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Biology of Reproduction 62, 1047-1051 (2000)
© 2000 Society for the Study of Reproduction, Inc.

Articles

Effect of Dose of Prostaglandin F2{alpha} on Steroidogenic Components and Oligonucleosomes in Ovine Luteal Tissue1

J.L. Juengela, J.D. Hawortha, M.K. Rollysona, P.J. Silvaa, H.R. Sawyera, and G.D. Niswender2,a

a Animal Reproduction and Biotechnology Laboratory, Colorado State University, Fort Collins, Colorado 80526


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
To determine whether prostaglandin (PG) F2{alpha} had a dose-dependent effect upon secretion of progesterone, oligonucleosome formation, or loss of luteal weight, ewes on Day 9 or 10 of the estrous cycle were administered 0, 3, 10, or 30 mg PGF2{alpha} per 60 kg BW (i.v.), and luteal tissue was collected 9 and 24 h after injection. All doses of PGF2{alpha} decreased (P < 0.05) concentrations of progesterone in sera by 9 h; however, in ewes treated with 3 mg PGF2{alpha}, concentrations of progesterone were similar to control values at 24 h and higher (P < 0.05) than those in the 10- or 30-mg groups. Concentrations of progesterone in sera over all dose levels were highly correlated to luteal concentrations of mRNA encoding steroidogenic acute regulatory protein (P < 0.001), cytochrome P450 side-chain cleavage (P < 0.02), and 3ß-hydroxysteroid dehydrogenase (P < 0.01). Corpora lutea collected at 24 h from ewes treated with the 10- and 30-mg doses of PGF2{alpha} weighed less (P < 0.05) than those from controls. Oligonucleosomes were not present in luteal tissues from control ewes. Surprisingly, all doses of PGF2{alpha}-induced oligonucleosomes in a majority of animals at 9 h and in a majority of ewes treated with 10 and 30 mg of PGF2{alpha} at 24 h. In conclusion, 3 mg of PGF2{alpha} per 60 kg BW transiently decreased serum concentrations of progesterone and induced oligonucleosome formation, but did not result in reduced luteal weight. The 10- and 30-mg doses of PGF2{alpha} decreased secretion of progesterone and induced oligonucleosome formation and luteolysis.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Luteal regression in the ewe is characterized by a rapid decline in concentrations of progesterone in serum followed by decreased luteal weight [1]. It is known that binding of prostaglandin (PG) F2{alpha} to its receptor decreases luteal synthesis of progesterone and causes luteal cell death [2]. The protein kinase C (PKC) and calcium second messenger pathways appear to mediate the actions of PGF2{alpha} [2]. Pharmacological activation of PKC mimics the antisteroidogenic effects of PGF2{alpha} [3, 4] but does not cause luteal cell death [4], which is thought to be caused by an influx of calcium [5]. Thus, decreased secretion of progesterone appears to be regulated by a different second messenger system than luteal cell death, although both processes are induced by PGF2{alpha}.

Administration of a luteolytic dose of PGF2{alpha} decreases mRNA encoding several proteins important for regulation of progesterone synthesis including the receptors (R) for LH [6, 7], low-density lipoprotein [8], and PGF2{alpha} [9–11], as well as steroidogenic acute regulatory (StAR) protein [12, 13], cytochrome P450 side-chain cleavage enzyme (P450scc) [14], and 3ß-hydroxysteroid dehydrogenase/{Delta}5,{Delta}4 isomerase (3ß-HSD) [4, 14, 15]. However, whether decreased concentrations of specific mRNAs, and presumably the specific protein, is the key to decreased concentrations of progesterone in sera following treatment with PGF2{alpha} is not clear. Quantities of cytochrome P450scc and 3ß-HSD proteins do not decrease until after secretion of progesterone has already declined [16]. Injection of PGF2{alpha} also induces oligonucleosome formation in luteal tissue, a biochemical indicator of apoptosis [4, 17–19]. Once a cell forms oligonucleosomes it is irreversibly committed to undergo cell death [20]. Induction of oligonucleosome formation occurs after concentrations of progesterone in serum and luteal tissue have decreased, but before observed decreases in luteal weight [14, 19]. Thus, formation of oligonucleosomes has been associated with loss of luteal tissue.

