Hum. Reprod. Advance Access originally published online on March 25, 2008
Human Reproduction 2008 23(6):1377-1384; doi:10.1093/humrep/den096
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Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice
Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan
1 Correspondence address. Tel: +81-4-7136-5424; Fax: +81-4-7136-3698; E-mail: aokif{at}k.u-tokyo.ac.jp
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Abstract |
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BACKGROUND: Mammals have two types of full-grown oocytes: those with germinal vesicles (GVs) in which the chromatin is condensed and surrounds the nucleolus (surrounded-nucleolus (SN)-type) and those in which the chromatin is less condensed and does not surround the nucleolus (non-surrounded-nucleolus (NSN)-type). Although SN oocytes possess higher meiotic and developmental competence than NSN oocytes, the factors underlying this difference are unknown.
METHODS AND RESULTS: The GVs of murine SN and NSN oocytes were exchanged by nuclear transfer and the nucleus/cytoplasm of each reconstructed oocyte was classified as follows: SN/SN, NSN/SN, SN/NSN or NSN/NSN. After reconstruction, the meiotic maturation and preimplantation development of the oocytes were analysed. Few mature SN/NSN and NSN/NSN oocytes were observed (20–26%). In contrast, 88% of the NSN/SN oocytes matured; however, they rarely developed to the blastocyst stage after fertilization (4%), whereas most of the SN/SN oocytes matured (84%) and reached the blastocyst stage (83%). When the metaphase II (MII) plates of in vitro-matured NSN/SN oocytes were transferred into enucleated MII oocytes in which the contents of the SN-type GVs were spread into the cytoplasm, they completed full-term development.
CONCLUSIONS: The differences in meiotic and developmental competence between SN and NSN oocytes are determined by factors in the cytoplasm and nucleus, respectively. In addition, material(s) within SN-type GVs, and not the chromatin configuration itself, is essential for full-term development.
Key words: chromatin configuration/developmental competence/meiotic competence/oocyte
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Introduction |
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The oocytes of female mice grow within the ovaries, where they develop large nuclei known as germinal vesicles (GVs), but the cells are arrested in prophase of meiosis I. In response to hormonal stimulation or upon removal from the ovaries, the full-grown oocytes (FGOs) resume meiosis; specifically, they undergo GV breakdown (GVBD) and subsequent emission of the first polar body (1st PB), and are then arrested at metaphase of meiosis II (MII). After fertilization, the second meiosis is completed and two pronuclei containing the maternal or paternal genome are formed. Finally, a blastocyst is formed in utero from the fertilized oocytes prior to implantation.
During their growth, oocytes synthesize and accumulate a large number of mRNAs and proteins required for meiotic maturation and early embryonic development. Concomitant with their increase in size, oocytes acquire meiotic competence, which is the ability to resume and complete meiosis, and developmental competence, which is the ability to complete preimplantation development (Sorensen and Wassarman, 1976
; Eppig and Schroeder, 1989; Erdogan et al., 2005). However, some FGOs lack meiotic or developmental competence.
Two different chromatin configurations have been reported in murine FGOs (Mattson and Albertini, 1990; Debey et al., 1993). In the first type, which is known as the SN (surrounded-nucleolus)-type, the chromatin is highly condensed and surrounds the nucleolus. In the second type, known as the NSN (non-surrounded-nucleolus) type, the chromatin is less condensed and does not surround the nucleolus. All of the growing oocytes in mice less than 15 days old have NSN-type nuclei; thereafter, some of the nuclei become SN type, whereas others retain NSN-type nuclei even as FGOs (Zuccotti et al., 1995). Oocytes with the SN-type nucleus (SN oocytes) complete meiotic maturation at a high frequency, whereas the frequency of maturation for oocytes with the NSN-type nucleus (NSN oocytes) is low (Zuccotti et al., 1998, 2002; Liu and Aoki, 2002). A correlation between chromatin configuration and meiotic competence has been reported in several mammals, including humans (porcine, Sun et al., 2004; bovine, Liu et al., 2006; canine, Lee et al., 2006; monkey, Schramm et al., 1993; human, Combelles et al., 2002). Furthermore, in mice, SN oocytes can develop to the blastocyst stage after fertilization, whereas almost all NSN oocytes cannot (Zuccotti et al., 2002). Thus, SN, but not NSN, oocytes possess meiotic and developmental competence.
