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In Vivo Oxytocin Release from Microdialyzed Bovine Corpora Lutea During Spontaneous and Prostaglandin-Induced Regression

^a Departments of Animal Science and Anatomy, Physiological Sciences, and Radiology, North Carolina State University, Raleigh, North Carolina 27695

	ABSTRACT

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The release of luteal oxytocin during spontaneous and prostaglandin-induced luteolysis was investigated in cows. A continuous-flow microdialysis system was used in 11 cows to collect dialysates of the luteal extracellular space between Days 12 and 24 postestrus. Seven cows were untreated and were expected to exhibit spontaneous luteolysis during sampling, whereas 4 cows received prostaglandin F₂ (PGF₂) systemically between Days 13 and 15 to induce luteolysis during sampling. Oxytocin was detectable in the dialysate of all cows before Day 16 postestrus and occurred as 2 or 3 discrete pulses per 12-h sampling period. For non-PGF₂-treated cows, dialysate oxytocin content began to decline spontaneously on Day 15 postestrus and was undetectable by Day 17 postestrus. Oxytocin decay curves preceded onset of serum progesterone decline by at least 72 h and were not related temporally with onset of progesterone decline within cow. Exogenous PGF₂ (25 mg, i.m.) produced a 10-fold increase in dialysate oxytocin within 1 h (1.9 ± 0.3 pg/ml to 20.8 ± 3.0 pg/ml; P < 0.01). Dialysate oxytocin then declined to pretreatment concentrations within 2 h and was undetectable within 8 h posttreatment. A second PGF₂ injection given 20 h after the first did not result in a measurable increase in dialysate oxytocin, probably because luteolysis was underway. Although robust luteal oxytocin release was observed after treatment with a pharmacological dose of PGF₂, the lack of detectable oxytocin secretion during spontaneous luteolysis suggests that the contribution of luteal oxytocin in the cow may be less than that proposed for the ewe.

	INTRODUCTION

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Intensive study of the endocrine pathways governing reproductive cyclicity in ruminants has implicated oxytocin in the luteolytic process. Oxytocin is secreted in physiologically significant quantities from both the neurohypophysis and corpus luteum. The cumulative literature supports a model in which oxytocin drives uterine prostaglandin F₂ (PGF₂) release by binding specific, steroid-regulated receptors. Both PGF₂ and estradiol are capable of inducing further oxytocin release, creating a positive feedback loop that generates sufficient PGF₂ to initiate luteolysis [1].

A currently unresolved issue is the relative importance of luteal versus pituitary oxytocin in the luteolytic process. McCracken et al. [2] presented evidence suggesting that oxytocin of pituitary origin (central pulse generator) provided the control point while describing luteal oxytocin stores as supplemental and capable of amplifying the neural oxytocin signal in the ewe. That this amplification process is a prerequisite for luteolysis has not been conclusively demonstrated. Although equivalent experimental results are unavailable in cattle, Kotwica and Skarsynski [3] questioned the necessity of luteal oxytocin for luteolysis after failing to alter estrous cycle length for cattle in which 75% of luteal oxytocin had been depleted by noradrenaline. A related experiment demonstrated the ability of ovine corpora lutea to undergo PGF₂-induced luteolysis despite > 95% depletion of luteal oxytocin stores [4]. Although these experiments provide evidence that absence of luteal oxytocin release does not alter the luteolytic process, other researchers have demonstrated the concurrent release of luteal oxytocin and uterine prostaglandin in vivo in sheep [5].

We have previously demonstrated the ability of an in vivo microdialysis system (MDS) to continuously sample the extracellular space of the bovine corpus luteum [6]. The objective of the present study was to use in vivo microdialysis to characterize luteal oxytocin release during spontaneous and PGF₂-induced regression of the bovine corpus luteum. These data were expected to quantify the hypothesized contribution of luteal oxytocin during luteolysis in the cow.

	MATERIALS AND METHODS

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Animals and Sampling

All procedures were approved by the Institutional Lab Animal Care and Use Committee. Multiparous, nonlactating Holstein cows were fitted with jugular cannulae and moved to individual stanchions, where they were allowed to acclimate for at least 3 days before surgery. Estrus had been synchronized by use of 2 injections (25 mg, i.m.) of PGF₂ (Lutalyse; The Upjohn Company, Kalamazoo, MI), given 11 days apart, and the ovaries of each cow were examined by transrectal ultrasonography to confirm corpus luteum position and consistency. To ensure MDS placement into solid luteal tissue, cows possessing fluid-filled corpora lutea were omitted from the study. All surgeries were conducted between Days 12 and 14 of an estrous cycle (estrus was defined as Day 0). Seven cows received no further treatments and were expected to exhibit spontaneous luteolysis during the sampling period. Four cows were given an intramuscular injection of 25 mg PGF₂ at 1200 h on the first or second day postsurgery and 15 mg at 0800 h of the following day to induce luteolysis. Jugular blood was sampled twice daily beginning 3 days before surgery and continued for the duration of the experiment.