In the ewe and cow, PGF2{alpha} is released from the uterus in a pulsatile manner towards the end of the estrous cycle to induce luteolysis. Pulses of PGF2{alpha} increase in both frequency and amplitude during the period of luteal regression [21–23]. However, the largest peaks of PGF2{alpha} occur after concentrations of progesterone in sera have already dramatically decreased. Thus, the physiological role of these large pulses of PGF2{alpha} in luteal regression is unclear. Therefore, the hypothesis to be tested was that a single, low dose of PGF2{alpha} would decrease secretion of progesterone without causing luteolysis, whereas a single, high dose of PGF2{alpha} would result in both decreased secretion of progesterone and luteolysis.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Western range ewes were used in all experiments and observed for estrus (Day 0) with the aid of vasectomized rams. Ewes were weighed 1 day before the start of the experimental protocol, and PGF2{alpha} was administered on a per kilogram of body weight basis. The average body weight of the ewes used for experiment 1 was 60 kg. All experimental protocols were approved by the Colorado State University Animal Care and Use Committee.

Experimental Design

Experiment 1 Ewes on Day 9 or 10 of the estrous cycle were administered a single intrajugular injection of 0, 1, 3, 10, or 30 mg PGF2{alpha} (Lutalyse; Upjohn Company, Kalamazoo, MI) per 60 kg BW (n = 4 ewes per dose). Doses of PGF2{alpha} were administered in 1 ml saline with ewes in the 0 dose group receiving only saline. Dilutions of PGF2{alpha} were made within 2 h of injection. The i.v. route of injection was used to ensure that corpora lutea in ewes within a treatment group would be exposed to similar doses and to prevent variation due to site of injection and absorption rates seen with i.m. injection. Ewes were bled -1, 0, 2, 4, 6, 9, 12, 24, 36, and 48 h relative to the time of injection of PGF2{alpha}, and concentrations of progesterone in sera were determined by RIA [24].

Experiment 2 Ewes on Day 9 or 10 of the estrous cycle received injections of 0, 3, 10, or 30 mg PGF2{alpha} per 60 kg BW into the jugular vein as described for experiment 1. Corpora lutea were collected 9 or 24 h after injection of PGF2{alpha} (n = 5 ewes per time per dose). These times were based on the results of experiment 1, in which progesterone levels reached their nadir at 9 h, and by 24 h were back to pre-injection levels in ewes receiving the 3-mg dose of PGF2{alpha}. After collection, corpora lutea were decapsulated, weighed, frozen in liquid nitrogen, and stored at -70°C until isolation of poly A+ RNA and DNA. Blood samples were collected by jugular venipuncture at the time of tissue collection for determination of serum concentrations of progesterone.

Determination of Concentrations of Progesterone in Sera

Concentrations of progesterone in sera from experiments 1 and 2 were determined in 4 RIAs [24]. Intraassay coefficients of variation (CV) averaged 8%, and the interassay CV was 12.4%. The limit of sensitivity of all assays was less then 56 pg/ml.

Quantification of mRNAs Encoding LHR, PGF2{alpha}-R, StAR, P450scc, and 3ß-HSD

Unless otherwise specified, all materials were purchased from Sigma Chemical Company (St. Louis, MO) or Fisher Scientific (Denver, CO). Polyadenylated RNA (Poly A+ RNA) was isolated using oligodeoxythymidine (dT) cellulose as previously described [6, 25]. Tissue samples from one ewe treated with the 3-mg and 10-mg doses of PGF2{alpha} collected at 9 h were lost during isolation and therefore not included in RNA analysis. Concentrations of mRNA in isolated samples were determined by absorbance at 260 nm.

Concentrations of mRNAs encoding LHR [6], PGF2{alpha}-R [9], StAR [12], P450scc [26], and 3ß-HSD [27] were determined by slot blot analysis as previously described. Radioactive cDNAs were generated with the random primer method [28] and had specific activities ranging from 0.4 to 0.5 x 109 dpm/µg DNA. Standard curves were linear, with correlations (r2) between amount of standard added and the resulting densitometric readings ranging from 0.95 to 0.99. Intraassay CVs were 10%, 11%, 12%, 14%, and 16% for mRNAs encoding LHR, PGF2{alpha}-R, StAR, P450scc, and 3ß-HSD, respectively. Sensitivity of the assay, as determined by the lowest detectible point on the standard curve, was 1.79, 0.53, 1.98, 0.46, and 1.7 fmol/µg poly A+ RNA for mRNAs encoding LHR, PGF2{alpha}-R, StAR, P450scc, and 3ß-HSD, respectively. Presence of oligonucleosomes in luteal samples was determined by ethidium bromide staining of DNA following gel electrophoresis [17].

