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J. Anim. Sci. 2003. 81:1830-1836
© 2003 American Society of Animal Science

Oxytocin-induced secretion of prostaglandin F2{alpha} in postpartum beef cows: Effects of progesterone and estradiol-17ß treatment1

K. R. Kieborz-Loos*, H. A. Garverick*, D. H. Keisler*, S. A. Hamilton*, B. E. Salfen2, R. S. Youngquist{dagger} and M. F Smith*,3

* Animal Sciences Department and and {dagger} Department of Veterinary Medicine and Surgery, University of Missouri, Columbia 65211

3 Correspondence:
160 Animal Sciences Center (phone: 573-882-8239; fax: 573-882-6827; E-mail:
Smithmf{at}missouri.edu).


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The purpose of the present study was to determine the effect of progesterone or progesterone + estradiol-17ß on oxytocin-induced prostaglandin F2{alpha} (PGF2{alpha}) secretion in postpartum beef cows. Thirty-four anestrous postpartum beef cows were ovariectomized (d 32 [Groups 1 to 3] or d 23 [Groups 4 to 6] postpartum [d 0 = parturition]) and allotted to six treatments (Group 1; negative control) to simulate short (Groups 2 through 5) or normal (Group 6) length estrous cycles. Steroid treatments for the respective groups were as follows: Group 1) no estradiol-17ß or progesterone treatment (n = 8; negative control); Group 2) progesterone (d 34 to 40; n = 6); Group 3) estradiol-17ß (d 32 to 33) and progesterone (d 34 to 40; n = 6); Group 4) progesterone (d 23 to 29), no estradiol-17ß (d 32 to 33), and progesterone (d 34 to 40; n = 5); Group 5) progesterone (d 23 to 29), estradiol-17ß (d 32 to 33), and progesterone (d 34 to 40; n = 5); and Group 6) progesterone (d 23 to 29), estradiol-17ß (d 32 to 33), and progesterone (d 34 to 50; n = 4; positive control). Oxytocin (100 IU) was injected (i.v.) at the end of each treatment to test the ability of the postpartum uterus to secrete PGF2{alpha} as measured by a stable metabolite of PGF2{alpha}, 15keto-13,14 dihydro-PGF2{alpha} (PGFM). Peak concentrations of PGFM (P ≤ 0.08) and total PGFM secreted (area under the curve; P < 0.05) were increased on d 6 following first (Group 2) or second (Group 4) exposure to progesterone and were similar to peak concentrations and total PGFM secreted 16 d following a simulated normal estrous cycle (Group 6). Administration of estradiol-17ß before first progesterone exposure (Group 3) did not reduce peak concentrations of PGFM or total PGFM secreted relative to the preceding groups. Peak concentrations of PGFM (P ≤ 0.08) and total PGFM secreted (P < 0.05) were reduced following a second progesterone exposure, provided that cows were pretreated with estradiol-17ß (Group 5). In summary, oxytocin-induced release of PGFM was inhibited on d 6 following second exposure to progesterone only when cows were pretreated with estradiol-17ß. Therefore, estradiol-17ß and progesterone were both associated with the timing of PGF2{alpha} secretion in postpartum cows.

Key Words: Cattle • Postpartum Period • Prostaglandins • Steroids • Uterus


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Short luteal phases frequently occur following the first ovulation postpartum in cattle and are due to an advance in the timing of uterine secretion of prostaglandin F2{alpha} (PGF2{alpha}; for a review, see Garverick et al., 1992). Although the mechanism by which the timing of PGF2{alpha} secretion is advanced in domestic ruminants during a short luteal phase has not been elucidated, a role for progesterone, estradiol-17ß, and oxytocin has been proposed (Hunter, 1991). Progestogen pretreatment is necessary for normal luteal lifespan and timing of uterine secretion of PGF2{alpha} following the first estrus postpartum in cattle and sheep (Lishman and Inskeep, 1991). However, it is unclear whether progestogen pretreatment has an indirect and/or direct effect on the timing of uterine PGF2{alpha} secretion.

