| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
ARTICLES |
-Induced Oxytocin Secretion and Intracellular Calcium Mobilization in Cultured Bovine Luteal Cells1
a Laboratory of Reproductive Endocrinology, Faculty of Agriculture, Okayama University, Okayama 700-8530, Japan
b Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10-718 Olsztyn-Kortowo, Poland
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
released from the uterus has been shown to cause regression of the bovine corpus luteum (CL), the neuroendocrine, paracrine, and autocrine mechanisms regulating luteolysis and PGF2 action in the CL are not fully understood. A number of substances produced locally in the CL may be involved in maintaining the equilibrium between luteal development and its regression. The present study was carried out to determine whether noradrenaline (NA) and nitric oxide (NO) regulate the sensitivity of the bovine CL to PGF2 in vitro and modulate a positive feedback cascade between PGF2 and luteal oxytocin (OT) in cows. Bovine luteal cells (Days 8–12 of the estrous cycle) cultured in glass tubes were pre-exposed to NA (10-5 M) or an NO donor (S-nitroso-N-acetylpenicillamine [S-NAP]; 10-4 M) before stimulation with PGF2 (10-6 M). Noradrenaline significantly stimulated the release of progesterone (P4), OT, PGF2, and PGE2 (P < 0.01); however, S-NAP inhibited P4 and OT secretion (P < 0.05). Oxytocin secretion and the intracellular level of free Ca2+ ([Ca2+]i) were measured as indicators of CL sensitivity to PGF2. Prostaglandin F2 increased both the amount of OT secretion and [Ca2+]i by approximately two times the amount before (both P < 0.05). The S-NAP amplified the effect of PGF2 on [Ca2+]i and OT secretion (both P < 0.001), whereas NA diminished the stimulatory effects of PGF2 on [Ca2+]i (P < 0.05). Moreover, PGF2 did not exert any additionally effects on OT secretion in NA-pretreated cells. The overall results suggest that adrenergic and nitrergic agents play opposite roles in the regulation of bovine CL function. While NA stimulates P4 and OT secretion, NO may inhibit it in bovine CL. Both NA and NO are likely to stimulate the synthesis of luteal PGs and to modulate the action of PGF2. Noradrenaline may be the factor that is responsible for the limited action of PGF2 on CL and may be involved in the protection of the CL against premature luteolysis. In contrast, NO augments PGF2 action on CL and it may be involved in the course of luteolysis.
calcium, catecholamines, corpus luteum, corpus luteum function, signal transduction
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
. Moreover, the bovine CL produces high concentrations of oxytocin (OT) [2], and the pulsatile secretion of PGF2 at luteolysis may involve a positive feedback loop between luteal and/or neurohypophysial OT and uterine PGF2 [3–5]. Nevertheless, neuroendocrine, paracrine, and autocrine mechanisms regulating luteolysis and PGF2 action on the bovine CL are not fully understood, and a number of substances produced in the CL locally have possible roles in maintaining the equilibrium between luteal development and regression.
It has been found that the unresponsiveness of early CL to PGF2 is not due to a lack of high-affinity PGF2 receptors in bovine CL [6–8]. Moreover, it has been shown that the decreasing sensitivity of bovine CL to extragonadal PGF2 depends on locally produced PGs, OT, and P4 [9]. We have shown that luteal OT, PGs, and P4 are components of the auto/paracrine positive feedback cascade in bovine CL. They also play roles in regulating the functions of PGF2 receptors and the PGF2-intracellular calcium ([Ca2+]i)-protein kinase C cascade. This auto/paracrine positive feedback loop can be a mechanism for protection against premature luteolysis during the early and midluteal phase. Nevertheless, at the end of the luteal phase the sensitivity of bovine CL to PGF2 actions dramatically increases [10]. Therefore, each of the factors that directly affect PGs, OT, and P4 secretion by luteal cells may also indirectly involve the regulation of the function of PGF2 receptors and may also be responsible for the varying sensitivity of bovine luteal cells to PGF2.
