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Biology of Reproduction 59, 17-21 (1998)
©Copyright 1998 Society for the Study of Reproduction, Inc.

Luteolysis Induced by a Prostaglandin F2{alpha} Analogue Occurs Independently of Prolactin in the Rat1

Erik Bjurulf2,3,a, Ove Toffiaa, Gunnar Selstama, , and Jan I. Olofsson3,a,b

a Department of Physiology, Umeå University, S-90187 Umeå, Sweden b Department of Obstetrics and Gynecology, Umeå University Hospital, S-90185, Umeå, Sweden


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The hypothesis that prolactin exerts a stimulatory dominance over the luteolytic effect of prostaglandin (PG) F2{alpha} on corpus luteum maintenance and progesterone production was experimentally tested.

A dose-dependent effect of the stable PGF2{alpha} analogue cloprostenol (dose range 200 ng<<014>>5 µg) was found 12 h after s.c. injection, in Day 9 adult pseudopregnant rats: 1) LH receptor mRNA levels, as measured by RNase protection assay, were dramatically decreased (by 67%) by a single s.c. dose of 200 ng cloprostenol; and 2) serum progesterone levels were significantly (p < 0.05) decreased (by 43%) whereas 20{alpha}-dihydroprogesterone significantly (p < 0.05) increased (by 80%) initially at a 0.5-µg dose of cloprostenol.

To study the integrated response to prolactin and PGF2{alpha}, we investigated the effect of cloprostenol treatment in sterile-mated female rats with or without circulating prolactin. Prolactin secretion was inhibited by s.c. injection of bromocriptine (1 mg) in the morning of the ninth day of pseudopregnancy. A group of rats was left prolactin-depleted; in another group prolactin was reintroduced by adding 8 IU ovine prolactin. It was found that after injection of 0.5 µg cloprostenol the LH receptor mRNA levels and the serum progesterone/20{alpha}-dihydroprogesterone ratio were not significantly different whether the rats had circulating endogenous/exogenous prolactin or were prolactin-depleted.

Therefore, although prolactin exerts a stimulatory influence on both progesterone production and corpus luteum LH receptor gene expression, the conclusion is reached that prolactin alone cannot antagonize the luteolytic effect of PGF2{alpha}.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It is a classic observation that LH receptor stimulation induces a hyperemic response [1] and increases steroidogenesis in the ovary [2]. In the absence of detectable ß-subunit expression of chorionic gonadotropin [3, 4], the dominant regulator of corpus luteum function in the rodent species most likely exerts its action via stimulation of the prolactin receptor (for review see [5]). After sterile or nonsterile mating on the day of estrus, stimulation of the cervix uteri leads to a circadian secretion of pituitary prolactin, with peak levels seen twice daily [6, 7]. In the event of implantation, hormones secreted from the placenta and decidua are hypothesized to maintain corpus luteum function throughout pregnancy [8]. Of these hormones, several have been proven to bind to the prolactin receptor [9]. The exact mechanism(s) by which stimulation of the prolactin receptor exerts its luteotropic action is not fully understood; however, inhibition of prolactin secretion induces functional luteolysis [10] coinciding with decreased LH binding capacity [11]mediated via decreased LH receptor gene expression [12], induction of 20{alpha}-hydroxysteroid dehydrogenase [13, 14], and decreased cholesterol esterase activity [15]. Confoundingly, in hypophysectomized rats, prolactin is capable of inducing structural luteolysis [16] but only after functional luteolysis has occurred [17]—an effect that involves immune system activation [18].

Prostaglandin (PG) F2{alpha} initiates functional luteolysis in most animals (for review see [19]), and binding sites for PGF2{alpha} are found in luteal tissue in all mammalian species studied [20]. However, the possible influence of prolactin receptor-mediated inhibition of LH receptor gene expression in response to PGF2{alpha} has hitherto been unexplored. The rat luteal LH receptor expression is dependent on prolactin receptor stimulation at both the protein level [11] and the mRNA level [12, 21]. Furthermore, LH receptor mRNA concentrations in the rat ovary are dramatically down-regulated in a time- and tissue-specific manner after treatment by PGF2{alpha} [22]. The study reported here was performed in order to determine whether or not prolactin could antagonize the luteolytic effect of the stable PGF2{alpha} analogue cloprostenol on luteal steroidogenesis and LH receptor gene expression.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animals

