handled by the rules stipulated by the Animal Care and Use Committee of Shandong Agricultural University.
In vivo matured oocytes
Female mice, 6–8 weeks after birth (weighing around 30 g), were induced to superovulate with eCG (10 IU, i.p.) followed 48 h later by hCG (10 IU, i.p.). Both eCG and hCG used in this study were from Ningbo Hormone Product Co., Ltd, Hangzhou city, P.R. China. The superovulated mice were killed at 15 h after hCG injection (Fig. 2) and the oviductal ampullae were broken in M2 medium to release ovulated oocytes.
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In vitro maturation of oocytes
Oocytes at the germinal vesicle stage were washed three times in M2 medium and once in maturation medium. After washing, the oocytes were placed in 100 µl drops maturation medium (around 30 per drop) and cultured for 14 h at different temperatures in a humidified atmosphere of 5% CO2 in air (Fig. 2). The maturation medium was TCM-199 (Gibco) supplemented with 10% (v/v) FCS (Gibco), 1 µg/ml 17 β-estradiol, 24.2 mg/l sodium pyruvate, 0.05 IU/ml FSH, 0.05 IU/ml LH and 10 ng/ml EGF. To reduce variation of temperature during oocyte culture, two CO2 incubators of the same type (CO2 Water Jacketed Incubator Series II, Model: 3110 Series; Forma Scientific Inc., Marietta, OH, USA) were used; while one incubator was always set at 37 °C, the other was used for different temperatures. The inside temperature of an incubator was monitored by simultaneously examining three clinical thermometers placed inside the incubator. Every time to change the temperature, the temperature inside the incubator was checked for constancy every 6 h for at least 1 day before oocyte culture. The door of incubator was kept closed during the whole maturation period (14 h), and the temperature inside was examined again at the end of culture.
Chromosome spindle transfer
Oocytes at the metaphase II stage of either in vitro or in vivo origin were stripped of their cumulus cells by pipetting in M2 medium containing 0.1% hyaluronidase. Denuded oocytes were treated for 15 min in the micromanipulating medium (M2 containing 5 mg/ml cytochalasin B) before micromanipulation. The micromanipulation procedures were carried out using a Leica differential interference contrast microscope, under which the mouse spindle was identifiable as a translucent region. An injection pipette with a flattened tip and an inner diameter of 15–18 µm, driven by a piezo system, was used for both removal and injection of the metaphase II chromosome spindles. The metaphase II spindle with a small amount of ooplasm was pinched off from each oocyte. Isolated karyoplasts from heat stressed oocytes were inserted into the perivitelline space of enucleated non-stressed oocytes while those from the non-stressed oocytes were inserted into the enucleated stressed oocytes.
After rinsing in M2, the karyoplast–cytoplast pairs were equilibrated in fusion medium (0.3 M mannitol, 0.1 mM MgSO4, 0.1 mg/ml polyvinyl alcohol and 3 mg/ml BSA) for 3 min. Fusion between karyoplasts and cytoplasts was then induced with a single DC pulse of 1.0 kV/cm for 30 µs, using a BEX LF201 (Nepa Gene Co., Ltd, Shioyaki Ichikawa Chiba, Japan) with two microelectrodes. Thirty minutes later, fused karyoplast–cytoplast pairs were selected for activation treatment.
Oocyte activation and embryo culture
Procedures used for oocyte activation were those reported by Ma et al. (2005) with a few modifications. The activating medium used was Ca2+-free Chatot–Ziomek–Bavister (CZB) medium supplemented with 10 mM SrCl2. After maturation culture or spindle transfer, the in vitro matured oocytes and oocytes reconstructed with in vitro matured ooplasts were aged for 8–10 h at 37 °C in the maturation medium, before activation treatment, while the oocytes reconstructed with in vivo matured ooplasts were treated for activation immediately after spindle transfer (Fig. 2). Oocytes were stripped of their cumulus cells, if any, by pipetting in M2 containing 0.1% hyaluronidase. After being washed twice in M2 and once in activating medium, the oocytes were incubated first in activating medium for 2.5 h and then in regular CZB without SrCl2 for 3.5 h at 37 °C in a humidified atmosphere with 5% CO2 in air. Both the activating medium and CZB for subsequent short culture of oocytes were supplemented with 5 µg/ml cytochalasin (CB) to diploidize the parthenotes. Six hours after the onset of activation treatment, the oocytes were examined with a microscope for the evidence of activation. Oocytes were considered activated when each contained one (1PN) or two well developed pronuclei (2PN).
The Sr2+-activated oocytes were cultured for 4 d in the regular CZB without CB (20 embryos per 60 µl drop) at 37.5 °C under humidified atmosphere with 5% CO2 in air. Glucose (5.5 mM) was added to CZB when 2/3 of the embryos cultured and developed to the 4-cell stage. Assessment of embryo development was performed at 24 h (2-cell stage), 48 h (4-cell stage), and 96 h (blastocyst) after the onset of activation. Some of the blastocysts were mounted on a slide, stained with Hoechst 33342 and observed for cell counts under a fluorescence microscope.
