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and Heat Shock Protein 90 Messenger Ribonucleic Acid in the Gravid Horn and Nongravid Horn in Sheep during Betamethasone-Induced Labor1
Laboratory for Pregnancy and Newborn Research, Cornell University College of Veterinary Medicine, Ithaca, New York 14853
Address all correspondence and requests for reprints to: Dr. Peter W. Nathanielsz, Laboratory for Pregnancy and Newborn Research, Department of Biomedical Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York 14853-6401. E-mail: pwn1{at}cornell.edu
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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(ER), and
heat shock protein 90 (Hsp90) messenger RNA (mRNA) expression in the
nongravid horn of pregnant sheep and compared them with their
expression in the gravid horn that is exposed to a greater degree of
stretch. We also examined the regulatory effects of estrogen and
progesterone on OTR mRNA expression in ovariectomized nonpregnant
sheep. In addition, we determined the ontogeny of mCAP expression in
the gravid horn throughout late pregnancy and during spontaneous term
labor. Gravid horn and nongravid horn myometria were removed under
general anesthesia from control ewes not in labor at 130–140 days
gestational age (dGA; n = 3) and during betamethasone-induced
labor (n = 6) at the same gestational age. Gravid horn myometrium
was also collected from ewes not in labor at 95 dGA (n = 3),
101–110 dGA (n = 3), 111–120 dGA (n = 3), 121–130 dGA
(n = 3), 131–140 dGA (n = 3), and 141–145 dGA (n = 4)
and from ewes in spontaneous term labor (n = 4). All ewes were
carrying single fetuses. Myometrium was also collected from
ovariectomized nonpregnant ewes treated with saline (n = 5),
estradiol (50 µg/day; n = 5), progesterone (0.3 g,
intravaginally; n = 5), and estradiol plus progesterone (n =
5). Myometrial RNA was extracted and analyzed by Northern blot for OTR,
PGHS2, ER, and Hsp90 mRNA, normalized for 18S ribosomal RNA or
ß-actin. ER, Hsp90, OTR, and PGHS2 mRNA were all significantly
up-regulated during betamethasone-induced labor (P
< 0.01) in gravid and nongravid horn myometrium. The level of gravid
horn OTR mRNA during labor was 3 times the level of nongravid horn OTR
mRNA (P < 0.0001). Gravid horn PGHS2 mRNA was also
higher than nongravid horn PGHS2 (P < 0.02). In
contrast, in spontaneous term labor nongravid horn, ER and Hsp90
mRNA were similar to gravid horn. Myometrial ER and Hsp90 mRNA
remained unchanged throughout late pregnancy and increased at
spontaneous term labor (P < 0.05). In contrast,
myometrial OTR increased around 130 dGA (P < 0.01)
and further increased at spontaneous term labor (P
< 0.02). Progesterone significantly inhibited myometrial OTR mRNA
expression in nonpregnant sheep and estradiol antagonized
progesterone’s inhibitory effect. Mechanical stretch differentially
regulated mCAP mRNA expression in the ovine gravid horn and nongravid
horn. Mechanical stretch appears largely responsible for increased OTR
mRNA and to a lesser degree PGHS2 mRNA. In addition, endocrine factors
may be required for full activation of OTR and PGHS2 mRNA associated
with labor. ER and Hsp90 mRNA are not under the control of uterine
stretch in keeping with our previous results, indicating that systemic
hormones such as estradiol, are prime regulators for these two mCAP
mRNA expression during labor. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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(ER) and heat shock protein 90 (Hsp90). The regulation of mCAP expression has been extensively studied throughout gestation and during labor (2, 6, 7, 8, 9). A major focus has been on the effects of the two steroid hormones, estrogen and progesterone, on the expression of mCAPs (8, 10, 11). Recently, there has been considerable interest in the spatial regulation of mCAP expression within the different regions of the uterus during pregnancy and labor. Several studies indicate differential changes in different mCAPs in relation to uterine topology (12, 13, 14, 15). Mechanical stretch is another factor that has been explored as a potential regulator of expression of mCAPs (16, 17). To date, studies have only been performed in rats and relate to three mCAPs: PTH-related peptide (17), connexin-43, and OTR (16, 18). When pregnancy is restricted experimentally to one uterine horn in the rat, PTH-related peptide (PTHrP), connexin-23, and OTR messenger RNA (mRNA) are increased in the gravid horn. Mechanical stretch of the nongravid horn reproduces the rise in mRNA for these mCAPs (16, 17).