MDS

Details of the system design and surgical procedure have been previously published [6]. In brief, a 1-cm window was created at the midpoint of a 1-m section of Silastic tubing (Dow Corning, Midland, MI). A single, hollow fiber (Amicon, Beverly, MA: molecular mass cutoff = 100 kDa) was fixed in the lumen of the Silastic tube such that the window was completely filled by dialysis fiber. Access to the ovary was gained via a paralumbar laparotomy. Placement of the tubing through the ovary was aided by fixing the shaft of a 20-gauge, 3.8-cm hypodermic needle on one end of the Silastic tubing. The Silastic tubing was pulled through the corpus luteum as the needle was inserted and pulled through the opposing side. Once the window containing the dialyzing fiber was completely contained within the luteal parenchyma, the tubing was fixed to the ovarian serosa with tissue glue. Both free ends of the Silastic tubing were exteriorized through the lateral body wall. One free end was connected to a peristaltic pump while the other was used for fraction collection.

Dialysate medium was lactated Ringer's solution (Baxter Health Care, Deerfield, IL) containing 0.1% BSA (Sigma Chemical Co., St. Louis, MO). A flow rate of approximately 3.5 ml/h was maintained continuously for 7–9 days depending on day of the estrous cycle at surgery (Days 12–14 of the estrous cycle). Therefore, fraction collection was maintained through Days 21–23 of the estrous cycle. Fractions were collected at 30-min intervals for 12 h each day. Preliminary experiments (unpublished results) revealed no diurnal variation in dialysate oxytocin content or oxytocin release profiles. Further, our previously published work [6] showed no loss of membrane diffusion capacity for progesterone or tumor necrosis factor during 9 days of dialysis. Therefore, we considered 12 h of sampling per day and the total duration of the experiment to be satisfactory provided that the exogenous treatments (PGF₂) were given during a sampling interval.

Assay Methods

Oxytocin antiserum was provided by Dr. D. Schams, Technical University of Munich-Weihenstephan, Freising, Germany. Measurement of dialysate oxytocin content was performed using a previously described method [7]. Oxytocin was measured using 200 µl per tube of dialysate medium across 8 replicate assays. The only variant to this protocol was the use of unextracted dialysate medium. Inter- and intraassay coefficients of variation were determined by use of pooled dialysate medium containing added oxytocin. Limit of assay detection was 0.2 pg per tube, and inter- and intraassay coefficients of variation were 13.6% and 7.2%, respectively. Serum progesterone concentrations were determined using the method of Shaw and Britt [6]. Twenty-five microliters of unextracted bovine serum was used in the assay. Inter- and intraassay coefficients of variation were 14.6% and 5.1%, respectively, for 3 replicates.

Statistical Analysis

The oxytocin decay curve was analyzed by use of the PROC GLM procedure of Statistical Analysis Systems (SAS) [8]. Linear and exponential regression equations were computed until the best fit was determined. Parameter estimates, correlation coefficients, and probability values are reported for a model in which oxytocin was the dependent variable and days postestrus was the source of variation. To determine responses following PGF₂ treatment, 6 fractions immediately before PGF₂ treatment were averaged and used as baseline. Individual posttreatment fractions were compared to baseline by use of ANOVA. Oxytocin and fraction were the dependent and independent variables, respectively.

	RESULTS

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Oxytocin was detectable in the dialysate of all 11 cows. Figure 1 profiles dialysate oxytocin content for 3 non-PGF₂-treated cows. Two or three discrete oxytocin pulses during each 12-h sampling period are evident. Cow A was representative of 2 cows that did not show spontaneous luteolysis, based on progesterone values, by the end of the sampling period (Day 23 postestrus). These 2 cows had undetectable dialysate oxytocin after Day 15 postestrus even though progesterone was maintained at midluteal concentrations. Cows B and C exhibited spontaneous luteolysis on Days 18 and 22 postestrus, respectively, and are representative of 5 cows. Oxytocin was undetectable beyond Day 15 postestrus for these cows. Among all 7 cows originally expected to exhibit spontaneous luteolysis, dialysate oxytocin decreased significantly (P < 0.01) from Day 15 through Day 17 postestrus (Fig. 2), whether or not luteolysis occurred. Oxytocin was not detectable in any fractions collected from Day 16 through Day 23 postestrus, and oxytocin decay was not temporally related to onset of serum progesterone decline within any cow.