In addition to a difference in chromatin configuration, various other differences exist between murine SN and NSN oocytes. For example, phosphorylated centrosomes that nucleate short microtubules have been observed in SN oocytes (Wickramasinghe and Albertini, 1992; Can et al., 2003). A few microtubule organizing centers (MTOCs) form around the GVs of SN oocytes, whereas no typical MTOCs form in NSN oocytes (Debey et al., 1993; Can et al., 2003). In addition, the nucleoli of NSN oocytes are vacuolated and less compact than those of SN oocytes (Debey et al., 1993). The microvilli in the oolemma are also denser and shorter in SN oocytes (Cecconi et al., 2006). Moreover, NSN oocytes are transcriptionally active, whereas SN oocytes are transcriptionally inactive (Bouniol-Baly et al., 1999; Miyara et al., 2003). Finally, the extent of epigenetic modification such as DNA methylation, histone acetylation and histone methylation is greater in SN oocytes (Kageyama et al., 2007). Thus, several cytoplasmic, nuclear and epigenetic properties differ between SN and NSN oocytes; however, the factors underlying the differences in meiotic and developmental competence between these two types of oocytes are unknown.
In this study, to determine which factors in the cytoplasm or nucleus contribute to meiotic and developmental competence in FGOs, we exchanged the nuclei of SN and NSN oocytes. Our results indicate that meiotic competence is largely dependent on cytoplasmic factor(s), whereas developmental competence in FGOs depends on material in the GV.
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Collection, classification and culture of oocytes and embryos
Fully grown oocytes at the GV stage were obtained from 8- to 11-week-old B6D2F1 mice (CLEA Japan Inc., Tokyo, Japan) that had not been subjected to hormonal stimulation. The ovaries were removed from the mice and transferred to HEPES-buffered KSOM (synthetic oviductal medium enriched with potassium) (Lawitts and Biggers, 1993
) supplemented with 1 mg/ml bovine serum albumin (BSA; Sigma, St Louis, MO, USA) and 0.2 mM 3-isobutyl-1-methylxanthine (IBMX; Sigma–Aldrich, St Louis, MO, USA). The ovarian follicles were punctured with a 27-gauge needle, and the cumulus cells were gently removed from the cumulus–oocyte complexes using a narrow-bore glass pipette. Only those oocytes with a diameter greater than 75 µm were used in the following experiments. The oocytes were classified as SN or NSN type as described previously (Inoue et al., 2007). Briefly, GV-stage oocytes were incubated in 
-minimum essential medium (MEM) (Gibco–BRL, Grand Island, NY, USA) containing IBMX, 5% fetal bovine serum (FBS; Sigma–Aldrich), and 10 ng/ml epidermal growth factor (EGF; Sigma–Aldrich). After 1 h of incubation, some of the cells exhibited a perivitelline space (PVS). A very high correlation has been shown to exist between PVS formation and chromatin configuration. More than 90% of oocytes that form a PVS have a GV with the SN-type configuration, while all of the oocytes that lack a PVS have a GV with the NSN-type configuration (Inoue et al., 2007).
For in vitro maturation, the oocytes were washed in IBMX-free -MEM supplemented with 5% FBS and 10 ng/ml of EGF and incubated in a humidified atmosphere of 5% CO2/95% air at 38°C.
For IVF, the oocytes that had reached the MII stage after in vitro maturation were transferred to human tubal fluid (HTF) medium (Quinn and Begley, 1984) supplemented with 10 mg/ml BSA. Spermatozoa were obtained from the caudal epididymides of adult ICR male mice (SLC Japan Inc., Shizuoka, Japan). The oocytes were inseminated with spermatozoa that had been capacitated by preincubation for 2 h in HTF medium. Six hours after insemination, those fertilized oocytes with two pronuclei were washed and cultured in KSOM.
For parthenogenetic activation, the oocytes that had reached the MII stage after in vitro maturation were transferred to 10 mM SrCl2 in Ca2+-free Whitten's medium (Whitten, 1971) containing 5 µg/ml cytochalasin B (CB; Sigma–Aldrich) to obtain diploid embryos. After 90 min, the embryos were washed and cultured in Whitten's medium containing CB. Six hours after activation, the embryos were washed and cultured in KSOM.
