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BOR - Papers in Press, published online ahead of print October 17, 2002.
Biol Reprod 2002, 10.1095/biolreprod.102.007906
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BIOLOGY OF REPRODUCTION 68, 651–654 (2003)
DOI: 10.1095/biolreprod.102.007906
© 2003 by the Society for the Study of Reproduction, Inc.

Embryo

MuERV-L Is One of the Earliest Transcribed Genes in Mouse One-Cell Embryos1

Daisuke Kigamia, Naojiro Minami2,a, Hanae Takayamaa, and Hiroshi Imaia

a Laboratory of Reproductive Biology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The expression pattern and function of the murine endogenous retrovirus-like (MuERV-L) gene in mouse preimplantation embryos was investigated. MuERV-L was rapidly transcribed from the beginning of S phase (8 h after fertilization) in the first cell cycle. MuERV-L expression was completely repressed when transcription from the zygotic genome was inhibited by {alpha}-amanitin. These results reveal that MuERV-L is transcribed from the zygotic genome and that it is expressed earlier than any other genes previously reported. In addition, MuERV-L was expressed even when the first round of DNA synthesis was inhibited by aphidicolin, suggesting that its expression is controlled by the zygotic clock. The function of MuERV-L in the development of mouse embryos was also examined using antisense oligonucleotides. The developmental competence of embryos was markedly suppressed after the 4-cell stage when they were treated with antisense oligonucleotides. This result suggests that MuERV-L plays an important role in the development of mouse embryos at the early preimplantation stage.

developmental biology, early development, embryo, gene regulation


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In mouse embryos, the onset of zygotic genome activation (ZGA) has been shown to occur during the 1-cell stage [1]. Maternal mRNAs are progressively degraded following fertilization until the 2-cell stage [2–4], when ZGA becomes clearly evident [5]. For the first time, we demonstrate that transcription appears to be coupled to translation at the 2-cell stage [6] when synthesis of zygotic proteins begins [7]. ZGA, which occurs through the S/G2 phase of the first cell cycle to the G2 phase of the second cell cycle, involves a 2-step process, and maternal transcripts continue decreasing through the second activation phase [3, 8]. In mice, a minor ZGA phase is initiated at the late 1-cell stage (G2 phase) with very weak transcriptional activity [1, 9–14]. Next, some of the proteins are synthesized at the early 2-cell stage (G1/S phase) for the next, major phase of ZGA, which occurs at the late 2-cell stage (G2 phase). The major phase of ZGA is characterized by a sharp transcriptional activation and increase of translational activity followed by a dramatic change in the pattern of protein synthesis [5, 7, 15–18]. However, the molecular mechanisms of the minor and major phases of ZGA remain unknown.

In mouse embryos, several methods have been used to investigate patterns of gene expression. The generation of cDNA libraries for preimplantation embryos at different stages of development, coupled with subtraction hybridization methods [19], has made it possible to identify the genes that are transiently expressed at each developmental stage. The mRNA differential display method, as adapted for mammalian embryos [20–23], provides an ideal approach to identifying genes whose expressions increase or decrease in a transient manner. Using various methods, U2afbp-rs, hsp70.1, mTEAD-2, and eIF-4C were identified as rapidly expressed genes in early preimplantation development [13, 20, 24–26]. In the absence of appropriate activation of the zygotic genome, the embryo fails to develop further [27], thus ZGA is likely to be one of the first critical events in mouse preimplantation embryos.

During analysis of mouse preimplantation embryos, we identified a gene that was increasingly expressed at the G2 phase of the second cell cycle, the murine endogenous retrovirus-like (MuERV-L) gene. Early transcription of MuERV-L was recently reported in 2-cell stage nuclei, however, its expression at the early 1-cell stage has not been examined [28]. In the present study, to investigate the timing of the onset of ZGA, we examined the expression pattern and the function of MuERV-L in the mouse preimplantation embryo. It thus appeared that the expression of MuERV-L might help to clarify the timing of the onset of ZGA.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
In Vitro Fertilization and Embryo Culture

In vitro fertilization (IVF) and embryo culture were carried out as previously described [22]. Briefly, 3- to 5-wk-old female Crj:CD-1(ICR) mice (Charles River Japan Inc., Tokyo, Japan) were superovulated with eCG and hCG. Ovulated oocyte-cumulus complexes were collected from ampullae of the oviduct 15 h after hCG injection and placed in a 200-µl droplet of fertilization medium. Five hours after insemination, fertilized eggs were washed three times with modified Whitten medium containing polyvinyl pyrrolidine (PVP) (m-WM-PVP) and cultured in 50 µl of m-WM-PVP with an ampulla. All incubations were performed in a humidified atmosphere containing 5% CO2 and 95% air at 37°C.

