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research-article |
Graduate School of Animal and Food Hygiene3 and Department of Clinical Veterinary Science,4 Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080-8555, Japan
ABSTRACT
Luteolysis is caused by a pulsatile release of prostaglandin F2alpha (PGF2alpha) from the uterus in ruminants, and a positive feedback between endometrial PGF2alpha and luteal oxytocin (OXT) has a physiologic role in the promotion of luteolysis. The bovine corpus luteum (CL) produces vasoactive substances, such as endothelin 1 (EDN1) and angiotensin II (Ang II), that mediate and progress luteolysis. We hypothesized that luteal OXT has an additive function to ensure the CL regression with EDN1 and Ang II, and that it has an active role in the luteolytic cascade in the cow. Thus, the aim of the present study was to observe real-time changes in the local secretion of luteal OXT and to determine its relationship with other local mediators of luteolysis. Microdialysis system (MDS) capillary membranes were implanted surgically into each CL of six cyclic Holstein cows (18 lines total among the six cows) on Day 15 (estrus == Day 0) of the estrous cycle. Simultaneously, catheters were implanted to collect ovarian venous plasma ipsilateral to the CL. Although the basal secretion of OXT by luteal tissue was maintained during the experimental period, the intraluteal PGF2alpha secretion gradually increased up to 300% from 24 h after the onset of luteolysis (0 h; time in which progesterone started to decrease). In each MDS line (microenvironment) within the CL, the local releasing profiles of OXT were positively associated with PGF2alpha and EDN1 within the CL in all 18 MDS lines implanted in the six CLs (OXT vs. PGF2alpha, 50.0%; OXT vs. EDN1, 72.2%; P < 0.05). On the other hand, the intraluteal OXT was weakly related to Ang II (OXT vs. Ang II, 27.7%). In the ovarian vein, the peak concentration of PGF2alpha increased significantly when the peak of PGF2alpha coincided with the peak of OXT after the onset of spontaneous luteolysis (P < 0.05). In conclusion, intraluteal OXT may locally modulate secretion of vasoactive substances, particularly EDN1 and PGF2alpha within the CL, and thus might be one of the luteal mediators of spontaneous luteolysis in the cow.
corpus luteum,, corpus luteum function, endothelin 1, luteolysis, ovary, oxytocin, progesterone, prostaglandinF2
In nonpregnant domestic ruminants, luteolysis is caused by prostaglandin F2 (PGF2) secreted from the endometrium, where PGF2 drastically induces a decrease in progesterone (P) secretion from the corpus luteum (CL) and in the CL volume [1, 2]. The CL has the ability to synthesize neuropeptide oxytocin (OXT) [3, 4]. In the bovine CL, the expression of OXT mRNA level is high during the early luteal phase [5–7], and OXT peptide is expressed at a higher level during the midluteal phase [7, 8]. In addition, bovine luteal cells of any luteal phase of the estrous cycle have specific binding sites for OXT [9]. PGF2 stimulates OXT secretion from the CL [4], and OXT in turn stimulates uterine secretion of PGF2 [10, 11]. Thus, endometrial PGF2 and luteal OXT comprise a positive feedback mechanism that acts between the uterus and the CL to enhance luteal regression [12]. However, previous studies reported a luteotropic action of luteal OXT in which OXT directly stimulates P secretion in the luteal cell [13, 14]. Moreover, treatment of noradrenalin infusion to reduce the total amount of OXT within the CL did not affect both spontaneous luteolysis and estrous cycle duration in the midluteal phase in the cow [15]. Therefore, the role of luteal OXT within the CL is not well established in the cow.
Endothelin 1 (EDN1) [16–24] and angiotensin II (Ang II) [25–27], the predominant vasoconstrictive peptides, have roles to mediate and progress luteal regression in the bovine and ovine CL. In addition to PGF2 released from the endometrium, the CL is recognized as a site of PGF2 production [28–30]. PGF2 stimulates the release of EDN1 and Ang II both in vitro and in vivo [19, 25, 31]. Both EDN1 and Ang II have been shown to inhibit P secretion by bovine luteal cells [16, 18, 25]. Thus, it was suggested that these vasoactive substances may interact with each other in the regressing CL [32].
