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B. K. Campbell
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R. J. Scaramuzzi
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Ewes with ovarian autotransplants received either inhibin antiserum (10 ml i.v.; n = 6) or sheep serum (10 ml i.v.; n = 5) on day 10 of the luteal phase with additional daily injections (1 ml i.v.) from 48 h after the initial injection until the end of blood sampling, 9 days later. Luteal regression was induced by injection of prostaglandin F (PGF) 4.2 days after the initial plasma injection. Jugular and ovarian venous blood samples were taken every 4 h over the experimental period, and more frequent samples (every 10–15 min for 2–3 h) were taken to examine pulsatile secretory responses from the ovary to GnRH-induced (150 ng i.m. 1 and 4 days after initial treatment) or endogenous LH pulses (24 and 48 h after injection of PGF). Plasma FSH concentrations, ovarian steroid secretion and ovarian follicular development were measured. Immunization against inhibin resulted in a two- to threefold increase (P < 0.001) in plasma FSH concentrations, which remained higher than controls until injection of PGF. Within 24 h of immunization, there was an increase in the number of small ovarian follicles (P < 0.01) and by 4 days after treatment, immunized ewes had four or five (P < 0.01) large ovarian follicles and, despite little change in the basal steroid secretion, a four- to sixfold increase (P < 0.05) in the amplitude of the steroidogenic response to a GnRH-induced LH pulse. After induction of luteolysis, basal oestradiol and androstenedione secretion increased markedly to a preovulatory peak three- to fivefold higher (P < 0.01) than that of controls and occurring 24 h earlier (P < 0.001). As a result, the time of the preovulatory LH surge was also advanced 24 h in immunized ewes (P < 0.001). Induction of luteal regression by injecting PGF resulted in a decrease in FSH concentrations in both treatment groups, but this decrease was more marked in immunized animals (50% of value before PGF was given; P < 0.001) than in controls (20% of value before PGF was given; P < 0.05), so that by 16 h after PGF injection, FSH values were no longer significantly different in the two treatment groups. This large fall in FSH concentrations had no deleterious effects on steroid secretion or the number of large follicles in immunized ewes and, as shown by a marked increase in ovarian size and a threefold increase (P < 0.001) in progesterone concentration during the subsequent luteal phase, these animals had multiple ovulations. We conclude that oestradiol alone can modulate FSH within physiological limits in the absence of inhibin negative feedback during the follicular phase and that the increase in ovulation rate that occurs after inhibin immunization is not caused by attenuation of the follicular phase suppression in FSH.

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C. J. H. Souza
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B. K. Campbell
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D. T. Baird
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The dynamics of ovarian follicular development and its relationship to ovarian and pituitary hormones during seasonal anoestrus were investigated for 10 days in nine ewes with autotransplanted ovaries in a longitudinal study. The size and position in the ovary of individual follicles over 2.5 mm in diameter were recorded by daily ultrasonography. Samples of ovarian and jugular venous blood were collected at intervals of 12 h, before and after a GnRH challenge (250 ng GnRH, i.v.) so that basal and LH-stimulated ovarian steroid secretion could be determined. Throughout the experimental period, all animals developed at least one large antral follicle > 5 mm, which secreted increased (P < 0.05) amounts of oestradiol and androstenedione in response to an LH challenge as the diameter of the follicle increased. However, a decrease (P < 0.05) in ovarian steroid secretion preceded any significant change in follicular diameter, indicating a dissociation between morphological and functional stages of dominance in sheep. We conclude that follicular growth and ovarian steroid secretion in sheep occur in wave-like forms, with the ascending and static part of both waves being synchronous but with a decline in steroid secretion preceding any changes in follicular diameter. Therefore, in sheep, follicular size alone is not an adequate parameter to assign dominance, and the secretory status of the follicle at any given time must be taken into account when studying the dynamics of follicular growth.