All animal experiments were performed in accordance with the institutional animal care and use committee and the Guide for Care and Use for Laboratory Animals as adopted and promulgated by the Society for the Study of Reproduction.

Analysis of DNA Replication

To detect initiation of DNA replication at the 1-cell stage, 1-cell embryos were incubated for 5, 6, 7, or 8 h after IVF in culture medium containing 100 µM 5-bromodeoxyuridine (BrdU) (1296736; Roche Diagnostics Corp., Indianapolis, IN) for 1 h, and then fixed in 100% methanol for 15 min at room temperature. After fixation, embryos were transferred to 2% Triton-X 100 in PBS for 10 min and then incubated in 4 N HCl solution for 2 h at room temperature. BrdU incorporation was detected using a primary anti-BrdU mouse monoclonal antibody (Roche) and a fluorescein isothiocyanate-labeled secondary anti-mouse-immunoglobulin antibody (Roche) according to the instructions of the manufacturer. Fluorescence was detected with a fluorescence microscope (BX50, Olympus, Japan).

Alpha-Amanitin and Aphidicolin Treatment

Alpha-amanitin (161284; Roche) was used to inhibit mRNA synthesis from the zygotic genome at a concentration of 11 µg/ml. A concentrated stock solution of {alpha}-amanitin was dissolved in PBS at 1 mg/ml and stored at -20°C. Aphidicolin (A0781; Sigma Chemical Co., St. Louis, MO) was used to inhibit DNA replication at the 1-cell stage at a concentration of 1.5 µg/ml. A concentrated stock solution of aphidicolin was prepared in dimethyl sulfoxide at 1 mg/ml and stored at -20°C. One-cell embryos were incubated with each of the chemicals from 7 to 23 h after IVF.

Antisense Treatments

The phosphorothioate-modified antisense oligodeoxynucleotide (S-oligo) for the MuERV-L gene used in this study was designed to be complementary to 20 bases, including the initiation codon of the MuERV-L mRNA. The sequence of the antisense MuERV-L S-oligo was 5'-GATTCATCCTTGTACTTCTG-3', which hybridizes to nucleotides 525 to 544 of MuERV-L mRNA (GenBank accession number Y12713) containing the start codon. The randomized sequence oligo (nonsense S-oligo) has the same base composition as the antisense MuERV-L S-oligo. The sequence of the nonsense S-oligo was 5'-ATGGTATTCGCCCTTTCATT-3'. The sequence of the sense S-oligo, 5'-CAGAAGTACAAGGATGAATC-3', is complementary to the antisense MuERV-L S-oligo. Both the nonsense and sense S-oligos were used as controls.

Oligofectamine reagent (12252-011; Invitrogen, Carlsbad, CA) was used to transfect oligonucleotides into embryos. Oligofectamine reagent interacts spontaneously with oligonucleotides to form transfection complexes. Four ml of 25 µM stock oligonucleotides was mixed with 86 µl of m-WM-PVP (without antibiotic agents). Three µl of oligofectamine reagent was mixed with 7 µl of m-WM-PVP (without antibiotic agents) and incubated at room temperature for 5–10 min. Diluted oligofectamine reagent and diluted oligonucleotide were mixed gently, and then incubated at room temperature for 15–20 min. The mixture was added to 100 µl of m-WM-PVP (without antibiotic agents). Five hours after IVF, 1-cell embryos were placed in 200 µl of culture medium containing the complex (without antibiotic agents) for 4 h. These embryos were washed twice with m-WM-PVP and transferred into 50 µl of m-WM-PVP and then cultured for 5 days.

Embryo Collection

Fifty embryos at 5, 8, 10, 12, 14, and 17 h after IVF and 50 embryos treated with oligonucleotide (antisense, nonsense, or sense S-oligo) were collected and used for semiquantitative reverse transcriptase-polymerase chain reaction (RT-PCR). Fifty embryos at the 2-cell, 4-cell, morula, and blastocyst stages and 50 embryos treated with {alpha}-amanitin or aphidicolin were collected 23 h after IVF and used for RT-PCR. The collected embryos in <5 µl of culture medium were frozen in liquid nitrogen and stored at -80°C until use (for 1 mo at most).

