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Titrating Luteinizing Hormone Surge Requirements for Ovulatory Changes in Primate Follicles. I. Oocyte Maturation and Corpus Luteum Function^*

M. B. ZELINSKI-WOOTEN, S. E. LANZENDORF, D. P. WOLF, Y. ALADIN CHANDRASEKHER and R. L. STOUFFER

Division of Reproductive Biology and Behavior, Oregon Regional Primate Research Center Beaverton, Oregon 97006
Department of Physiology, Oregon Health Sciences University Portland, Oregon 97201

Address requests for reprints to: R. L. Stouffer, Ph.D., Oregon Regional Primate Research Center, 505 NW 185th Avenue, Beaverton, Oregon 97006.

The amplitude and duration of the midcycle LH surge required for ovulatory maturation of the follicle and its enclosed oocyte in primates are unknown. To titrate periovulatory LH requirements, female rhesus monkeys received human gonadotropins (FSH with/without LH) for 9 days beginning at menses to promote the development of multiple preovulatory follicles. The next day, animals (n = 4-6/group) received: 1) no ovulatory stimulus; 2) 1000 IU hCG, im; 3) one injection of 100 µg GnRH, sc (GnRH-1); 4) three injections of GnRH (GnRH- 3) at 3-h intervals (0800,1100, and 1400 h); or 5) two injections of 50 µg GnRH agonist (GnRHa), sc, 8 h apart (0800 and 1700 h) to induce ovulatory maturation. Follicles were aspirated 27 h after the hCG or initial GnRH/GnRHa injection or on days 8 and 10 in animals receiving no ovulatory stimulus. Nuclear maturity of oocytes was evaluated as a marker for reinitiation of meiosis. Estradiol and progesterone levels were determined in daily serum samples by RIA. Levels of LH(-like) bioactivity were measured at selected intervals after hCG injection and within 24 h of GnRH/GnRHa treatment. In all groups, estradiol continuously rose to similar peak levels on day 10. The hCG treatment markedly elevated circulating LH-like bioactivity for up to 3 days. In GnRH-1, bioactive LH increased to 433.1 ± 170.2 ng/mL (mean ± SEM; n = 3) within 1–2 h, but then decreased to baseline (4.9 ± 1.5 ng/mL) within 6 h. GnRH-3 and GnRHa treatment extended the interval of elevated bioactive LH to 8 and 14 h, respectively. There was no difference in the peak levels of LH(-like) bioactivity reached after hCG, GnRH, or GnRHa injection. Functional luteal phases were absent in monkeys receiving no ovulatory stimulus, whereas hCG treatment increased progesterone levels to 101 ± 9 nmol/L (n = 6) and elicited functional luteal phases of 11.8 ± 0.4 days. In contrast, only one animal in the GnRH/GnRHa groups (i.e. one GnRH- 3 monkey) displayed elevated progesterone levels in the luteal phase. Of the total cohort of oocytes aspirated from follicles, a greater (P < 0.05) proportion were classified as being in metaphase I or II of meiosis after hCG treatment (86%) compared to no ovulatory stimulus (13%), GnRH-1 (0%), GnRH-3 (43%), and GnRHa (12%). Thus, GnRH elicits a transient LH surge that can be extended by GnRH-3 or GnRHa in stimulated cycles of monkeys. However, LH exposure reminiscent of the duration of midcycle surges in rodents (4–6 h) or domestic animals (10–16 h) is insufficient to reinitiate meiotic maturation of oocytes or support the early function of the corpus luteum in primates. Ovulatory changes in primate follicles appear to require more than 14 h of the typical 48-h LH surge in the menstrual cycle.

^* This work was supported by NIH Grants HD-20869 (to R.L.S.), HD-18185 (to IVF-EE and Hormone Assay Laboratories), and RR-00163. Oregon Regional Primate Research Center publication 1796.

Present address: Department of Obstetrics and Gynecology, Department 620, Prentice Suite 1580, Northwestern Memorial Hospital, 333 East Superior Street, Chicago, Illinois 60611.

Received October 12, 1990.

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