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Regular Article |
Injection in the Cow1
a Department of Animal Science
b University Farm, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080-8555, Japan
c Departamento de Fisiologia, Facultad de Ciencias Veterinarias, Universidad Nacional de Asuncion, San Lorenzo, Paraguay
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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is to decrease ovarian blood flow. However, before Day 5 of the normal cycle, the corpus luteum (CL) is refractory to the luteolytic action of PGF2. Therefore, we aimed to determine in detail the real-time changes in intraluteal blood flow after PGF2 injection at the early and middle stages of the estrous cycle in the cow. Normally cycling cows at Day 4 (early CL, n = 5) or Days 10–12 (mid CL, n = 5) of the estrous cycle (estrus = Day 0) were examined by transrectal color and pulsed Doppler ultrasonography to determine the blood flow area, the time-averaged maximum velocity (TAMXV), and the volume of the CL after an i.m. injection of a PGF2 analogue. Ultrasonographic examinations were carried out just before PG injection (0 h) and then at 0.5, 1, 2, 4, 8, 12, 24, and 48 h after the injection. Blood samples were collected at each of these times for progesterone (P) determination. The ratio of the colored area to a sectional plane at the maximum diameter of the CL was used as a quantitative index of the changes in blood flow within the luteal tissue. Blood flow within the midcycle CL initially increased (P < 0.05) at 0.5–2 h, decreased at 4 h to the same levels observed at 0 h, and then further decreased to a lower level from 8 h (P < 0.05) to 48 h (P < 0.001). Plasma P concentrations decreased (P < 0.05) from 4.7 ± 0.5 ng/ml (0 h) to 0.6 ± 0.2 ng/ml (24 h). The TAMXV and CL volume decreased at 8 h (P < 0.05) and further decreased (P < 0.001) from 12 to 24 h after PG injection, indicating structural luteolysis. These changes were not detected in the early CL, in which luteolysis did not occur. In the early CL, the blood flow gradually increased in parallel with the CL volume, plasma P concentration, and TAMXV from Day 4 to Day 6. The present results indicate that PGF2 induces an acute blood flow increase followed by a decrease in the midcycle CL but not in the early CL. This transitory increase may trigger the luteolytic cascade. The lack of intraluteal vascular response to PG injection in the early CL appears to be directly correlated with the ability to be resistant to PG.
corpus luteum, corpus luteum function, ovary, progesterone
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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A rapid decrease in the luteal blood flow has been proposed as one of the main luteolytic actions of prostaglandin (PG) F2. This decrease in luteal blood flow occurs during both normal and PGF2-induced luteolysis [5, 6]. In the cow, the increase in the uterine release of PGF2 observed at Days 17–18 of the normal cycle has been associated with luteolysis [7]. Luteal regression is initiated by an exogenous injection of PGF2 given after Day 7 of the normal estrous cycle [8]. However, the same luteolytic dose of PGF2 did not induce luteolysis before Day 5 [9]. Recently, we demonstrated that an injection of a luteolytic dose of PGF2 analogue to the cow at the middle stage of the estrous cycle increases the intraluteal production of vasoactive substances such as endothelin-1 (ET-1) [10] and angiotensin II (Ang II) [11], both of which play important roles in the luteolytic cascade [10, 12–17].
Color Doppler ultrasonography is a useful, noninvasive tool for evaluating ovarian vascular function, allowing a visual observation of the changes in the blood flow in a delimited area within the CL [18] or in the wall of preovulatory follicles [19]. During luteolysis, electromagnetic flow probes implanted around the ovarian artery demonstrated a close correlation between the decrease in ovarian blood flow and the systemic P concentration in the cow [20, 21]. Using the same method, we found that ovarian blood flow acutely increases after a luteolytic dose of PGF2 analogue injection to the cow at the middle stage of the estrous cycle [16]. However, detailed information on the changes in blood flow within the early and midcycle CL of the cow is still lacking. Thus, we aimed to determine in detail the real-time changes in intraluteal blood flow after PGF2 analogue injection at the early and middle stages of the estrous cycle in the cow.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Normally cycling Holstein cows at the early (n = 5) or middle (n = 5) stages of the estrous cycle were used for this study. Five hundred micrograms of a PGF2 analogue (cloprostenol [estrumate]; Sumitomo Pharmaceutical Co., Osaka, Japan) was injected i.m. at Day 4 (early CL) or at Days 10–12 (midcycle CL) of the estrous cycle (estrus = Day 0). Ultrasonographic examinations were carried out just before PG injection (0 h) and at 0.5, 1, 2, 4, 8, 12, 24, and 48 h after the injection (Fig. 1). Blood samples were collected at each of these times for P determination.