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B. K. Campbell
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D. T. Baird
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R. Webb
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The study reports the development of a serum-free culture system for sheep thecal cells that overcomes the problem of spontaneous luteinization and the use of this system to study the control of proliferation and differentiation. Theca cells were isolated by enzymatic dispersion from small follicles (< 3.5 mm) and the effect of plating densities (25–100 × 103 cells per well), LH (0.001–100 μg l−1), insulin (1–5000 μg l−1), insulin-like growth factor I (IGF-I) analogue (1–100 μg LR3-IGF-Il−1) and epidermal growth factor (EGF) (0.005–50 μg l−1) on the number of cells and androstenedione and progesterone production were determined. Plating density had a marked effect on the pattern of hormone secretion with densities between 50 and 75 × 103 cells per well resulting in a high androstenedione: progesterone ratio at optimum doses of LH (0.1 μg l−1: P < 0.001). In the first 48 h, the production of both androstenedione and progesterone was stimulated in a dose-dependent manner by LH (P < 0.001). However, the production of androstenedione was ten times higher than that of progesterone and was more sensitive to LH (ED50 value 0.08 μg l−1 for androstenedione and 1 μg l−1 for progesterone). From 48–144 h of culture higher doses of LH (> 1 ng ml−1) inhibited androstenedione (P < 0.001) and stimulated progesterone (P < 0.001) and resulted in a marked change in cell morphology, thus reflecting both functional and morphological luteinization. At optimum doses of LH, both insulin and IGF stimulated cell proliferation (P < 0.001) and androstenedione production (P < 0.001) in a dose responsive manner and there was a significant (P < 0.001) interaction between them. In contrast, both insulin and IGF-I inhibited (P < 0.001) progesterone production in a dose responsive manner. EGF stimulated cell proliferation (P < 0.001) and progesterone production (P < 0.001), but inhibited androstenedione production (P < 0.001), in a dose responsive manner. In conclusion, this culture system exhibits physiologically relevant responses to known in vivo modulators of follicle development. The biphasic nature of the theca cell response to LH emphasises the exquisite sensitivity of theca cells to LH stimulation and highlights the importance of dose–response relationships in the gonadotrophic control of ovarian function.

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B. K. Campbell
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R. J. Scaramuzzi
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R. Webb
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A serum-free ovine granulosa cell culture system is described that allows the induction of FSH-responsive oestradiol production by undifferentiated cells from small (< 3.5 mm) follicles (P < 0.001) and the maintenance of oestradiol production by differentiated cells from large (≥3.5 mm) follicles. Physiological doses of FSH stimulated (P < 0.01) proliferation of cultured granulosa cells from both small and large follicles. The synthesis of immunoreactive inhibin and progesterone by granulosa cells from small and large follicles increased (P < 0.01) with time of culture, and was not dependent on FSH. Inhibin secretion expressed on a per cell basis was not FSH responsive. Insulin and insulin-like growth factor I (IGF-I), in the presence of FSH, stimulated (P < 0.001) cell proliferation and oestradiol and inhibin production by granulosa cells from small and large follicles. There was a significant (P < 0.001) interaction between insulin and IGF-I in the stimulation of granulosa cell proliferation and differentiation. Both epidermal growth factor (EGF) and transforming growth factor α (TGF-α) in the presence of FSH stimulated cellular proliferation (P < 0.001) in a dose-responsive manner and concomitantly inhibited (P < 0.001) oestradiol and inhibin secretion. The development of this granulosa cell culture system will make it possible to study, in vitro, the cascade of events that controls granulosa cell differentiation and ultimately follicle selection in sheep.