View larger version (29K): [in this window] [in a new window]   FIG. 1. Dialysate oxytocin and serum progesterone (P4) profiles for 3 non-PGF2-treated cows. The sampling period occurred between 0800 h and 2000 h each day (24 consecutive fractions). Gaps between bar series on each day represent nonsampling periods (2030 h and 0730 h). Bars represent dialysate oxytocin, and lines with diamonds represent serum progesterone

View larger version (14K): [in this window] [in a new window]   FIG. 2. Mean (± SEM) cumulative oxytocin content for each 12-h sampling period. Cumulative totals were derived by multiplying the concentration per milliliter by the fraction volume and the number of fractions collected. Best-fit linear regression yielded y = 22.12x - 1.32, R2 = 0.32 (P < 0.01)

PGF₂ treatment induced functional luteolysis for all treated cows as confirmed by the reduction of serum progesterone to below assay detection limits within 48 h of PGF₂ treatment (Fig. 3). Three of 4 PGF₂-treated cows had measurable dialysate oxytocin content on the day of PGF₂ treatment (Fig. 3). Because oxytocin was not detectable before or after PGF₂ injection for one cow, graphical data for this cow were omitted. However, statistical calculation included all 4 animals. The first PGF₂ injection elicited a 10-fold increase (P < 0.01) in dialysate oxytocin that peaked within 2 fraction intervals (1 h) of treatment (Fig. 4). Oxytocin returned to baseline levels within 3–4 fractions (1.5–2 h) and could not be detected in any fractions beyond the day of initial PGF₂ treatment (Fig. 3). The second PGF₂ injection, given 20 h after the first, did not produce detectable changes in dialysate oxytocin content.

View larger version (33K): [in this window] [in a new window]   FIG. 3. Dialysate oxytocin and serum progesterone (P4) profiles for 3 PGF2-treated cows. The sampling period occurred between 0800 h and 2000 h each day (24 consecutive fractions). Gaps between bar series on each day represent nonsampling periods (2030 h and 0730 h). Bars represent dialysate oxytocin, and lines with diamonds represent serum progesterone. Arrows indicate time of PGF2 treatment. **Day 14 was the day of surgery for Cow F; therefore, no fractions were collected

View larger version (12K): [in this window] [in a new window]   FIG. 4. Mean (± SEM) oxytocin content of fractions collected around the time of first PGF2 treatment for all 4 cows. Six fractions before treatment (-5 to 0) were averaged and used as baseline for statistical comparison. Fractions 1 through 4 represent the first 4 fractions posttreatment and are significantly different from baseline (P < 0.01).

	DISCUSSION

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The reduction in luteal oxytocin secretion observed during late diestrus is consistent with other reports on domestic ruminants. For both sheep and cattle, luteal oxytocin content was maximal by the midluteal phase and gradually declined thereafter [9, 10]. This depletion in storage has been attributed to a decrease in oxytocin mRNA synthesis after the third day postestrus. As mRNA degradation continued, viable message became insufficient to maintain intracellular oxytocin stores past the midluteal phase [11, 12]. The general profile of luteal oxytocin content throughout the estrous cycles reported herein is similar to the profile of peripheral plasma oxytocin concentrations reported by Schams [7]. These studies imply that a significant portion of circulating oxytocin originates from the corpus luteum during early to mid diestrus.

