Ovarian Follicular Development in the Untreated and
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1 Ovarian Follicular Development in the Untreated and PMSG-treated Cyclic Rat Hajime MIYAMOTO, Goro KATSUURA and Takehiko ISHIBASHI Department of Animal Science, College of Agriculture, Kyoto University, Kyoto 606 (Received February 28, 1978) Abstract The present study was designed to examine the follicular development in the untreated and PMSG-treated rats during estrous cycle by using the number of layers of granulosa cells surrounding the oocyte and the presence or absence of antrum (ra). The total numbers of follicles with 2 or more layers of granulosa cells per ovary of the untreated virgin rats were 67.7 to 87.8 and there was no cyclic variations in the number of these follicles in the estrous cycle. In all phases of the cycle of the untreated virgin rats, the proportion of follicles with 2 or 3 (stage I), 4 or 5 (stage II), 6 or 7 (stage III) and 8 or more layers (stage IV) of granulosa cells to total number of counted follicles was 38.8 to 42.7, 9.1 to 20.8, 0.4 to 2.3 and 0.7 to 1.2%, respectively. The proportion of follicles with incipient antra (stage V) and a well-formed single antrum (stage VI) was 29.9 to 43.1 and 3.4 to 6.0%, respectively. Slightly more stage VI follicles have a tendency to be present at proestrus than at other phases of the cycle, but the differences were not significant. The total number of preantral follicles with 2 or more layers of granulosa cells and antral follicles per ovary and the pattern of follicular development at each phase of estrous cycle were essentially the same for virgin and delivery experienced rats. The number of stage VI follicles per ovary was significantly greater in rats treated with 30 IU PMSG 54 or 78 hr previously than in the untreated rats. The number of atretic and degenerating (follicle without oocyte nucleus) antral follicles did not vary systematically with the phases of the estrous cycle. The treatment with 30 IU PMSG did not decrease the number of atretic and degenerating follicles. The follicle is the major ovarian component and produces the ova and the steroid hormones that regulate its own growth and stimulate the genital tracts for the transport of gametes and the implantation. The granulosa and theca cells are the major components of the follicle and the syn- hydrogenase activity than theca cells, and so efficiently convert pregnenolone to progesterone1). They also synthesize and secrete substances such as mucopolysaccharides2) and proteins3) into the follicular fluid. Recently it has been shown that the granulosa cells exert an inhibitory action on oocyte meiosis, keeping the oocyte in the dictyate stage within the follicle4,5) Various classifications have been used to describe stages of follicular developments6,7): the thickness of the theca and granulosa cells, the shape of the granulosa cells, the diameter or volume of the follicle, and the number of layers of granulosa cells surrounding the oocyte. Studies of the quantitative aspects of the ovarian follicular development in the rat have been made in
2 Follicular Development in Rat Ovary some detail, and it is generally believed that the total number of large follicles varies systematically with the estrous cycle of the rat8-10). These authors8-10) used the diameter or the volume of the follicle as the distinguishing criterion to describe the stage of follicular development. MANDL and ZUCKERMAN11) showed that the total number of follicles 2 or more layers of granulosa cells did not vary systematically with the estrous cycle. However they did not examine the quantitative aspects of follicular development during estrous cycle. This paper reports the follicular development in the untreated or PMSG-treated rat during the estrous cycle by using the number of layers of granulosa cells surrounding the oocyte and the presence or absence of antrum(ra) as the distinguishing criteria. Materials and Methods Virgin and delivery experienced rats of the Wistar strain, ranging from 4 to 9 months of age, cycle (00:00 hr was defined as the middle of dark period in the colony. Lights on at 5:30 AM and off at 6:30 PM). Vaginal smears were examined dairy for at least 3 cycles before the ovaries were removed. The untreated each 3 animals, which were virgin and delivery experienced, for phases of the estrous cycle were autopsied at 1:30 PM on days of proestrus, estrus, metestrus and diestrus, and other 3 animals were also autopsied at 8:30 PM on proestrus. Another 20 virgin rats were given a single subcutaneous injection of 30 IU PMSG at 7:30 AM on estrus. They were autopsied 6, 30, 54 or 78 hr after the PMSG injection (Text-fig. 1). Both ovaries were removed from each animal, fixed in Bouin's fluid and embedded in paraffin. The ovaries the nucleolus in the oocyte were counted in every 4th section at a magnification of 100 X. The one exception is that all antral follicles were counted whether the nucleolus was present or absent in the sections that were scanned. Only follicles that were histologically normal were counted. Follicular development was divided into 6 stages according to the classification previously used by GREENWALD12): Text-Fig. 1. Experimental schedules in relation to the estrous cycle and artificial was defined as the middle of dark period in the colony. 809