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H. M. Picton
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B. K. Campbell
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M. G. Hunter
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Studies were carried out to investigate the conditions required for maintenance of aromatase activity and expression in long-term cultures of pig granulosa cells. Cells from large (> 2 mm) and small (≤ 2 mm) follicles were cultured at 37°C with 5% CO2 in McCoys 5a medium supplemented with 0.1% (w/v) BSA, testosterone (100 μg l−1), insulin (10 μg l−1) and long R3 insulin-like growth factor I (IGF-I) (100 μg l−1). Cells were cultured with five concentrations of USDA pFSH-I-2 (0–100 μg l−1) for 48, 96 or 144 h with or without fetal calf serum (FCS). The number of cells and oestradiol, progesterone and inhibin production were measured. In marked contrast to oestradiol production from cells cultured in plates precoated with FCS, 1 μg FSH l−1 was optimal for the maintenance of high oestradiol production by granulosa cells from large follicles after 144 h of serum-free culture. Culture with FCS promoted cell proliferation, reduced oestradiol production, and supported FSH-dependent (P < 0.01) increased progesterone and inhibin production indicating cellular luteinization. Northern blot analysis of total RNA from cells cultured with 1 μg FSH l−1 detected 2.5 and 1.8 kb transcripts encoding aromatase cytochrome P450 (P450arom) and cholesterol side-chain cleavage cytochrome P450 (P450scc), respectively. Transcript expression was hormone sensitive, irrespective of the presence of FCS. High concentrations of FSH (100 μg l−1) stimulated expression of P450scc, but inhibited P450arom expression as the cells luteinized after 144 h of culture. This serum-free system, which maintains the aromatase enzyme complex, is fundamental if physiologically relevant observations are to be made of the mechanisms regulating follicle hierarchy development from long-term cultures of pig cells.

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B K Campbell
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N R Kendall
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V Onions
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R J Scaramuzzi Division of Human Development, Department of Veterinary Basic Sciences, School of Clinical Sciences, University of Nottingham, Q.M.C., Nottingham NG7 2UH, UK

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Glucose is a critical metabolic fuel in most mammals although many foodstuffs also contain high levels of the monosaccharides, galactose and fructose. The aims of this work were to determine the insulin response to challenges of these sugars (experiment 1) and to examine the effect of systemic (experiment 2) and direct ovarian (experiment 3) infusion of these monosaccharides on ovarian function in ewes with autotransplanted ovaries. In experiment 1, both fructose (fourfold increase peaking in 2 h) and galactose (twofold increase; 30 min) elicited markedly different (P<0.001) insulin responses than glucose (sevenfold increase; 20 min) although the total amount released following fructose and glucose challenge was similar. In experiment 2, low-dose systemic fructose infusion had no acute effect on insulin but did depress FSH (P<0.05), and following the end of fructose infusion, a transient increase in FSH and insulin was observed (P<0.05), which was associated with an increase (P<0.05) in ovarian oestradiol and androstenedione secretion. Systemic infusion of neither glucose nor galactose had a significant effect on ovarian steroidogenesis although glucose acutely suppressed insulin levels. In contrast, ovarian arterial infusion of fructose and glucose had no effect on ovarian function whereas galactose suppressed ovarian follicle number and steroid secretion (P<0.05). In conclusion, this work indicates that fructose and galactose can influence ovarian function in vivo in sheep and that different mechanisms are involved. Thus, fructose exerts stimulatory effects through indirect modulation of peripheral insulin and/or gonadotrophin levels whereas galactose exerts primarily suppressive effects by direct actions on the ovary.

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A Somchit-Assavacheep Departments of Veterinary Basic Sciences, Veterinary Clinical Sciences, Department of Animal Husbandry, Division of Obstetrics and Gynaecology, Sutton Bonnington Campus, UMR Physiologie de la Reproduction et des Comportements, Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK
Departments of Veterinary Basic Sciences, Veterinary Clinical Sciences, Department of Animal Husbandry, Division of Obstetrics and Gynaecology, Sutton Bonnington Campus, UMR Physiologie de la Reproduction et des Comportements, Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK

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B K Campbell Departments of Veterinary Basic Sciences, Veterinary Clinical Sciences, Department of Animal Husbandry, Division of Obstetrics and Gynaecology, Sutton Bonnington Campus, UMR Physiologie de la Reproduction et des Comportements, Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK

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M Khalid Departments of Veterinary Basic Sciences, Veterinary Clinical Sciences, Department of Animal Husbandry, Division of Obstetrics and Gynaecology, Sutton Bonnington Campus, UMR Physiologie de la Reproduction et des Comportements, Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK

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N R Kendall Departments of Veterinary Basic Sciences, Veterinary Clinical Sciences, Department of Animal Husbandry, Division of Obstetrics and Gynaecology, Sutton Bonnington Campus, UMR Physiologie de la Reproduction et des Comportements, Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK

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R J Scaramuzzi Departments of Veterinary Basic Sciences, Veterinary Clinical Sciences, Department of Animal Husbandry, Division of Obstetrics and Gynaecology, Sutton Bonnington Campus, UMR Physiologie de la Reproduction et des Comportements, Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK
Departments of Veterinary Basic Sciences, Veterinary Clinical Sciences, Department of Animal Husbandry, Division of Obstetrics and Gynaecology, Sutton Bonnington Campus, UMR Physiologie de la Reproduction et des Comportements, Royal Veterinary College, Hawkshead Lane, North Mimms, Hertfordshire AL9 7TA, UK

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An experiment was conducted on 48 ewes during follicular and luteal phases of the oestrous cycle to determine the effect of a 5-day lupin grain supplementation (500 g/day) on folliculogenesis, plasma concentrations of glucose, insulin, FSH and oestradiol-17β (E2), follicular fluid concentrations of glucose, E2, androstenedione and progesterone and the levels of P450 aromatase and insulin receptor substrate 1 (IRS-1), -2 and -4 in theca and granulosa cells. Average weight did not differ between lupin-fed and control groups. The numbers of follicles were increased (P<0.05; χ2) in the lupin-fed group. The plasma concentrations of glucose (P<0.05; ANOVA) and insulin (P<0.001; ANOVA) were higher in lupin-fed ewes. The plasma concentrations of FSH were not different but those of E2 were decreased (P<0.001) in the lupin-fed group. Both the follicular fluid concentration of E2 (P<0.05) and the level of P450 aromatase in granulosa cells (P<0.05; ANOVA) were decreased in the lupin-fed group, but only during the follicular phase. The level of P450 aromatase in granulosa cells was positively correlated with the concentration of E2 in follicular fluid (r=0.820; P<0.001; ANOVA). The levels of IRS-1 and -2 in theca and granulosa cell lysates were increased in the lupin-fed group. These data suggest that insulin has a local role in the control of folliculogenesis and is likely to be a mediator of the effects of dietary energy intake on ovulation rate. We suggest that insulin acting through IRS proteins mediates the reproductive actions of insulin in the follicle and that IRS-1 and -2 are nutritionally regulated mediators of the action of insulin in the follicle.

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B. K. Campbell
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H. M. Picton
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A. S. McNeilly
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D. T. Baird
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Summary. In Exp. 1, 7 Finn–Merino ewes which had one ovary autotransplanted to a site in the neck had jugular and timed ovarian venous blood samples collected at 10-min intervals for 2 h before and 3 h after injection of 5 μg NIAMDD-oFSH-S16. In Exp. 2, 8 Finn–Merino ewes with ovarian autotransplants had jugular and timed ovarian venous blood samples collected at 15-min intervals for 2 h before and 12 h after bolus injection of 40 μg NIAMDD-oFSH-S16 and infusion of oFSH-S16 at 6 μ/min for 4 h. In Exp. 2 the follicular population of the ovary was assessed by real-time ultrasound at the beginning and end of the experimental period.

