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Changes in the Concentration of Gonadotrophic and Steroidal Hormones in the Antral Fluid of Ovarian Follicles Throughout the Oestrous Cycle of the Sheep

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Changes in the Concentration of Gonadotrophic and Steroidal Hormones in the Antral Fluid of Ovarian Follicles Throughout the Oestrous Cycle of the Sheep Aust. J. BioI. Sci., 1981,34,67-80 Changes in the Concentration of Gonadotrophic and Steroidal Hormones in the Antral Fluid of Ovarian Follicles throughout the Oestrous Cycle of the Sheep K. P. McNatty,A,B M. Gibb/ C. Dobson,A D. C. ThurleyA and J. K. Findlaye A Wallaceville Animal Research Centre, Private Bag, Upper Hutt, New Zealand. B Present address: Department of Obstetrics and Gynecology, University Hospital, Rijnsburgerweg 10, Leiden, The Netherlands. C Reproduction Research Section, Department of Physiology, University of Melbourne, Parkville, Vic. 3052; present address: Medical Research Centre, Prince Henry's Hospital, St Kilda Road, Melbourne, Vic. 3004. Abstract The concentrations of follicle-stimulating hormone (FSH), luteinizing hormone (LH), prolactin, progesterone, androstenedione and oestradiol were determined in the antral fluid of ovarian follicles > 1 mm in diameter as well as in ovarian venous or peripheral venous plasma, or both, from at least four different animals on each day throughout the oestrous cycle of the sheep. The individual steroid hormones in antral fluid were examined in relation to the steroid-secretion rates in ovarian venous plasma, follicle size and the hormone levels in jugular venous plasma. The range of levels of FSH, LH and prolactin in antral fluid was comparable to that in peripheral plasma. Irrespective of follicle size, the highest concentrations of FSH were present in follicles with high levels of oestrogen whereas the lowest were found in those follicles with low levels of oestrogen. In most follicles, the levels of LH were below 4 ng/ml but rose to high values at the time when a pre-ovulatory rise of LH was recorded in plasma. Prolactin was present in significantly higher concentrations in large follicles (~5 mm diam.) compared with small follicles (> 1 to < 5 mm diam.) except during the follicular phase when there was a progressive decline in prolactin levels in large, but not small, follicles to low values before ovulation. The steroid levels in antral fluid were up to 500000 times higher than those in peripheral plasma. In most follicles progesterone concentration was normally below 100 ng/ml, but increased to about 700 ng/ml in large follicles (~8 mm diam.) before ovulation and reached values of 2000 ng/ml in the newly formed corpus luteum. Androstenedione concentration in antral fluid varied between 2 and 70 ng/ml without any obvious pattern and the concentrations in large follicles (~5 mm) were not significantly different from those in small follicles. Oestradiol concentration in antral fluid varied between 10 and 1000 ng/m!. There were higher levels in large follicles than in small follicles and peak concentrations occurred in large follicles just before the onset of oestrus and also in similar-sized follicles on the third day after oestrus. It is suggested that the intrafollicular hormonal milieu may be important for the development of the antral follicle, maturation of the oocyte and the secretory status of the granulosa cells both before and after ovulation. Introduction The granulosa cells and oocyte of the·antral follicle do not have direct access to a blood supply but are bathed in a fluid whiCh contains most serum proteins, variable amounts of gonadotrophins and high concentrations of steroids (McNatty 1978). The endocrine micro-environment of the mammalian follicle has been correlated with the mitotic and biosynthetic activities of granulosa cells and the nuclear and cytoplasmic maturation of the oocyte (McNatty and Sawers 1975; Moor and Trounson 1977; Moor et al. 1978; McNatty et al. 1979a, 1979b). However, infor­ mation on the hormonal milieu in antral fluid of sheep follicles of different sizes on different days of the ovarian cycle is limited (Edgar 1953; Brand 1970; McNatty and Gibb 1977; Moor et al. 1978). 68 K. P. McNatty et al. In the sheep ovary, androstenedione and oestradiol are secreted mainly from large antral follicles (Hay and Moor 1975; Baird and Scaramuzzi 1976) whereas progesterone is secreted mainly from the corpus luteum (Baird et al. 1975). Therefore, the rate of androgen and oestrogen secretion into ovarian venous blood provides some indication of the level of follicular activity (Moore et al. 1969; Cox et al. 1971; Baird et al. 1976). However, the relationships between the steroids secreted by the follicles into the blood stream and those accumulated within the avascular follicular tissues are poorly understood. In the present study, peripheral or ovarian venous blood, or both, and ovarian antral fluid were collected from ewes at varying stages of the ovarian cycle, and the levels of luteinizing hormone (LH), follicle stimulating hormone (FSH), prolactin, androstenedione, oestradiol