3 MIYAMOTO, KATSUURA and ISHIBASHI Explanation of Figures Sections of rat ovaries. Ovaries were fixed in Bouin's fluid, sectioned with hematoxylin and eosin. Follicular development was divided into following six stages. Fig. 1. Stage I follicle (preantral follicle with 2 to 3 layers of granulosa cells surrounding Fig. 2. Stage II follicle (preantral follicle with 4 to 5 layers of granulosa cells). Fig. 3. Stage III follicle (preantral follicle with 6 to 7 layers of granulosa cells). Fig. 4. Stage IV follicle (preantral follicle with 8 or more layers of granulosa cells). Fig. 5. Stage V follicle (follicle with early antrum formation). Fig. 6. Stage VI follicle (antral follicle characterized by large, well-formed antral cavity). 810
4 Follicular Development in Rat Ovary Stage I Preantral follicle with 2 or 3 layers of granulosa cells (Fig. 1). Stage II. Preantral follicle with 4 or 5 layers of granulosa cells (Fig. 2). Stage III. Preantral follicle with 6 or 7 layers of granulosa cells (Fig. 3). Stage IV. Preantral follicle with 8 or more layers of granulosa cells (Fig. 4). Stage V. Incipient antral follicle as evidenced by a series of isolated lacunae that are the forerunners of the antral cavity (Fig. 5). Stage VI. Antral follicle characterized by a single coalesced cavity (Fig. 6). An attempt was also made to separate normal from atretic antral follicles. Antral follicles were considered atretic when pyknotic nuclei formed a layer on the inner boundary of granulosa cells13). Antral follicles whose oocyte nuclei were no longer visible were diagnosed as degenerat- ovary and the average were based on 6 ovaries from 3 animals for untreated each group and 10 ovaries from 5 animals for group treated with PMSG. The results were analysed by means of t-tests. To examine the ovulation by the treatment of gonadotrophins, another series of rats were injected subcutaneously with 30 IU PMSG at 7:30 AM on estrus. Animals were autopsied 96 hr after PMSG treatment and a number of ovulated ova was counted. Some of PMSG-treated rats were followed by 30 IU HCG 52 hr later and autopsied 24 hr after HCG treatment. Results When mature rats were given 30 IU PMSG at 7:30 AM on estrus, none of 6 rats ovulated 96 hr after PMSG injection. When 5 rats were given 30 IU PMSG at 7:30 AM on estrus followed by 30 IU HCG 52 hr later and killed 24 hr after HCG injection, all rats ovulated and a PMSG-treated rats and untreated ones. The total numbers of follicles with 2 or more layers of granulosa cells per ovary of the untreated virgin rats were 67.7 to 87.8 (Table 1), and there was no cyclic variations in the number of these follicles during the estrous cycle. In all phases of the cycle of the untreated virgin rats, 38.8 to 42.7% of the total number of counted follicles were those with 2 or 3 layers of granulosa cells (stage I), and 9.1 to 20.8% were follicles with 4 or 5 layers (stage II). From 29.9 to 43.1% of the total follicle counted were the early antral follicles (stage V) and 3.4 to 6.0% were antral follicles with a well-formed single cavity (stage VI). The number of stage VI follicles at proestrus diestrus was 4.0, 5, 2, 2.5, 2. 5 and 4.2, respectively. (1:30 PM and 8:30 PM), estrus, metestrus and The greater number of stage VI follicles, therefore, had a tendency to occur at proestrus but differences were not significant. The total number of follicles per ovary and the pattern of follicular development at each phase of estrous cycle were essentially the same for virgin and delivery experienced The number of stage VI follicles per ovary at 6, 30, 54 and 78 hr after the injection of PMSG at 7:30 AM of estrus was 0.6, 4.8, 12.4 and 9.1, respectively. rats. The number of stage VI follicles was significantly greater (P <0.05) in animals treated with PMSG 54 or 78 hr previously than in the untreated animals. Following a single injection of 30 IU PMSG the number of stages I, II and V follicles was likely to increase in comparison with that of untreated animals although no significant differences were observed under the present experimental conditions.