Statistical Analysis

All statistical analyses were performed with the general linear model procedure of SAS [29]. To determine whether the number of ewes in the PG2{alpha} treatment groups that contained oligonucleosomes in their corpora lutea was different from the number in the saline-treated group, chi-square analysis was performed. To account for variability in baseline concentrations of progesterone in sera among ewes, all values post-injection were expressed as a percentage of the average value of the -1-h and 0-h samples. Because of non-normal distribution (Wilk-Shapiro test) and heterogeneous variance (Fmax test), respectively, data regarding concentrations of progesterone in sera 9 h after injection in experiment 1 and data regarding concentrations of mRNA encoding PGF2{alpha}-R were transformed before final statistical analysis. However, the means ± SEM of raw data are presented. Differences between least-squares means were determined by least-significant differences. Significance of correlation coefficients between parameters was determined with Pearson's test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Experiment 1

Injection of all doses of PGF2{alpha} decreased (P < 0.05) concentrations of progesterone in sera within 4 h when compared to values obtained from saline-treated control ewes (Fig. 1). Concentrations of progesterone in sera returned to values that were not different from those in controls in ewes receiving injections of 1, 3, or 10 mg PGF2{alpha}/60 kg BW by 12, 18, and 24 h after injection, respectively (Fig. 1). However, ewes treated with 30 mg of PGF2{alpha}/60 kg BW had less (P < 0.05) progesterone in sera than did controls at all times sampled after 4 h post-injection (Fig. 1).



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  		FIG. 1. Mean concentrations of progesterone in sera after administration of 1 of 5 doses of PGF2{alpha}. The data are expressed as a percentage of the average value of the -1- and 0-h samples. All values below the asterisk are less than (P < 0.05) the time-matched 0 dose

Experiment 2

There were no significant differences in any parameter measured between the control groups at 9 and 24 h. Concentrations of progesterone in sera were lower (P < 0.05) in ewes treated with any dose of PGF2{alpha} at 9 and 24 h after injection than values obtained from controls (Table 1). However, concentrations of progesterone in sera in ewes treated with 3 mg PGF2{alpha} per 60 kg BW were greater (P < 0.05) than values obtained from ewes that had received 10 or 30 mg PGF2{alpha}. Corpora lutea collected from ewes treated with 10 or 30 mg, but not 3 mg, PGF2{alpha}/60 kg BW 24 h before collection weighed less (P < 0.05) than those collected from saline-treated ewes (Table 1). Luteal tissue collected 9 h after treatment contained oligonucleosomes in 4 of 5, 3 of 5, and 5 of 5 ewes treated with 3, 10, or 30 mg PGF2{alpha}, respectively (Fig. 2; Table 1). None of the ewes that received saline showed evidence of oligonucleosome formation. By 24 h after injection of PGF2{alpha}, luteal tissue collected from 4 of 5 or 5 of 5 ewes that had received 10 or 30 mg PGF2{alpha}/60 kg BW contained oligonucleosomes. However, there were no oligonucleosomes present in luteal tissue collected from 4 of 5 ewes that received 3 mg PGF2{alpha}/60 kg BW or in any ewes treated with saline (Table 1).


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  		TABLE 1. Effects of varying doses of PGF2{alpha} (mg/60 kg BW) on P4 in sera, luteal weight, and percentage of ewes with luteal oligonucleosome formation 9 and 24 h after injection



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  		FIG. 2. Representative ethidium bromide-stained DNA isolated from luteal tissue. Migration of DNA standards (base pairs; Hi-LH DNA markers; Minnesota Molecular, Bloomington, MN) is indicated on the left. Time of tissue collection and dose (mg/60 kg BW) of PGF2{alpha} administered is indicated at the top. Two representative samples per group are shown