Nuclear transfer
All micromanipulations were performed in HEPES-buffered KSOM supplemented with 1 mg/ml BSA. To enucleate a GV-stage oocyte, part of the zona pellucida was dissolved by slowly adding acidic MEMCO (Evans et al., 1995) with a glass pipette (inner diameter 5–10 µm) because the zona pellucida of the oocytes without PVS could not be cut with a sharp glass needle or a Piezo impact-driven micromanipulator (Prime Tech Ltd, Ibaraki, Japan). After treatment, the oocytes were incubated in HEPES-buffered KSOM containing 0.2 mM IBMX, 10 µg/ml CB and 0.1 µg/ml colcemid (Sigma) at 38°C for 15 min before aspiration of the GV. The GV was removed with minimal cytoplasm and fused with an enucleated oocyte using Sendai virus (HVJ; Ishihara Sangyo Co., Ltd, Osaka, Japan). The manipulated oocytes were cultured in -MEM containing IBMX for 1 h to ensure complete fusion.
For MII plate transfer, ovulated MII-stage oocytes were obtained from the oviducts of 3-week-old B6D2F1 mice that had been superovulated by injection with 5 IU of pregnant mare's serum gonadotropin (ASKA Pharmaceutical Co., Ltd, Tokyo, Japan), followed 48 h later by 5 IU of HCG (ASKA Pharmaceutical Co., Ltd). The oocytes were enucleated in HEPES-buffered KSOM containing 5 µg/ml of CB. Donor MII plates were collected from oocytes that had extruded their 1st PBs after in vitro maturation and transferred into enucleated MII oocytes using Sendai virus. The manipulated oocytes were cultured in -MEM for 60–90 min to ensure complete fusion.
Embryo transfer
Embryos that had developed to the blastocyst stage in vitro were transferred into the uterine horns of 2.5-day-postcoitus (dpc) pseudopregnant ICR females (SLC Japan Inc.). All females were killed at 19.5 dpc and the numbers of implantation sites and pups were recorded. The pups were raised by lactating ICR females. The body weights of the pups were measured weekly.
Immunocytochemistry
The oocytes were fixed in 3.7% paraformaldehyde in phosphate-buffered saline (PBS) for 1 h, washed with PBS containing 1 mg/ml BSA, permeabilized with 0.5% Triton X-100 for 15 min, incubated with 50 µg/ml RNase (Roche, Indianapolis, IN, USA) for 40 min, and then immunostained with a 1:100 dilution of the primary antibody against acetylated histone H4 (H4ac; Upstate Biotechnology Inc., Lake Placid, NY, USA) for 1 h at room temperature. The antibody was probed with a 1:50 dilution of a fluorescein isothiocyanate-conjugated anti-rabbit immunoglobulin (Ig) G (Jackson Immuno-Research, West Grove, PA, USA) for 1 h at room temperature. The oocytes were mounted on a glass slide in Vectashield anti-bleaching solution (Vector Laboratories, Burlingame, CA, USA) containing 100 µg/ml propidium iodide (Sigma–Aldrich). Fluorescence was detected under a laser-scanning confocal microscope (Carl Zeiss MicroImaging GmbH, Oberkochen, Germany).
Statistical analysis
Data were analysed by a 
2-test. A value of P < 0.05 was considered statistically significant.
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Meiotic competence of the GV-exchanged oocytes
To investigate whether a nuclear or cytoplasmic component is involved in determining meiotic competence in FGOs, GVs were exchanged between SN and NSN oocytes. First, the SN-type GV was transferred to an enucleated SN or NSN oocyte, and then the NSN-type GV was transferred to an enucleated SN or NSN oocyte. Thus, the following four types of reconstructed oocytes were created: SN nucleus/SN cytoplasm (SN/SN), SN nucleus/NSN cytoplasm (SN/NSN), NSN nucleus/SN cytoplasm (NSN/SN) and NSN nucleus/NSN cytoplasm (NSN/NSN). More than 85% of the reconstructed oocytes were alive after GV transfer in all groups. The reconstructed oocytes were transferred to IBMX-free medium and examined for GVBD and emission of the 1st PB after 4 and 16–17 h, respectively.