Preovulatory concentrations of estradiol-17ß were lower preceding a short vs. a normal-length luteal phase (Sheffel et al., 1982; Garcia-Winder et al., 1986; Garverick et al., 1988). Progestogen pretreatment may indirectly affect the timing of PGF2{alpha} secretion by increasing preovulatory concentrations of estradiol-17ß. In cows exhibiting a normal luteal phase, the elevated preovulatory concentrations of estradiol-17ß may induce uterine progesterone receptors and thereby permit progesterone to program the secretion of PGF2{alpha} to occur later in the luteal phase. Alternatively, progestogen pretreatment may have a direct effect on the secretion of PGF2{alpha} because the postpartum bovine uterus increases secretion of PGF2{alpha} soon after the first exposure to exogenous progestogen (Cooper et al., 1991). However, there is no evidence at this time to indicate that progesterone can directly advance the timing of PGF2{alpha} secretion from the uterus in domestic animals with short luteal phases. The objective of this study was to determine the effect of progesterone alone or in combination with estradiol-17ß on oxytocin-induced PGF2{alpha} release in postpartum beef cows.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
Animals
Beef cows in moderate body condition (n = 34) were assigned to six treatment groups at parturition (d 0) according to age and breed (Figure 1Go). From calving until ovariectomy, ovarian activity was monitored by estrous detection and determination of serum concentrations of progesterone collected three times weekly via jugular venipuncture. Cows detected to be in standing estrus or with an increase in serum concentrations of progesterone (>1 ng/mL) at any time preceding ovariectomy were classified as having luteal tissue and were not included in the present study.



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  		Figure 1. Outline of the experimental design indicating the time of ovariectomy (Ovex), steroid treatment (estradiol-17ß and/or progesterone [Prog]), and oxytocin treatment for each group (d 0 = parturition). Steroid treatments were designed to simulate short (Groups 2 to 5) or normal (Group 6; positive control) duration estrous cycles. Group 1 served as a negative control.

 
Steroid Replacement Treatment
Cows were ovariectomized via para-lumbar laparotomy on either d 32 (Groups 1 to 3) or d 23 (Groups 4 to 6) following calving (d 0). Calves were weaned at ovariectomy. Steroid treatments for the respective groups (Figure 1Go) were as follows: Group 1) no estradiol-17ß or progesterone treatments (n = 8; negative control); Group 2) progesterone (d 34 to 40; n = 6); Group 3) estradiol-17ß (d 32 to 33) and progesterone (d 34 to 40; n = 6); Group 4) progesterone (d 23 to 29, no estradiol-17ß (d 32 to 33), and progesterone (d 34 to 40; n = 5); Group 5) progesterone (d 23 to 29), estradiol-17ß (d 32 to 33), and progesterone (d 34 to 40; n = 5); and Group 6) progesterone (d 23 to 29), estradiol-17ß (d 32 to 33), and progesterone (d 34 to 50; n = 4; positive control). The purpose of Groups 1, 2, and 3 was to determine the effect of progesterone (d 34 to 40) with or without estradiol-17ß pretreatment (d 32 to 33) on oxytocin-induced PGF2{alpha} secretion on d 6 of progesterone treatment (d 40). The purpose of Groups 4 and 5 was to determine the effect of progesterone (d 34 to 40) following progesterone pretreatment (d 23 to 29) with or without estradiol-17ß (d 32 to 33) on oxytocin-induced PGF2{alpha} secretion. Group 6 served as a positive control for oxytocin-induced PGF2{alpha} release. Progesterone was delivered via a progesterone-releasing intravaginal device (PRID; Sanofi Animal Health, Watford, U.K.) and estradiol-17ß was delivered by i.m. injection (100 µg) every 8 h for 48 h. Serum concentrations of progesterone and estradiol-17ß following steroid treatment are depicted in Figures 2Go and 3Go, respectively.



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  		Figure 2. Serum concentrations of progesterone in ovariectomized cows following no treatment (Group 1) or administration of one (Groups 2 and 3) or more progesterone-releasing intravaginal devices (PRID; Groups 4 to 6). Day 0 pertains to the day the first PRID was administered and duration of PRID treatment is indicated by the black horizontal bars.

 


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  		Figure 3. Serum concentrations of estradiol-17ß in ovariectomized cows following i.m. injections (arrows) of estradiol-17ß (100 µg) every 8 h for 48 h. Blood samples were collected hourly for 12 h beginning 1 d before the first injection of estradiol-17ß (0 h) and continuing for 4 d. Arrows indicate when injections were given.