Adult female Sprague-Dawley rats were purchased from Møllegaard Ltd. (Ejby, Denmark). They were kept under controlled environmental conditions (22°C, 45–55% humidity, lights-on between 0600 and 1800 h) and had free access to pellets (type R34 from Lactamin Ltd., Stockholm, Sweden) and tap water. Pseudopregnancy was induced at 2–3 mo of age by keeping 3–4 previously unmated females with a vasectomized male. The females were examined each morning for the presence of a vaginal plug, and Day 1 of pseudopregnancy was defined as the day when a vaginal plug was recovered. Animals were decapitated and trunk blood was collected. Ovaries were promptly removed and chilled in ice-cold 0.15 M NaCl solution. The corpora lutea of pseudopregnancy were identified under a stereomicroscope using earlier established criteria [12] and were dissected free from the remainder of the ovary. Tissues were quickly blotted on filter paper, weighed, and frozen in liquid nitrogen. Samples were kept at -70°C until analysis.

The experimental protocols were approved by the local committee for ethical review of animal experiments in Umeå, Sweden.

Experimental Procedures

In order to establish whether a dose-response relationship exists in vivo, a single s.c. injection of different doses of the potent PGF2{alpha} analogue cloprostenol (Estrumat; Pitman-Moore Ltd., Harefield, UK), dissolved in 0.25 ml 0.15 M NaCl, was administered to female adult pseudopregnant rats nine days after mating. Controls received a similar volume of saline. On the basis of the earlier finding that a maximal decrease in luteal LH receptor mRNA levels was seen 12 h after injection [22], all animals were decapitated at this time, and trunk blood was collected for subsequent hormone analysis.

To determine whether prolactin can interfere with the luteolytic effect of PGF2{alpha}, the following protocol was used: On Day 9 at 1030 h, adult pseudopregnant rats received either an s.c. injection of 1 mg bromocriptine (Novartis Ltd., Basel, Switzerland) dissolved in 0.25 ml 75% (v:v) ethanol or of vehicle only. This was followed 1 h later by injection of 8 IU ovine prolactin (NIDDK, Baltimore, MD) dissolved in 0.25 ml buffer (0.03 M NaHCO3 and 0.15 M NaCl, pH 9.5), or of the vehicle only, thoroughly emulsified with an equal volume of 45% (w:v) polyvinylpyrrolidone (Mr = 160 000; Fluka, Buchs, Switzerland) by the use of a double cannula. At 1400 h, injections of 0.5 µg cloprostenol dissolved in 0.25 ml 0.15 M NaCl or of saline only were administered. The different treatments groups are depicted in Table 1.


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  		TABLE 1. Treatment of the different groups of rats on Day 9 of pseudopregnancy.

Quantification of LH Receptor mRNA Concentrations

Total cellular RNA was isolated by centrifugation through silica gel columns using a commercially available kit (RNeasy; Qiagen, Hilden, Germany) after homogenization with a polytron. RNA integrity was verified by 1% denaturizing agarose gel electrophoresis in the presence of ethidium bromide followed by visualization under UV light. RNA concentrations were determined by measuring the A260.

To quantitate mRNA levels, an RNase protection assay (RPA) in solution was used, as described earlier [21], with the exception that RNA preparations were used instead of total nucleic acid preparations. In brief, a 299-basepair (bp) LH receptor cDNA [23] subcloned into the Ava I-HindIII site of a pGEM3Z plasmid (Promega, Madison, WI) linearized with HindIII was used to obtain a [35S]cytidine triphosphate (CTP)-labeled antisense RNA probe. To establish a standard curve, sense RNA was synthesized using the same plasmid but linearized with Ava I. An excess of labeled cRNA probe was hybridized in solution overnight with RNA samples or known amounts of synthesized LH receptor sense RNA, whereafter samples were treated with RNases, precipitated, collected by use of Whatman GF/C filters (Whatman, Clifton, NJ) and a vacuum filtration manifold (Schleicher and Schuell, Keene, NH), washed several times, and solubilized from the filters. Scintillation fluid (Opti-Phase; LKB, Rockville, MD) was added, and samples were counted for radioactivity in a liquid scintillation counter (Rackbeta; LKB-Wallac, Turkku, Finland). The amount of LH receptor mRNA present in each sample was expressed as femtomoles of LH receptor mRNA per micrograms of RNA. The insert-containing plasmid used here was sequenced using the thermo sequenase fluorescent-labeled primer cycle sequencing kit (Amersham, Buckinghamshire, UK) with a Cy5-labeled M13 universal primer (Pharmacia, Uppsala, Sweden) on an ALF express automated sequencer (Pharmacia). The nucleotide sequence was identical to the cDNA sequence reported by McFarland et al. [24].