In both experiments the secretion rates of inhibin (1–3 ng/min) and oestradiol (0·5–8 ng/min) were similar to those observed during the luteal phase of the cycle in the breeding season, indicating significant follicular development in these animals. In Exp. 1 there was no change in the secretion of oestradiol or inhibin after the injection of FSH which resulted in a 25% increase (P < 0·05) in the concentration of FSH in plasma. Inhibin secretion was pulsatile but there was no difference in inhibin pulse frequency before (1·6 ± 0·2 pulses/h) or after (1·2 ± 0·5 pulses/h) injection of FSH. In Exp. 2 injection of FSH resulted in an increase (P < 0·001) in plasma concentrations of FSH in the sample taken 10 min after injection from a baseline of 1·2 ± 0·2 ng/ml to a peak of 10·6 ± 1·0 ng/ml (mean ± s.e.m.). FSH concentrations remained elevated over pretreatment values for 10 h after the beginning of the treatment. The concentration of LH in jugular venous plasma increased (P < 0·001) after the bolus injection of FSH from a baseline of 1·4 ± 0·5 ng/ml to a peak of 6·7 ± 0·6 ng/ml. The ovarian rate of inhibin secretion did not change significantly following the injection and infusion of FSH. There was no difference in inhibin pulse frequency before (0·4 ± 0·2 pulses/h) or after 0·5 ± 0·1 pulses/h) injection of FSH. The rate of oestradiol secretion by the ovary increased (P < 0·001) after the injection of the FSH preparation, an effect that can be attributed to contamination of the FSH preparation with LH. Increasing jugular venous concentrations of FSH for 10 h had no effect on the ovarian follicle population.

We conclude that the ovarian secretion of inhibin is not acutely responsive to stimulation by FSH in anoestrous ewes.

Keywords: sheep; inhibin; FSH; ovary; anoestrus

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B. K. Campbell
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R. J. Scaramuzzi
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G. Evans
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J. A. Downing
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Summary. Two experiments were undertaken to determine the hormonal response of Merino ewes to immunization against androstenedione (Fecundin®). In Exp. 1 peripheral concentrations of LH, FSH and progesterone were monitored in spontaneously cycling ewes (20 immunized and 21 controls). In Exp. 2(10 immunized and 10 controls) the same hormones were measured in ewes before and after prostaglandin (PG)-induced luteolysis and, in addition, the pattern of pulsatile LH secretion was determined during the luteal (PG + 12 days), early follicular (PG + 24 h) and late follicular (PG + 40 h) phase of the oestrous cycle. Ovulation rates were measured in both experiments.

The results of these experiments indicate that androstenedione-immune animals have elevated ovulation rates (0·6–0·7 greater than control animals; P < 0·05) associated with elevated plasma concentrations of LH and progesterone. The magnitude of the increase in plasma progesterone was correlated with androstenedione antibody titre (r = 0·6, P < 0·001). LH pulse frequency of androstenedione-immune ewes tended to be higher at all stages of the oestrous cycle, but this difference was only significant (P < 0·05) during the luteal phase.

Mean plasma concentrations of FSH did not differ significantly between immunized and control ewes at any stage of the cycle. Analysis of periodic fluctuations in FSH during the luteal phase revealed that androstenedione-immune animals had a similar number of fluctuations of a similar amplitude to those of control animals, but the nadir of these fluctuations was lower (P < 0·05) in immunized animals. A significant (P < 0·05) negative correlation existed between androstenedione antibody titre and the interval between FSH peaks (r = − 0·49) and androstenedione antibody titre and FSH nadir concentrations (r = −0·46).

It is concluded that plasma FSH concentrations are not a determinant of ovulation rate in androstenedione-immune ewes and that increased LH concentrations, or perturbation of normal intraovarian mechanisms, may be responsible for the increase in ovulation rate observed in ewes immunized against androstenedione.

Keywords: androstenedione-immunity; ovulation rate; LH; FSH; progesterone; sheep

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B. K. Campbell
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H. M. Picton
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G. E. Mann
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A. S. McNeilly
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D. T. Baird
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Summary. Treatment of ewes with steroid-free ovine follicular fluid (oFF) during the follicular phase of the oestrous cycle results in the immediate inhibition of the ovarian secretion of oestradiol, inhibin and androgens. An experiment was conducted to determine whether this effect of oFF was due to inhibin, or to direct inhibition of ovarian function by other factors in oFF.