The sheep is an animal model that has been used extensively to evaluate
changes that occur at parturition. In this species, uterine occupancy
of the gravid horn can be compared with the nongravid horn to examine
the effect of stretch on mCAP activation both before and during labor.
In light of our previous data on estrogen’s stimulatory effect on
mCAPs such as ER, Hsp90, and PGHS2 in the nonpregnant sheep
myometrium (10, 11, 19) as well as data on the effects of stretch on
PTHrP and OTR expressions in the rat uterus (16, 17), we hypothesized
that mechanical stretch would differentially control expression of
mCAPs between the gravid horn and the nongravid horn in sheep during
betamethasone-induced labor. We further hypothesize that up-regulation
of mCAPs during betamethasone-induced labor in the gravid horn is
partially regulated by the endocrine factors that operate at the time
of the switch from myometrial contractures to contractions. To examine
our hypotheses, we first compared OTR, PGHS2, ER, and Hsp90 mRNA
expression in the gravid horn and nongravid horn of the pregnant sheep
bearing a single fetus during betamethasone-induced labor. We also
determined gestational age-related mCAP expression in the gravid horn
throughout late pregnancy and during spontaneous term labor to dissect
out the effects of stretch from the effect of labor. Finally, we
examined the regulatory control of estrogen and progesterone on
expression of myometrial OTR mRNA in the ovariectomized nonpregnant
sheep uterus.
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Materials and Methods |
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Betamethasone (celestone phosphate, Schering AG, Kennilworth, NJ; 10 µg/h; n = 6) was administered iv into the fetal jugular vein continuously over a period of 48 h to precipitate betamethasone-induced premature labor. Tissues were removed from ewes under halothane anesthesia in well established labor at 130–140 dGA. Myometrium was obtained from ewes in betamethasone-induced premature labor as well as contemporary control ewes (n = 3) whose fetuses were infused with saline at the same stage of gestation (130–140 dGA). These ewes were designated as controls, not in labor, as myometrial EMG showed only contractures and no contractions. Myometrium was also collected from ewes at 95 dGA (n = 3), 101–110 dGA (n = 3), 111–120 dGA (n = 3), 121–130 dGA (n = 3), 131–140 dGA (n = 3), and 141–145 dGA (n = 4). These ewes were also known not to be in labor, as judged from their myometrial EMG activity pattern that showed only contractures. In addition, myometrium was also collected from ewes (n = 4) in spontaneous term labor (143–147 dGA) as judged from a well established myometrial EMG contraction pattern.
Twenty nonpregnant ewes were ovariectomized on the day of ovulation. Forty days later ewes were treated with saline (controls; n = 5) or estradiol infused iv for 2 days (50 µg/day; n = 5) in 2 ml saline/h or an intravaginal progesterone sponge (Carter Holt Harvey Plastic Products, Hamilton, New Zealand) for 10 days (containing 0.3 g progesterone; n = 5) or an estradiol plus progesterone group in which the intravaginal progesterone sponge was placed for 10 days, and estradiol (50 µg/day) was infused iv on days 9 and 10 with the progesterone sponges still in place. At the end of each treatment period tissues were removed under halothane general anesthesia before necropsy.
Total RNA preparation and Northern blot analysis
Total RNA was isolated from the myometrium by homogenization in
4.2 M guanidinium thiocyanate solution. RNA was pelted
through a 5.7-M cesium chloride cushion. Purified RNA was
resuspended in 1 mM EDTA and stored at -80 C.
Polyadenylated RNA was extracted from flash-frozen myometrial samples
obtained from nonpregnant sheep stored at -80 C by
oligo(deoxythymidine)-cellulose affinity chromatography using a
commercial kit (Fast Track 2.0, Invitrogen, San Diego,
CA). The RNA purity and recovery of each tissue were determined by UV
spectrophotometry (260 and 280 nM).