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The CL was examined by transrectal ultrasonography using an ultrasound scanner (Aloka SSD-1700; Mitaka, Tokyo, Japan) equipped with a 7.5-MHz convex transducer. During each ultrasonographic examination, the volume (V) of the CL was estimated using the following equation for a modified prolate ellipsoid: V = 0.523 x A x B, where A represents the maximum length and B represents the transverse diameter. After morphological evaluation, the flow mode was activated for blood flow mapping. Color signals were used to generate images in which blood flow was detectable within the CL. Using these images, the blood flow was evaluated at the apex, middle, and base of the CL. In addition, the image obtained in a vertical plane from the apex to the base of the CL, designated as the overall image (Fig. 1), was used to determine the sectional area (SA) of the CL: SA = 
/4 x (SD)2, where SD is the sectional diameter. The ratio of the colored area in the image obtained in a vertical plane at the maximum diameter of the CL from the apex to the base was used as a quantitative index to express the changes in blood flow within the CL.
Blood flow velocity wave forms were recorded during 3 cardiac cycles to determine the time-averaged maximum velocity (TAMXV) in the base of the CL by placing the sample volume across the main vessel and switching on the pulsed Doppler mode. The pulsed Doppler sample volume was set at a 1-mm width. All scans were performed at a pulse repetition frequency of 6 Hz. Identical color gain settings were used for all scanning. During each scanning, the distance between the transducer face and CL was minimized (1–2 cm) to reduce signal attenuation. The angle of insertion was adjusted to obtain the maximum color intensity. Scan records (images) were stored on an MO disk drive for a personal computer (Macintosh; Apple Corp., San Jose, CA) and then viewed on the monitor. The colored area was selected and changed to a black-and-white image using Adobe Photoshop 5.5 software (Adobe Systems, San Jose, CA). The same image was used to calculate the area of the CL, and the colored area was quantified using the NIH Image program (version 1.62) developed at the U.S. National Institutes of Health (http://rsb.info.nih.gov/nih-image). The ratio of the area of the CL and the sum of the areas in which blood flow was detected were calculated from at least 5 different cows per group at each time point and expressed as the percentage of the area of the CL.
Progesterone and Cortisol Assays
Blood samples were obtained by caudal venipuncture just before each scanning using sterile 10-ml tubes containing 200 µl of a stabilizer solution (0.3 M EDTA, 1% acetyl salicylic acid, pH 7.4). All tubes were immediately chilled in ice water for 10 min, centrifuged at 2000 x g for 10 min at 4°C, and the obtained plasma was stored at -30°C until the analysis of the plasma levels of P and cortisol. At the end of the experiment, all samples from each cow were analyzed in the same assay in duplicate using a second antibody enzyme immunoassay (EIA) after extraction. The EIA for P was done as previously described [22]. The standard curve ranged from 0.05 to 25 ng/ml, and the ED50 of the assay was 2.4 ng/ml. The intra- and interassay coefficients of variation (CVs) were 4.7% and 6.5%, respectively. The recovery rate of P (5 ng) added to 1-ml plasma samples was 92% (n = 10). The cortisol EIA was identical to the EIA for P. Standards or samples (15 µl) were incubated with 100 µl polyclonal antibody (raised in a rabbit against cortisol-3-CMO-BSA; Cosmo Bio Co., Tokyo, Japan) solution (1:70000) and 100 µl cortisol-3-CMO-horseradish peroxidase (1:300000; Cosmo Bio Co.) for 16 h at 4°C. The standard curve ranged from 0.08 to 80 ng/ml, and the ED50 of the assay was 2.5 ng/ml. The intra- and interassay CVs were 6.8% and 8.6%, respectively. The cross-reactivities of the antibody were 100% for cortisol, 11.5% for 11-deoxycortisol, 4% for cortisone, 2% for corticosterone, 0.2% for 17-hydroxy-11-deoxy-corticosterone, 0.035% for progesterone, 0.02% for testosterone, 0.06% for androstenedione, and less than 0.01% for aldosterone, pregnenolone, dehydroepiandrosterone, and estradiol. The recovery rate of cortisol (1 ng or 10 ng) added to 1-ml plasma samples was 94% (n = 10 for each concentration).
Statistical Analysis
The time of PGF2 analogue injection was defined as 0 h. Plasma concentration of P, volume of the CL, and TAMXV are presented as means ± SEM. The colored area with a detectable blood flow within the CL was expressed as the percentage of the CL area. Data were examined by repeated measures ANOVA with time as the variable tested. Where significant effects of time were found (P < 0.05), the test of least significant difference was used to identify which points were different from the pre-PG injection period.