5 MIYAMOTO, KATSVVRA and ISHIBASHI Table 1. Number of follicles per ovary of rats killed at 4 phases of the estrous cycle or killed at various hr after injection of 30 IU PMSG at 7:30 AM on estrus. *** For definition of stages see Materials and Methods section. Table 2 shows the number of atretic and degenerating antral follicles at different phases of the estrous cycle and the effects of doses of PMSG on the number of these follicles are also summarized. The number of atretic and degenerating antral follicles did not vary systematically with the phases of the estrous cycle. The treatment with 30 IU PMSG showed an increasing tendency in the number of these follicles but the differences were not significant. Discussion Various classification have been used to define stages of follicular development in ovary and each classification has some merits and demerits. The classification by the number of layers of granulosa cells and the presence or absence of antrum(ra) has following characteristics: (1) Granulosa cells play an important role in synthesizing and secreting substances such as steroid hormones1) and proteins3). It is, therefore, reasonable to use the number of layers as the criterion. To obtain a more precise estimate it is necessary to know the number of granulosa cells, but counting the number of cells is too complicated. (2) It is easy and precise to count the number 812
6 Follicular Development in Rat Ovary Table 2. Number of atretic and degenerating follicles with antrum(ra) per ovary of rats killed at 4 phases of the estrous cycle or killed at various hr after injection of 30 IU PMSG at 7:30 AM on estrus. * 00 : 00 hr was defined as the middle of dark period in the colony. of layers. To contrary the follicle diameter is taken as the mean of the maximun dimension of the follicle and the maximum dimension at right angles to it. To obtain a more precise estimate of the mean diameter of the follicle, it is necessary to measure the third diameter but it is impossible9). (3) There are some differences in the number of layers of granulosa cells even in the same dimension of the follicle. This is one of disadvantages. Using the diameter or the volume of the follicles as the distinguishing criterion, it was shown that the total number of large follicles varies according to the phases of the estrous cycle of the rat8.9). In the present study we used the number of layers of granulosa cells surrounding the oocyte and the presence or absence of antrum(ra) as the criteria, and showed that the number of antral follicles characterized by large, well-formed antral cavity (stage VI) has a tendency to vary with the phase of the cycle. This result may confirm the earlier report8,9) that the number of large follicle varies with the phases of the cycle. Contrary to results8) that the number of medium and large follicles (i. e. follicles with a diam- the numbers of preantral (stages I-IV) and incipient antral (stage V) follicles do not vary according to the phases of the cycle, although.the number of stage VI follicles varies cyclically. The present results may, therefore, support the finding of MANDL and ZUCKERMAN9). The number of stage VI follicles increased during proestrus and decreased at estrus. With the recent development of radioimmunoassay method, it has been shown that the concentrations of serum FSH and LH during the estrous cycle of the rat are elevated on the late afternoon of 813
7 MIYAMOTO, XATSUURA and ISHIBASHI proestrus14.15). The elevation in the concentrations of FSH and LH during estrous cycle coincides with the increase in number of stage VI follicles. Slightly more the early antral follicles (stage V) were also likely to be present at proestrus (1:30 PM) than at other phases of the cycle. Ovulation in the rat conceivably results from the direct action of LH or FSH alone, or the interaction of these gonadotrophins on the mature follicles16-19). FSH and LH also may stimulate the growth of the next crop of rat follicles, destined to ovulate approximately 5 days later as described in the hamster12). When immature rats were treated with 50 IU PMSG, the number of follicles with 2 or more layers of granulosa cells did not increase, but after 5 days' treatment with 10 IU PMSG the number of those follicles increased20). Hamster follicles with 1 layer