We hypothesized that luteal OXT has an additive function to ensure the regression of the CL with EDN1 and Ang II and also has an active role in the luteolytic cascade in the cow. To test this hypothesis, we used an in vivo microdialysis system (MDS) implanted in the CL that functions as an artificial capillary vessel, which offers an effective approach for observing the changes in local secretory function in the microenvironment within the CL in intact animals, and we observed in detail the real-time changes of luteal OXT, PGF2, EDN1, and Ang II in the local secretion within the CL during spontaneous luteolysis in the cow.
Animals and Experimental Design
The experiments were carried out at the Field Center of Animal Science and Agriculture, Obihiro University, and the experimental procedures complied with the Guide for Care and Use of Agriculture Animals of Obihiro University. Six multiparous, nonlactating Holstein cows were used for this study. They had at least two estrous cycles of normal length (21–22 days) before being used. Luteolysis was induced by i.m. injection of 500 µg of the PGF2 analogue cloprostenol (Estrumate; Takeda. Co., Osaka, Japan), and 100 µg GnRH (Conceral; Takeda. Co.) was injected i.m. 60 h after the PGF2 injection to ensure ovulation. The day of estrus was designated as Day 0. The cows received surgical implants of MDS membranes into the CL, and the ovarian veins were simultaneously catheterized on Day 15 of the estrous cycle. After surgery, cows were moved to individual stanchions and were fed with hay and water ad libitum. Sample collection started 24 h after surgery and continued until the next estrus. After the experimental period, the MDS was surgically removed and the cow was ovariectomized. The occurrence of luteolysis was confirmed by a macroscopic observation of dissected the CL [33]. The time schedule of the study is shown in Figure 1.
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Surgical Implantation of the MDS into the CL
The MDS was implanted surgically into the CL on Day 15 of the estrous cycle via lateral laparotomy under epidural anesthesia, as described previously [19]. Before surgery, ovaries were monitored by transrectal ultrasonography to determine that the CL was normal and had no cystic cavity. Basically, two to five dialysis capillary membranes (cutoff: 1000 kDa, 0.2-mm diameter, 10 mm long; Fresenius SPS 900 Hollow Fibers; Fresenius AG, St. Wendel, Germany) were implanted into the CL. Both ends of the capillary membranes were glued to 25-cm long pieces of silicone elastomer tubing (inner diameter, 0.3 mm) and connected to the MDS. The tubing was fixed on the surface of the CL by Histoacryl blau (B. Braun-Dexon GmbH, Spangenberg, Germany), and the dialysis pieces with silicone tubing were connected to Teflon tubing that led to the outside of the abdomen. The exteriorized bundle of afferent and efferent Teflon tubing was fixed on the back of the cow. One end of the MDS was connected to a multiple-line peristaltic pump, and the other was connected to a multiple-line fraction collector. The MDS was continuously perfused with Ringer solution at a flow rate of 2.5 ml/h throughout the experiment, and fractions of perfusate were collected at 4-h intervals. Sample collection started 24 h after surgery, and all MDS samples were immediately frozen at –30°C after collection until further analysis.
Venous Catheterization and Collection of Ovarian Venous Plasma (OVP)
At the time of surgery, a catheter was placed into the ovarian vein ipsilateral CL, about 5 cm away from the ovary, and was propelled about 8–10 cm, and the position of the front edge of the catheter was checked within the ovarian vein. Blood samples were collected from MDS-implanted cows into sterile 10-ml glass tubes containing 200 µl stabilizer solution (0.3 M EDTA, 1% acetyl salicylic acid, pH 7.4) at 4-h intervals until the end of the experiment. All blood samples were immediately chilled in ice water for 10 min, centrifuged at 2000 x g for 15 min at 4°C, and the plasma was frozen at –30°C until further analysis.