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RESULTS |
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Changes in the Plasma Concentration of P and the Volume of the CL
In spite of the injection of a luteolytic dose of PGF2 analogue into cows with an early CL, the plasma concentration of P increased from 0.7 ± 0.6 ng/ml at Day 4 to 2.7 ± 0.07 ng/ml at Day 6 (P < 0.01). During the same period (Days 4–6), the volume of the CL also increased from 2.8 ± 0.6 cm3 to 4.6 ± 0.6 cm3 (P < 0.05), indicating normal CL development (Fig. 2, left panels, and Fig. 3). However, in the cows with midcycle CLs, the same dose of PGF2 analogue induced a rapid decrease in the plasma concentration of P from 0.5 h (P < 0.05) to 24 h (P < 0.001) after injection. The volume of the CL decreased at 8 h (P < 0.05) and further decreased from 12 to 24 h (P < 0.001) after PG injection, indicating structural luteolysis (Fig. 2, right panels, and Fig. 4).
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Changes in Intraluteal Blood Flow Area and TAMXV
In the preliminary experiment using 3 cows at the middle stage of the estrous cycle (Days 10–12), we did not detect any significant change in the luteal blood flow as the result of manipulations or handling of the animals throughout a 3-h period of continuous observation. In addition, PGF2 analogue injection did not affect the plasma concentration of cortisol in the cows with midcycle CL over the experiment period in this study (3.5 ± 0.3 ng/ml and 3.2 ± 0.2 ng/ml for pre-PG and post-PG period, respectively). These findings suggest that the manipulations for ultrasonographic examination were not stressful enough to affect ovarian blood flow and CL function. Thus, each cow at time 0 (before PGF2 injection) was considered its own control to compare blood flow changes over time after PGF2 analogue injection.
Color Doppler images of the early and midcycle CL relative to the time of PGF2 injection are shown in Figures 3, 4, and 5. The red color was generated by the blood flow toward the transducer's face, and the blue color indicated blood flow away from the transducer's face. When the transducer was placed close to the CL, the blood flow captured by the transducer appeared as different color intensities on the monitor. As the velocity of the flow increased, the color intensity increased. Throughout the experiments, the color gain of the flow mode was set to detect movement of at least 2 cm/sec.
In early CLs, most of the colored area was observed in the basal part of the CL. The TAMXV increased at 48 h (P < 0.05; Fig. 6, lower left panel). In contrast, in the midcycle CL before PGF2 injection, the colored area with detectable blood flow was mostly observed around the CL. This area represented about 20% of the total CL area. At 30 min after PGF2 injection, the detectable blood flow area acutely expanded to the internal part of the CL, occupying 35–45% of the CL. These values remained higher than those in the preinjection period at 0.5–2 h (P < 0.05), decreased at 4 h to the same levels observed at 0 h, and then further decreased to a lower level from 8 h (P < 0.05) to 48 h (P < 0.001; Figs. 4 and 6, upper right panel). The TAMXV decreased from 8 h to 24 h (P < 0.05–0.001), and the pulse image was undetectable in the midcycle CL at 48 h.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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analogue during the midluteal phase of the estrous cycle in the cow. These results confirmed the results of previous studies showing a parallel reduction in luteal blood flow and plasma P concentration after similar injection of a luteolytic dose of PGF2 analogue. In the midcycle CL, an acute increase in blood flow was detected between 30 min and 2 h after PGF2 injection. These changes were not detected in the early CL (Day 4) in which parallel and gradual increases in the CL volume, plasma P concentration, and TAMXV were observed from Day 4 to Day 6 in spite of the PGF2 injection. The results suggest that an initial increase in intraluteal blood flow induced by PG injection in the midcycle CL may trigger the initiation of the luteolytic process in the cow. In the present study, plasma concentration of cortisol did not change throughout the experimental period, indicating that handling and manipulation did not induce significant stress on the cows used. Thus, the acute increase in blood flow observed only in the midcycle CL probably was due to the luteolytic PG injection.