Assay for intracellular GSH
Intracellular content of GSH was measured as described by Funahashi et al. (1994). Cumulus-free oocytes were washed three times in M2. Five micro-liters of distilled water containing 35–40 oocytes was transferred to a 1.5 ml microfuge tube, and then 5 µl of 1.25 M phosphoric acid were added to the tube. Samples were frozen at –80 °C and thawed at room temperature. This procedure was repeated three times. Then, the samples were stored at –20 °C until analyzed. Concentrations of total GSH in the oocyte were determined by the 5, 5' dithio-bis (2-nitrobenzoic acid) (DTNB)-oxidized glutathione (GSSG) reductase-recycling assay. Briefly, 700 µl of 0.33 mg/ml NADPH in 0.2 M sodium phosphate buffer containing 10 mM EDTA (stock buffer, pH 7.2), 100 µl of 6 mM DTNB in the stock buffer, and 190 µl distilled water were added and mixed in a microfuge tube. Ten micro-liters of 250 IU/ml GSH reductase (G-3664) were added with mixing to initiate the reaction. The absorbance was monitored continuously at 412 nm with a spectrophotometer for 3 min, with reading recorded every 0.5 min. To measure the concentrations of GSSG, the samples (10 µl) were vigorously mixed with 0.2 µl 2-vinylpyridine and 0.6 µl triethanolamine. After 60 min, the sample was assayed as described above in the DTNB-GSSG reductase-recycling assay. Standards (0.01, 0.02, 0.1, 0.2, and 1.0 mM) of GSH and a sample blank lacking GSH were also assayed. The amount of GSH in each sample was divided by the number of oocytes to get the intracellular GSH concentration per oocyte. The GSH values were calculated from the difference between total (GSSG + GSH) and GSSG for each oocyte and expressed as pmol/oocyte.
Immunofluorescence microscopy
Cortical granule staining
Zona pellucida was removed by treating oocytes with 0.5% pronase (Roche) in M2. After being washed three times in a washing solution (M2 supplemented with 0.3% BSA and 0.01% Triton X-100), oocytes were fixed with 3.7% paraformaldehyde in M2 for 30 min at room temperature. The oocytes were then blocked three times for 5 min each in a blocking solution (M2 containing 0.3% BSA and 100 mM glycine). After permeabilization for 5 min in M2 containing 0.1% Triton X-100, oocytes were washed twice again for 5 min each in blocking solution. They were then cultured in 100 µg/ml FITC (FITC)-labeled lens culinaris agglutinin in M2 for 30 min in the darkness. Finally, the oocytes were washed three times in the washing solution, and stained with 10 µg/ml PI for chromatin examination.
Mitochondria staining
Denuded oocytes were washed in M2 and incubated in 10 µg/ml Rhodamine 123 in M2 at 37 °C for 15 min. Then, the oocytes were washed three times in M2 and stained for 5 min at room temperature with 10 µg/ml Hoechst 33342 in M2.
Spindle (-tubulin) staining
Cumulus-free oocytes were fixed with 4% formaldehyde in PHEM buffer (60 mM, 25 mM Hepes, 10 mM EGTA, 4 mM MgSO4, PH 7.0) for 20 min at room temperature. The fixed oocytes were rinsed three times for a total of 15 min in PBS and then treated for 10 min in 1% Triton-X100 in PHEM. After they were briefly washed in PBS, oocytes were blocked in 20% goat serum in PHEM at 4 °C overnight. Fixed oocytes were incubated for 1 h at room temperature in PHEM containing FITC-conjugated monoclonal anti--tubulin (1:50) and 5% goat serum. The oocytes were then washed and stained with 10 µg/ml Hoechst 33342 for chromosome examination.
MAD2 staining
Cumulus-free oocytes were fixed in 4% paraformaldehyde/PHEM (60 Mm Pipes, 25 mM Hepes at pH 6.9, 10 mM EGTA, 8 mM MgSO4) for 20 min and washed three times in PBS containing 0.05% PVP. The oocytes were then treated in 0.5% Triton X-100/PHEM for 5 min and washed rapidly three times in PBS with 0.05% PVP. After being blocked in 1% BSA/PHEM with 100 mM glycine at room temperature for 1 h, the oocytes were incubated in anti-MAD2 antibody (1:100 in 1% BSA/PHEM with 100 mM glycine) at 4 °C overnight. After four washes in PBS with 0.05% Tween 20, the oocytes were incubated with FITC-conjugated goat-anti-rabbit IgG (1:200 in 1% BSA/PHEM with 100 mM glycine) for 45 min. After three washes in PBS with 0.05% Tween 20, the oocytes were stained with PI (10 µg/ml) for examination of chromosomes.
Laser confocal microscopy
After washing, the stained oocytes were mounted on glass slides and observed with a Leica laser scanning confocal microscope. Hoechst 33342 labeled nuclear chromatin was excited with the 405 nm line of a diode laser. The FITC, PI, and Rhodamine 123 fluorescence was obtained by excitation with 488 nm line of an Ar/ArHr laser and the emitted light was passed through a 488 nm filter. The individual optical sections were pseudo-colored and digitally recombined into a single composite image using the Leica Confocal Software.
Data analysis
We conducted at least three replicate trials for each treatment. The percentage data were arc sine transformed and the transformed data were tested to verify ANOVA assumptions (normally distributed and homogenous variance) before being analyzed with ANOVA. A Duncan multiple comparison test was used to locate differences. The software used was SPSS (Statistical Package for Social Sciences, version 11.5, SPSS Inc., Chicago, IL, USA). Data were expressed as means±S.E.M. and P<0.05 was considered significant.
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Declaration of interest |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsDeclaration of interestReferences |
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Funding |
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Received August 9, 2008
First decision September 29, 2008
Accepted November 21, 2008
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References |
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