Our data indicate that the cytoplasm and not the nucleus is an important determinant of meiotic competence (Table I). Eighty percent of NSN/SN oocytes underwent GVBD. This value was slightly, but significantly (2 analysis, P < 0.05), lower than those of SN/SN (92%) and control SN oocytes (88%) that had not been subjected to nuclear transfer. However, meiotic competence in the NSN/SN oocytes seemed to be comparable to that in the SN/SN and control SN oocytes since the percentage of NSN/SN oocytes (88%) that extruded their 1st PB was not significantly greater than the percentages of SN/SN (84%) and control SN oocytes (82%). Thus, although some of the NSN/SN oocytes seemed to delay GVBD, they ultimately completed meiosis. In contrast, few oocytes with the NSN cytoplasm completed meiotic maturation (Table I). Only 5 and 3% of SN/NSN and NSN/NSN oocytes, respectively, underwent GVBD, and only 
20% of them showed 1st PB emission. These results demonstrate that meiotic competence is largely dependent on factor(s) in the cytoplasm, and not in the nucleus, of FGOs. We confirmed that the NSN-type GV transferred into SN cytoplasm did not change its chromatin configuration to the SN type after 2 h of incubation with IBMX following the completion of fusion (Fig. 1). In addition, since the global acetylation level of histone H4 is higher in SN oocytes than in NSN oocytes (Kageyama et al., 2007), we also examined the level of hyperacetylated histone H4 (H4ac) and confirmed that the acetylation level did not increase in NSN-type GVs after transfer into SN cytoplasm (Fig. 1).
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Developmental competence of GV-exchanged oocytes following in vitro maturation
After in vitro maturation, the SN/SN and NSN/SN oocytes that had extruded their 1st PBs were fertilized and observed for preimplantation development. No significant difference in fertilization rate was observed between the two types of reconstructed oocytes. Preimplantation development to the 4-cell stage was observed in significantly fewer (P < 0.05) fertilized NSN/SN oocytes than in SN/SN oocytes, and only one oocyte (4%) developed to the blastocyst stage (Table II and Fig. 2). In contrast, 83% of the fertilized SN/SN oocytes developed to the blastocyst stage; this is comparable to the percentage for the control SN oocytes, which were not subjected to GV transfer. To eliminate possible paternal effects, we also examined parthenogenetic embryos. Like the fertilized oocytes, parthenogenetically activated NSN/SN oocytes showed a low level of developmental competence, while the level of competence in the SN/SN oocytes was comparable to that in the controls (Table III). These results indicate that the difference in developmental competence between FGOs originates in the nucleus.
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Note that the morphology of the pronucleus differed between the SN/SN and NSN/SN embryos. Two types of pronuclei, which differed in the distribution of the nucleolus, were observed in the parthenogenetically activated 1-cell embryos: those with a single large nucleolus (mono-type) and those with several small nucleoli (multi-type). Nearly 80% of the 1-cell embryos derived from SN/SN and control oocytes had mono-type pronuclei, whereas mono-type pronuclei were observed in only 31% of those derived from NSN/SN oocytes (Fig. 3).
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Full-term development of oocytes with NSN-type GVs and SN-type GV material
We next analysed whether the low developmental competence of NSN/SN oocytes was caused by a lack of material(s) found in NSN-type GVs. The MII plate of a reconstructed oocyte that had matured to the MII stage was transferred into an enucleated MII oocyte obtained from the oviduct after hormonal stimulation (Fig. 4). The recipient MII oocyte contained GV materials in its cytoplasm since the nuclear membrane had been dissolved, allowing the contents of the GV to spread into the cytoplasm after GVBD (Fig. 4). After fusion of the MII plate from the NSN/SN or SN/SN oocyte with the recipient MII oocyte, the cells were inseminated. Fertilized oocytes with two pronuclei were culled and observed for preimplantation development (Table IV). Reconstructed embryos containing chromosomes from NSN/SN oocytes developed into blastocysts at a frequency that was comparable to those of SN/SN oocytes and control-ovulated oocytes, which had not been subjected to GV or MII plate transfer. Similar results were obtained when the reconstructed oocytes were parthenogenetically activated instead of being fertilized (data not shown). These results demonstrate that material(s) from the GVs of oocytes is responsible for the difference in developmental competence among FGOs. Note that the percentage of mono-type pronuclei increased in the NSN/SN embryos, i.e. 67 and 31% with and without MII plate transfer, respectively (data not shown).