Samples of total RNA (40 µg/lane) or polyadenylated RNA (5 µg/lane) were denatured in 17.4% (vol/vol) formaldehyde, 50% (vol/vol) formamide, 20 mM MOPS [3-(N-morpholino)propanesulfonic acid], 5 mM sodium acetate, and 1 mM EDTA, pH 7.0, for 5 min at 65 C and separated on a 1% (wt/vol) agarose-0.66 M formaldehyde gel. Ethidium bromide-stained ribosomal RNA bands were visualized (UV) to ensure that RNA degradation had not occurred and an equal amount of RNA was loaded into each lane. After electrophoresis, RNA was transferred to a nylon membrane (Gene Screen Plus, NEN Life Science Products, Wilmington, DE) by capillary blotting for 24 h in 10 x SSC (1 x SSC is 0.15 M NaCl and 0.015 M sodium citrate, pH 7.0). Completion and uniformity of transfer were assessed by determining transfer of 28S and 18S ribosomal RNA from the gel. Membranes were prehybridized at 42 C for 5 h in hybridization solution [50% (vol/vol) deionized formamide, 50 mM sodium phosphate, 0.8 M NaCl, 2% (wt/vol) SDS, 100 µg salmon sperm DNA/ml, 20 µg transfer RNA/ml, and 1 x Denhardt’s (50 x = 1% solution of BSA, Ficoll, and polyvinylpyrrolidone].
A 131-bp complementary DNA (cDNA) probe encoding part of the sheep
endometrial OTR, which was generated by PCR, was made available to us
by Dr. Flint (21). Recombinant sheep PGHS2 cDNA was purchased from
BIOMOL Research Laboratories, Inc. (catalogue no. Z100,
Plymouth Meeting, PA). Recombinant human ER cDNA containing the
entire coding region was made available by Dr. Pierre Chambon
(University of Strasbourg, Strasbourg, France). Recombinant human Hsp90
(catalogue no. 78313) cDNA was purchased from American Type Culture Collection (Manassas, VA). The cDNA probes were labeled
with [-32P]deoxy-CTP using the random priming method
(NEN Life Science Products-DuPont) to specific activities
of approximately 1 x 109 cpm/µg. Labeled cDNA was
used at a final concentration of 1 x 106 cpm specific
probe/ml hybridization solution.
Hybridization was carried out at 42 C for 20 h in hybridization solution containing each of specific probes. Membranes were washed sequentially in 2 x SSC (standard saline citrate) at room temperature for 10 min and in 0.5 x SSC with 0.1% SDS at 65 C for 30 min. Kodak X-OMAT AR film (Eastman Kodak, Rochester, NY) was exposed to the membrane with intensifying screens at -80 C. Exposure durations were varied to achieve hybridization signals within the linear range for densitometry (2–7 days).
Membranes were hybridized with [-32P]deoxy-CTP-labeled
18S or ß-actin probe to normalize each mRNA level. Autoradiographed
signals were quantified by scan densitometry (Biosoft,
Cambridge, UK).
Statistical analysis
Results are presented as the mean ± SEM and
were analyzed by ANOVA followed by multiple comparisons using the
Turkey-Kramer procedure.
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Results |
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, Hsp90, OTR, and PGHS2 mRNA were all at similar
levels (P > 0.05) in gravid horn and nongravid horn
myometria in the absence of labor (Figs. 1
and 2).
All four mRNAs were significantly up-regulated in the gravid horn as
well as the nongravid horn during betamethasone-induced labor
(P < 0.001; Figs. 1 and 2). Most importantly, the
level of gravid horn OTR mRNA during labor was 3 times the level of
nongravid horn OTR mRNA in labor (Fig. 1; P < 0.0001).
Similarly, gravid horn PGHS2 mRNA in labor was higher than nongravid
horn PGHS2 in labor (Fig. 1; P < 0.02). In contrast,
ER (Fig. 2) and Hsp90 (Fig. 2) mRNA increased to the same level in
the gravid and nongravid horns during labor.
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), but this increase did not reach
significance. Progesterone treatment alone significantly decreased the
OTR mRNA level (P < 0.01; Fig. 3). Estradiol
antagonized the inhibitory effect of progesterone on OTR mRNA
expression in the nonpregnant sheep myometrium.
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, Hsp90, and OTR mRNA were all detectable in the gravid
horn throughout late gestation. ER and Hsp90 mRNA in myometrium
remained unchanged throughout late pregnancy and only increased during
spontaneous term labor (Fig. 4;
P < 0.01). In contrast, OTR mRNA increased in
myometrium around 130 dGA (P < 0.02), with a further
increase during spontaneous term labor (Fig. 4; P <
0.01).
