In order to measure the content of β- and γ-actin mRNA in mouse oocytes and ovulated eggs, Northern and slot blots were hybridized to complementary RNA probes transcribed from mouse isotype-specific cDNA sequences. The blots included samples of isotype-specific sense strand RNA standards prepared from the same cDNA sequences. Total actin mRNA content was estimated to be 40 fg per preovulatory full-grown oocyte or egg, consisting of one-third β-actin mRNA and two-thirds γ-actin mRNA. Ninety per cent of the actin mRNA is on polysomes in full-grown oocytes. The per cent of actin mRNA in polysomal mRNA is similar to the per cent of actin in newly synthesized proteins.

Measurements on other developmental stages showed that, in mid-growth-phase oocytes, each actin mRNA reaches a level twofold higher than in full-grown oocytes. Thereafter, all modulations of the two isotypic mRNAs occur in parallel; that is, they are maintained at constant levels during the late growth phase (oocytes from females 8−14 days old); gradually degraded in oocytes that have completed their rapid growth phase (oocytes from females 15−18 days old), in maturing oocytes, and in 1- and 2-cell embryos; and deadenylated after about 7 h of progression into meiotic maturation.

The full-grown mouse oocyte contains a large amount of maternal polyadenylated mRNA, estimated as 83pg/oocyte (De Leon et al. 1983), used to direct protein synthesis during meiotic maturation and early development to the 2-cell stage (see Bachvarova, 1985). Deadenylation, adenylation, and degradation of preexisting molecules during maturation result in a loss of about 30% of the polyadenylated RNA and a net deadenylation of an additional 30 % (Bachvarova et al. 1985; Paynton et al. 1988). During the 2-cell stage most maternal mRNA is degraded (Bachvarova & De Leon, 1980; Clegg & Piko, 1983) and, from this time on, protein synthesis is directed primarily by embryonic mRNA (Flach et al. 1982).

The mRNA for cytoskeletal actin was one of the first specific mRNAs examined in this system. In full-grown oocytes, actin mRNA carries a poly(A) tail and is actively translated, but during maturation it is largely deadenylated and actin synthesis declines to a low rate (Wassarman, 1983; Bachvarova et al. 1985; Paynton et al. 1988). The amount of actin mRNA declines more than tenfold from fertilization to the 2-cell stage, and by the late blastocyst newly synthesized message accumulates to a level about sixfold higher than in the egg (Giebelhaus et al. 1983, 1985; Paynton et al. 1988).

Measurement of the absolute amount of a specific mRNA provides a standard for future molecular experiments involving mRNA and, as applied here, to calculate translational efficiency. Absolute values for a few RNAs in mouse oocytes and/or embryos have been reported (Piko et al. 1984; Graves et al. 1985; Piko & Taylor, 1987; Philpott et al. 1987). The amount of actin mRNA has been measured as 430 fg per egg (Giebelhaus et al. 1985). Using currently available techniques, we have reassessed this value, and we present data on its association with polysomes.

Previous results indicate that the control of expression and degradation of maternal messages is sequence-specific (Paynton et al. 1988). ft- and y-actin mRNAs largely share coding sequences and are highly divergent in untranslated regions. Here, we have followed these two messages individually to determine whether they are modulated in parallel or show divergent behavior.

RNA from full-grown oocytes, maturing oocytes, ovulated eggs, embryos, liver and brain was extracted and Northern blots prepared as described (Paynton et al. 1988; Bachvarova, 1988).

