Biology of Reproduction 62, 365-369 (2000)
© 2000 Society for the Study of Reproduction, Inc.
Effects of Progesterone and Estradiol on Uterine Secretion of Prostaglandin F2
in Response to Oxytocin in Ovariectomized Sows1
Lee A. Edgertona,
Michael A. Kaminskia, and
William J. Silvia2,a
a Department of Animal Sciences, University of Kentucky, Lexington, Kentucky 40546-0215
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ABSTRACT
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Thirty ovariectomized sows were used in an experiment designed to determine whether the ability of the porcine uterus to release prostaglandin (PG) F2
in response to oxytocin is regulated by progesterone (P4) and estradiol (E2). Sows were assigned to one of four treatment groups: 1) no steroids (ovariectomized controls; n = 8), 2) E2 (n = 8), 3) P4 (n = 7), or 4) E2 + P4 (n = 7). P4 and E2 were administered so as to mimic the normal temporal changes that occur in these hormones during the estrous cycle. A group of intact sows (n = 9) was included for comparison. All sows received an injection of oxytocin (30 IU, i.v.) on Days 12, 15, and 18 postestrus. Jugular venous blood samples were collected from 60 min before through 120 min after injection of oxytocin for quantification of 13,14-dihydro-15-keto-PGF2 (PGFM). Preinjection baseline concentrations of PGFM, the magnitude of the PGFM response above baseline, and area under the PGFM response curve (AUC) were calculated for each sow on each day and compared among treatment groups by ANOVA. Among the ovariectomized sows receiving steroid replacement, baseline concentrations of PGFM were low on Day 12 postestrus in all four groups. On Days 15 and 18, baseline concentrations remained low in the two groups that did not receive P4 but increased in those that did. Both the magnitude of the response to oxytocin and AUC were small on Day 12 postestrus in all 4 groups. By Day 15, the magnitude of the response and AUC increased in the group that received both P4 and E2 but remained low in the other three groups. By Day 18, responses to oxytocin were greater in both groups that received P4 than in those that did not. Baseline concentrations were similar in intact sows and in those that received both P4 and E2 on all three days examined. The magnitude of the response and the AUC were greater in the ovariectomized sows receiving P4 and E2 replacement than in the intact control sows on Days 15 and 18 postestrus. From these results, we conclude that P4 and E2 interact to control the time when the uterus begins to secrete PGF2 in response to oxytocin and the amount of PGF2 secreted.
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INTRODUCTION
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In nonpregnant sows, luteal regression is initiated by prostaglandin (PG) F2 secreted from the uterus [1]. The endocrine factors that regulate this secretion are poorly understood. In ruminants, three hormones—oxytocin, progesterone (P4), and estradiol (E2)—may play major roles in regulating uterine secretion of PGF2 [2]. Oxytocin is an acute stimulus for PGF2 secretion. P4 and E2 regulate uterine secretion of PGF2, in part, by controlling both the timing and the magnitude of uterine secretory responsiveness to oxytocin. Oxytocin can stimulate uterine secretion of PGF2 in sows [3,4]. However, the effects of ovarian steroids on uterine secretory responsiveness to oxytocin have not been thoroughly investigated in this species. Uterine secretory responsiveness to oxytocin can be induced to occur prematurely by supplementation with P4 on Days 1–5 after the onset of estrus [5]. Therefore, it appears that P4 may play a critical role in determining when the uterus becomes responsive to oxytocin, just as in ruminants [2]. The effects of E2 on uterine secretion of PGF2 have been studied more extensively, but from the perspective of its role as a signal for maternal recognition of pregnancy. When administered acutely, during the latter half of the luteal phase, it suppresses both basal and oxytocin-induced secretion of PGF2 [6–10]. However, the contribution of basal, follicular E2 in regulating uterine PGF2 secretion in nonpregnant sows has not been investigated. The objective of the experiment described below was to characterize the roles of P4 and E2 in regulating uterine secretory responsiveness to oxytocin in nonpregnant sows. This was accomplished by examining the temporal development of uterine secretory responsiveness to oxytocin in ovariectomized sows that receive P4 and E2 replacement.