The concentrations of P, OXT, PGF2, EDN1, and Ang II in plasma and perfusate fractions of the MDS were determined in duplicate by second-antibody enzyme immunoassays (EIAs) after extraction using 96-well ELISA plates (NUNC-Immuno Plate; NUNC Brand Products, Roskilde Denmark).
The P concentrations in perfusate fractions of the MDS were assayed directly [34]. The standard curve ranged from 0.05–50 ng/ml, and the effective dose (ED50) of the assay was 2.4 ng/ml. The intraassay and interassay coefficients of variation (CVs) averaged 6.2% and 9.3%, respectively.
To extract PGF2, the plasma (2 ml) and MDS perfusates (6 ml) were adjusted to pH 3.5 using HCl and were extracted using diethyl ether as described previously [35]. The residue was dissolved in 2 ml and 200 µl assay buffer (40 mM PBS, 0.1% BSA, pH 7.2). The samples were concentrated 30-fold for the MDS perfusate. The recovery rate in the plasma and MDS perfusate were estimated to be 60% and 65%, respectively. The EIAs for PGF2 [36] were described previously. The standard curve for PGF2 ranged from 9.5 to 9500 pg/ml, and the ED50 of the assay was 145 pg/ml. The intraassay and interassay CVs were 7.7% and 9.7%, respectively.
For the purpose of peptide extraction, 3 ml plasma was diluted 2-fold with 3 ml distilled water and adjusted to pH 2.5 with 5 M hydrochloric acid. BSA (fraction V; Sigma Chemical Co., St. Louis, MO) was added to 6 ml of the MDS samples to a final concentration of 1 mg/ml, and the pH was adjusted to 2.5 with acetic acid. All samples were then applied to a SepPak C18 Cartridge (Waters, Millford, MA) as described previously [18]. The residue was evaporated and then dissolved in 250 µl assay buffer (42 mM Na2HPO4, 8 mM KH2PO4, 20 mM NaCl, 4.8 mM EDTA, 0.05% BSA, pH 7.5) for peptide EIAs. The plasma samples and the MDS fractions were concentrated 15-fold and 24-fold, respectively as a result of this process, enabling us to determine peptide concentrations in the EIAs within the range of the standard curve. The recovery rates of OXT, EDN1, and Ang II that had been added to Ringer solution were 81%, 61%, and 82%, respectively. The EIAs for OXT [18], EDN1 [18] and Ang II [25] were described previously. The standard curve for OXT ranged from 1.6 to 200 pg/ml, and the ED50 of the assay was 21 pg/ml. The intraassay and interassay CVs were 6.2% and 8.6%, respectively. The standard curve for EDN1 ranged from 0.5 to 500 pg/ml, and the ED50 of the assay was 25 pg/ml. The intraassay and interassay CVs were 8.7% and 12.6%, respectively. The standard curve for Ang II ranged from 5 to 5000 pg/ml, and the ED50 of the assay was 125 pg/ml. The intraassay and interassay CVs were 6.4% and 8.7%, respectively.
A large variation was observed in the absolute amount of substances released into each of the microdialysis capillary membranes implanted in different cows. Thus, for analysis of changes in concentrations of substances in the MDS fractions, the mean concentrations of the first six fractions (24 h) were used for calculation of an individual proportion of the baseline. All concentrations in the fractions collected were then expressed as a proportion of this individual baseline. This treatment enables an evaluation of the relative changes of substance values between the CL of different animals. The time point when P concentration in MDS fractions started to decrease was considered as 0 h for the data analysis. For statistical analysis, the experimental period was divided into 18 stages, and each represents the assortment of the data from an 8-h period (two fractions). Changes in hormonal release after the onset of luteolysis were tested on the basis of individual time points throughout the experiment as compared with the baseline. They were analyzed by repeated-measures ANOVA followed by a t-test with the Bonferroni method to separate the means. Differences were considered significant at a probability of less than 5% (P < 0.05).