All standards and probes were derived by transcription of mouse β- and γ-actin cDNA sequences (Tokunaga et al. 1988) contained in transcription vectors. The full-length β-actin sequence of 1892 nucleotides (Tokunaga et al. 1986) was inserted into the PstI site of pGEMl (Promega). A (Lactin antisense probe containing 629 out of the 684 nucleotide isotype-specific 3’ UTR was produced by transcription of the full-length β-actin cDNA plasmid linearized with Fspl. The β-actin sense standard was prepared from a pGEMl plasmid containing 668 nucleotides of the 3’ UTR extending from an A/wI site to the 3’ end. The γ-actin 3’ UTR antisense probe was derived from a pTZ19R (Pharmacia) plasmid containing a Xbal to PstI fragment with 691 out of 701 nucleotides of the 3’ UTR. The β3-actin sense standard was prepared from a pGEMl plasmid containing the entire 3’ UTR extending from the Xbal site.

The specific activity of the antisense probes was 3·9×108ctsmin-1μg-1, and of the sense strand standards was l·35×106ctsmin-1μg-1, using [β-32P]UTP as a precursor according to Melton et al. (1984). The concentrations of the standards were corrected for base composition. The yield calculated from optical density gave a value 35 % higher on average than that calculated from the specific activity; all values for the amount of actin mRNA have been corrected upward by this amount. Transcripts analysed by denaturing agarose gel electrophoresis migrated primarily as one species of the expected molecular weight.

Filters from Northern and slot blots were prehybridized and hybridized to the high-specific-activity antisense probes (5×106cts min-1μl−1) according to Melton et al. (1984) at 60°C. The final wash at 80°C in 0·l×SSC, 01% SDS eliminated nonspecific hybridization. Autoradiograms were scanned in a Hoefer densitometer.

Subpolysomal (<100S) and polysomal (>100S) fractions from lysates of full-grown oocytes and eggs were collected from sucrose gradients essentially as described (De Leon et al. 1983), brought to 0·2% SDS, 10Mm-EDTA, and phenol/ chloroform extracted with 20 μg carrier tRNA. ficients ranged from 0·96 to 100), and the absolute amount of each mRNA calculated for each sample.

An example of a Northern blot used for quantification of β-actin mRNA in liver, oocytes, and eggs is shown in Fig. 1. A slot blot hybridized sequentially to all three high specific activity probes is shown in Fig. 2. No cross reaction between the /L and y-actin 3’ UTRs was observed, while the β-actin 3’ UTR and full-length sequences crossreacted as expected. Hybridization of the full-length probe with cellular RNA relative to that with the full-length standard provides an estimate of the total amount of actin mRNA, since the β-actin and γ-actin coding sequences share 89% homology (Tokunaga et al. 1986, 1988).

Fig. 1.

Amount of β-actin 3’ UTR in oocyte, egg and liver RNA, A Northern blot was hybridized to the β-actin 3’ UTR probe. Lane 1: 0·13 μg of liver cytoplasmic RNA. Lane 2: RNA from 470 ;full-grown oocytes. Lane 3: RNA from 491 eggs. Lanes 4·7: 0·35pg, 0·6pg, 1·0pg, and 2·0pg of βactin 3’ UTR sense strand standard.

Fig. 1.

Amount of β-actin 3’ UTR in oocyte, egg and liver RNA, A Northern blot was hybridized to the β-actin 3’ UTR probe. Lane 1: 0·13 μg of liver cytoplasmic RNA. Lane 2: RNA from 470 ;full-grown oocytes. Lane 3: RNA from 491 eggs. Lanes 4·7: 0·35pg, 0·6pg, 1·0pg, and 2·0pg of βactin 3’ UTR sense strand standard.

Fig. 2.

Amounts of /3- and y-actin 3’ UTRs and of fulllength actin mRNA in oocyte, egg, liver and brain RNA. A slot blot was prepared according to Piko & Taylor (1987) with two columns of slots; it was hybridized sequentially to the γ- and γactin 3’ UTR probes, and to the full-length (FL) fl-actin probe as indicated at the top. The slots contained standards for the 0- or y-actin 3’ UTRs, or for the full-length fl-actin mRNA, or cellular RNAs. Samples are indicated on the left for the left column and on the right for the right column. Amounts of standards are in pg, and of liver and brain cytoplasmic RNA in ug. The numbers of oocytes and eggs used for extraction of RNA are indicated.