 
Blood Collection and Oxytocin Treatment
Blood samples were collected via venipuncture daily from ovariectomy until oxytocin treatment to determine serum concentrations of progesterone. To characterize serum concentrations of estradiol-17ß following injection, blood samples were collected hourly for 12 h during a 5-d period beginning 1 d before the first injection of estradiol-17ß. Injections of oxytocin have been used to test the ability of the uterus to secrete PGF2{alpha} as measured by the stable metabolite 15-keto-13,14 dihydro- PGF2{alpha} (PGFM) (LaFrance and Goff, 1985; Zollers et al., 1989). Oxytocin (100 IU) was injected (i.v.) into each cow on d 40 (Groups 1 to 5) or d 50 (Group 6). Blood was collected via venipuncture every 15 min for 1 h preceding oxytocin injection and for 4 h post injection. Blood was allowed to clot at room temperature for 1 h and placed at 4°C overnight. Serum was collected following centrifugation and stored frozen at -20°C until concentrations of PGFM were determined by RIA. Changes in peripheral concentrations of PGFM have been shown to accurately reflect changes in uterine PGF2{alpha} secretion (Kindahl et al., 1976; Guilbault et al., 1984).

Radioimmunoassay
Serum concentrations of progesterone (Cantley et al., 1975), estradiol-17ß (Rozell and Keisler, 1990), and PGFM (Zollers et al., 1989) were determined by validated RIA. Inter- and intraassay CV were 10 and 8% for progesterone, 11 and 9% for estradiol-17ß, and 18 and 15% for PGFM, respectively.

Statistical Analysis
Data analyses were conducted using SAS (SAS Inst., Inc., Cary, NC, version 8.1). Serum concentrations of PGFM were analyzed by ANOVA for repeated measures (Gill and Hafs, 1971). Means were separated using preplanned comparisons of least squares means generated with the PDIFF function. The GLM was treatment, time, and treatment x time interaction. Cow within treatment was used as the error term for testing treatment effects.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
Administration of a PRID increased serum concentrations of progesterone in ovariectomized cows to within the physiological range during the luteal phase and simulated luteal phases of short (Groups 2 to 5) or normal (Group 6) duration (Figure 2Go). Following injection (i.m.) of 100 µg of estradiol-17ß, serum concentrations of estradiol-17ß increased to between 20 and 25 pg/mL within 1 h of injection and decreased to between 4 and 5 pg/mL 7 h later (Figure 3Go).

As expected, peak concentrations of PGFM and total PGFM secreted (area under the curve) following oxytocin injection were less in cows that received no steroid treatment (Group 1; Figure 4Go). Conversely, peak concentrations of PGFM and total PGFM secreted were increased (P ≤ 0.08 and P < 0.05, respectively) on d 16 of the second progesterone treatment when animals were pretreated with both progesterone and estradiol-17ß (Group 6; simulated normal estrous cycle; positive control; Figure 4Go). Peak concentrations of PGFM and total PGFM secreted in response to oxytocin were increased (P ≤ 0.08 and P < 0.05, respectively) on d 6 following the first (Group 2) or second (Group 4) treatment with progesterone compared with no steroid treatment (Group 1; Figure 4Go). Furthermore, peak concentrations of PGFM secreted on d 6 of a simulated short estrous cycle (Groups 2 and 4) were similar to peak concentrations of PGFM and total PGFM secreted on d 16 of a simulated normal estrous cycle (Group 6; Figure 4Go). Administration of estradiol-17ß before first progesterone treatment (Group 3) did not reduce peak concentrations of PGFM or total PGFM secreted relative to progesterone treatment alone (Groups 2 and 4; Figure 4Go). However, when progesterone treatment was preceded by progesterone and estradiol-17ß (Group 5), the total PGFM secreted on d 6 was decreased (P < 0.05) and similar to no steroid treatment (Group 1; Figure 4Go).



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  		Figure 4. Effect of oxytocin treatment (100 IU injected i.v. on d 40 in Groups 1 to 5 and d 50 in Group 6) on peak concentration of 15- keto-13,14 dihydro-PGF2{alpha} (PGFM; pg/mL) and total PGFM secreted (pg/[mL x h] x100) for Groups 1 to 6. Steroid treatments for the respective groups were: Group 1) no estradiol-17ß or progesterone treatments (n = 8; negative control); Group 2) progesterone (d 34 to 40; n = 6); Group 3) estradiol-17ß (d 32 to 33) and progesterone (d 34 to 40; n = 6); Group 4) progesterone (d 23 to 29, no estradiol-17ß (d 32 to 33), and progesterone (d 34 to 40; n = 5); Group 5) progesterone (d 23 to 29), estradiol-17ß (d 32 to 33), and progesterone (d 34 to 40; n = 5); and Group 6) progesterone (d 23 to 39), estradiol-17ß (d 32 to 33), and progesterone (d 34 to 50; n = 4; positive control). Means that have different superscripts differed for peak concentration of PGFM (P ≤ 0.08) and total PGFM secreted (P < 0.05).

