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RESEARCH |
Department of Animal Sciences, University of Florida, Gainesville, Florida 32611-0910, USA
Correspondence should be addressed to P J Hansen; Email: Hansen{at}animal.ufl.edu
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Abstract |
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Introduction |
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The mechanisms for the disruption in oocyte maturational processes by heat shock are likely to be complex and to involve the cytoskeleton. This is so because nuclear maturation is dependent upon extensive rearrangement of the cytoskeleton (Gallicano 2001, Shin & Kim 2003). Indeed, nuclear maturation can be disrupted by addition of drugs that inhibit microtubule formation (Ruder & Murry 1996, Kim et al. 2000, Brunet et al. 2003) and microfilament assembly (Kim et al. 2000). Additionally, cytoskeletal elements are sensitive to disruption by heat shock (Coss & Linnemans 1996). Exposure of somatic cells to heat shock during the S phase can result in spontaneous premature chromosome condensation and formation of micronuclei (Swanson et al. 1995). Heat shock during the M phase can result in disassembly of the mitotic spindle, polyploidy and failure of cytokinesis (Coss et al. 1982, Vidair et al. 1993). Many studies evaluating effects of heat shock on the cytoskeleton involve temperatures higher than would be seen in mammals exposed to heat stress. Recently, however, more physiologically relevant temperatures of 41–41.5 °C have been shown to cause alterations in microtubule and microfilament structure in matured bovine oocytes (Tseng et al. 2004), porcine oocytes subjected to heat shock during maturation (Ju & Tseng 2004) and two-cell bovine embryos (Rivera et al. 2004a).
The fact that nuclear maturation is dependent upon the cytoskeleton and that heat shock can disrupt cytoskeletal elements leads to the hypothesis tested in these studies that effects of heat shock on oocyte maturation involve alterations in nuclear maturation. A second objective was to evaluate the relationship between oocyte apoptosis (Roth & Hansen 2004a) and nuclear changes in the heat-shocked oocyte. Recently, Roth & Hansen (2004b) demonstrated that maturation in the presence of sphingosine 1-phosphate (S1P), a sphingomyelin metabolite, reduced the deleterious effect of heat shock during maturation on the proportion of bovine oocytes that could cleave and progress in development following insemination. Therefore, a third objective was to determine whether S1P acts to improve maintenance of oocyte function during heat shock by allowing nuclear maturation to take place.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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-tubulin were from Molecular Probes (Eugene, OR, USA). Mouse IgG1
, S1P and Hoechst 33342 dye were from Sigma-Aldrich. The in situ cell death detection kit (fluorescein) was obtained from Roche. Polyvinylpyrrolidone (PVP) was purchased from Eastman Kodak (Rochester, NY, USA), the Prolong Antifade Kit was from Molecular Probes, and RQ1 RNA-free DNase was from Promega. Oocyte collection medium (OCM) was Tissue Culture Medium 199 (TCM-199) with Hanks’ salts and without phenol red (Hyclone, Logan, UT, USA) supplemented with 2% (v/v) bovine steer serum (containing 2 U/ml heparin; Pel-Freez, Rogers, AR, USA), 100 U/ml penicillin-G, 0.1 mg/ml streptomycin and 1 mmol/l glutamine. Oocyte maturation medium (OMM) was TCM-199 with Earle’s salts (Invitrogen) supplemented with 10% (v/v) steer serum (Pel-Freez), 22 µg/ml sodium pyruvate, 20 µg/ml follicle stimulating hormone (Follotropin–V; Vetrepharm Canada, London, ON, Canada), 2 µg/ml estradiol 17-ß, 50 µg/ml gentamicin and 1 mmol/l glutamine. Hepes–Tyrode’s Lactate (Hepes-TL), in vitro fertilization Tyrode’s Lactate (IVF-TL) and Sperm-TL were obtained from Cell and Molecular Technologies (Lavallette, NJ, USA) and used to prepare Hepes-Tyrode’s Albumin Lactate Pyruvate (TALP), IVF-TALP and Sperm-TALP (Parrish et al. 1986). BSA Fraction V and essentially fatty-acid-free BSA were purchased from Sigma-Aldrich. Percoll was from Amersham Pharmacia Biotech. Frozen semen from various bulls was donated by Southeastern Breeders Service (Wellborn, FL, USA).