Luteal concentrations of mRNA encoding StAR were decreased by all doses of PGF2{alpha} 9 h after injection (Table 2). However, by 24 h after injection, ewes receiving the 3-mg dose of PGF2{alpha} had concentrations of StAR mRNA that were not different from those obtained from saline-treated ewes (Table 2). Concentrations of StAR mRNA and progesterone in sera were highly correlated (R = 0.74, P < 0.001). Concentrations of mRNA encoding P450scc (Table 2) were decreased within 9 h in ewes administered 30 mg PGF2{alpha} and at 24 h in ewes administered 10 mg or 30 mg PGF2{alpha}/60 kg BW. This parameter was also correlated with concentrations of progesterone in sera (R = 0.40, P < 0.02). The 3-mg dose of PGF2{alpha} did not decrease luteal concentrations of mRNA encoding 3ß-HSD at 9 or 24 h following injection (Table 2). However, 10 mg or 30 mg of PGF2{alpha} decreased 3ß-HSD mRNA at 9 h, and 30 mg PGF2{alpha} also suppressed concentrations of mRNA encoding 3ß-HSD 24 h after injection. Concentrations of mRNA encoding 3ß-HSD were also correlated with concentrations of progesterone in sera (R = 0.46, P < 0.01). While 3 mg of PGF2{alpha}/60 kg BW did not affect concentrations of mRNA encoding LHR, higher doses of PGF2{alpha} decreased LHR mRNA at both 9 and 24 h after injection (Table 2). Concentrations of mRNA encoding the PGF2{alpha}-R were decreased by all doses of PGF2{alpha} 9 h following injection. However, only the highest dose of PGF2{alpha} suppressed concentrations of mRNA encoding PGF2{alpha}-R 24 h after injection.


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  		TABLE 2. Effects of varying doses of PGF2{alpha} (mg/60 kg BW) on mRNAs encoding StAR, P450scc, 3ß-HSD, LHR, and PGF2{alpha}-R 9 and 24 h after injection


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The low dose (3 mg/60 kg BW) of PGF2{alpha} decreased secretion of progesterone without causing luteolysis, whereas high doses of PGF2{alpha} (10 and 30 mg/60 kg BW) caused both decreased secretion of progesterone and luteolysis. One very interesting observation was that PGF2{alpha}-induced oligonucleosome formation in corpora lutea collected from most ewes by 9 h after injection, including 4 of 5 ewes that received 3 mg/60 kg BW PGF2{alpha}. However, at 24 h, only 1 of 5 ewes that had received the 3-mg dose of PGF2{alpha} had oligonucleosomes in luteal tissue. Thus, it would appear that corpora lutea from these ewes had recovered from the PGF2{alpha} injection and that induction of oligonucleosomes in luteal tissue was not a good indicator of impending luteolysis.

In morphological studies of the ovine corpus luteum, most of the cells observed with apoptotic characteristics were capillary endothelial cells, and no more than 5% of parenchymal cells showed signs of apoptosis at any one time following PGF2{alpha}-induced luteolysis [30]. Thus, it is likely that a majority of the cells that were undergoing apoptosis in the current study were endothelial cells. However, there are conflicting data regarding the identification of cells undergoing apoptosis during luteolysis [17–19, 30–39]. It has been estimated that if as few as 3% of the cells contain oligonucleosomes, 25% of the tissue will be destroyed within 24 h [40].

Treatment with PGF2{alpha} reduced concentrations of all mRNAs examined when given at the 30 mg/kg BW dose. This result was similar to results previously obtained for these mRNAs [4, 6–15, 27]. However, even a nonluteolytic dose of PGF2{alpha} (3 mg/kg BW) induced severe reductions in mRNA encoding StAR and PGF2{alpha}-R at 9 h post-treatment, although concentrations of these mRNAs returned to values similar to those in controls within 24 h. In contrast, concentrations of mRNA encoding P450scc and LHR appeared to be less sensitive to PGF2{alpha}, and higher doses of PGF2{alpha} were necessary to cause suppression, although concentrations of progesterone in sera were reduced by all doses of PGF2{alpha}. Thus, reduced levels of mRNA encoding LHR and P450scc and their associated protein are probably not involved in the PGF2{alpha}-induced decrease in progesterone secretion. In addition, we and others have shown that the reduction in concentrations of mRNA encoding 3ß-HSD following PGF2{alpha} injection did not lead to reduced 3ß-HSD protein or its enzyme activity [14, 27] until well after secretion of progesterone had decreased. In contrast, mRNA encoding StAR and mitochondrial StAR protein levels are highly correlated in bovine corpora lutea [13], and StAR has an effective half-life of 3–5 min [41, 42]. Thus, reduced concentrations of StAR mRNA would be expected to rapidly lead to reduced StAR protein. Since StAR is essential to gonadal steroid synthesis [43], reduced StAR protein would lead to reduced progesterone synthesis. Indeed, we observed a very strong correlation between mRNA encoding StAR and concentration of progesterone in serum.