Fig. 2.

Amounts of /3- and y-actin 3’ UTRs and of fulllength actin mRNA in oocyte, egg, liver and brain RNA. A slot blot was prepared according to Piko & Taylor (1987) with two columns of slots; it was hybridized sequentially to the γ- and γactin 3’ UTR probes, and to the full-length (FL) fl-actin probe as indicated at the top. The slots contained standards for the 0- or y-actin 3’ UTRs, or for the full-length fl-actin mRNA, or cellular RNAs. Samples are indicated on the left for the left column and on the right for the right column. Amounts of standards are in pg, and of liver and brain cytoplasmic RNA in ug. The numbers of oocytes and eggs used for extraction of RNA are indicated.

The quantitative data on ) β-, γ-, and total actin mRNA contents from Northern and slots blots is presented in Table 1. The value for total actin mRNA obtained as the sum of β- plus γ-actin mRNAs was approximately twofold higher than that obtained directly (compare lines 5 and 6 in Table 1). This may be

Table 1.

Content of β- and γ-actin mRNA in full-grown preovulatory mouse oocytes and ovulated eggs

Content of β- and γ-actin mRNA in full-grown preovulatory mouse oocytes and ovulated eggs
Content of β- and γ-actin mRNA in full-grown preovulatory mouse oocytes and ovulated eggs

Samples of total RNA from known numbers of oocytes or eggs and of cytoplasmic RNA from brain or liver were analysed on Northern blots and slot blots in parallel with several amounts of sense strand standards. β- and γ-actin mRNAs were analysed separately using isotype-specific 3’ UTRs for standards and hybridization to 3’ UTR antisense probes. The resulting autoradiograms were scanned, a least-squares line fit to the values obtained for the standard (the correlation coef-due to the presence of less than full-length molecules in this long sense standard, resulting in an underestimate of the number of molecules in the standard. Also, the lack of complete homology between the β- and γ-actin coding region may lead to decreased efficiency of hybridization of the β-actin probe to γ-actin mRNA. For further consideration, we assume the higher value is more valid.

For liver and brain, the ratios of β- to γ-actin mRNA were 3·4 and 1·3, and the total amount of actin mRNA represented 0·1% and 0·4% of total mRNA, respectively (assuming 4 % of cytoplasmic RNA is polysomal). In these experiments, the data for full-grown oocytes and eggs were not significantly different, and the values have been combined to give 38 fg per full-grown preovulatory oocyte or ovulated egg, with the content of γ-twice that of β-actin mRNA.

To determine the amount of actin mRNA being translated, RNA from polysomal and subpolysomal fractions of oocyte and egg lysates centrifuged on sucrose gradients were analysed on Northern blots (Fig. 3). Averages from three runs showed 89% ± 3% of the actin mRNA is on polysomes in full-grown oocytes, while 74% ±9% is subpolysomal in eggs. Treatment with 20 mw EDTA released most of the message from polysomes of full-grown oocytes (data not shown).

Fig. 3.

Subpolysomal and polysomal RNA of full-grown oocytes and eggs on a Northern blot hybridized to the fulllength β-actin probe. Lanes 1 and 2: subribosomal and polysomal fractions from 1061 oocytes, respectively. Lane 3: 0·1 pg liver cytoplasmic RNA. Lanes 4 and 5: subribosomal and polysomal fractions from 830 eggs, respectively. Longer exposure showed that the RNA in lane l.was not degraded.

Fig. 3.

Subpolysomal and polysomal RNA of full-grown oocytes and eggs on a Northern blot hybridized to the fulllength β-actin probe. Lanes 1 and 2: subribosomal and polysomal fractions from 1061 oocytes, respectively. Lane 3: 0·1 pg liver cytoplasmic RNA. Lanes 4 and 5: subribosomal and polysomal fractions from 830 eggs, respectively. Longer exposure showed that the RNA in lane l.was not degraded.