and progesterone were determined. In addition, the secretion rates of androstenedione and oestradiol by the individual ovaries were estimated before ovariectomy. These data were used to investigate the interrelation­ ships among the concentrations of pituitary and steroid hormones in antral fluid, the level of follicular activity (as assessed by the steroid secretion rates into ovarian venous plasma), follicle size and the hormone levels in plasma. Materials and Methods Experimental Animals One hundred and sixteen parous New Zealand Romney ewes (aged 2·5-4·5 years and bodyweight 38-66 kg) grazed on open pasture, were used in these studies. Most animals were recorded in oestrus on two previous occasions before undergoing surgery. Ewes were examined twice daily for oestrous activity detected by vasectomized rams fitted with marking harnesses. On the day before oestrus (Le. 16 days after the previous day of oestrus; day - 1) and on the expected day of oestrus (i.e. 17 days after the previous day of oestrus; day 0) the animals were examined for oestrous activity three to five times per day. The average cycle length preceding the one in which the animals under­ went surgery was 17·1±0·1 days (mean ±s.e.m., 116 observations). The seventeenth day after previous day of oestrus was classified as day - 0 if the animals had not displayed oestrous activity before surgery and as day +0 if the animals were in oestrus before surgery. Jugular and ovarian venous blood samples, and ovarian tissues were collected from at least four different animals on each day of a complete 17-day ovarian cycle. Recovery of Blood Samples, Ovarian Tissues and Antral Fluid The ewes were anaesthetized by Lv. injection of 5 % (w/v) sodium thiopentone (Intra val; May and Baker, New Zealand), and maintained in an anaesthetized state with either a halothane (Fluothane; ICI, New Zealand)-oxygen mixture (80 animals) or with additional sodium thiopentone when required (36 animals). A ventral abdominal incision was made and the uterus and ovaries exteriorized, taking care not to handle the ovaries. 25000 Lu. of heparin were administered to the animal via a jugular venous cannula and a 40-ml blood sample taken from the jugular vein. Before removal of the ovaries, the largest ovarian vein draining each ovary was cannulated using the largest vinyl tube (range 2·5-4·0 mm o.d.) capable of being accommodated by the vein. During the blood­ collection period, any ovarian vein that was not cannulated was clamped so that the entire venous effluent could be collected over a known time period. The length of the cannula was reduced to a minimum, usually 150 mm, and up to 25 ml of blood was collected during a recorded interval into a heparinized volumetric flask. In some animals, jugular venous blood samples (10 ml) were taken once daily throughout one complete oestrous cycle before the one in which they underwent surgery. All blood samples were centrifuged (4000 g for 15 min at 6°C) immediately after collection and aliquots of the plasmas were recovered and frozen to -20°C for subsequent hormone determinations. Immediately after ovariectomy, the ovaries were weighed and their gross morphology recorded. The excised tissues were then carefully dissected so that all antral follicles (> 1 mm diam.), corpora lutea, corpora albicantiae and the stroma could be isolated and individually weighed. Subsequently, Hormones in Sheep Ovarian Follicles 69 the fluid from each follicle and the fluid in the central cavity of the corpus luteum were gently aspirated through a 26-gauge needle into a I-ml syringe. Each fluid specimen was then transferred to a 0·5-ml plastic ampoule which was sealed and stored frozen at - 20D C until assayed for hormones. No attempts were made to recover the oocytes or other individual ovarian cell types. Moreover, no attempt was made to assess whether the follicles were healthy or atretic. Calculation of Ovarian Secretion Rates The secretion rate of ovarian steroids was calculated from a knowledge of the time taken to collect a certain volume of blood (blood flow), the concentration of steroid in ovarian venous plasma and haematocrit. The haematocrits were determined in an MSE (Crawley, UK) Microhaemotocrit centrifuge (at 16000 rpm for 2 min) using heparinized capillary tubes (Terumo Corp., Tokyo, Japan). The results were not corrected for any steroid which may have been adsorbed onto the red-cell surfaces. Hormone Assays LH and FSH The radioimmunoassays for LH and FSH in plasma and follicular fluid were based on those described previously (Scaramuzzi et al. 1970; Salamonsen et al. 1973). The pituitary LH preparation for both standard and the iodinated tracer was NIH-LH-S11 (biopotency 0·81 xNIH-LH-Sl). The LH antibody, raised in a rabbit against NIH-LH-S11, was used at an initial dilution of 1 : 50000. The assays of LH in plasma were performed in duplicate whereas those in antral fluid were made on single samples. The volume of plasma used in the LH assay varied from 0·05 to 0·40 ml whereas the volume of antral fluid varied from 0·01 to 0·05 ml.
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