In vitro maturation and fertilization of oocytes
Oocyte maturation and fertilization were performed using procedures described earlier (Roth & Hansen 2004a). Briefly, ovaries were sliced and cumulus–oocyte complexes (COCs) were collected into a beaker containing OCM. COCs were washed and matured in groups of ten in 50 µl drops of OMM overlaid with mineral oil for 22 h at 38.5°C in an atmosphere of 5% (v/v) CO2 in humidified air. Groups of 30 COCs were then transferred to four-well plates containing 600 µl IVF-TALP per well and fertilized with 25 µl (~1 x 106) Percoll-purified spermatozoa supplemented with 25 µl 0.5 mmol/l penicillamine, 0.25 mmol/l hypotaurine and 25 µmol/l epinephrine in 0.9% (w/v) NaCl. After 18 h, putative zygotes were removed from fertilization wells, denuded of cumulus cells by vortexing COCs with 100 µl hyalurinidase (1000 U/ml in 1 ml Hepes-TALP medium for 5 min), and washed two or three times in Hepes-TALP. Matured oocytes were harvested after 22 h of maturation and putative zygotes were collected 18 h after fertilization for further examination.
Effect of heat shock during maturation on nuclear maturation and apoptosis
Freshly collected COCs were placed in maturation drops as described earlier and cultured for 22 h at either 38.5°C for 22 h or 40 or 41°C for 12 h followed by 38.5°C for 10 h. The period of 12 h was chosen because this duration of heat shock caused changes in oocyte competence for embryonic development in an earlier study (Edwards & Hansen 1997) and because the period of elevated body temperatures during heat stress can be that long (Rivera & Hansen 2001). The gaseous atmosphere was CO2 in humidified air. The percent CO2 was adjusted to ensure that the concentration of dissolved CO2 was similar between treatments and to maintain pH at ~7.4 (5, 6 and 7% for 38.5, 40 and 41°C respectively). Matured oocytes were harvested after 22 h of maturation and denuded of cumulus cells by vortexing COCs with 100 µl hyaluronidase (1000 U/ml in 1 ml Hepes-TALP medium for 5 min) and processed for TUNEL and Hoechst labeling. In particular, oocytes were removed from culture medium, washed three times in 100 µl drops of 10 mmol/l KPO4, pH 7.4 containing 0.9% (w/v) NaCl (PBS) and 1 mg/ml PVP (PBS-PVP), fixed in 4% (w/v) paraformaldehyde in PBS for 1 h at room temperature, and stored in PBS-PVP at 4 °C for up to 2–3 weeks before assay. The experiment was replicated six times using 163–212 oocytes per treatment.
The procedure for duallabeling of DNA using Hoechst 33342 and DNA fragmentation using the TUNEL procedure was as described by Roth & Hansen (2004a). Briefly, oocytes were permeabilized in 100 µl drops of 0.1% (v/v) Triton X-100 containing 0.1% (w/v) sodium citrate in PBS for 30 min at room temperature. Specimens were then incubated in 50 µl drops of TUNEL reaction mixture for 1 h at 37 °C in the dark, washed in PBS-PVP, and transferred to 50 µl drops of 1 µg/ml Hoechst 33342 in PBS-PVP for 30 min at room temperature. Each TUNEL procedure contained samples treated with RQ1 RNase-free DNase (50 U/ml) at 37 °C for 1 h as a positive control and oocytes or embryos incubated in the absence of the terminal deoxynucleotidyl transferase as a negative control. Labeling was observed using a Zeiss Axioplan fluorescence microscope (Carl Zeiss, Inc., Göttingen, Germany). Images were acquired using AxioVision software and an AxioCam MRm digital camera (Zeiss). Each oocyte was evaluated for the stage of meiosis and for the presence of TUNEL labeling of chromatin.
Effect of S1P on nuclear maturation
For three replicates of the above experiment, the ability of S1P to prevent effects of a 41 °C heat shock on nuclear maturation was tested by performing maturation in medium with either 50 nmol/l S1P or an equivalent amount of vehicle (0.1% (v/v) methanol). A total of 56–80 oocytes per treatment were examined.
Effects of heat shock during maturation on cytoskeletal organization
COCs were placed in maturation drops and cultured for 22 h at either 38.5°C for 22 h or 41°C for 12 h followed by 38.5°C for 10 h as described above. Oocytes were then harvested, denuded of cumulus cells, and processed for localization of actin, tubulin and DNA. A total of 33–54 oocytes per treatment were analyzed.