Bovine ovaries are richly supplied by adrenergic nerves [11] as well as nerves synthesizing nitric oxide (NO) [12]. Catecholamines such as noradrenaline (NA) stimulate the secretion of ovarian OT and P4 in cattle [13, 14]. Moreover, it has been recently shown that NA increases PG synthesis in bovine luteal cells [15]. On the other hand, several lines of evidence indicate that NO downregulates ovarian P4 secretion [15–18]. In addition, it has been recently found that NO may directly regulate PGF2 secretion from bovine CL in vivo [19] and in vitro [15]. Thus, both NO and NA play opposite roles in the regulation of bovine CL function and may have different effects on the function of PGF2 receptors regulating the secretion of luteal OT, P4, and PGs [9]. Therefore, the present studies were designed to determine whether ovarian NA and NO modulate the PGF2 action on bovine CL. Because PGF2 rapidly stimulates OT secretion [10] as well as increases [Ca2+]i [20] in a dose- and threshold-dependent fashion, we measured both OT and [Ca2+]i levels as indicators of CL sensitivity to PGF2.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Ovaries with CL were collected from Holstein cows at a local abattoir within 10–15 min after exsanguination and were submerged in ice-cold physiological saline before being transported to the laboratory. The stage of the estrous cycle was defined by macroscopic observation of the ovaries and the uterus [21]. The enzymatic dissociation of the luteal tissue and the culture of luteal cells in glass tubes in a shaking water bath were performed as previously described [9]. Cell viability was higher than 85% as assessed by trypan blue exclusion. The cells were adjusted to 2.5 x 105 or to 5 x 105 viable cells/ml of cultured medium: Dulbecco's modified Eagle's medium and F-12 Ham's medium (DMEM/Ham's F-12; 1:1 [v:v]; Sigma Chemical Co., St. Louis, MO, cat. no. D-8900) supplemented with 0.1% BSA (Boehringer Mannheim GmbH, Mannheim, Germany, cat. no. 735078), 0.5 mM ascorbic acid (Wako Pure Chemical Industries Ltd., Osaka, Japan, cat. no. 013-12061), 5 ng/ml sodium selenite (Sigma, S-5261), 5 µg/ml holo-transferrin (Sigma, T-3400), and containing 20 µg/ml gentamicin (Gibco Laboratories, Grand Island, NY, cat. no. 600-5750AD). The obtained cell suspension contained few endothelial cells or fibrocytes (10%), no erythrocytes, and 
20% of large and 70% of small luteal cells. The cells were stimulated simultaneously with various reagents as follows:
Experiment 1
The purpose of this experiment was to evaluate the influence of NA and NO on P4, OT, PGF2, and PGE2 secretion by midcycle luteal cells (Days 8–12 of the estrous cycle). The cells (2.5 x 105 cells/ml; four separate experiments, each performed on two to three CL) were incubated in glass tubes in 2 ml culture medium for a total of 16 h with solvent only (control: 20 µl of 10% dimethylsulfoxide [DMSO]) and solvent with either NA (10-5 M), an NO donor, S-nitroso-N-acetylpenicillamine (S-NAP; RBI, Natick, MA, cat. no. N-152; 10-4 M) or with bovine LH (USDA-bLH-B-6; 100 ng/ml) as a control. After 12 h of incubation, the medium was replaced, after centrifugation for 5 min at 50 x g, by fresh medium containing NA, S-NAP, or LH. The days of the estrous cycle, the cell number, and all doses of reagents chosen in the present study were based on data from previous experiments [9, 15]. The viability of the control, NA-, and S-NAP-treated cells after 16 h of incubation was similar (96.5%; P > 0.05) as assessed by trypan blue exclusion. Because the actions of PGF2 on luteal cells (experiment 2) were measured after 12 h of preincubation with NA or S-NAP, the samples in this experiment were collected only from the last 4 h of culture for comparison with data from the next experiment. After sampling, the cultured medium was stored at -30°C until the P4, OT, PGF2, and PGE2 could be determined.
Experiment 2
The purpose of this experiment was to examine the possible effect of NA and NO on PGF2-stimulated OT secretion by midcycle luteal cells. The cells (2.5 x 105 cells/ml; four separate experiments, each performed on two to three CL) were preincubated in glass tubes in 2 ml of culture medium with solvent only (DMSO; 20 µl of 10% DMSO) and solvent with either NA (10-5 M) or S-NAP (10-4 M) in a shaking water bath. After 12 h of preincubation, the medium was replaced with fresh medium with or without PGF2 (10-6 M) and with solvent only, NA, or S-NAP in solvent. After an additional 4 h of incubation, culture media were collected and stored at -30°C until the OT could be determined.
