.Secretion of Granules by the Luteal Cells of the Sheep and the Goat during the Estrous Cycle and Pregnancy T. GEMMELL,' B. D. STACY AND C. D. NANCARROW Division ofAnimaZProduction, C.S.I.R.O., The Ian Clunks Ross Animal Research Laboratory, P.0.Box 239, Blacktown, iV S. U? 2148, Australia

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ABSTRACT The fine structure of luteal tissue from sheep and goats a t the mid-stage of the estrous cycle and during pregnancy was examined. A t the midstage of the estrous cycle, when the corpus luteum of both species is secreting progesterone, the ultrastructure of the luteal cells is similar in that granule secretion is prevalent. In late pregnancy, the corpus luteum of the sheep produces very little progesterone and there is an absence of granule secretion. In the pregnant goat, the production of progesterone from the corpus luteum is high and there is plentiful evidence of granule formation and secretion. The corpus luteum of the sheep continues to secrete progesterone until about the one hundred and twentieth day of pregnancy (Edgar and Ronaldson, '58; Lindner, Sass and Morris, '641, but subsequent study by Linzell and Heap ('68)demonstrated that placental secretion of progesterone may be up to five times greater than that from the corpus luteum in late pregnancy. These results are supported by the finding that ewes can be ovariectomised after the 50th day without interruption to pregnancy (Casida and Warwick, '45; Denamur and Martinet, '55). The concentration of progesterone in the peripheral plasma during the first 50 days of pregnancy is not significantly higher than that during the luteal phase in cycling non-pregnant ewes and between 50 and 120 days the plasma progesterone concentration increased steadily to values two to five times that found in early pregnancy (Bassett et al., '69). Quite a different sequence of events takes place in the goat; progesterone is mainly produced by the ovaries throughout pregnancy, without the placenta making an appreciable contribution (Linzell and Heap, '68). Bilateral ovariectomy a t any stage of pregnancy causes peripheral progesterone concentration to fall and the animals subsequently abort (Thorburn and Schneider, '72).Administration of a luteolytic dose of the prostaglandin analogue (ICI 79939) will readily abort goats a t all stages of pregnancy (Holst and Nancarrow, '75). The secretion of progesterone by the ovaANAT.

REC., 189: 161-168.

ry of the goat is essential for the maintenance of pregnancy. Recently, evidence has been reported that the luteal cells in the ovary of the cycling sheep secrete progesterone in the form of granules (Gemmell et al., '74). It was therefore of interest to compare corpora lutea of pregnancy in sheep and goats to see whether differences in the functional state of the gland might be reflected in morphological changes associated with the mechanism of progesterone secretion. MATERIALS AND METHODS

Luteal tissue from two adult sheep and from two adult goats a t the mid-stage of the estrous cycle was examined. The animals were kept a t pasture and estrus was detected by testing the animals daily with a vasectomised male. Luteal tissue was also taken from two pregnant sheep (125 days gestation), and from two pregnant goats (112 days and 140 days). The ovaries were fixed in situ by perfusion of the ovarian artery with a paraformaldehyde-glutaraldehyde solution (Gemmell et al., '74). Strips of luteal tissue were subsequently post-fixed in buffered osmium tetroxide, dehydrated and embedded in Araldite. The thin sections were sequentially stained with uranyl acetate and lead citrate prior to examReceived Oct 18, '76 Accepted Mar 31, '77 ' Present address Department of Anatomy, University of Queens land, St Lucia, Queensland 4067

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ination in a Hitachi HU-11C electron microscope. In some experiments, blood samples for the determination of progesterone (Thorburn and Schneider, '72) were taken from the jugular vein and from the ovarian vein just before perfusion of the ovary with fixative.

