Differential response to gonadotropins and prostaglandin E2 in ovarian tissue during prenatal and postnatal development in cattle

Abstract

In cattle, growing follicles are present in fetal ovaries during the last part of gestation. This study examines the extent of changes in basal and hormone-stimulated adenylyl cyclase (AC) activity in ovaries of the bovine fetus when the first follicles begin to grow. The first growing follicles appeared in fetal ovaries around Day 180 and consisted mainly of primary and secondary follicles; few antral follicles were present before Day 220 of gestation. Basal AC activity in ovarian membranes increased simultaneously with the beginning of follicle growth in the fetus (5.8 ± 0.9 vs. 9.3 ± 1.3 pmol cAMP/mg protein/min at 130-180 and 180-210 days of gestation, respectively p < 0.05). During the same time period, there was a significant increase in both the absolute (16.1 ± 1.2 to 39.9 ± 1.4 pmol cAMP/mg protein/min) and the relative (2.8 ± 0.1 to 4.3 ± 0.3 times the basal level, p < 0.05) effects of guanosine triphosphate (GTP). After birth, basal and GTP-stimulated AC activities (pmol cAMP/mg protein/min) increased markedly in ovarian membranes of 1-wk-old calves and then decreased with age; the lowest levels were measured in mature cyclic cows. However, the relative effect of GTP (times the basal level) did not show this age-related variation. Prostaglandin E2 (PGE2) stimulation of AC in ovarian membranes from fetuses was high even on Day 120 (2.1 ± 0.3 times the control level). This effect of PGE2 increased (p < 0.05) between 130 and 180 days of gestation to nearly 3-fold and decreased in postnatal calves to a constant level, approximately twice the control level. FSH and LH stimulations of AC were undetectable in fetal ovarian membranes even after the beginning of follicle growth. However, the effect of FSH increased after birth from 1.2 ± 0.1 to 1.5 ± 0.09 times the control level after 1 and 8 wk, respectively, remaining constant thereafter. In granulosa cell membranes, LH responsiveness was lower in 1-wk-old calves compared to older animals (p < 0.05). The effect of FSH was also lower in 1-wk-old calves than in mature cyclic cows (p < 0.05). The maximum response to, but not the ED50 for FSH stimulation in granulosa cell membranes was higher in mature cyclic cows than in 1-wk-old calves (5.3 ± 0.3 vs. 3.0 ± 0.2 times the control level, respectively, p < 0.05). Collectively, these results suggest that (1) PGE2 modulates ovarian AC activity in the bovine fetus, though these effects are not necessarily associated with follicular growth; (2) some changes occur in the transduction capacity of the AC system when follicles begin to grow in the fetus; and (3) FSH responsiveness develops rapidly in ovarian tissues after birth, but the capacity of granulosa cells to respond to FSH is lower in 1-wk-old calves than in mature cyclic cows.