In conclusion, we propose that low concentrations of PGF2{alpha} decrease synthesis of progesterone in luteal tissue, at least in part through down-regulation of mRNA encoding StAR. Larger doses of PGF2{alpha} are then released from the uterus and cause luteolysis. Luteolysis involves the induction of apoptosis, probably in capillary endothelial cells, which then leads to collapse of the vascular system and death of additional luteal cells. The corpus luteum can recover from a low concentrations of PGF2{alpha} even though oligonucleosomes may be detected 9 h after treatment. It is possible that the reduced synthesis of progesterone in luteal tissue is a necessary prerequisite for apoptotic cell death; however, it would not appear to be the initiating factor as mimicking the antisteroidogenic effects of PGF2{alpha} by administration of agents that activate the PKC pathway does not induce oligonucleosome formation or luteolysis [4]. Finally, since the corpus luteum can recover from low doses of PGF2{alpha} and secrete normal amount of progesterone, we hypothesize that the high concentrations of PGF2{alpha} observed late in the period of luteal regression [21–23] ensure destruction of the luteal tissue to prevent inappropriate progesterone synthesis by the corpus luteum during the periovulatory period.


   ACKNOWLEDGMENTS
 
The authors would like to thank Dr. M. Waterman, Department of Biochemistry, Vanderbilt University, Nashville, TN, for the gift of the cDNA encoding bovine P450scc. We appreciate the invaluable technical expertise of M. Gallegos, B. Meberg, C. Moeller, and Xiaoming Sha.


   FOOTNOTES
 
First decision: 17 April 1999.

1 This research was supported by NIH grant HD 11590 and the Colorado Agricultural Experiment Station. Back

2 Correspondence. FAX: 970 491 3557; gniswend{at}cvmbs.colostate.edu Back

Accepted: November 12, 1999.

Received: March 15, 1999.


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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K. A Vonnahme, D. A Redmer, E. Borowczyk, J. J Bilski, J. S Luther, M. L. Johnson, L. P Reynolds, and A. T Grazul-Bilska
Vascular composition, apoptosis, and expression of angiogenic factors in the corpus luteum during prostaglandin F2{alpha}-induced regression in sheep.
Reproduction, June 1, 2006; 131(6): 1115 - 1126.
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V. K. Yadav, R. R. Sudhagar, and R. Medhamurthy
Apoptosis During Spontaneous and Prostaglandin F2{alpha}-Induced Luteal Regression in the Buffalo Cow (Bubalus bubalis): Involvementof Mitogen-Activated Protein Kinases
Biol Reprod, September 1, 2002; 67(3): 752 - 759.
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L. E. Anderson, Y.-L. Wu, S.-J. Tsai, and M. C. Wiltbank
Prostaglandin F2{{alpha}} Receptor in the Corpus Luteum: Recent Information on the Gene, Messenger Ribonucleic Acid, and Protein
Biol Reprod, April 1, 2001; 64(4): 1041 - 1047.
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K. K. Olson, L. E. Anderson, M. C. Wiltbank, and D. H. Townson
Actions of Prostaglandin F2{{alpha}} and Prolactin on Intercellular Adhesion Molecule-1 Expression and Monocyte/Macrophage Accumulation in the Rat Corpus Luteum
Biol Reprod, March 1, 2001; 64(3): 890 - 897.
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P.J. Silva, J.L. Juengel, M.K. Rollyson, and G.D. Niswender
Prostaglandin Metabolism in the Ovine Corpus Luteum: Catabolism of Prostaglandin F2{alpha} (PGF2{alpha}) Coincides with Resistance of the Corpus Luteum to PGF2{alpha}
Biol Reprod, November 1, 2000; 63(5): 1229 - 1236.
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