In sheep, pulse amplitude of late-diestrus oxytocin release was reduced in the presence of a conceptus [13]; however, the fact that oxytocin concentrations were not different between pregnant and nonpregnant cows generates questions about the importance of luteal oxytocin during luteolysis in this species [10]. The contribution of luteal oxytocin to luteolysis in the cow was also questioned by Kotwica and Skarzynski [3], who failed to extend the luteal phase in cows after depleting 75% of luteal oxytocin stores by treating cows with noradrenaline. Kotwica et al. [14] extended their argument that oxytocin may not be required for luteolysis in cattle after failing to inhibit luteolysis in heifers treated with the oxytocin antagonist CAP-527. Sheldrick and Flint [4] also demonstrated that exogenous PGF₂ would induce luteolysis in ewes possessing corpora lutea that contained < 5% of midluteal oxytocin concentrations relative to controls. Their findings prompted these authors to suggest that luteal oxytocin was unlikely to mediate PGF₂-induced luteolysis in the ewe. In marked contrast, McCracken et al. [2] estimated the contribution of oxytocin from the ovine neurohypophysis to be one tenth the amount provided by the corpus luteum during initiation of luteolysis. In their model, oxytocin pulses derived from the neurohypophysis stimulate uterine PGF₂ release provided that high-affinity oxytocin receptors have been induced by the appropriate steroid milieu. Uterine PGF₂ then amplifies the neural oxytocin signal by stimulating luteal oxytocin release [2]. Although this model is often applied to cattle, experiments equivalent to those of McCracken et al. [2] have not been reported for cattle.

If the McCracken model is applicable to the cow, we hypothesized that high-amplitude oxytocin pulses would be observed in the extracellular space of the corpus luteum during luteolysis, presumably in concurrence with PGF₂ pulses. We did observe a pulsatile release pattern for oxytocin in the extracellular space of the corpus luteum; however, the last fraction containing measurable oxytocin occurred at least 72 h before the onset of serum progesterone decline for cows exhibiting spontaneous luteolysis. One reason for our failure to observe luteal oxytocin release during luteolysis may have been that the oxytocin gradient across the dialyzing fiber was insufficient to produce measurable oxytocin within the dialysate. Jarry et al. [15] estimated dialysate oxytocin content to be 0.1% of the perfusate when cell-free media containing known amounts of oxytocin were dialyzed. Experiments in our laboratory (Shaw and Britt, unpublished results) and the published results of Blair et al. [16] have yielded similar results. Nevertheless, the range of oxytocin concentrations for our in vivo dialysate samples (4–40 pg/ml) were similar to vena caval plasma values reported by Walters et al. [17] using the same oxytocin assay. This suggests that dialysate recovery rates for oxytocin within luteal tissue are comparable to the dilutional effects of secretion from that tissue into the local vasculature. Both Schams [7] and Parkinson et al. [10] reported plasma oxytocin concentrations between Day 16 and 19 of the bovine estrous cycle that were similar to our midluteal dialysate concentrations. Despite those observations, neither the present study nor the experiments of Blair et al. [16] demonstrated intraluteal oxytocin release that was detectable during the period of luteolysis. If the majority of late diestrual oxytocin originated from the corpus luteum, as proposed in sheep, it seems likely that we would have observed this at the level of the corpus luteum.

The oxytocin profiles for our PGF₂-treated cows concur with numerous reports describing the ability of PGF₂ to stimulate oxytocin release in vivo [18, 19]. The pharmacological dose of PGF₂ used in this study produced an immediate increase in dialysate oxytocin content. Although the magnitude of the increase appeared to be greater than that observed for most spontaneous pulses, the duration of PGF₂-induced secretion and spontaneous pulses were similar. The mechanism(s) controlling early and mid luteal-phase oxytocin secretion are unknown. Given the temporal similarities between spontaneous and PGF₂-induced release of oxytocin, a common cellular pathway seems possible. The lack of response to the second PGF₂ injection may have resulted from a combination of oxytocin depletion and the inability of luteal cells to respond because luteolysis was underway. Large luteal cells possess the greatest oxytocin content and the majority of PGF₂ receptors [20]. By 20 h post-PGF₂, the majority of these cells were probably already committed to a lethal pathway and were no longer capable of a secretory response.

By use of an in vivo microdialysis technique, we have observed the rapid decline of luteal oxytocin secretion beyond the fourteenth day of the bovine estrous cycle. The absence of any measurable oxytocin secretion within the bovine corpus luteum during luteolysis suggests that the contribution of luteal oxytocin to the luteolytic process may be less than that proposed for the ewe.

	ACKNOWLEDGMENTS

 
The authors are grateful to Dr. Dieter Schams for providing RIA reagents and the Amicon Company for their gift of dialysis fibers.

	FOOTNOTES

 
First decision: 19 November 1998.

¹ Correspondence and current address: Doug Shaw, Department of Veterinary Preventive Medicine, The Ohio State University, 1900 Coffey Rd., Columbus, OH 43210. FAX: 614 292 4142; shaw.184{at}osu.edu

² Current address: Jack Britt, University of Tennessee, 101 Morgan Hall, Knoxville, TN 37996.

Accepted: October 8, 1999.

Received: October 19, 1998.

	REFERENCES

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