Experiment 3
The purpose of this experiment was to examine the possible effect of NA and NO on PGF2-mobilized free cytosolic [Ca2+]i. The luteal cells were prepared as described above from midcycle CL (three separate experiments, two to three CL in each experiment) and were adjusted to 5.0 x 105 viable cells/ml before incubation for 12 h in glass tubes in 3 ml of culture medium containing solvent only (control: 30 µl of 10% DMSO) and solvent with either NA (10-5 M) or S-NAP (10-4 M). After 12 h of incubation, the medium was replaced after centrifugation as described above with Hanks' balanced salt solution (Sigma, H-2387; pH 7.4) supplemented with 0.14 g CaCl2/L and 0.1% BSA, and [Ca2+]i was determined.
Hormone Determination
Measurement of P4 in the culture media was performed using a direct enzyme immunoassay (EIA) as described previously [22]. Antiserum of P4 (OK-1) was used at a final dilution of 1:600 000. The standard curve ranged from 0.39 to 100 ng/ml and the effective dose for 50% inhibition (ID50) of the assay was 4.5 ng/ml. The intra- and interassay coefficients of variation were 5.5% and 8.5%, respectively.
The concentration of PGF2 was also determined directly in the media by EIA as described previously [23]. The PGF2 standard curve ranged from 15.6 to 4000 pg/ml, and the ID50 of the assay was 250 pg/ml. The intra- and interassay coefficients of variation were 6.5% and 9.8%, respectively.
The PGE2 concentration was determined with EIA as described previously [15]. The PGE2 standard curve ranged from 0.11 to 28.2 ng/ml and the ID50 of the assay was 0.97 ng/ml. The intra- and interassay coefficients of variation were 4.9% and 8.2%.
The EIA for OT was based on the second antibody method using the biotin-streptavidin-peroxidase technique as described previously [9]. Anti-rabbit OT antiserum (R-1) was used at a final dilution of 1:150 000. The standard curve ranged from 3.91 to 1000 pg/ml, and the ID50 of the assay was 38.7 pg/ml. The intra- and interassay coefficients of variation were 7.2% and 11.4%, respectively.
Measurement of [Ca2+]i Concentration
Intracellular Ca2+ concentrations were determined by the use of the fluorescent Ca2+ indicator Fura-2 [24]. After 12 h of incubation with or without NA or S-NAP, the cells were centrifuged (5 min at 50 x g), and washed and resuspended in Hanks' solution. Fura-2 AM (Dojindo, Kumamoto, Japan, cat. no. 348-05831), the lipophilic acetoxymethylester form of Fura-2, was dissolved in DMSO to form a 1 mM stock solution, and 10 µl was added to 2 ml of cell suspensions (final concentration 5 µM) to preload the cells with dye. The cells were incubated at 37°C for 40 min and then washed three times in Hanks' solution. After washing, the cells were postincubated for 30 min in Hanks' solution at room temperature to ensure full hydrolysis of the Fura-2 ester. Spectrofluorometric measurements were conducted in 1.5-ml samples continuously stirred in a quartz-glass cuvette and thermostatically maintained at 37°C. Fluorescence was monitored using a Shimadzu spectrofluorometer RF-5000 (Shimadzu, Kyoto, Japan). Fifteen microliters of a 10-6 M solution of PGF2 in DMSO or 15 µl of DMSO only as a control were added into the cuvette through a port in the sample compartment connected to a tuberculin syringe. Excitation and emission wavelengths were 340 nm and 490 nm, respectively, with slit widths of 5 nm for both wavelengths. Intracellular [Ca2+]i concentrations were calculated from the equation:
A value of 224 nM was used for the Kd for Fura-2 at 37°C [24]. Maximum and minimum fluorescence (Fmax and Fmin) were measured by rapidly saturating Fura-2 with Ca2+ by permeabilizing the cells with 0.2% Triton X-100 (Fmax) and by adding 5 mM EGTA in Tris-HCl buffer, pH 8.5, to determine the basal fluorescence (Fmin) when virtually no Ca2+ was bound to Fura-2.