To allow for an external control of changes in mRNA formation, a housekeeping gene was implemented. A 342-bp human glyceraldehyde-3 phosphate dehydrogenase (G3PDH) cDNA, corresponding to nucleotides 441-782 [25] subcloned into theHindIII-Xba I site of a pBluescript II KS-plasmid (Stratagene, La Jolla, CA) was used. Plasmid DNA was linearized with HindIII, and an RNA probe was synthesized using procedures similar to those described above. To obtain a standard curve, G3PDH sense RNA was synthesized in the same way as the probe with the exceptions that the plasmid was linearized with Xba I and T3 polymerase was used in the absence of radioactive nucleotides. The RPA was run as described for the LH receptor, but in different vials.

Determinations of Serum Progestins

Serum was extracted with diethyl ether and assayed by RIA for concentrations of progesterone or 20{alpha}-dihydroprogesterone (20{alpha}-DHP) exactly as described earlier [21].

Statistics

Values are presented as mean ± standard error of the mean (SEM). Group comparisons were made using Kruskal-Wallis one-way analysis of variance and the two-tailed Mann-Whitney U-test. Differences were considered significant for p values of 0.05 or less.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Dose-Response Relationship of Cloprostenol Treatment

As depicted in Table 2, a dose-response relationship with increasing doses of cloprostenol and decreasing steady-state levels of mRNA for the LH receptor was seen. Interestingly, LH receptor mRNA was markedly down-regulated by a dose of cloprostenol as low as 200 ng, whereas the levels of the constitutively expressed G3PDH mRNA remained unchanged. The serum progesterone levels were decreased with all but the lowest dose of cloprostenol, whereas the 20{alpha}-DHP reached maximal levels after a dose of 2.0 µg (Table 2). The numbers of corpora lutea did not differ between groups, and luteal weights were not affected by the treatments.


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  		TABLE 2. Dose response relationship of s.c. cloprostenol injections on luteal parameters (means ± SEM).

Integrated Response to Prolactin and Cloprostenol on LH Receptor mRNA and Serum Progestin Levels

The concentrations of LH receptor mRNA in the corpus luteum were similarly high in the two control groups, in which the rats received vehicle only (group A) or prolactin was reintroduced to bromocriptine-treated rats (group B). Inhibition of prolactin secretion with bromocriptine (treatment group C) did not decrease the LH receptor mRNA expression significantly (Fig. 1).



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  		FIG. 1. LH receptor mRNA concentrations (mean ± SEM), in Day 9 corpora lutea of adult pseudopregnant rats. Animals (n = 6-8/group) were decapitated 12 h after the last injection. Endo, endogenous prolactin maintained; Exo, injection of prolactin following prolactin secretion inhibition; Inh, prolactin secretion inhibition by bromocriptine injection. All treatments were followed by cloprostenol (+) or vehicle injection (Veh) (see Table 1). Bars with different superscripts differ significantly from each other (p < 0.05).

As expected, the LH receptor mRNA levels were significantly decreased after injection of 0.5 µg cloprostenol in rats with endogenous or exogenous prolactin (groups D and E). Comparison of cloprostenol-treated groups showed no differences in LH receptor mRNA levels between rats that endogenously secreted prolactin (D), that had endogenous prolactin secretion blocked and exogenous prolactin reintroduced (E), and that had prolactin secretion blocked and not replaced (F), as shown in Figure 1. Neither treatment affected the expression of the housekeeping gene G3PDH (Table 3).


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  		TABLE 3. Luteal parameters in rats treated as shown in Table 1 (means ± SEM).

The serum progesterone levels were decreased in the cloprostenol-treated groups and in treatment group C, in which prolactin secretion was blocked, whereas serum 20{alpha}-DHP levels were increased only in the cloprostenol-treated groups (Table 3). Similar to the group in which prolactin was inhibited (group C), all groups with cloprostenol treatment (D–F) showed ratios of individual serum progesterone:20{alpha}-DHP concentrations that were significantly different from those of the control groups (A and B) (Fig. 2).



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  		FIG. 2. Mean ± SEM of individual ratios of serum progesterone:20{alpha}-DHP concentrations of adult pseudopregnant rats (n = 6-8/group) treated as described in Table 1. Bars with different superscripts differ significantly (p < 0.05).

