Distinguishing the Steroidogenic Roles of Granulosa and Theca Cells of the Dominant Ovarian Follicle and Corpus Luteum*

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Abstract
In order to determine the relative contribution of granulosa cells and follicular fluid of the preovulatory follicle to ovarian and peripheral vein levels of principal steroids in the late follicular phase, as well as the importance of granulosa cells and theca cells in subsequent corpus luteum function, 32 rhesus and cynomolgus monkeys were studied. In group one (n = 10), they were bled from the femoral vein daily throughout the cycle and sera assayed for FSH, LH, estradiol, and progesterone. In addition, they were laparotomized in the late follicular phase when serum estradiol (by rapid assay) had exceeded 150 pg/ml for about 24 h. Ovarian vein blood was taken ipsilateral to the dominant follicle, followed by aspiration of follicular contents and rinsing of the antrum to remove as many granulosa cells as possible without disturbing the thecal layers. Also, blood from the contralateral ovarian vein was obtained, as well as a second collection from the ipsilateral ovarian vein 15 min after follicular aspiration; a second peripheral sample was obtained immediately thereafter. Ovarian vein asymmetry of estradiol, progesterone, and androstenedione, but not 17-OH progesterone, was noted in every case (i.e. higher steroid levels were associated with the putative dominant follicle). After follicular aspiration, high concentrations of estradiol, progesterone, and androstenedione in ovarian venous effluent fell (P < 0.001) by nearly 70% from preaspiration levels; concurrently, peripheral levels of estradiol and progesterone were reduced by about 40%. Conversely, 17-OH progesterone was unaffected. Integrated progesterone levels throughout the subsequent luteal phase, but not serum estradiol, were significantly (P < 0.001) less in the experimental monkeys (after aspirating/rinsing) compared to controls, although luteal phase length was unchanged (14.33 vs. 14.83 days). Groups two (n = 7) and three (n = 15) were employed to assess the influence of vascular trauma caused by either continuous cannulation or serial (up to six insults) venipuncture, on the concentrations of the principal ovarian steroids in ovarian vein blood. We conclude that during the follicular phase of these primates: 1) granulosa cells and follicular fluid of the periovulatory dominant follicle make the principal contribution to ovarian vein levels of estradiol, androstenedione, and progesterone; 2) aspiration of follicular contents results in subnormal progesterone secretion by the subsequent corpus luteum (P < 0.001), although estradiol secretion and luteal phase length remained near normal; and 3) traumatization of ovarian veins by continuous cannulation or repetitive venipuncture may slow venous blood flow and artificially reelevate steroid concentrations, thereby obscuring the real decline in estradiol, androstenedione, and progesterone secretion after evacuation of granulosa cells and follicular fluid from the preovulatory dominant follicle.