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METHODS AND MATERIALS
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Thirty ovariectomized (OVX), multiparous crossbred (Yorkshire x Hampshire) sows were used in this experiment. Ovaries were removed through a midventral incision while sows were under halothane anesthesia. Sows were allowed to recover from surgery for at least 30 days, during which time endogenous ovarian steroids were cleared from the circulation. All sows were then administered a steroid pretreatment regimen designed to mimic the changes in endogenous P4 and E2 that occur during the last 5 days of a luteal phase and the subsequent follicular phase. This type of a pretreatment has been shown to be essential for the uterus to develop the capability of secreting PGF2 in response to oxytocin at the appropriate stage of the estrous cycle in OVX ewes [11]. Both steroids were administered by i.m. injection in corn oil vehicle. The timing and doses of P4 and E2 administered are described in Figure 1a. In a previous study, 160 mg P4 was administered twice daily and was shown to maintain concentrations of P4 at luteal phase levels when administered to OVX sows [12]. We confirmed this observation in a preliminary study. However, we found that the clearance of P4 following cessation of these injections was too slow to adequately represent changes that occur during normal luteolysis. Therefore, we reduced the dose to 80 mg. As expected, this change resulted in a reduction in the maximum circulating concentrations of P4 to about 20 ng/ml, approximately one half of the maximum concentrations observed during the estrous cycle (Fig. 1b). This was considered acceptable because these concentrations were well above the minimum concentration required to maintain pregnancy in OVX sows [13], and the decline in P4 following cessation of injections more closely simulated the normal decline observed during luteolysis. The doses of E2 administered during the pretreatment period were developed empirically. The final E2 injection protocol was judged to be effective on the basis of its ability to consistently induce estrous behavior in OVX sows after pretreatment with P4 as previously described. Estrous behavior was observed approximately 12 h after the last E2 injection. The first day of estrus was designated as Day 0 of the estrous cycle.
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FIG. 1. P4 and E2 replacement protocols during the pretreatment and treatment periods. a) Timing and dose of injection for P4 (closed diamonds) and E2 (open diamonds) during the pretreatment and treatment periods. b) Concentrations of P4 during the pretreatment and treatment periods in intact control sows (triangles), and in OVX sows receiving no steroids (open squares) or receiving E2 (solid squares), P4 (open circles), or P4 + E2 (solid circles). For effects within sow (time postestrus and time x treatment), residual (error) mean square in repeated-measures ANOVA was 8.24 with 306 df.
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After the pretreatment was completed, sows were assigned randomly to receive one of the four following treatments: 1) no steroids (OVX controls; n = 8), 2) E2 (n = 8), 3) P4 (n = 7), or 4) E2 + P4 (n = 7). E2 was administered using silicone elastomer implants (3.35 mm i.d., 4.65 mm o.d., 3 cm long each) packed with crystalline E2 as described previously for sheep [14]. Three implants were used in each sow to account for the larger body size of pigs compared to sheep. Sows assigned to groups that did not receive E2 were given three similar silicone elastomer implants that contained no steroid. Implants were inserted on Day 1 s.c. in the back fat between the shoulder blades. P4 was administered by twice-daily injection in corn oil vehicle. The P4 pattern was designed to mimic the normal formation, maintenance, and regression of corpora lutea in nonpregnant sows. The timing and doses of P4 administered are described in Figure 1b. Sows assigned to groups that did not receive P4 were given twice-daily injections of corn oil vehicle in volumes equal to that received by sows in the P4-treated groups. Nine additional intact, cycling sows were also included in this experiment to determine whether the complete steroid replacement protocol adequately restored normal secretory responsiveness to oxytocin.
The jugular vein of each sow was cannulated as described previously [5]. OVX sows were cannulated 1 day before the onset of pretreatment. Intact sows were cannulated on Day 1 of the estrous cycle. Jugular venous blood samples (10 ml) were collected daily through Day 18 of the treatment period (OVX sows) or of the estrous cycle (intact sows). After sampling, 10 ml of a dextrose solution (50 g/100 ml of sodium citrate saline) was flushed through the cannula. Samples were allowed to clot at 4°C for 4–8 h. Serum was collected and stored at -20°C for quantification of P4.