The number of corpora lutea did not significantly differ in the individual groups, and corpus luteum weights did not change according to the different treatments (Table 3). Throughout the experiments, no significant changes in rat body weights in the various treatment groups could be detected (data not shown).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study was designed to determine whether the luteotropic action following prolactin receptor stimulation is exerted via an inhibition of the luteolytic response to PGF2{alpha}-receptor-mediated action. The results obtained do not support the concept that prolactin secretion can maintain LH receptor mRNA expression or progesterone production after a luteolytic stimulus by cloprostenol. However, it cannot be dismissed that prolactin may exert an anti-luteolytic effect by some other mechanism, i.e., by inhibiting luteal prostaglandin formation, although findings in a previous study have indicated that this is not the case [21].

PGF2{alpha} exerts a luteolytic dominance over corpus luteum function, classically referred to as inhibiting steroidogenesis [26], an effect that recently has been described to involve an inhibitory control of the steroidogenic acute regulatory protein (StAR) [27]. Furthermore, PGF2{alpha} positively influences the number of resident and transient immune cells in the ovary [28], and release of reactive oxygen species [29, 30]. These events are followed by a rigidification of luteal cell membranes [31] and apoptosis [32, 33]. Ultimately, structural regression occurs as a dissolution of the extracellular matrix [34], possibly involving an activation of the tissue plasminogen activator system [35, 36]. To mimic the physiological events during functional luteolysis in vivo in a time-restricted and controlled manner, in the present study a dose-response relationship using the potent PGF2{alpha}-receptor agonist cloprostenol was established. Notably, a significant 77% reduction in steady-state levels of LH receptor mRNA was seen at a dosage 25 times lower than previously used (200 ng vs. 5.0 µg), whereas peripheral progesterone concentrations were not significantly decreased until a dose of 0.5 µg was used. In the subsequent experiments, a 0.5-µg dose was chosen in order to allow for an optimal discrimination of the signal-response relationship in search for a putative effect of prolactin-mediated inhibition of the luteolytic response to the cloprostenol challenge.

Bromocriptine, a selective dopamine D2 receptor agonist [37], was used in this study to inhibit the endogenous prolactin secretion. This treatment has been demonstrated to decrease circulating prolactin concentrations to diminutive levels [38, 39] and to exert a abortifactant effect [12, 40, 41]. This effect may use several mechanisms, including diminished gonadotropic stimulation by LH via a decrease in LH receptor gene expression [12]. Additionally, a direct impairment in steroidogenesis by a decrease in lipid mobilization via cholesteryl ester hydroxylase activity [15], as well as an increased conversion of progesterone into its inactive metabolite 20{alpha}-DHP [13, 14], has been reported. Notably, at the time-point used here (12 h), inhibition of prolactin secretion decreased progesterone levels without altering 20{alpha}-DHP levels, partly in contrast to the earlier reports [13, 14] in which a later time-point (24–96 h) was used. The exogenous administration of ovine prolactin has previously been shown to bind to and activate the rat prolactin receptor [42]. Moreover, this regimen has proven to be effective, since a similar add-back regimen of prolactin could abolish the abortifactant effect of bromocriptine [12, 40, 41], and it maintained elevated levels of serum progesterone and LH receptor mRNA for several days in the corpus luteum [21].

In summary, we found that the luteolytic effect of PGF2{alpha} was not dependent on whether endogenous prolactin was present or whether exogenous hormone was reintroduced to prolactin-depleted animals. Thus the study results seems to indicate that functional luteolysis occurs because of an earlier event induced by intrinsic luteolytic agents rather than the mere absence of a pregnancy-related luteotropic stimulus.


   ACKNOWLEDGMENTS
 
Bromocriptine was a generous gift of Novartis, Basel, Switzerland and prolactin was a kind gift from NIDDK, Baltimore, MD.


   FOOTNOTES
 
1 The present study was supported by the Medical Research Council of Sweden (11556, 11832, and 12604), Novo Nordisk foundation, The Swedish Society of Medicine, and The Swedish Society for Medical Research. Back

2 Correspondence: Erik Bjurulf, Department of Obstetrics and Gynecology, Umeå University Hospital, S-90185, Umeå, Sweden. FAX: 46-90- 7866683; erik.bjurulf{at}physiol.umu.se Back

3 Reprint requests: Jan Olofsson, Department of Obstetrics and Gynecology, Umeå University Hospital, S-90185, Umeå, Sweden. FAX: 46-90- 773905; jan.olofsson{at}obstgyn.umu.se Back

Accepted: February 10, 1998.

Received: December 9, 1997.


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 DISCUSSION
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