Statistical Analysis
The data are presented as the means ± SEM of three to four separate experiments each performed in triplicate. Because NA and S-NAP influence the basal rate of OT secretion (Fig. 1), OT secretion after PGF2 treatment was expressed as a percentage of internal control groups (Fig. 2). The baseline was removed by using the computer program GraphPad PRISM (GraphPad Software, San Diego, CA). The total PGF2-induced increase in [Ca2+]i in the cells pretreated or not pretreated with NA or S-NAP was measured by calculating the area under the curve (GraphPad PRISM). The baseline for [Ca2+]i was defined based on data from the resting period before PGF2 or DMSO treatment (see Fig. 3). The statistical significance of differences between controls and treated groups was assessed by one-way ANOVA followed by Bonferroni's multiple comparison test (GraphPad PRISM).
|
|
|
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
, and PGE2 by Luteal Cells Incubated with Adrenergic or Nitrergic Agents
The changes of P4, OT, PGF2, and PGE2 secretion observed in response to NA or S-NAP treatments are shown in Figure 1. LH (USDA-bLH-B-6) stimulated P4 secretion (P < 0.001) from cultured luteal cells on Days 8–12 of the estrous cycle, indicating that the cells cultured with the present experimental design were reactive (Fig. 1a). Whereas NA significantly stimulated the release of P4, OT, PGF2, and PGE2 (P < 0.01), S-NAP inhibited P4 and OT secretion (P < 0.05). On the other hand, secretion of PGE2 and PGF2 from the cells was stimulated by S-NAP (both P < 0.001).
Secretion of OT in Response to PGF2 Treatment on Cultured Bovine Luteal Cells Incubated with Adrenergic or Nitrergic Agents
The effects of PGF2 on OT secretion in DMSO- (solvent: 0.1% DMSO), NA-, and S-NAP-pretreated cells are shown in Figure 2. Prostaglandin F2 significantly stimulated OT secretion (to 203% of the baseline; P < 0.01) by cultured cells preincubated with DMSO only. Pretreatment of the cells with S-NAP augmented the effect of PGF2 on the stimulation of OT secretion to 381% of the baseline secretion in the internal standard group (P < 0.01) and to 148.7% (P < 0.05) compared to the value in only PGF2-treated cells. On the other hand, PGF2 did not exert any additional effects on OT secretion in NA-pretreated cells.
Cytosolic Free Ca2+ in Bovine Luteal Cells Preincubated with NA or S-NAP in response to PGF2 Treatment
The increases of [Ca2+]i observed in response to PGF2 from one representative experiment are shown in Figure 3. The mean resting level of [Ca2+]i in bovine luteal cells before PGF2 addition was approximately 48.8 nM in three separate cell preparations. While preincubation of the cells with S-NAP elevated the resting level of [Ca2+]i (54.4 nM; P < 0.05), NA inhibited it (37.8 nM; P < 0.05) in comparison with the values in both DMSO-pretreated groups. The DMSO did not stimulate [Ca2+]i level in cultured cells (P > 0.05). Treatment with PGF2 (10-6 M) resulted in two phases in the [Ca2+]i response, i.e., a rapid and transient rise immediately after the addition of PGF2 (initial phase), followed by a sustained secondary increase (influx of extracellular Ca2+). The duration of the initial phase was 20–50 sec (the period from the rise to the decay of the peak). In the cells that were preincubated with DMSO, PGF2 increased [Ca2+]i to 223% of the baseline (Table 1). However, pretreatment of the cells with NA (Fig. 3a) inhibited the effect of PGF2 on the stimulation of [Ca2+]i, resulting in [Ca2+]i levels of 128% of the baseline (P < 0.001; Table 1). In contrast to the NA action, preincubating the cells with S-NAP magnified the PGF2-induced increase in [Ca2+]i (to 322% of the baseline; P < 0.001).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
, and PGE2 secretion [9] that plays para/autocrine roles during the development and maintenance of the bovine CL [8, 9, 25]. In addition to these direct effects, NA prevents actions of exogenous PGF2 on bovine luteal cells. In the present study, PGF2 did not exert any additional effects on OT secretion in NA-pretreated cells (Fig. 2). This effect of NA is not likely to be due to depleting the luteal cells of OT during the 12-h preincubation period. Although our previous in vivo studies have shown that NA induces a large release of OT [14] and that multiple NA infusions markedly reduced the total amount of OT in mid- and late cycle bovine CL [26], in the present experiments, the cells after 12 h of preincubation with NA showed an ability to release large quantities of OT (Fig. 1). Moreover, it has been recently shown that NA activates in vitro terminal enzymes in the pathway of OT synthesis [27] and actively induces OT production in bovine CL. The latter result was confirmed in the present study (Fig. 1b). Thus, it should be emphasized that the observed phenomenon in the present study, i.e., the lack of additional effects of PGF2 on OT secretion in the NA-pretreated cells, is not due to depleting the luteal cells of OT.