Each sow received an injection of oxytocin (30 IU in 3 ml of sterile saline) on Days 12, 15, and 18 postestrus. Oxytocin was injected into the jugular vein through the cannula. This was followed immediately by 10 ml of saline to force any residual oxytocin solution into the vein. Jugular venous blood samples (5 ml) were collected at 60, 45, 30, 15, and 0 min before and 2, 5, 10, 15, 30, 45, 60, 90, and 120 min after the injection of oxytocin. Saline with 2.5% sodium citrate was flushed into the cannula between samples to prevent clotting. At the end of the sampling period, 10 ml of a dextrose solution (50 g/100 ml of sodium citrate saline) was flushed through the cannula. Blood samples were allowed to clot at 4°C for 4–8 h. Serum was separated and stored at -20°C for quantification of 13,14-dihydro-15-keto PGF2 (PGFM).
RIAs
Concentrations of P4 in serum samples collected daily throughout the estrous cycle were quantified with a commercial, solid-phase RIA kit (Coat-a-Count; Diagnostic Products, Los Angeles, CA) as described previously [5]. Samples were evaluated in 13 assays. Within- and between-assay CVs for P4 assays were 6% and 19%, respectively. Concentrations of PGFM in samples collected during the oxytocin challenge were quantified by RIA as described previously [4]. The samples were evaluated in 25 assays, and the within- and between-assay CVs were 13% and 29%, respectively.
Statistical Analyses
The effect of steroid replacement on the response to oxytocin was determined by comparing postinjection concentrations of PGFM on Days 12, 15, and 18 of the estrous cycle. Baseline PGFM was defined as the mean of the concentrations in samples collected at -60, -45, -30, -15, and 0 min before the oxytocin injection. Magnitude of the PGFM response was defined as the maximum concentration of PGFM, above baseline, during the 2-h postinjection period. The area under the PGFM response curve (AUC) above baseline was calculated for the 2-h postinjection period as well. Baseline, magnitude of the PGFM response, and AUC were determined for each sow. For each day on which oxytocin was injected, the effect of steroid replacement on PGFM baseline, magnitude of the PGFM response, and AUC was determined by ANOVA using the General Linear Models (GLM) procedure of Statistical Analysis Systems (SAS) [15]. PGFM baseline, magnitude of the PGFM response, and AUC were also compared between intact sows and OVX sows receiving replacement with both P4 and E2. Standard errors of the means (SEM) reported in Figures 1b and 2 were determined using the repeated-measures option of the GLM procedure of SAS and are the maximum standard errors of the least-squares means.
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RESULTS
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Concentrations of P4 in sows from this experiment are presented in Figure 1b. A normal pattern of P4 concentrations was observed in the intact control sows. Concentrations of P4 peaked at about 40 ng/ml on Days 12–14. Luteolysis began on Day 15 in most sows. Concentrations of P4 in OVX sows were elevated after twice daily injections of P4 during the pretreatment period. Concentrations reached about 20 ng/ml. A cyclic pattern of P4 was produced in OVX sows that received P4 injections during the treatment period. However, the absolute levels of P4 achieved lagged behind those of the intact sows by about 2 days and reached a maximum concentration that was only about one half of that reached in the intact sows.
The concentration of PGFM in jugular venous serum during the three bleeding periods for each group of sows is presented in Figure 2. Baseline concentrations of PGFM were similar among the four steroid replacement groups on Day 12 of the treatment period (Fig. 3). No effects of steroid treatments were detected. However, on Days 15 and 18, baseline concentrations of PGFM were higher in sows that received P4 replacement. Baseline concentrations remained low in sows that did not receive P4.