Eight ewes in which the left ovary and vascular pedicle had been autotransplanted to a site in the neck were studied during the breeding season. Luteal regression was induced in all animals by injection of cloprostenol (100 μg i.m.; PG) on Day 10 of the luteal phase. The animals were divided into two groups (n = 4) and treated with either steroid-free oFF (oFF; 3 ml s.c.; 3·2 μg p1-26α inhibin/ml) or steroid-free oFF in which the inhibin content had been reduced by >90% (IFoFF; 3 ml s.c.; 0·3 μg p1-26α inhibin/ml) by affinity chromatography, 24 and 36 h after PG. Samples of ovarian and jugular venous blood were collected at (i) intervals of 4 h from 16 h before until 120 h after PG and (ii) intervals of 10 min from 48 to 52 h after injection of PG to investigate the pattern of pulsatile secretion of ovarian hormones. All ewes had previously been monitored during a normal PG-induced follicular phase.

Injection of oFF resulted in an increase (P < 0·05) in the concentration of inhibin in jugular venous plasma and a profound (P < 0·001) and prolonged decrease in the peripheral concentration of follicle-stimulating hormone (FSH). Injection of IFoFF had no significant effect on peripheral concentrations of inhibin or FSH in the first 24 h after treatment; thereafter inhibin concentrations fell (P < 0·01) progressively until 40 h and then increased (P < 0·01) until 72 h after treatment. In both treatment groups, however, within 24–36 h of treatment the concentration of FSH increased 5–10-fold (P < 0·001) to a peak that occurred within 48–60 h and then declined to basal concentrations within 72–84 h of treatment. The concentration of luteinizing hormone (LH) in jugular venous plasma increased in both groups after treatment (P < 0·01), although the rise after injection of oFF only started after 24 h. Thereafter, there was a progressive increase in the concentration of LH, peaks occurring 48–60 h after treatment. The preovulatory LH surge was delayed by ∼48 h in both groups of ewes, being detected at 114 ± 5 h and 110 ± 4 h after PG in ewes treated with oFF and IFoFF, respectively (P < 0·001). The effects of oFF and IFoFF on ovarian hormone secretion were similar, the secretion rate of oestradiol, androstenedione and inhibin beginning to decline within 8 h of the first injection (P < 0·001). The rate of decrease was more marked for the steroids, a mean nadir of < 1 ng/min being reached within 12–24 h of treatment whereas inhibin secretion did not reach a nadir until 36–44 h after treatment.

Androstenedione secretion began to increase (P < 0·05) within 24 h of treatment whereas inhibin and oestradiol secretion did not begin to increase significantly (P < 0·05) until 48–60 h after treatment. Generally, ovarian hormone secretion tended to increase until 72 h after treatment, after which mean secretion rates reached a plateau. In ewes treated with oFF or IFoFF the episodic secretion of oestradiol and inhibin was markedly suppressed and the amplitude of androstenedione pulses reduced, although the amplitude of LH pulses was greater than in normal untreated ewes. Injection of oFF or IFoFF caused a marked decline (P < 0·01) in the number of large follicles within 48 h of treatment and, concomitant with the rebound release of FSH, an increase (P < 0·01) in the number of small follicles/ovary. By 96 h after treatment, the number of large follicles/ewe had increased (P < 0·05) to pretreatment levels, concomitant with a decline (P < 0·05) in the number of small follicles. In individual animals, changes in gonadotrophin concentrations, ovarian hormone secretion rates and ovarian follicle populations were temporally related.

We conclude that oFF contains a factor that acts directly on the ovary to induce atresia of large preovulatory follicles and results in immediate suppression of ovarian inhibin, oestradiol and androstenedione secretion. The lack of feedback by ovarian hormones results in a rebound release of FSH, which stimulates the growth of ovarian follicles, and the re-establishment of ovarian hormone secretion and normal cyclicity.

Keywords: follicle-stimulating hormone; inhibin; oestradiol; androgen; follicular fluid; sheep

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