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
Corpora lutea with short lifespans have been detected at puberty in cattle (Gonzalez-Padilla et al., 1975) and sheep (Berardinelli et al., 1980) and following the first postpartum ovulation in cattle (Odde et al., 1980) or following induction of ovulation in anestrous ewes (Haresign et al., 1975). Several pieces of evidence indicate that short luteal phases in cattle and sheep are due to premature uterine secretion of PGF2{alpha}. First, hysterectomy prevented regression of corpora lutea anticipated to have short lifespans in prepuberal ewe lambs (Keisler et al., 1983), anestrous ewes (Southee et al., 1988), and postpartum cows (Copelin et al., 1987). Second, active immunization of postpartum cows against PGF2{alpha} extended the lifespan of corpora lutea anticipated to have a short lifespan (Copelin et al., 1989). Third, oxytocin induced the release of PGFM in cattle on d 5 of a short, but not a normal, luteal phase (Zollers et al., 1989). Fourth, basal and oxytocin-induced secretion of prostaglandins in vitro from bovine endometrium was increased on d 5 of a short vs. normal-length luteal phase (Zollers et al., 1991). Fifth, mean concentrations of PGF2{alpha} in the vena cava were greater on d 4 to 9 of a short vs. normal luteal phase in postpartum cows (Cooper et al., 1991). Sixth, mean concentrations of PGFM in plasma were increased from d 3 to 5 in ewes anticipated to have short luteal phases (Hunter et al., 1989).

A role for ovarian steroids and oxytocin in the regulation of uterine secretion of PGF2{alpha} has been proposed (McCracken et al., 1984; Silvia et al., 1991). McCracken et al. (1984) hypothesized that during an estrous cycle of normal duration, progesterone, through binding to its endometrial receptor, inhibits synthesis of endometrial oxytocin receptors during the early luteal phase, a time when the uterus is under the dominant effect of progesterone. As the bovine estrous cycle progresses through the mid-luteal phase, concentration of progesterone receptors in the endometrium decreases (Meyer et al., 1988). The preceding loss of progesterone receptors has been hypothesized to permit synthesis of endometrial oxytocin receptors. Consequently, the uterus becomes responsive to oxytocin and a positive feedback mechanism is established between oxytocin (luteal and/or posterior pituitary origin) and endometrial PGF2{alpha} secretion. However, treatment of cows with an oxytocin antagonist did not inhibit luteolytic PGF2{alpha} secretion (Kotwica et al., 1997). Consequently, the role of oxytocin in the luteolytic cascade requires further investigation.

In nonpregnant heifers, concentrations of PGFM after oxytocin injection were elevated on d 17 to 19, but not on d 6 or 13 of the estrous cycle (d 0 = estrus; Lafrance and Goff, 1985). Similarly, in the present study, oxytocin-induced release of PGFM was increased on d 16 (Group 6), but not d 6 (Group 5) of a simulated normal luteal phase. Consequently, the steroid treatment (Groups 5 and 6) simulated uterine responsiveness during a normal bovine estrous cycle.

At the time of luteolysis in cattle and sheep, luminal epithelial cells have oxytocin receptors and secrete PGF2{alpha} (Vallet et al., 1990; Silvia et al., 1991; Mann and Lamming, 1994). Although endometrial oxytocin receptors were elevated in ovariectomized cows, oxytocin-induced release of PGFM was less (Lamming and Mann, 1995). Similarly, the oxytocin-induced PGFM release was less in ovariectomized ewes (Vallet et al., 1990) and in Group 1 of the present study. Lamming and Mann (1995) proposed that progesterone, but not estradiol-17ß treatment, is required for oxytocin receptors to become functionally linked to PGF2{alpha} secretion in ovariectomized cows. In addition, progesterone has been reported to induce uterine prostaglandin synthetase activity in ewes (Salamonson et al., 1991). Consequently, it is likely that progesterone is required for endometrial PGF2{alpha} secretion in ruminants.