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Following in vitro culture to the blastocyst stage, the embryos were transferred into the uterine horns of pseudopregnant females. Pups were obtained from NSN/SN embryos at a frequency similar to those from the SN/SN and control embryos (Table V). No abnormalities were observed in the pups from the NSN/SN embryos; their growth rates were normal (Fig. 5), and the animals were fertile (data not shown). Thus, SN-type chromatin is not essential for full-term development.
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Discussion |
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The results of this study show that the difference in meiotic and developmental competence between SN and NSN oocytes is determined by factors in the cytoplasm and nucleus, respectively. Therefore, the factors that determine meiotic and developmental competence in FGOs are likely different from each other. In addition, we were able to produce pups from NSN-type GVs by transferring them into the enucleated SN oocytes followed by MII plate transfer. This demonstrates that SN-type chromatin is not essential for full-term development following meiotic maturation and fertilization.
Previous studies have reported a high correlation between meiotic and developmental competence in mammalian oocytes. When the meiotic and developmental competence of oocytes was evaluated after sorting by chromatin configuration, cytoplasmic appearance, the characteristics of the surrounding cumulus cells and the position of the follicle in the ovary, an increased rate of development to the blastocyst stage was observed in those oocytes that had completed meiotic maturation with high frequency (Arlotto et al., 1996; Stojkovic et al., 2001; Zuccotti et al., 2002). These results suggest that the developmental competence is influenced by the process of meiotic maturation. However, in this study, NSN/SN oocytes exhibited higher meiotic competence but lower developmental competence (Table s I–III), indicating that oocytes with higher meiotic competence do not necessarily possess higher developmental competence. Therefore, the determining factor for developmental competence should be different from that for meiotic competence in FGOs. This idea is consistent with a previous study suggesting that the progression of nuclear maturation is independent of that of cytoplasmic maturation (Eppig et al., 1994). Metaphase I (MI)-arrested oocytes that had failed to complete meiotic maturation were shown to be able to develop into blastocysts after fertilization (Eppig et al., 1994).
Our data indicate that a cytoplasmic factor(s) determines meiotic competence in FGOs (Table I), which is consistent with the findings of several previous studies. Kono et al. (1996) demonstrated that reconstructed FGOs whose GVs were replaced with a nucleus from a non-growing oocyte in 1-day-old mice extruded their 1st PB at a high frequency. Furthermore, Ogushi et al. (2005) reported that in enucleated porcine oocytes, the kinetics of CDK1 and mitogen-activated protein kinase activity was similar to that in intact oocytes during meiotic maturation. Therefore, a cytoplasmic factor seems to determine meiotic competence, although a correlation between chromatin configuration and meiotic competence has been reported (Schramm et al., 1993; Zuccotti et al., 1998; Combelles et al., 2002; Sun et al., 2004; Lee et al., 2006; Liu et al., 2006). NSN-type chromatin becomes SN-type chromatin around the time of antrum formation (Mattson and Albertini, 1990; De La Fuente, 2006). Thus, oocytes may acquire the cytoplasmic factor(s) involved in meiotic competence coincident with the transition to large-scale chromatin configuration, resulting in a correlation between chromatin configuration and meiotic competence.