RT-PCR and Semiquantitative PCR

Total RNA was isolated from each of the 50 embryos using an RNA isolation kit (Stratagene, La Jolla, CA) according to the manufacturer's instructions. Before RNA was extracted from the embryos, 5 ng of rabbit {alpha}-globin mRNA was added as an internal control. Briefly, total RNA was resuspended with 50 µl diethylpyrocarbonate-treated water, treated with DNase for 30 min at 37°C, extracted with phenol/chloroform, ethanol precipitated with 2.5 µl of glycogen (20 mg/ml), and reverse transcribed in 20 µl of reaction solution using random primers (Invitrogen) and Superscript II (200 units, Invitrogen) according to the manufacturer's instructions.

PCR reactions were performed on cDNA obtained from an equivalent of 0.025 to 0.5 embryo in 20 µl reaction mixtures containing 200 µM deoxynucleotide triphosphates (dNTPs), 0.5 U Taq polymerase (Takara, Kyoto, Japan), single-strength reaction buffer (provided with the enzyme), and a pair of primers specific for the MuERV-L gene, {alpha}-globin or ß-actin (10 pmol each) (Table 1). The samples were subjected to PCR on a thermal cycler (PTC-100, MJ Research, Watertown, MA) first for 2 min at 94°C, and then in cycles at 94°C for 30 sec, 60°C for 30 sec, and 72°C for 1 min (35 cycles for MuERV-L and ß-actin, and 30 cycles for {alpha}-globin). The last cycles were followed by a 5-min extension at 72°C. The PCR products were then subjected to electrophoresis. The relative band intensities were determined with a model 4.0 ATTO densitograph (ATTO Inc., Tokyo, Japan). Intensities were expressed relative to the intensity of the band for {alpha}-globin expression and the averages of three to five trials were compared and analyzed in each treatment.


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  		TABLE 1. Oligonucleotides used as primers for PCR reaction

Statistical Analysis

The developmental rates and the relative amount of MuERV-L gene expression were compared using the Tukey method following ANOVA. All analyses were conducted using the general linear models procedure of Statistical Analysis Systems (SAS Institute, Cary, NC). A value less than 0.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Transcription of the MuERV-L gene was rapidly activated from 8 to 10 h after IVF (Fig. 1). The result of the BrdU experiment showed that the S phase of the first cell cycle begins at around 6 to 7 h after IVF (Table 2). These results indicate that activation of the MuERV-L gene starts at the beginning of the S phase.



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  		FIG. 1. Densitometric quantification of the MuERV-L gene expressed from 5 to 17 h after IVF. The relative ratios were obtained by dividing the intensity of the MuERV-L gene by the intensity of {alpha}-globin gene at each time. Data are presented as the mean ± SEM (n = 3)


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  		TABLE 2. DNA replication in 1-cell embryos fertilized in vitro

Expression of the MuERV-L gene was completely repressed in embryos treated with {alpha}-amanitin. However, expression of the gene was detected by RT-PCR in embryos treated with aphidicolin (Fig. 2).



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  		FIG. 2. Expression of the MuERV-L gene in mouse embryos treated with (+) or without (-) {alpha}-amanitin or aphidicolin 23 h after IVF

To confirm that MuERV-L synthesis is required for the development of mouse embryos, we treated embryos with antisense oligonucleotides designed to disrupt translation of MuERV-L mRNA. The embryos were treated with antisense oligonucleotide using oligofectamine from 5 to 9 h after IVF. Both nonsense (scrambled sequence) and sense oligonucleotides (complementary sequence) were used as controls. In addition, embryos cultured without oligonucleotides were treated with oligofectamine reagent alone (control).

Figure 3 shows the developmental rate to the 4-cell stage of embryos treated with antisense S-oligo was significantly inhibited (30.0%) compared with that of embryos treated with the nonsense S-oligo (59.5%), the sense S-oligo (56.5%), or oligofectamine alone (61.2%, control). However, the developmental rates to the morula and blastocyst stages calculated as a fraction of 4-cell stage embryos did not differ significantly.



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  		FIG. 3. Developmental rates of embryos treated with antisense, nonsense, or sense oligonucleotides. Developmental rates of morula and blastocyst stage embryos are expressed as a fraction of 4-cell stage embryos. Asterisk on the error bar differs significantly (P < 0.05). Data are representative of five replicates

To confirm the amount of MuERV-L mRNA in embryos treated with each oligonucleotide, MuERV-L mRNA was semiquantitatively measured by RT-PCR using 2-cell embryos recovered 24 h after the treatment. The results showed that MuERV-L gene expression was significantly inhibited in embryos treated with antisense oligonucleotide (relative amount to {alpha}-globin was 0.45 compared with 0.88 in control, 0.93 in nonsense and 0.85 in sense treated embryos; Fig. 4).