Significant coincidence was observed in increased points between the releases of two peptides. Pulsatile releases of OXT, PGF2, EDN1, and Ang II in the MDS during spontaneous luteolysis were examined. The relationship among peaks of OXT, PGF2, EDN1, and Ang II in the MDS were analyzed using a chi-square test of independence for contingency. The increased point was identified with the occurrence of peaks (episodic increase on the every 4-h basis) when the proportional changes of OXT, PGF2, EDN1, and Ang II increased from basal values to at least over 3-fold of the intraassay CV of EIAs.
The estrous signs were observed in all cows between Days 21 and 23 from the last estrus, and CLs implanted with MDS were collected by ovariectomy after the estrus. The regression of CLs was confirmed by macroscopic observation.
Intraluteal Changes in P, OXT, and PGF2 Concentrations During Spontaneous Luteolysis
The basal releases (100%) of P, OXT, and PGF2 into MDS fractions implanted in the CL were 1.54 ± 0.27 ng/ml, 14.15 ± 1.67 pg/ml, and 18.52 ± 1.52 pg/ml (mean ± SEM), respectively. These basal releases of P, OXT, and PGF2 were constant before the onset of luteolysis. The intraluteal P secretion started to decrease on Days 17–18 (the onset of luteolysis = 0 h), and declined further to about 20% of the baseline by the end of the experiment (Fig. 2A). Intraluteal OXT secretion was maintained during the experimental period (Fig. 2B). The intraluteal PGF2 secretion began to increase at 24 h to about 300%, and it maintained a high level toward the estrus (Fig. 2C).
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Relationship of Intraluteal OXT Secretion with PGF2, EDN1, and Ang II
A relationship between the intraluteal OXT peaks and intraluteal PGF2, EDN1, and Ang II is shown in Table 1. In all 18 MDS lines (microenvironment) within the regressing CL, the local releasing profiles of OXT with PGF2 and EDN1 within the CL were highly positively associated with each other (P < 0.05) when these lines were implanted in the six CLs (OXT vs. PGF2, 50.0%; OXT vs. EDN1, 72.2%). On the other hand, the relationship between intraluteal OXT and Ang II showed a lower proportion than intraluteal OXT with PGF2 and EDN1 (OXT vs. Ang II, 27.7%). An example of the intraluteal secretion of OXT with PGF2, EDN1, and Ang II in a single MDS line (microenvironment) is shown in Figure 3. Furthermore, we examined the peak occurrence and relationship of OXT, PGF2, EDN1, and Ang II secretion in each MDS line (n = 18 for six cows) and drew a comparison of peak occurrence before, between, and after the onset of spontaneous luteolysis. In addition, peak occurrence of OXT coincident with PGF2, EDN1, and Ang II also increased after the onset of luteolysis (Table 1).
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Changes in OXT and PGF2 Concentrations in OVP During Spontaneous Luteolysis
The release of OXT and PGF2 into ovarian venous in two cows (Cows B and C) is shown in Figure 4. Peak concentration in OVP compared before, between, and after the onset of spontaneous luteolysis is shown in Table 2. At peak concentration, the mean concentrations of the peak (total peak average) of both OXT and PGF2 were not different throughout the experiment. Also, the peak concentration of OXT in OVP was not significantly different before and after luteolysis, whether this was coincident or not with the PGF2 peak. However, only the peak concentration of PGF2 in OVP increased significantly when the peak of PGF2 coincided with that of OXT after the onset of spontaneous luteolysis.
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The results of the present study provide in vivo evidence for close relationships in intraluteal release of OXT with PGF2 and EDN1, but not with Ang II, during spontaneous luteolysis in the cow. The data show that intraluteal OXT may have a role in modulating the local secretion of vasoactive substances within the CL.