For localization, oocytes were fixed in 3.7% (v/v) formaldehyde in PBS for 10 min at 39°C, washed three times in PBS-PVP and stored in PBS-PVP at 4 °C for up to 2 weeks. Samples were then permeabilized with 0.1% (v/v) Triton X-100 in PBS for 5 min followed by three washes with PBS-PVP. To block nonspecific binding, samples were preincubated in 10% (v/v) normal goat serum in PBS (PBS + S) at room temperature for 30 min. Samples were incubated for 30 min in a labeling solution that consisted of 120 µl phalloidin conjugated to Alexa Flour 594, 40 µl mouse anti-bovine -tubulin labeled with Zenon Alexa Fluor 488 and 40 µl 5 µg/ml Hoechst 33342 in PBS + S. The phalloidin conjugated to Alexa Flour 594 was prepared by dilution of 5 µl 200 U/ml methanolic phalloidin in a final volume of 200 µl PBS + S. The anti-tubulin was labeled with Zenon Alexa Flour 488 by incubation of 1 µg anti--tubulin (200 µg/ml stock solution in PBS containing 1% (w/v) BSA) with 5 µl Zenon IgG labeling reagent for 5 min at room temperature followed by incubation of the reaction mixture with 5 µl of blocking reagent (from the labeling kit). Following incubation of specimens with the labeling mixture, slides were washed three times in PBS + S, fixed again in 3.7% (v/v) formaldehyde for 15 min at room temperature, washed three times in PBS-PVP and placed on a glass slide with a cover slip mounted with 5 µl ProLong Antifade solution. Negative controls were stained similarly except that phalloidin was omitted from the reaction mixture and 1 µg IgG1k was used instead of 1 µg anti--tubulin for preparation of the antibody-Zenon complex. Specimens were viewed using a Zeiss Axioplan 2 epifluorescent microscope connected to an AxioCam MRm digital camera and images were acquired using AxioVision software (Carl Zeiss).
Effect of heat shock during maturation on fertilization
COCs were matured at either 38.5°C for 22 h or 41°C for 12 h followed by 38.5°C for 10 h as described earlier. Thereafter, oocytes were fertilized at 38.5°C in an atmosphere of 5% CO2 in humidified air. After 18 h, putative zygotes were removed from fertilization wells, denuded of cumulus cells with hyaluronidase, and processed for Hoechst staining of DNA as described above. A total of 46–61 oocytes per treatment were analyzed.
Statistical analysis
The CATMOD procedure of SAS (SAS System for Windows, Release 8.20; Cary, NC, USA) was used to determine whether treatments affected the distribution of oocytes into various classes of nuclear maturation as well as the proportion of oocytes that were apoptotic.
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Results |
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). Heat shock affected (P < 0.001) the distribution of oocytes into these different classes (Fig. 2). In particular, a higher proportion of oocytes matured at 38.5°C reached MII (characterized by a metaphase plate and formation of the first polar body; see Fig. 1e) than oocytes matured at 40 and 41°C. Since heat shock reduced the proportion of oocytes that reached MII, there was a corresponding increase in the proportion of heat-shocked oocytes at other stages. For oocytes at 40°C, oocytes that were arrested were distributed in approximately equal numbers at the various stages of meiosis (Fig. 2). For oocytes at 41°C, however, more arrested oocytes were at MI than at later stages (Fig. 2).
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). As illustrated in Fig. 1f–j
, TUNEL-positive chromatin was observed at all stages of nuclear maturation.
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). There was a temperature xS1P interaction (P < 0.001) on distribution of oocytes into nuclear classes because S1P blocked the effect of heat shock on progression to MII. As illustrated in Fig. 5, S1P also blocked the increase in percentage of oocytes that were classified as apoptotic based on TUNEL assay (temperature x treatment, P < 0.005).
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The pattern of microfilament localization was affected by stage of nuclear maturation and by heat shock. Oocytes at the MI stage were characterized by condensed chromatin, a large metaphase plate and lack of a polar body (for representative picture see Fig. 1b and g). At this stage, microfilaments were observed within the oocyte cytoplasm but did not surround the pronucleus (Fig. 6a and 6a). At MII stage, the polar body was present and microfilaments were associated with this structure (Fig. 6e and 6e). Actin microfilaments were more distinct in the cytoplasm of heat-shocked oocytes than in oocytes cultured at 38.5°C (compare Fig. 6a and Fig. 6a). An intense ring of actin was present under the plasma membrane in oocytes matured at 38.5°C (Fig. 6a, c and e). Microfilaments were also observed to transverse the zona pellucida of this group of oocytes. In contrast the pericellular actin ring and trans-zonal actin processes were generally absent for oocytes matured at 41°C (Fig. 6a and 6e). Microtubules were identified within the meiotic spindle of pronuclei at MI, AI, TI and MII stages (Fig. 6, all images) and, for MII oocytes, in the first polar body (Fig. 6f and 6f).