Although a period of progesterone priming is necessary for uterine PGF2{alpha} secretion (Lamming and Mann, 1995), it is unknown whether progesterone directly or indirectly coordinates the timing of uterine PGF2{alpha} secretion in cattle. In the present study, oxytocin-induced release of PGFM was increased 14 to 16 d following progesterone treatment (Group 6), and similar results have been reported in ovariectomized ewes administered progesterone for 10 to 12 d (Vallet et al., 1990). In the preceding study, the most normal pattern of PGFM occurred when ewes were exposed to a sequence of progesterone, estradiol, and progesterone. This steroid sequence is similar to Group 6 in the present study. In postpartum cows, uterine secretion of PGF2{alpha} increased within 3 to 5 d of first ovulation (Zollers et al., 1989; Cooper et al., 1991) or progestogen treatment (Cooper et al., 1991). Similarly, oxytocin-induced PGFM secretion was increased after 6 d of progesterone treatment in ovariectomized postpartum cows (Group 2). In long-term ovariectomized cows, Lamming and Mann (1995) reported that oxytocin-induced release of PGFM was increased after 6, 12, or 18 d of progesterone treatment. However, treatment with estradiol-17ß alone did not increase oxytocin-induced release of PGFM at any of the preceding time points. Secretion of PGFM was also increased on d 6 after the second treatment with progesterone (Group 4). Consequently, progesterone priming (in the absence of estradiol-17ß) did not prevent an increase in oxytocin-induced PGFM secretion following the second exposure to progesterone.

Progestogen pretreatment increased preovulatory concentrations of estradiol-17ß and prolonged luteal lifespan in cattle (Garverick et al., 1988). Estradiol-17ß has been shown to increase uterine progesterone receptors in sheep (Zelinski et al., 1980) and may permit progesterone to coordinate the timing of PGF2{alpha} secretion. Preovulatory concentrations of estradiol-17ß were lower preceding a short vs. normal-length luteal phase (Sheffel et al., 1982; Garcia-Winder et al., 1986; Garverick et al., 1988). In cows exhibiting a short luteal phase, the reduced concentrations of estradiol-17ß detected during the preovulatory period may not induce an adequate number of endometrial progesterone receptors to program the secretion of PGF2{alpha} to occur at a later time in the luteal phase. In support of the preceding hypothesis, Zollers et al. (1993) reported that concentration of endometrial progesterone receptor was lower and concentration of endometrial oxytocin receptor was greater on d 5 in cows anticipated to have a short vs. normal luteal phase. However, when injections of estradiol-17ß preceded progesterone treatment for 6 d (Group 3), oxytocin-induced PGFM secretion was similar to that following a first (Group 2) or second (Group 4) treatment with progesterone alone. The only treatment that prevented an oxytocin-induced secretion of PGFM on d 6 that was similar to the release at the end of a simulated normal estrous cycle (Group 6) was the estradiol-17ß/progesterone treatment preceded by progesterone priming. Consequently, progesterone priming followed by an increase of estradiol-17ß for 2 d was necessary to prevent an advance in the timing of PGF2{alpha} secretion. The mechanism by which progesterone priming permits estradiol-17ß and progesterone to prevent an advance in the timing of PGF2{alpha} secretion is not known and requires further investigation.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
Short luteal phases commonly occur before the first ovulatory estrus in peripuberal heifers and anestrous postpartum cows. Previous studies have demonstrated that short luteal phases are due to an advance in the timing of uterine prostaglandin F2{alpha} secretion. Although progesterone, estradiol-17ß, and oxytocin are generally believed to have a role in the regulation of uterine prostaglandin F2{alpha} secretion during the estrous cycles of cows, there is very little information available regarding the steroid regulation of prostaglandin F2{alpha} secretion in postpartum cows. The current study indicates that progesterone alone is not capable of establishing a normal timing of prostaglandin F2{alpha} secretion in postpartum cows. Rather, both progesterone and estradiol-17ß are required to delay the advance in uterine prostaglandin F2{alpha} secretion that normally occurs during a short luteal phase.


   Footnotes
 
1 This research was funded by the Missouri Agric. Exp. Stn. and USDA Grant CSRS 90-37240-5777. Back

2 Current address: USDA-ARS, Columbia, MO, 65211. Back

Received for publication July 2, 2002. Accepted for publication April 11, 2003.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


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