To follow modulation of β- and γ-actin mRNAs during development, samples of growing oocytes were collected from 8-, 11-, and 14-day-old females. As shown in Table 2, the content of both isotypes was elevated about twofold in these mid-through late-growth-phase oocytes as compared to preovulatory oocytes and eggs.

Table 2.

Actin mRNA contents in growing oocytes

Actin mRNA contents in growing oocytes
Actin mRNA contents in growing oocytes

In our previous report, we demonstrated that actin mRNA is deadenylated around 7h of in vitro oocyte maturation, as detected by a decrease in molecular weight of the message (see Fig. 1) (Paynton et al. 1988). The time course of the deadenylation is essentially identical for (3- and y-actin mRNA, with poly(A) tails of variable length present at 7h (data not shown).

Finally, the time course of degradation of each isotype was comparable in 1- and 2-cell embryos, while β-actin predominated in newly synthesized mRNA of blastocysts (Fig. 4). After scanning the autoradiograph of Fig. 4, it was calculated that β-actin mRNA is elevated 50-fold, γ-actin mRNA 16-fold, and total actin mRNA 27-fold in the late blastocyst relative to the level in full-grown oocytes and eggs.

Fig. 4.

Relative levels of ft- and y-actin mRNA in early embryos. Upper panel: Northern blot hybridized to the β- actin 3’ UTR probe. Lower panel: hybridized to the y-actin 3’ UTR probe. Lanes 1 and 2: 0·48 yg and 0·048 μg liver cytoplasmic RNA. Lane 3: RNA from 400 preovulatory oocytes. Lane 4: RNA from 400 ovulated eggs. Lane 5: RNA from 392 early 2-cell embryos. Lane 6: RNA from 392 late 2-cell embryos. Lane 7: RNA from 50 expanded blastocysts. Lanes 8 and 9: 0·05 μg and 0·2 brain cytoplasmic RNA.

Fig. 4.

Relative levels of ft- and y-actin mRNA in early embryos. Upper panel: Northern blot hybridized to the β- actin 3’ UTR probe. Lower panel: hybridized to the y-actin 3’ UTR probe. Lanes 1 and 2: 0·48 yg and 0·048 μg liver cytoplasmic RNA. Lane 3: RNA from 400 preovulatory oocytes. Lane 4: RNA from 400 ovulated eggs. Lane 5: RNA from 392 early 2-cell embryos. Lane 6: RNA from 392 late 2-cell embryos. Lane 7: RNA from 50 expanded blastocysts. Lanes 8 and 9: 0·05 μg and 0·2 brain cytoplasmic RNA.

The amount of cytoskeletal actin mRNA in mouse eggs has been reevaluated using Northern and slot blots with single-stranded RNA standards. The value obtained is about 40 fg or 40 000 mRNA molecules per egg, approximately tenfold lower than that reported by Giebel-haus et al. (1985). The higher value obtained by these workers is probably explained (1) by their use of nick-translated cDNA probes (which can form networks) and a heterologous reaction between globin mRNA and its probe as the standard reaction and/or (2) by overestimation of the amount of globin mRNA in the standard (Schultz, G.A., personal communication).

Taylor & Piko (1987) obtained some data on the relative abundance of β- and y-actin mRNAs by hybridizing labeled cDNAs prepared from poly(A)+ RNA of various embryonic stages to human β- and γ-actin 3’ UTR sequences bound to filters. From the intensity of the reaction, it appeared that β-actin mRNA is about 30-fold more abundant than γ-actin mRNA in eggs, and total actin mRNA content is threefold greater in eggs than in early blastocysts. The unusually high value for β-actin mRNA in the egg could be explained by a nonspecific reaction of the egg cDNA with the β-actin 3’ UTR under the relatively low stringency conditions of hybridization used.