The present study indicated that the release of intraluteal OXT was maintained at the same levels during spontaneous luteolysis in the cow. This result is consistent with our recent study in which we detected luteal OXT secretion using the same MDS during PGF2-induced luteolysis in the cow [19]. However, a previous study by other researchers using MDS reported that the luteal OXT content began to decline on Day 15 and was undetectable by Day 17 of the estrous cycle in the cow [37]. Moreover, luteal OXT was undetectable within 8 h after PGF2-induced luteolysis in the cow [37]. That study measured the luteal OXT concentration using unextracted dialysate perfusion, whereas we used an extraction method followed by a 24-fold concentration of samples. Therefore, the discrepancy between our present study and the other study [37] is likely due to the different method of extraction of MDS samples. The present study clearly showed that OXT is actively released even after the onset of spontaneous luteolysis in the cow.
The bovine CL is composed of several cell types, including small and large luteal cells, endothelial cells, smooth muscle cells, fibrocytes, and immune cells. Especially, vascular endothelial cells represent more than 50% of the total number of cells in the CL [38, 39]. Moreover, intraluteal vasoactive molecules such as PGF2, EDN1, and Ang II may play an essential role and establish a local positive feedback mechanism within the CL during luteolysis in the cow [16, 18, 19, 21–25, 27, 31]. In the present study we observed that the intraluteal release of OXT in each MDS line (microenvironment) was highly positively associated with intraluteal PGF2 and EDN1 in 18 MDS lines (OXT vs. PGF2, 50.0%; OXT vs. EDN1, 72.2%), but was not associated with intraluteal Ang II (OXT vs. Ang II, 27.7%) during spontaneous luteolysis in the cow. The OXT peak coincided with PGF2 or EDN1 and increased significantly after rather than before the onset of luteolysis (Table 1). In fact, OXT stimulates the release of PGF2 in luteal cells [40] and EDN1 in luteal endothelial cells [17]. Also, PGF2 stimulates OXT secretion in vivo [4] and in vitro [41, 42]. Recent studies have shown that EDN1 induced the release of OXT in vivo [43] and in vitro [18]. Thus, we propose that luteal OXT, PGF2, and EDN1 may establish a local positive feedback loop within the microenvironment to ensure the regression of the CL.
In contrast to the relationship of intraluteal OXT with PGF2 or EDN1, we observed a weak correlation between intraluteal OXT and Ang II in each MDS line (27.7%). There is little information on the relationship between OXT and Ang II during luteolysis. However, in this study, a peak occurrence of OXT coincided with the Ang II peak after luteolysis, and it increased significantly compared with before luteolysis (Table 1). Moreover, we previously indicated that the local releasing profiles of PGF2, EDN1, and Ang II were positively associated with each other at a high ratio (PGF2 vs. EDN1, 44.4%; PGF2 vs. Ang II, 55.6%) [32], suggesting that intraluteal OXT might be associated with Ang II indirectly via the stimulation of PGF2 and/or EDN1 by OXT. Therefore, intraluteal OXT may amplify the frequency of vasoactive substance secretion after the onset of luteal regression within the CL.
On the other hand, the present study indicated that intraluteal PGF2 secretion began to increase at 24 h after the onset of luteolysis and that high levels were maintained toward estrus. In fact, systemic injection of indomethacin, a potent prostaglandin synthase inhibitor, resulted in heavier CL than found in the control, indicating that the systemic administration of prostaglandin synthesis inhibitors delayed the structural luteolysis in rats [44]. Thus, these data, together with our present study, suggest that intraluteal PGF2 is essential for structural luteolysis to ensure luteal regression.