Our results also suggest that GV material(s) determines the developmental competence of oocytes, and that the SN-type, but not NSN-type, GVs contain it. The NSN/SN oocytes in which GVs from NSN oocytes had been transferred into the cytoplasm of SN oocytes matured to the MII stage, but after fertilization, they rarely developed to the blastocyst stage (Table II). When MII plates of NSN/SN oocytes that had matured to the MII stage were transplanted into the cytoplasm of MII-stage oocytes, the reconstructed oocytes showed a high developmental competence comparable to that of control MII oocytes after fertilization (Table s IV and V), suggesting that GV materials that had been spread into cytoplasm after the breakdown of SN-type GVs support embryonic development. However, in this experiment, in vivo-ovulated MII oocytes were used as the recipients of MII plates. Since such in vivo-ovulated oocytes possess higher developmental potential compared to in vitro-matured oocytes, their cytoplasm might support the development of the MII-plate-transplanted oocytes. However, this possibility can be excluded. When the MII plates of NSN/SN oocytes were transferred into in vitro-matured and -enucleated MII oocytes, 76% of the reconstructed oocytes developed into blastocysts after fertilization. This figure was comparable to the 67% of control in vitro-matured oocytes that had not been subjected to GV or MII plate transfer. After transfer into the uterine horns of pseudopregnant females, pups were obtained from NSN/SN embryos.
Several small nucleoli were observed among the pronuclei of NSN/SN embryos (Fig. 3), and the number of nucleoli decreased when GV materials were provided, suggesting that NSN-type GVs may lack some factor(s) responsible for nucleolar organization in 1-cell embryos. Since the nucleoli of NSN-type GVs are assembled in FGOs, the factor responsible for nucleolar organization in 1-cell embryos may be different from that in the GVs of oocytes. Previous reports have shown a correlation in human embryos between the distribution of the nucleoli in pronuclei and developmental competence (Tesarik and Greco, 1999; Gianaroli et al., 2003). In our study, we also observed the association between nucleolar organization in pronuclei and developmental competence. Therefore, the disorganization of the nucleoli in the pronuclei might cause incomplete preimplantation development. Indeed, a loss of developmental competence was observed in Npm2-null mouse embryos with disorganized nucleoli (Burns et al., 2003). A recent study also demonstrated that 1-cell embryos which had been enucleolated at GV stage did not form nucleoli in their pronuclei and showed a failure of embryonic development (Ogushi et al., 2008). However, the possibility exists that nucleolar disorganization in the pronuclei may not affect subsequent development and that oocytes may instead acquire the factors responsible for nucleolar organization, coincident with the switch from NSN- to SN-type configuration.
Genomic imprinting, which affects parent-specific expression, is established during oocyte growth. Bisulfate analysis revealed that differentially methylated regions of maternally imprinted genes are gradually methylated during growth (Lucifero et al., 2004; Hiura et al., 2006). Methylation is complete in the oocytes of 25-day-old mice, but not in those of 15-day-old mice (Lucifero et al., 2004). When the GVs of growing murine oocytes aged 1–15 days were transferred to enucleated FGOs and subsequently subjected to MII plate transfer after in vitro maturation, no pups were obtained (Kono et al., 1996; Bao et al., 2000). However, when GVs from growing oocytes aged 16–20 days and FGOs from adult (6- to 8-week-old) mice were used as donors, the percentage of live pups increased with the age of the donor mice (Bao et al., 2000). Since growing oocytes with SN-type chromatin first appear in ovaries around 16 days after birth and the percentage of SN oocytes increases thereafter (Inoue et al., 2007), chromatin configuration seems to be involved in establishing the genomic imprints. However, in the present study, when NSN-type GVs from adult mice were used as donors for nuclear transfer to enucleated SN oocytes, we obtained pups at a frequency similar to that of when SN-type GVs were used as donors (Table V). This indicates that DNA methylation during genomic imprinting occurs independently of the change in chromatin configuration in the GVs.
Incomplete meiotic maturation or embryonic development failure is one of the major causes of human infertility (Hartshorne et al., 1999; Levran et al., 2002; Neal et al., 2002; St John, 2002). Although the mechanisms underlying these types of infertility have not been clarified, they are likely caused by a failure to produce oocytes that possess meiotic and developmental competence. Our data may lead to treatments for patients with these types of infertility based on the transfer of GVs from their FGOs to enucleated ones possessing both types of competence, followed by subsequent MII plate transfer, although some biological and ethical concerns remain (De Rycke et al., 2002; Hawes et al., 2002). To our knowledge, this is the first study to demonstrate that pups can be obtained using GVs without the SN-type configuration, which has been reported to be associated with meiotic and developmental competence.
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This work was supported by Ministry of Education, Science, and Culture Grants HD 17380166 (to FA).
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Submitted on November 7, 2007; resubmitted on February 14, 2008; accepted on March 4, 2008.
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