DISCUSSION

The present observations show that the fine structure of the luteal cell varies significantly depending on whether or not the corpus luteum is secreting progesterone. Goats and sheep have a broadly similar pattern of progesterone secretion during the estrous cycle (Thorburn and Schneider, '72; Throburn et al., RESULTS '691, and in line with this the ultrastructure The predominant cell type within the cor- of the actively secreting luteal cell is similar pus luteum of the sheep and the goat is the in cycling animals of both species. Despite large polyhedral luteal cell, about 30p m in di- these resemblances, the two species show deameter, and it is to this type that the follow- cisive differences in late pregnancy when the ing descriptions refer. corpus luteum in the sheep produces very litThe ultrastructure of the luteal cells of the tle progesterone whilst in the goat the luteal sheep throughout the estrous cycle has been secretion is high and obligatory if abortion is described previously (Gemmell et al., '74). At to be averted. The differences are exemplified the mid-stage of the estrous cycle of the by the concentrations of progesterone in sheep, days 9 to 11, maximum secretion of ovarian venous blood, the values (700 and 190 small densely staining granules 0.2 p m in di- ng/ml) in the two sheep were very much lowameter, from the luteal cell is observed (fig. er than the single value (2,500 ng/ml) in the 1). The progesterone concentration of the pe- goat a t 140 days of gestation. The ultraripheral plasma is 4 to 5 ng/ml and of the structure of the corpus luteum of pregnancy ovarian vein plasma 2,000 to 3,000 ng/ml. shows species-specific differences compatible The structure of the luteal cell of the goat with the differences in endocrine status. The at day 12 of the estrous cycle is similar to that low level of secretory activity in the ovint corobserved in the sheep a t days 9 to 11, secretion pus luteum in late pregnancy is reflected by a of densely staining granules is a characteris- paucity of densely staining granules in the tic feature a t this stage (fig. 2). The concen- luteal cell and an absence of any sign of grantration of progesterone in the peripheral ule secretion. A very different picture is seen plasma is 4-5 ng/ml. No samples of ovarian in the actively secreting corpus luteum in the vein plasma were collected. pregnant goat; the mitochondria in the luteal In the luteal cells from the pregnant sheep cells are typical of steroid secreting cells, and, (125 days) there were a few densely staining as in the luteal phase of the estrous cycle, granules within the cytoplasm but no obvious there is plentiful evidence of granule formasigns of granule secretion could be detected tion and secretion. (fig. 3). The cells appeared shrunken, mitoLITERATURE CITED chondria were in close proximity to each other Bassett, J. M., J. Oxborrow, I. D. Smith and G. D. Thorburn and the cristae did not have the characteris1969 The concentration of progesterone in the periphtics of mitochondria in actively secreting eral plasma of t h e pregnant ewe. J. Endocr., 45: 449-457. steroid cells (compare figs. 1, 3). The concen- Casida, L. E., and E. J., Warwick 1945 The necessity of the corpus luteum for maintenance of pregnancy in t h e ewe. tration of progesterone in the peripheral J. Anim. Sci.. 4: 34.36. plasma of the two ewes was 26 ng/ml and 9.8 Denamur, R., a n d J. M a r t i n e t 1955 Effets d e ng/ml, and in ovarian venous plasma i t was I'ovariectomie chez la brebis pendant la gestation. C. R. S k n c Soe. Biol., 149: 2105-2107. 700 ng/ml and 190 ng/ml respectively. Abundant evidence of granule secretion Edgar, D.G., and J. W. Ronaldson 1958 Blood levels of progesterone in the ewe. J. Endocr., 16; 378-384. was seen in luteal cells from two pregnant Gemmell, R. T., B. D. Stacy and G. D. Thorburn 1974 U1goats (fig. 4). No blood samples were obtained trastructural study of secretory granules in the corpus luteum of the sheep during the estrous cycle. Biol. from the animal a t 112 days after conception; Reprod., 11: 447-462. blood samples from the other animal (140 P. J., and C. D. Nancarrow 1975 Intramuscular days gestation) had a progesterone concentra- Holst, administration of a prostaglandin analogue during pregtion of 3.8 ng/ml in the peripheral plasma and nancy in the goat. J. Reprod. Fert., 43: 404-405. 2,500 ng/ml in plasma from the ovarian vein. Lindner, H. R., M. B. Sass and B. Morris 1964 Steroids in

LUTEAL CELL GRANULES ovarian lymph and blood of conscious ewes. J. Endocr., 30: 361-376. Linzell, J . L., and R. B. Heap 1968 A comparison of progesterone metabolism in the pregnant sheep and goat; sources of production and a n estimation of uptake by some target organs. J. Endocr., 42; 433-438.

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Thorburn, G. D., J. M.Bassett and I. D. Smith 1969 Progesterone concentration in the peripheral plasma of sheep during the oestrous cycle. J. Endocr., 45: 459-469. Thorburn, G.D.,and W. Schneider 1972 The progesterone concentration in the plasma of t h e goat during the oestrous cycle and pregnancy. J. Endocr., 52: 23-36.

PLATE 1 EXPLANATION O F FIGURES

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1

P a r t of a 1utt:al cell from a sheep a t day 10 of t h e estrous cycle. Note t h e secretion of granules (-1. X 19,000.

2

Secretion of granules x 19,000.

1-1

from a goat luteal cell at day 12 of t h e estrous cycle.

LUTEAI, CELL GKANULES R. T. Gemmell. B. D. Stacy and C. D Nancarrow

F’I.ATF: 1

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PLATE 2 EXPLANATION OF FIGURES

3 Part of sheep luteal cell, at 125 days of pregnancy; a few granules are seen within the cell but there is no evidence of granule secretion. X 19,000.

4 Secretion of granules (-1 X 19,000.

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by a luteal cell in a goat at day 140 of pregnancy.

LUTEAL CELL GRANU1,ES H. T Gernmell. B D Stacy and C D Nnncarrow

PLATE 2

Secretion of granules by the luteal cells of the sheep and the goat during the estrous cycle and pregnancy.

Secretion of Granules by the Luteal Cells of the Sheep and the Goat during the Estrous Cycle and Pregnancy T. GEMMELL,' B. D. STACY AND C. D. NANCARR...
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