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  		FIG. 4. Densitometric quantification of the MuERV-L gene treated with (antisense, nonsense, and sense) or without (control) oligonucleotides. The relative ratio was obtained by dividing the intensity of the MuERV-L gene by the intensity of {alpha}-globin gene. Data are presented as the mean ± SEM (n = 5). Asterisk indicates significant difference (P < 0.05)


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Transcription of the MuERV-L gene was rapidly activated at the beginning of the S phase of the first cell cycle. Expression of the gene was completely inhibited by {alpha}-amanitin treatment, but in addition, expression occurred without the completion of DNA replication and cleavage. These results reveal that the MuERV-L gene is newly transcribed from the zygotic genome and that it is expressed earlier than any other genes previously reported (e.g., U2afbp-rs, 39 h after hCG; and hsp70.1, 30 h after hCG) [13, 24, 26].

In an investigation of the onset of paternal gene activation in early mouse embryos fertilized with transgenic mouse sperm, RNA transcripts of the exogenous injected gene are first detected in 1-cell embryos as early as 13 h after insemination [10]. Core histones replace protamines during paternal pronuclear formation within 8 h after insemination, before DNA replication [29, 30]. The paternal pronucleus incorporates four to five times more BrUTP than the maternal pronucleus [14]. In addition, immediately after fertilization (at the G1 phase of the first cell cycle), hyperacetylated histone H4 is associated with paternal but not maternal chromatin, and transcriptional differences were observed in the S/G2 phase of the first cell cycle [31]. This difference in chromatin structure early in the 1-cell stage may influence the minor ZGA that occurs at the late 1-cell stage. Our results reveal that transcription of the MuERV-L gene is rapidly activated within 8 h after IVF (23 h after hCG). This time coincides with the beginning of the S phase of the first cell cycle (Table 2). It appears that aphidicolin has no effect on MuERV-L gene expression; however, more precise experiments are needed because 1-cell embryos begin DNA synthesis as early as 6 h after IVF (Table 2).

The MuERV-L gene continues expressing until the blastocyst stage (data not shown), and using these data, together with our finding that a repression of MuERV-L mRNA (using the antisense MuERV-L S-oligo) at the 2-cell stage correlates with the inhibition of development to the 4-cell stage, suggests that MuERV-L gene expression at the 2-cell stage plays a role in development until the 4-cell stage. The effect on transfection of oligofectamine used in our experiment started at 24 h after treatment and continued for 48 h. However, the possibility that the antisense effect is a secondary effect of the presence of a large amount of double-stranded RNA in the cell cannot be ruled out. In mice, the 2-cell stage is the critical phase when transcriptions from the zygotic genome remarkably increase [3]. The development of 1-cell mouse embryos, except for some inbred strains and their F1 hybrids, is blocked at the 2-cell stage, a phenomenon that has been termed the 2-cell block [32]. The blocked stage is reported to coincide with the loss of most of the maternal mRNA and the beginning of abundant embryonic transcription [27].

The gag region of the MuERV-L gene has a strong similarity with the Fv1 (Friend virus susceptibility 1) gene, which controls the replication of murine leukemia retroviruses and prevents disease in mice infected with these viruses [33, 34]. The presence of endogenous retrovirus (ERV) within the placenta of humans and other mammals has been known for the past 25 years. Several recent studies (reviewed by Harris [35]) have raised the possibility that the gene products of ERV play roles in placental formation, placental function, and placental survival throughout pregnancy in humans. However, the function of the MuERV-L gene remains unknown. Some ERVs have an envelope (env) gene to form the viral particle. However, because the MuERV-L gene does not have an env gene, the gene product is unable to form viral particles and to exit the cell. This indicates that the function of the gene is restricted to inside the embryonic cell. The MuERV-L gene has a long terminal repeat sequence [33] that is involved in the random transfer of the gene into the chromosomes. Integrated retroviral DNA activates or inactivates the transcription of peripheral genes, suggesting that MuERV-L gene expression at the very early stage of preimplantation development affects the expression of other genes involved in the major phase of ZGA. The present study demonstrates the necessity of MuERV-L gene expression during mouse early preimplantation development. However, further studies are needed to reveal the function of the MuERV-L gene in mouse embryos.


   FOOTNOTES
 
1 Part of this work was supported by a grant from the Japan Society for the Promotion of Science (JPS-RFTF 97L00905 to N.M.). Back

2 Correspondence: FAX: 81 75 753 6329; naojiro{at}kais.kyoto-u.ac.jp Back

Received: 29 May 2002.

First decision: 13 June 2002.

Accepted: 5 September 2002.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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