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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, Hsp90, and PGHS2 associated with both
spontaneous term labor (2, 19) and betamethasone-induced premature
labor in sheep (19, 22, 23, 24). These findings were confirmed and extended
in the present studies. Our major objective in the present study was to
determine the extent to which stretch is a major regulatory mechanism
mediating these increased mCAPs both before and during labor. The
effect of stretch on the expression of each of the four mCAPs was
characterized. The bicornuate sheep uterus provides a powerful natural
experimental system in which the degree of stretch is much greater in
the gravid horn of sheep carrying a single fetus than the nongravid
horn. We present compelling new evidence that mechanical stretch
differentially regulates the expression of the different mCAPs in the
gravid horn compared with the nongravid horn during late gestation and
labor. The level of pregnant horn OTR mRNA during labor was 3 times higher than the level of nonpregnant horn OTR mRNA, whereas the increase in the nongravid horn was only slightly over 100%. These observations suggest that both the endocrine- and contractility-associated changes that occur during labor as well as the effect of stretch alter OTR gene expression. As there are no differences between the gravid and nongravid horns in any of the four types of mRNA when sheep is not in labor, it is clear that this degree of stretch alone is inadequate to alter mCAP mRNA expression. The differences between the two horns develop during labor. Stretch and the labor-related changes together appear to have a greater effect than labor-related changes alone. Further studies are needed to dissect out the various labor-related effects that result in the differences between gravid and nongravid horns during labor. Candidate mechanisms are a rise in estrogen, a fall in progesterone, and/or phasic myometrial contractions. In contrast to the changes observed in OTR mRNA, PGHS2 in the gravid horn only increased 2-fold during labor compared with that in the nongravid horn during labor. Taken together these observations suggest that mechanical stretch due to uterine occupancy appears to play a larger role in the increased OTR mRNA associated with betamethasone-induced labor than in the regulation of PGHS2 expression.
ER and Hsp90 mRNA changes during labor were not related to uterine
stretch. This finding is in keeping with our previous results that
systemic hormones such as estradiol are prime regulators for these two
mCAP expressions during labor (10, 19). In sheep, elevated plasma
estrogen concentrations at the end of pregnancy (25) and a decrease in
plasma progesterone (26) immediately before the onset of labor are the
most marked labor-associated hormone changes, which precede
labor-related increases in mCAPs. To evaluate the effects of these
steroid hormones, we previously performed a series of studies to
examine estradiol’s and progesterone’s regulatory effects on
myometrial ER (10), Hsp90 (19), and PGHS2 (11) expression using the
ovariectomized steroid-replaced nonpregnant sheep model. Estradiol
stimulated the expression of all three mCAPs. In the present study we
characterized estradiol and progesterone regulatory effects on OTR mRNA
expression in the ovariectomized nonpregnant sheep myometrium.
Progesterone treatment decreased OTR mRNA, suggesting that progesterone
withdrawal in this species in late gestation is a factor in producing
the labor-related differences we have demonstrated. Although the
estrogen-induced increase was not statistically significant we would
speculate that estrogen does play a role in the presence of
stretch.
To date the only published data on the effect of stretch on mCAPs involves the control of PTHrP (17); connexin-43, which encodes the major myometrial gap junction protein (18, 27); and OTR (16) in the rat. Our findings are in keeping with the studies in the rat (16) that demonstrate an important role for mechanical stretch in the regulation of myometrial OTR expression during parturition. As information is also available that addresses estrogen stimulatory and progesterone inhibitory effects on OTR expression in the pregnant rat (6, 16) and rabbit (28) uterus, we examined the roles of these two steroids in regulating myometrial OTR expression in the ovariectomized nonpregnant sheep uterus. Progesterone inhibited myometrial OTR mRNA expression in the ovariectomized nonpregnant sheep uterus. This finding is consistent with observations in rat (6, 16) and rabbit (28) uterus. Estrogen stimulated OTR mRNA expression, but this increase did not reach significance. When the observations in the pregnant and nonpregnant sheep are combined, our findings indicate that both mechanical stretch and endocrine factors are involved in the regulation of myometrial OTR mRNA expression. Although the OTR mRNA level increased during labor in the nongravid horn, the rise was much lower than that in the gravid horn, suggesting that the effect of stretch and endocrine change are additive. The observation that OTR mRNA in the gravid horn is more than double that in the nongravid horn at the time of labor further indicates that myometrial distention at labor is essential for the full activation of OTR expression,