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FIG. 2. Concentrations of PGFM after i.v. injection of oxytocin at 0 min on Days 12, 15 and 18 after estrus in intact control sows (triangles), and in OVX sows receiving no steroids (open squares) or receiving E2 (solid squares), P4 (open circles), or P4 + E2 (solid circles). For effects within sow (time postinjection and time x treatment), residual (error) mean square in repeated measures ANOVA was 28 315 with 248 df on Day 12, 65 415 with 232 df on Day 15, and 443 916 with 272 df on Day 18
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FIG. 3. Baseline concentrations of PGFM in OVX sows receiving no steroids (ovx), or receiving E2 (ovx+E), P4 (ovx+P), or P4 + E2 (ovx+P,E) on Days 12, 15, and 18 after estrus. Bars represent least-squares means. Lines above bars represent the standard error of the least-squares mean
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The magnitude of the response to oxytocin was low and similar in all four steroid treatment groups on Day 12 (Fig. 4). On Day 15, a significant interaction between E2 and P4 was observed (P < 0.01). Responses were extremely small in sows that received no steroid or replacement with either steroid alone. The only treatment group that responded to oxytocin on Day 15 was the group that received both steroids. By Day 18, the magnitude of the response was higher in both groups of sows that received P4 replacement (main effect of P4, P < 0.01). Responses remained low in the two groups that did not receive P4.
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FIG. 4. Magnitude of the PGFM response to an i.v. injection of oxytocin in OVX sows receiving treatments as described in Figure 3. Bars represent least-squares means. Lines above bars represent the standard error of the least-squares mean
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Effects of steroids on the AUC following oxytocin injection were similar to the effect on the magnitude of the response (Fig. 5). On Day 12, there was no effect of steroid treatment. Responses were small in all 4 groups. On Day 15, an interaction between the two steroids was observed (P = 0.08), as the response to oxytocin was increased only in the sows that received both steroids. Responses were extremely low in the other 3 groups. On Day 18, a main effect of P4 was observed (P < 0.01). In contrast to the effects of steroids on magnitude of the response, a main effect of E2 (P = 0.02) and an interaction of the two steroids (P = 0.04) were also observed. Each steroid appeared to exert beneficial effects on the AUC when added alone, and both steroids had a synergistic effect when added together.
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FIG. 5. AUC after an i.v. injection of oxytocin in OVX sows receiving treatments as described in Figure 3. Bars represent least-squares means. Lines above bars represent the standard error of the least-squares mean
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All three responses were also compared between sows that received both E2 and P4, and intact sows (Fig. 6). Baseline concentrations of PGFM were similar in the two groups on all three days. In contrast, the magnitude of responses and AUCs were greater in OVX sows receiving steroid replacement than in the intact sows on Days 15 and 18. The AUC in the OVX sows that received both P4 and E2 was greater on Day 12 as well, when responses in both groups were relatively low.
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FIG. 6. Baseline concentrations of PGFM, magnitude of the PGFM response, and AUC in intact sows (gray bars) and in OVX sows receiving P4 + E2 (black bars) on Days 12, 15, and 18 after estrus. Bars represent least-squares means. Lines above bars represent the standard error of the least-squares mean. *Difference (P < 0.05) between groups tested within day postestrus
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DISCUSSION
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Both the timing and the magnitude of uterine secretory responsiveness to oxytocin in OVX sows are regulated by ovarian steroids. Sows that received no steroid replacement during the treatment period secreted very little PGF2, either endogenously or in response to oxytocin. P4 had a very pronounced effect, particularly on baseline concentrations of PGFM. On both Days 15 and 18, baseline concentrations of PGFM were greater in sows that received P4 than in those that did not. OVX sows must receive P4 replacement for the uterus to develop secretory responsiveness to oxytocin. Thus, the pig is similar to ruminants in that P4 appears to play a critical role in inducing uterine secretory responsiveness to oxytocin. E2 appears to have important effects on PGF secretion as well. E2 was required for sows to develop uterine secretory responsiveness to oxytocin on Day 15 (the normal time). In the absence of E2, secretory responsiveness to oxytocin did not develop until Day 18 postestrus, even in OVX sows that received P4 replacement. On Day 18, E2 appeared to have a beneficial effect on the magnitude of the PGFM response, over and above that observed when P4 is administered alone. Our conclusions about the role of E2 in regulating PGF2 secretion need to be considered with caution because nonovarian sources of E2 may exist in the sow. Thus, it is more accurate to consider the observed effects to be due to the absence or presence of ovarian E2.
The beneficial effects of E2 described here are in extreme contrast to inhibitory effects of E2 when it is administered as an acute injection in larger doses during the middle portion of the estrous cycle. When E2 is administered in this way, it suppresses both endogenous [6–9] and oxytocin-induced secretion of PGF2 [10] and thereby induces pseudopregnancy [16–19].