One of the intriguing differences between the early and the midcycle CL is the inability of the former to undergo (PGF2-induced) luteolysis. In the midcycle CL, a transient but significant increase in intraluteal blood flow from 0.5 to 2 h after PGF2 injection was observed, but the early CL showed no acute changes in blood flow. This phenomenon may involve an acute change in the function of small intraluteal vessels (arterioles, venules, and/or capillaries) in which the flow was undetectable before PGF2 injection. The increase in blood flow (area) was independent of changes in blood velocity (TAMXV) detected in one of the main arteries at the base of the CL. The exact mechanism and physiological relevance of the initial increase in blood flow remains unknown. The transitory hyperemic reaction appears to involve the dilatation of arterioles, precapillary sphincters, and postcapillary venules. PGs modulate vascular resistance in most of the vascular beds of the body, including uterine and ovarian circulation [23, 24]. We recently found that an injection of a PGF2 analogue induced an acute release of PGE2 and PGF2 from the midcycle CL in the cow [11]. Moreover, the same PG injection acutely induced the expression of cyclooxygenase (COX)-2 from 1 to 4 h postinjection in the cow [9, 25] and the ewe [26] but did not affect the COX-2 expression in the early CL [23]. These findings suggest that PG synthesis from arachidonic acid and the enzymatic action of COX-2, including vasodilatory PGI2, may cause this acute increase in blood flow within the midcycle CL.
Nitric oxide (NO) is another local vasodilatory substance that may play a direct luteolytic role in the regressing CL [27]. Other researchers have demonstrated that PGs modulate luteal NO synthase (NOS) activity and P production, depending on the stage of the CL. PGF2 caused a 2.5-fold increase of NOS activity and a marked decrease in P production on Day 9 in rabbit CLs [28]. NO also acutely inhibited P release from Day 9 CLs of pseudopregnant rabbits [29].
In the present study, the changing profile of plasma P concentration during luteolysis was almost the same as those previously reported in the cow [10, 20]. A significant decrease in plasma P concentration was first observed 30 min after PG injection, and P concentration decreased further over time. The CL volume and TAMXV remained unchanged until 8 h. These results demonstrate that PGF2-induced decrease in plasma P concentration occurs before a detectable decrease in the volume of the CL and in luteal blood flow. In addition, the reduction in luteal blood supply at 8 h after PGF2 injection was coincident with the time of the initiation of structural luteolysis, which was reflected in the first significant decrease in the volume of the CL.
In the present study, vascular changes during luteolysis included an initial acute increase in blood flow expressed by an increase in the relative color area of the midcycle CL. However, such a change was not observed following the injection of PGF2 in the early CL. The absence of this change within the early CL, in which luteolysis did not occur, and the progressive vascular changes in the midcycle CL, in which luteolysis did occur, suggest that these vascular alterations are stage and PG dependent and are necessary for the induction of the local release of vasoactive peptides (ET-1 and Ang II), which further induce a decrease in the blood supply (flow) as a result of vasoconstriction. The initial acute increase in intraluteal blood flow at 0.5–2 h after PGF2 injection may be crucial for stimulating luteal endothelial cells to produce and release vasoactive substances necessary to trigger and achieve a cascade of luteolysis. This hypothesis is supported by the fact that the local releases of ET-1 [10] and Ang II [11] in the midcycle CL first increase at 2–4 h after PGF2 injection in vivo following the phase when the acute increase in intraluteal blood flow is prominent. Moreover, ET-1 inhibits P release in luteal cell culture [12] and in the microdialyzed CL in vitro [15]. Likewise, Ang II also inhibits the local secretion of P from midcycle CLs [30] but stimulates P release from early CLs [31].
In conclusion, the present results indicate that PGF2 induces an acute blood flow increase followed by a decrease within the midcycle CL but not in the early CL. This transitory increase may trigger the luteolytic cascade. The lack of intraluteal vascular response to PG injection in the early CL appears to be directly correlated with the ability to be resistant to PG.
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FOOTNOTES |
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1 This study was supported by a Grant-in-Aid for Scientific Research of the Japan Society for the Promotion of Science (JSPS) and the Novartis Foundation (Japan) for the Promotion of Science. T.J.A. is a postdoctoral fellow supported by JSPS. 
2 Correspondence. FAX: 81 155 49 5462; akiomiya{at}obihiro.ac.jp
3 Current address: Department of Animal Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080-8555, Japan
Accepted: October 12, 2001.
Received: July 13, 2001.
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M Ohtani, S Takase, M P B Wijayagunawardane, M Tetsuka, and A Miyamoto Local interaction of prostaglandin F2{alpha} with endothelin-1 and tumor necrosis factor-{alpha} on the release of progesterone and oxytocin in ovine corpora lutea in vivo: a possible implication for a luteolytic cascade Reproduction, January 1, 2004; 127(1): 117 - 124. [Abstract] [Full Text] [PDF]
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