In the present study, we suggest that NA modulates the PGF2-stimulated OT secretion on the receptor and/or postreceptor levels (Figs. 2 and 3; Table 1). In support of this, we have previously reported that blockers of adrenergic receptors may augment PGF2 action on OT secretion in conscious heifers [28]. Higher concentrations of OT were observed in heifers treated with PGF2 concomitantly with blockers of adrenergic receptors than in heifers treated with PGF2 alone. However, we did not have a clear explanation for this phenomenon at that time [28]. The data from experiment 3 in the present study could explain the mechanisms of this phenomenon [28]. As shown in Figure 3a and Table 1, NA inhibited the effect of PGF2 on the increase of [Ca2+]i. Therefore, NA acting through a ß-adrenergic receptor secondary messenger pathway [13, 14] may interact with the PGF2-[Ca2+]i-protein kinase (PK)C cascade. In support of this, some modulating interactions between the PKA and PKC signal transduction pathways have been well established in many cell types [29, 30] as well as in bovine luteal cells [31]. Therefore, summarizing the present and previous data [28], we assume that NA regulates the response of bovine luteal cells to extragonadal PGF2 through heterologous regulation of PGF2 receptors.
Alternatively, NA acts on CL function by the stimulation of PGs, OT, and P4 secretions (Fig. 1). Consequently, PGs, OT, and P4 could desensitize the bovine luteal cells to exogenous PGF2. Recently, we have shown that luteal OT and P4 could suppress the stimulatory effect of exogenous PGF2 on OT secretion and [Ca2+]i in bovine luteal cells at the receptor and/or postreceptor levels through their desensitization [9]. Moreover, homologous desensitization of PGF2 receptors in CL may be due to long-lasting stimulation by PGF2 produced locally [8, 9]. Based on these findings, we assume that both OT and P4 may indirectly (via PGF2) or directly (via heterologous desensitization) affect the PGF2 receptors and/or formation of second messengers through their luteotropic actions on the early to mid CL. Because treatment of the cells with NA stimulates P4, OT, and PGs (Fig. 1) and decreases the effect of PGF2 on bovine CL (Figs. 2 and 3), it could be assumed that NA is one of the factors that indirectly evoke the low reaction of luteal cells to PGF2 action during the early and midluteal phase in cattle [9, 10]. Therefore, this direct effect of NA, as well as the indirect effect of NA through P4, OT, or luteal PGs on the CL could be a mechanism for protection against premature luteolysis during luteal development and maintenance.
In contrast to NA, NO may be involved in the course of luteolysis. We have recently demonstrated that NO directly inhibit P4 secretion from bovine luteal cells [15], as shown previously in human [16], rabbit [32], and rat CL [17, 18]. In the present study, NO delivered by S-NAP also inhibited P4 secretion from luteal cells (Fig. 1) and augmented PGF2 action on luteal OT secretion (Fig. 2) and [Ca2+]i (Fig. 3 and Table 1). Thus, one could assume that NO increases the sensitivity of bovine luteal cells to exogenous PGF2 action. This hypothesis is supported by the fact that NO acts directly on cells via modulation of intracellular signalling pathways [33–35]. That is, the constitutive isoform of NO synthetase (NOS) requires Ca2+ and calmodulin for activation and production of NO. Then NO activates guanyl cyclase, resulting in the formation of cGMP. Cyclic GMP may then modulate secondary messengers in many cell types. It has also been reported that NO may have a direct influence on the basal [Ca2+]i [36–38] as well as endothelin 1-induced [Ca2+]i mobilization in cells [39]. Therefore, NO plays a role in regulation of bovine CL not only through the direct inhibitory effect on P4 secretion [15] but also by augmenting the response of luteal cells to PGF2 action on receptor and/or postreceptor levels. Nitric oxide may participate in the regulation of the PGF2 receptor functionality by directly modulating the PGF2-[Ca2+]i-protein kinase C cascade.