In the present study and the study performed in the rat (16), increased
OTR mRNA was observed in the gravid horn compared with that in the
nongravid horn during active labor. In contrast to our observations,
studies by Alexandrova and Soloff (29) and Fuchs (6) failed to show
increased OTR binding in the gravid vs. nongravid horn of
rats at term before labor. It may be possible that the effects of
stretch are primarily exerted during labor. To differentiate between
the additive effect of stretch plus labor and the effect of stretch
itself, we conducted an ontogenic study to determine myometrial OTR
mRNA expression from 95 dGA to term as well as during spontaneous term
labor. The sheep fetus enters its rapid growth phase at approximately
90 dGA. Maximal growth occurs around 130 dGA (30). We hypothesized that
if stretch has any effect on inducing OTR mRNA expression independent
of labor, there will be a gestation-associated increase in OTR mRNA in
the gravid horn associated with the rapid growth of the fetus and that
this effect would be maximal around 130 dGA. Data presented in Fig. 3
confirmed our hypothesis that OTR mRNA significantly increased around
130 dGA. In addition, we have demonstrated that the response of the
pregnant sheep myometrium to oxytocin was maximal around 130 dGA (31),
which further supports our hypothesis. In addition, our data show that
regulation of OTR after 130 dGA is not only at the message level, as
there is no significant decrease in the in vitro response of
the myometrium to OT (31). In contrast, there were no changes in
myometrial ER and Hsp90 mRNA across the period of gestation studied.
This difference between OTR and the other mCAPs support the views that
mechanical inputs specifically up-regulate OTR mRNA expression in the
gravid horn of the pregnant sheep.
To our surprise, myometrial OTR mRNA declined after 130 dGA and remained low at term with the onset of labor. This finding is consistent with the data from rats (6, 29). These data suggest that the rate of stretch, rather than the degree of stretch, might be an important factor. During pregnancy, stretch combined with the influence of high circulating steroid hormone levels results in hyperplasia and hypertrophy of uterus. Chronic stretch, imposed at a time when uterine contents are not increasing rapidly, actually results in a minimal increase in wall tension. Thus, there are two stages at which significant stretch is exerted: 1) at the period of maximal growth and 2) during strong phasic uterine contraction. We hypothesize that increased OTR mRNA expression is induced at both of these stages. This hypothesis is supported by the data in rat demonstrating that acute balloon distention in a virgin rat uterine horn (diameter, 4–8 mm) can produce a greater signal of PTHrP mRNA than is seen in a day 16 pregnant rat uterus (diameter, 12 mm) (17).
The mechanisms by which mechanical inputs are converted to biochemical signals in the pregnant uterus are not clear. Regulation of gene expression by mechanical forces is not confined to uterine smooth muscle. The atrial natriuretic peptide gene is a well characterized example of a gene that is regulated in part by stretch (32). At the present time the mechanotransducer of the stretch effect and how it allows force to direct an increase in mRNA expression have not been elucidated. It has been suggested that a unique cis-acting stretch-responsive element may exist (33).
In summary, mechanical stretch differentially regulated the mCAP mRNA
expression between the ovine gravid horn and the nongravid horn.
Mechanical stretch appears largely responsible for increased OTR and
PGHS2 mRNA. Endocrine factors are also required for full activation of
OTR and PGHS2 mRNA associated with labor. ER and Hsp90 mRNA are not
significantly controlled by uterine stretch, in keeping with our
previous findings that systemic hormones such as estradiol are prime
regulators of these two mCAP expressions during labor.
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Footnotes |
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Received June 23, 1999.
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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proteins in the upper
and lower segment of the human uterus during pregnancy and labor.
J Clin Endocrinol Metab 84:1705–1710, progesterone receptor
(PR), and oxytocin receptor (OTR) in the pregnant baboon myometrium
(Myo). J Soc Gynecol Invest [Suppl] 6:62A
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) and PGHS2 (
)
mRNA to 18S. Data are the mean ± SEM, except where
the error bar is too small to show. There was a significant increase in
myometrial OTR and PGHS2 mRNA during BL (a, P <
0.001) in both the gravid and nongravid horns. The level of gravid horn
OTR mRNA during labor was 3 times the level of nongravid horn OTR mRNA
(b, P < 0.0001). Gravid horn PGHS2 mRNA was also
higher than nongravid horn PGHS2 (b, P < 0.02).