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for examples). Rather, 76% of the heat-shocked oocytes at MI had abnormal spindles. For some oocytes, spindles had a rounded shape and some unaligned chromosomes (Fig. 7b), while for others spindles were of amorphous shape and with a large degree of disorganization of chromosomal alignment (Fig. 7c).
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). The percentage of putative zygotes with a normal pattern of two pronuclei was higher for oocytes that matured at 38.5°C than for oocytes matured at 41°C (for representative picture see Fig. 8a–c). Conversely, the proportion of oocytes that were unfertilized was higher for oocytes at 41°C. These unfertilized oocytes were observed to be at all stages of nuclear maturation from MI through MII (for examples, see Fig. 8d–f). The small subset of oocytes that had more than two pronuclei or were polyspermic was of similar abundance for oocytes at 38.5 and 41°C (see Fig. 8g–i for example).
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Thermal stress in vivo during oocyte maturation has been previously shown in mice to compromise the ability of oocytes to progress through meiosis and form embryos capable of developing to the blastocyst stage (Baumgartner & Chrisman 1981, Matsuzuka et al. 2004). Exposure of oocytes maturing in vitro to 43°C also blocks meiotic progression in mice (Kim et al. 2002). The temperatures used here to test effects of heat shock on maturation in vitro are much more physiologically relevant than the 43°C used by Kim et al.(2002); average maximal rectal temperatures in heat-stressed lactating cows experiencing infertility ranged from 40.1 to 40.5°C (Roth et al. 2000). Because a temperature as low as 40°C was sufficient to reduce meiotic progression in this study, effects of heat shock seen in vitro are likely to also occur in heat-stressed cows. Nonetheless, further experiments are necessary to determine whether this is the case. Exposure of oocytes to 41°C had more severe effects on meiosis since oocytes were less likely to pass MI after exposure to 41°C than oocytes exposed to 38.5 or 40°C.
Actions of heat shock on progression of the maturing oocyte through meiosis are the proximal cause for the reduction in fertilization rate for oocytes matured at 40 and 41°C as compared with oocytes at 38.5°C (present results and Roth & Hansen 2004a,b). Heat shock causes several changes in oocyte function that could contribute to the inhibition in progression through meiosis. Protein synthesis is required for nuclear maturation (Tatemoto & Horiuchi 1995) and heat shock can reduce protein synthesis by the oocyte (Edwards & Hansen 1996, 1997). Microtubules are critical for meiotic division (Brunet et al. 2003) as are microfilaments, which play a pivotal role in the migration of the MI spindle to the plasma membrane and extrusion of the first polar body and rotation of the MII plate before activation (Gallicano 2001). Effects of heat shock on microfilament organization in the present study were apparent as a decrease in membrane-associated microfilaments and a corresponding increase in cytoplasmic actin. Disruption of microtubules by heat shock was indicated by the increase in the frequency of deformed spindle apparatuses. A similar effect of heat shock on membrane-associated actin was reported for bovine two-cell embryos (Rivera et al. 2004a) and heat-shock-induced alterations in the spindle apparatus have been reported in matured porcine oocytes (Ju & Tseng 2004) and parthenogenetically activated bovine oocytes (Tseng et al. 2004).
Progression of meiosis is controlled by the spindle checkpoint mechanism that ensures proper chromosome segregation (Brunet et al. 2003). Incorrect chromosome positioning or improper attachment to the spindle microtubule activates the spindle checkpoint and delays onset of anaphase by inhibition of anaphase-promoting complex/cyclosome (Zhou et al. 2002, Cleveland et al. 2003). Checkpoint mechanisms could theoretically be engaged as a result of heat shock. Arrested oocytes at 41°C were more likely to be at MI than at later stages, which supports the idea that heat shock at this temperature activates the spindle checkpoint mechanism. However, the anaphase checkpoint is not likely to be the only mechanism affected at 40°C because heat-shocked oocytes at this temperature that failed to progress to MII were blocked at several stages. A checkpoint monitoring the anaphase-to-telophase transition has also been described in yeast (Muhua et al. 1998) and perhaps this mechanism is also activated by heat shock.