With the available data, we are now able to compute the fraction of total polysomal mRNA that is actin mRNA and to compare this to actin synthesis as a fraction of total protein synthesis. In growing and full-grown oocytes, only 15 % of total polyadenylated RNA is found on polysomes (or about 10 pg and 15 pg, respectively (De Leon et al. 1983)). Since 90 % of actin mRNA is translated (a reasonable assumption for growing oocytes), in mid-growth-phase oocytes, actin represents 0·68 % and, in full-grown oocytes, 0·23 % of polysomal mRNA. Wassarman (1983) reported briefly in a review that actin accounts for 0·9% of total newly synthesized protein in mid-growth-phase oocytes and for 0·3% in full-grown oocytes, both figures agreeing well with the fraction of actin mRNA on polysomes. Since no more actin mRNA is present in the full-grown oocyte than is required to account for the actin synthesized, it is not necessary to postulate that actin mRNA is translated less efficiently than other mRNAs (see Davidson, 1986, p. 403).

The differential expression of actin isotypes in various tissues is of some interest. Our data provide standards for the relative levels of isotype-specific actin mRNAs reported by Tokunaga et al. (1988). Our ratios for β- and γ-actin mRNA content correspond very closely to the ratios for β- and γ-actin protein content in brain and liver given by Otey et al. (1988). Moreover, the estimated amount of actin mRNA in liver as a fraction of total polysomal mRNA corresponds well with the fraction estimated by in vitro translation of liver mRNA (0·07 %, (Baumann & Held, 1981)). Thus there is no evidence for differential translation of the two isotypes in liver (see Erba et al. 1988). Of the various tissues analysed, the highest ratio of γ- to βactin and its mRNA is found in testis or spermatocytes (Otey et al. 1987; Hecht et al. 1984; Tokunaga et al. 1988; Waters et al. 1985), as well as in oocytes (data reported here). Perhaps there is a common regulatory-mechanism determining this ratio in male and female germ cells during meiotic prophase.

The differential accumulation of β- and γ-actin mRNAs in small growing oocytes, followed by parallel modulations in later development suggest the hypothesis that differential expression of the two isotypes is mediated primarily at the level of production of the message, while cytoplasmic modulations of the two messages are regulated in parallel. It would follow that sequences determining the rate of transcription and/or processing are isotype-specific and those determining modulations of the mRNA are shared by both isotypes. The long 700 nucleotide 3’ UTRs of β- and γ-actin mRNAs are dissimilar (do not cross hybridize) and are evolutionarily conserved (Ponte et al. 1984; Yaffe et al. 1985; Tokunaga et al. 1986, 1988; Chou et al. 1987), suggesting a role in isotype-specific modulations. Indeed, a 40 nucleotide sequence in the 3’ UTR of β-actin mRNA, absent in the 3’ UTR of γ-actin, was shown to mediate transcriptional activity of β-actin mRNA in myoblasts (DePonti-Zilli et al. 1988).

Mechanisms regulating adenylation, translation, and degradation of maternal mRNAs during oocyte maturation and early development are beginning to be explored. Recent work implicates a 103 nucleotide sequence at the 3’ terminus of tissue plasminogen activator mRNA in regulation of its translation and subsequent rapid degradation in maturing mouse oocytes (Strickland et al. 1988). In looking for sequences that might mediate parallel modulation,of the two actin mRNAs in oocytes and embryos (and perhaps in general), runs of up to 50 identical nucleotides occur in the coding sequence, and even within the 3’ UTRs there are nine regions of 8 to 10 nucleotide identity (Tokunaga et al. 1988). Further work is required to locate the sequences involved in regulating mRNA translation and degradation in mouse oocytes and embryos.

We are grateful to Bhavna Modh and Amy Houle for expert technical assistance, and to Adam Greenberg for pilot experiments. This work was supported by NIH grant HD06910 and by a Grant-in-Aid for a Comprehensive Ten-Year Strategy for Cancer Control from the Ministry of Health and Welfare, Japan.

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