of granulosa cells were stimulated in the PMSG-treated ovaries as a number of follicles with 1 to 4 layers of cells21). The total number of antral follicles and preantral ones with 2 or more cell layers was likely to be greater in the PMSG-treated hamster12). ISHIBASHI and ARATO22) showed that the treatment of of medium-sized and small follicles. In the present study the number of stage VI follicles at 54 and 78 hr after treatment with PMSG increased in comparison with that of untreated rats. The total number of preantral follicles with 2 or more cell layers and antral follicles was likely to be greater in rats treated with PMSG than in the controls. PMSG may therefore increase the number of antral and preantral follicles with 2 or more granulosa cell layers. None of 6 rats ovulated by the injection of PMSG alone. These results is similar to those of the earlier reports23.24). ISHIBASHI and AOKI23) reported that after mature rats were treated with 30 or 50 IU PMSG alone the number of ovulation was 3 out of 10 and 1 out of 10 rats, and the number of ovulated ova was 2.0 and 1.0, respectively. No ovulation was also observed in the immature mouse after treatment of PMSG alone25) but ovulation occurred in PMSG-treated mature mouse26). It was suggested that in PMSG-treated PMSG treatment is insufficient both for a normal number of ovulations and for the superovulation23,24). rats, the amount of endogenous LH released by Contrary to the result that superovulation can be induced in Wistar-Imamichi rats by the treatment of gonadotrophins23.27,26) no superovulation can be induced in the present experiment. These different results may be related to the differences of time of treatment with PMSG in estrous cycle and strain of rats. MANDL and ZUCKERMAN11) reported that the rate of atresia in rat follicle with 2 or more layers of granulosa cells does not vary systematically with the phase of estrous cycle. On the contrary ceived PMSG for 5 days had fewer atretic follicles containing a dividing oocyte than their litter-mate controls, and it was shown that PMSG hasten the disappearance of atretic oocytes from the ovary20). In contrast, when 22-day-old mice were injected with PMSG 24 hr before autopsy, the number of atretic large follicles was lower than that of controls29). We showed that the number of atretic and degenerating antral follicles (follicle without oocyte nucleus) do not vary systematically with the phase of rat cycle, and PMSG treatment does not decrease the number of these follicles under the present experimental conditions. 814
8 Follicular Development in Rat Ovary References 1) EDWARDS, R.G., J. Reprod. Fert., 37: ) ZACHARIAE, F., Acta Endocr., 26: ) BJORKMAN, N., Acta Anat., 51: , 4) FOOTE, W. D. and C. THIBAULT, Ann. Biol. Anim. Bioch. Biophys., 9: ) TSAFRIRI, A. and C. P. CHANNING, Endocrinology, 96: ) MAULEON, P., in Reproduction in Domestic Animals. 2nd ed. (COLE, H. H. and P. T. Cupes, eds.) Academic Press. New York ) PEDERSEN, T. and H. PETERS, J. Reprod. Fert., 17: ) LANE, C. E. and F. R. DAVIS, Anat. Rec., 73: ) MANDL, A. M. and S. ZUCKERMAN, J. Endocr., 8: ) BOLING, J. L., R. J. BLANDAU, A. L. SODERWALL and W. C. YOUNG, Anat. Rec., 79: ) MANDL, A. M. and S. ZUCKERMAN, J. Endocr., 6: ) GREEnWALD, G. S., Anat. Rec., 178: ) HOAGE, T. R. and I. L. CAMERON, Anat. Rec., 184: ) MONROE, S. E., R. W. REBAR, V. L. GAY and A. R. MIDGLEY, JR., Endocrinology, 85: ) DAANE, T. A. and A. F. PARLOW, Endocrinology, 88: ) CALIGARIS, L., J. J. ASTRADA and S. TALEISNIK, Endocrinology, 81: ) LOSTROH, A. J. and R. E. JOHNSON, Endocrinology, 79: ) RENNELS, E. G. and W. K. O'STEEN, Endocrinology, 80: ) MCCLINTOCK, J. A. and N. B. SCHWARTZ, Endocrinology, 83: ) INGRAM, D. L., J. Endocr., 19: ) GURAYA, S. S. and G. S. GREENWALD, Am. J. Anat., 116: ) ISHIBASHI, I. and H. ARATO, Jap. J. Zootech. Sci. (Suppl. ), 48: ) ISHIBASHI, I. and H. AOKI, Jap. J. Anim. Reprod., 21: ) WELSCHEN, R., J. Endocr., 48: lxv ) SASAMOTO, S., Bull. Fac. Agr. Tokyo Univ. Agr. Tech., 13: ) SASAMOTO, S., Jap. J. Anim. Reprod., 7: ) ISHIBASHI, I., Jap. J. Anim. Reprod., 12: ) ISHIBASHI, I. and H. AOKI, Jap. J. Anim. Reprod., 22: ) PETERS, H., A. G. BYSKOV, R. HIMELSTEIN-BRAW and M. FABER, J. Reprod. Fert., 45:
9 MIYAMOTO, KATSUURA and IsffiBASHI
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