The P4 replacement protocol used in this experiment was effective in producing a cyclic pattern of P4 that was, in some respects, similar to that observed during a normal estrous cycle. However, in absolute terms, it was deficient in two critical ways. First, concentrations of P4 increased more rapidly in intact sows than in OVX sows receiving P4 injections. Intact sows appeared to reach a given concentration of P4 approximately two days earlier. Intact sows also achieved a maximal concentration that was approximately twice that achieved in the OVX sows that received P4 replacement. Despite these apparent deficiencies in the P4 replacement protocol, the OVX sows that received both P4 and E2 replacement had preinjection baseline concentrations of PGFM and developed uterine secretory responsiveness to oxytocin at the same time as intact sows. Surprisingly, the magnitude and the AUC in OVX sows exceeded those observed in intact sows, despite the apparent deficiencies of the P4 protocol.
The ability to release PGFM in response to oxytocin on Day 15 was particularly interesting in light of a previous study in our laboratory. In that study, we observed that uterine secretory responsiveness to oxytocin could be induced to occur prematurely by administering very high doses of P4 on Days 1–5 of the estrous cycle [5]. We concluded that the duration of uterine exposure to P4 was the critical factor that determined when uterine responsiveness to oxytocin should develop. The data from the current experiment may indicate that the threshold concentration that P4 must achieve to initiate this response may be relatively low. The higher magnitude of the response to oxytocin in OVX sows that received both steroids may be due in part to our protocol, which produced a P4:E2 ratio more favorable to uterine PGF2 secretion than the ratio that typically occurs in intact sows. However, it must also be recognized that intact sows are actively secreting PGF2 during the luteolytic and postluteolytic period, as has been shown in numerous previous experiments [8,20,21] and as indicated by the high baseline level of secretion in intact sows observed in this experiment. It is possible that the uterus of intact sows may be less responsive to exogenous oxytocin because these sows are already actively secreting PGF2 or because the uterus has been desensitized by endogenous oxytocin.
The shape of the PGFM response curve was qualitatively different on Day 15 versus 18. On Day 15 in intact sows, the response to oxytocin was extremely acute, peaking at 2–5 min postinjection. Carnahan et al. [22] observed a similar acute response to oxytocin on Days 14 and 16 postestrus. On Day 18, the response was much more sustained, peaking at 45–60 postinjection. We observed the same pattern of acute and sustained responses to oxytocin on Days 15 and 18 postestrus in a previous study [10]. This characteristic temporal pattern of response was also observed in OVX sows receiving both P4 and E2 replacement in the present experiment. The acute nature of the response on Day 15 resulted in a relatively small AUC despite a relatively high magnitude of the response (compare Figs. 4 and 5). The physiological significance of this qualitative difference in the pattern of secretion is not apparent. OVX sows that only received P4 replacement did not respond to oxytocin on Day 15. On Day 18, they showed an acute response, similar to the response of OVX sows that received P4 and E2 replacement and of intact sows on Day 15. This again points out how uterine secretory responsiveness develops more slowly in the absence of E2.
In summary, P4 and E2 interact to control the onset and the magnitude of uterine secretory responsiveness to oxytocin in sows. Through this effect, these hormones determine the time when endogenous secretion of PGF2 begins and the timing of luteal regression.
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ACKNOWLEDGMENTS
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The authors are indebted to J. Monegue and the farm crew at the University of Kentucky swine unit for their assistance with the animals. The authors are also indebted to S. Hayes, D. Vanderwall, P. Burns, G. Graf, V. Printz, D. Fernandez, T. Kline, and J. Light for assistance with surgical procedures and/or collection of blood samples.
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FOOTNOTES
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First decision: 12 May 1998.
1 This research was supported by the Kentucky Agricultural Experiment Station and a grant from the USDA (90-37240-5055). It is published with the approval of the director of the KY Agricultural Experiment Station (98-07-57). 
2 Correspondence. FAX: 606 323 1027; wsilvia{at}ca.uky.edu
Accepted: September 13, 1999.
Received: April 9, 1998.
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ABSTRACT
INTRODUCTION