It is well known that OXT and PGF2 are released into the circulation in a pulsatile manner during the estrous cycle in the cows [12] and ewes [45]. We observed that the mean peak concentration of PGF2 but not of OXT has a tendency to increase after the onset of luteolysis than before it. The peak concentration of PGF2 in OVP increased significantly when the peak of PGF2 coincided with the OXT peak after the onset of spontaneous luteolysis. The ratio for peak occurrence of intraluteal OXT that coincided with intraluteal PGF2 significantly increased to 2-fold after the onset of luteolysis rather than before it. Furthermore, the peak concentration of PGF2 that coincided with the OXT peak into OVP was drastically enhanced more than 4-fold after the onset of luteolysis rather than before it (Table 2). In fact, OXT stimulates luteal [14] and uterine [10, 11] PGF2 secretion. In contrast, PGF2 can stimulate the release of OXT [4]. Therefore, our data indicate that intraluteal OXT may directly stimulate both uterine and luteal PGF2 in vivo in the cow, suggesting that luteal OXT affects the CL function to induce luteolysis. Additionally, Silvia and Raw [46] reported that although the number of PGFM (metabolized substance of PGF2) pulses in ovariectomized ewes receiving P replacement was similar to that observed in intact ewes, the magnitude of PGFM pulses in ovariectomized ewes receiving P replacement was much less than intact ewes. Ovarian secretory (such as luteal OXT) products may be required to achieve the full PGF2 magnitude, and that P plays an important role in regulating the number of pulsatile secretions of PGF2 from the uterus [46]. Given our results together with theirs, OXT has a role in regulating the amplitude of pulsatile secretion of PGF2, but not peak occurrence of PGF2, after the onset of luteolysis in the cow [47].
Although luteal OXT and uterine PGF2 comprise a positive feedback mechanism to enhance luteal regression [12], OXT directly stimulates but does not inhibit P secretion in the bovine luteal cells [13, 14]. The stimulatory effect of OXT on P secretion was highest at Days 5–7 of the estrous cycle and declined from Days 8–12; however, OXT no longer stimulated P secretion at Days 15–18 [48]. Therefore, it was suggested that luteal OXT affects the luteal function as a luteotropic autocrine/paracrine factor within the CL depending on the luteal phase [48]. On the other hand, when OXT receptors were blocked, the magnitude of PGF2 release decreased, suggesting that luteal OXT is not required to initiate pulsatile secretion of PGF2, but it may be essential to achieve full pulse amplitude to accelerate luteolysis [47]. Furthermore, the present study may add a novel local action of OXT in which the luteal OXT may regulate the secretion of both EDN1 and PGF2 to progress the luteolytic cascade within the CL. Thus, it is suggested that luteal OXT has an opposite function to both luteotropic (to increase P secretion during early luteal and midluteal phases) and luteolytic (to regulate the magnitude of uterine PGF2 and the secretion of intraluteal EDN1 and PGF2 after starting the luteolytic cascade) actions in the cow.
Taken together, intraluteal OXT may locally modulate secretion of vasoactive substances, particularly EDN1 and PGF2, within the CL, and thus their role might be one of luteal mediators of spontaneous luteolysis in the cow.
ACKNOWLEDGMENTS
The authors thank Dr. K. Okuda, Okayama University, Japan, for P antiserum; Dr. S. Ito, Kansai University of Medicine, Japan, for PG antiserum; Dr. K. Wakabayashi, Gunma University, Japan, for Ang II antiserum; Dr. D. Schams, Technical University of Munich, Germany, for OXT and ET antiserum; and Fresenius AG, St. Wendel, Germany, for microdialysis capillary membrane.
FOOTNOTES
1Supported by the Grant-in-Aid for Scientific Research of the Japan Society for the Promotion of Science (JSPS) and the 21st Century COE Program (A-1), Ministry of Education, Culture, Science, and Technology, Japan. K.S. and K.G.H. are supported by a JSPS Research Fellowship for Young Scientists. 
Correspondence: 2FAX: 81 155 49 5459; e-mail: akiomiya{at}obihiro.ac.jp
Received: 21 September 2006.
First decision: 12 October 2006.
Accepted: 30 January 2007.
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