In addition to the inhibitory effect on P4 production, NO delivered by S-NAP inhibited OT output from bovine luteal cells (Fig. 1). These in vitro results confirm recent in vivo data that NO inhibited OT output from microdialyzed bovine CL [19]. We have recently shown that inhibition of the autocrine/paracrine OT action on luteal cells augmented the CL sensitivity to exogenous PGF2 action [9]. Thus, NO, by inhibiting OT secretion from luteal cells, may then result in the higher reaction of luteal cells to exogenous PGF2. Moreover, these increased effects of PGF2 on luteal cells pre-exposed to NO suggest that NO priming of bovine CL is needed to complete the regression of bovine CL. This supposition is supported by the finding that NO induced a transient decrease in [Ca2+]i [37]. After this transient decrease, [Ca2+]i recovered to control levels and then strongly increased over the basal values [37]. The latter result was confirmed in the present study (Fig. 3b). Moreover, the expression of an inducible isoform of NOS is correlated with cytotoxic/cytostatic events and results in a sustained synthesis of NO, which, in turn, induces apoptotic cell death [34, 35, 40]. Furthermore, [Ca2+]i-mobilizing agents and cytokines elicit an apoptotic response in the vascular endothelial cells through mechanisms that require NO synthesis [41]. It has been found recently that NO is produced in bovine CL mainly at late luteal phase. Activity of NADPH-diaphorase is present in bovine CL with the highest activity at mid- and late luteal stages. The endothelial isoform of NOS was observed with the strongest immunolabeling in the late CL. Also, the indicible isoform of NOS is expressed in bovine CL with the highest intensity at the late luteal stage [42]. Finally, the inhibition of ovarian NO production by perfusion of CL with an inhibitor of NOS prolonged the duration of the estrous cycle in conscious cows [19]. Therefore, one might assume that NO is a component of an autocrine/paracrine cascade in bovine CL and plays an important role in regulating functional and structural luteolysis in cattle.
In conclusion, the overall results suggest that adrenergic and nitrergic agents play opposite roles in the regulation of bovine CL function. While NA stimulates P4 and OT secretion, NO may inhibit it in bovine CL. Both NA and NO modulate the synthesis and action of PGs throughout the bovine luteal phase. Noradrenaline may be the factor that is responsible for the limited action of PGF2 on CL, and it may be involved in protection of the CL against premature luteolysis. In contrast, NO augments extragonadal PGF2 action on CL and it may be involved in the course of luteolysis.
|
ACKNOWLEDGMENTS |
|---|
and PGE2, and the National Hormone and Pituitary Program, University of Maryland School of Medicine and the National Institute of Diabetes and Digestive and Kidney Disease for bovine LH (USDA-bLH-B6). The authors are indebted to Dr. Jan Kotwica (Institute of Animal Reproduction and Food Research, Olsztyn, Poland) for critical review of this manuscript. |
FOOTNOTES |
|---|
1 This research was supported by Grants-in-Aid for Scientific Research (nos. 11460129 and 11556054) from the Ministry of Education, Science, Sports and Culture of Japan, the Polish National Research Council (grant KBN 5 P06K 027 13), and by the Japanese Society for the Promotion of Science (JSPS). D.J.S. was a postdoctoral fellow supported by the JSPS (no. 96346). 
2 Correspondence. FAX: 81 86 251 8388; kokuda{at}cc.okayama-u.ac.jp
Accepted: May 10, 2000.