While not studied here, it is also possible that heat shock can inhibit the onset of meiosis by interfering with germinal vesicle breakdown. However, there was no effect of heat shock at the germinal vesicle stage on the proportion of roscovitine-treated bovine oocytes that completed germinal vesicle breakdown (Payton et al. 2004).
The fact that resumption of meiosis was attenuated by heat shock in a parallel manner with induction of oocyte apoptosis suggests that more than one mechanism is involved in heat-shock-induced disruption of oocyte competence and confirms the earlier finding of Roth & Hansen (2004a) that heat shock during maturation induces apoptosis mediated by caspase activation in bovine oocytes. Apoptosis appears to be the key event that leads to arrest of fertilization failure (and presumably nuclear arrest). This conclusion is based on findings that effects of heat shock on nuclear maturation can be blocked by inhibition of apoptosis, either by addition of a z-DEVD-fmk, an inhibitor of group II caspases, as described by Roth & Hansen (2004a) or by addition of S1P, as reported here for meiotic progression and earlier for cleavage (Roth & Hansen 2004b).
It is possible that alterations in the cytoskeleton caused by heat shock serve as a trigger for apoptosis. Anti-micro-tubule agents are known to promote apoptosis of tumor cells (Wang et al. 1999, Masuda et al. 2003). Alternatively, alterations in cytoskeletal architecture may be the result of activation of execution caspases. If the former possibility is true (cytoskeletal changes induce apoptosis), these changes in cytoskeleton induced by heat shock are not capable of preventing fertilization in the absence of apoptosis (Roth & Hansen 2004a). Since one would presume that fertilization is unlikely in the absence of nuclear maturation, one must conclude that either heat-shocked oocytes treated with apoptosis inhibitor do not experience a disruption of the cytoskeletal architecture or that these changes become reversed and the oocyte eventually completes nuclear maturation. Interestingly, the bovine two-cell embryo is capable of development to the eight-cell stage after heat shock despite extensive changes in organellar structure (Rivera et al. 2004b).
That S1P prevents the effect of heat shock on nuclear maturation provides evidence that alterations in nuclear maturation and apoptosis are linked features of the oocyte response to heat shock. S1P is a sphingomyelin metabolite that regulates a wide variety of cellular processes including growth, survival and cytoskeleton rearrangement (Pyne & Pyne 2000) and which is involved in maturation of porcine (Lee et al. 2003) and bovine oocytes (Roth & Hansen 2004b). Involvement of S1P in cytoskeletal rearrangement is mediated by a family of specific G protein-coupled receptors called S1P1–5 receptors. For example, binding of S1P to S1P1 receptor mediated cortical actin assembly and Rac activation (Spiegel & Milstien 2002). Binding of S1P to S1P2 and S1P3 induces stress fiber formation and activation of Rho family proteins that are important for cytoskeleton rearrangement (Okamoto et al. 2000). Thus, S1P could improve nuclear maturation in the face of heat shock by affecting the cytoskeleton. In addition, the thermoprotective action of S1P may involve anti-apoptotic effects also because S1P counteracts the pro-apoptotic effects of ceramide (Cuvillier et al. 1998).
Segregation errors during either the first or the second meiotic division can result in a chromosomally abnormal embryo. For example, oocytes of mice lacking the Formin homology gene (Fmn2–/–), which is required for progression through metaphase, cannot correctly position the metaphase spindle during MI and cannot form the first polar body. Fertilization of Fmn2–/–oocytes resulted in formation of a polyploid embryo and pregnancy loss (Leader et al. 2002). Moreover, postimplantation embryos produced by mice exposed to thermal stress during the periovulatory period had a higher incidence of chromosomal abnormalities (Baumgartner & Chrisman 1988). To verify whether this is the situation in heat-shocked bovine oocytes, the effect of heat shock on nuclear status in one-cell stage embryos was determined at 18 h after fertilization. Only a few oocytes matured at 41°C had more than two pronuclei or were polyspermic. The majority of heat-shocked oocytes failed to undergo fertilization and were blocked at the MI or through MII stages.
Taken together, these findings indicate that disruption in resumption of meiosis caused by heat shock is associated with oocyte apoptosis and cytoskeletal modifications. These alterations are likely to be involved in the mechanism underling heat-shock-induced disruption of oocyte competence and the reduction in fertility of heat-stressed females.
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Footnotes |
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Received 28 June 2004
First decision 27 August 2004
Revised manuscript received 27 September 2004
Accepted 12 November 2004
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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