Received: March 7, 2000.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
production in cows by progesterone and oestradiol. J Reprod Fertil 1995; 103:69–73 in initiated luteolysis in cattle. Res Vet Sci 1999; 66:1–5[CrossRef][Medline] receptor in bovine corpora lutea throughout the oestrous cycle and pregnancy. J Reprod Fertil 1995; 103:99–105 receptor in the early bovine corpus luteum. Biol Reprod 1995; 52:74–78[Abstract] and luteinizing hormone receptors in various bovine luteal cell types. Biol Reprod 1998; 58:849–856 is dependent on progesterone, oxytocin and prostaglandins. Biol Reprod 1999; 60:1292–1298 treatment in cattle. Theriogenology 1997; 48:733–742 stimulates phosphatidylinositol 4,5-bisphosphate hydrolysis and mobilizes intracellular Ca2+ in bovine luteal cells. Proc Natl Acad Sci U S A 1987; 84:3728–3732 a trigger for the initiation of prostaglandin F2 release at luteolysis in cattle? Biol Reprod 2000; 62:1109–1115 in bovine theca and granulosa cells luteinized in vitro. Biol Reprod 1992; 46:786–792[Abstract] analogue on oxytocin and progesterone release in heifers: catecholamines are not involved in this process. Anim Reprod Sci 1991; 25:1–10-induced signaling pathways. Endocrinology 1999; 140:4601–4608This article has been cited by other articles:
|
|
 |
|
  M. P. Goravanahally, M. Salem, J. Yao, E. K. Inskeep, and J. A. Flores Differential Gene Expression in the Bovine Corpus Luteum During Transition from Early Phase to Midphase and Its Potential Role in Acquisition of Luteolytic Sensitivity to Prostaglandin F2 Alpha Biol Reprod, May 1, 2009; 80(5): 980 - 988. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Shirasuna, S. Watanabe, T. Asahi, M. P B Wijayagunawardane, K. Sasahara, C. Jiang, M. Matsui, M. Sasaki, T. Shimizu, J. S Davis, et al. Prostaglandin F2{alpha} increases endothelial nitric oxide synthase in the periphery of the bovine corpus luteum: the possible regulation of blood flow at an early stage of luteolysis Reproduction, April 1, 2008; 135(4): 527 - 539. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Shibaya, K. M. Deptula, A. Korzekwa, K. Okuda, and D. J. Skarzynski Involvement of the Cytoskeleton in Oxytocin Secretion by Cultured Bovine Luteal Cells Biol Reprod, January 1, 2005; 72(1): 200 - 205. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T.P. Neuvians, D. Schams, B. Berisha, and M.W. Pfaffl Involvement of Pro-Inflammatory Cytokines, Mediators of Inflammation, and Basic Fibroblast Growth Factor in Prostaglandin F2{alpha}-Induced Luteolysis in Bovine Corpus Luteum Biol Reprod, February 1, 2004; 70(2): 473 - 480. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Skarzynski, M. M. Bah, K. M. Deptula, I. Woclawek-Potocka, A. Korzekwa, M. Shibaya, W. Pilawski, and K. Okuda Roles of Tumor Necrosis Factor-{alpha} of the Estrous Cycle in Cattle: An In Vivo Study Biol Reprod, December 1, 2003; 69(6): 1907 - 1913. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. J. Jaroszewski, D. J. Skarzynski, and W. Hansel Nitric Oxide as a Local Mediator of Prostaglandin F2{alpha}-Induced Regression in Bovine Corpus Luteum: An In Vivo Study Experimental Biology and Medicine, October 1, 2003; 228(9): 1057 - 1062. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. J. Jaroszewski, D. J. Skarzynski, R. M. Blair, and W. Hansel Influence of Nitric Oxide on the Secretory Function of the Bovine Corpus Luteum: Dependence on Cell Composition and Cell-to-Cell Communication Experimental Biology and Medicine, June 1, 2003; 228(6): 741 - 748. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Skarzynski, J. J. Jaroszewski, M. M. Bah, K. M. Deptula, B. Barszczewska, B. Gawronska, and W. Hansel Administration of a Nitric Oxide Synthase Inhibitor Counteracts Prostaglandin F2-Induced Luteolysis in Cattle Biol Reprod, May 1, 2003; 68(5): 1674 - 1681. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Tamanini, G. Basini, F. Grasselli, and M. Tirelli Nitric oxide and the ovary J Anim Sci, February 1, 2003; 81(14_suppl_2): E1 - 7. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
