Summary
The growth of tertiary follicles, i.e., the proliferation of cells in the stratum granulosum and in the capillary network of the theca interna, after injection of ovulation-inducing human chorionic gonadotropin (HCG), was investigated in the rabbit by means of autoradiographic and morphometric methods.
Based on the frequency distribution of follicles with different sizes and on the labeling index (LI) of granulosa cells as a function of follicle size and of time prior to and after HCG stimulation, two groups of tertiary tollicles can be distinguished: growing (250–900 μm in diameter) and mature (>900 μm in diameter) elements. The growth of both groups is influenced by the release of gonadotropins.
After HCG stimulation, follicles belonging to the first group grow rapidly. During, and a short time after ovulation, almost all non-ruptured follicles larger than 600 μm in diameter become atretic. Within 35–50 h the ruptured and atretic mature follicles (>900 μm in diameter) are replaced by follicles out of the group of growing follicles.
From these results the following concept for regulation of follicle growth is derived: In principle, all growing follicles possess the potential to develop into mature follicles. When a sufficient number of mature follicles is generated, these mature follicles determine the number of succeeding growing follicles. Follicles that are not required for providing mature follicles become atretic as soon as they reach a diameter of 700 μm. When the majority of mature follicles is lost during ovulation (by rupture or atresia), this inhibition regulated by mature follicles is abolished, and all of the growing follicles again are capable to develop into mature follicles.
The relative amount of capillaries in the theca interna of growing and mature follicles remains constant with increasing follicle size. This means that the capillary network grows parallel to the increasing size of follicles. No differences are found between intact and atretic follicles; advanced atretic follicles were excluded from this study.
The labeling index (LI) of granulosa cells in the stratum granulosum and of endothelial cells in the theca interna, as a function of follicle size and of time after HCG stimulation, are closely correlated. A change in the LI of granulosa cells is usually followed with a certain delay by a similar alteration of the LI of endothelial cells in the theca interna. This suggests that granulosa cells have a certain regulatory function on capillary growth.
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References
Asami G (1920) Observations on the follicular atresia in the rabbit ovary. Anat Rec 18:323–343
Bagnell CA, Mills TM, Costoff A, Mahesh VB (1982) A model for the study of androgen effects on follicular atresia and ovulation. Biol Reprod 27:903–914
Bjersing L, Cajander S (1974) Ovulation and the mechanism of follicle rutpure I. Light microscopic changes in rabbit ovarian follicles prior to induced ovulation. Cell Tissue Res 149:287–300
Boucek RJ, Telegdy G, Savard K (1967) Influence of gonadotropin on histochemical properties of the rabbit ovary. Acta Endocrinol 54:295–310
Brand A, de Jong WHR (1973) Qualitative and quantitative micromorphological investigations of the tertiary follicle population during the oestrus cycle in sheep. J Reprod Fert 33:431–439
Byskov AGS (1974) Cell kinetic studies of follicular atresia in the mouse ovary. J Reprod Fert 37:277–285
Byskov AG (1978) Follicular atresia. In: Jones RE (ed) The vertebrate ovary. New York and London, Plenum Press pp 533–562
Cajander S, Janson PO, LeMaire WJ, Källfelt BJ, Holmes PV, Ahren K, Bjersing L (1984) Studies on the morphology of the isolated perfused rabbit ovary II. Ovulation in vitro after HCG-treatment in vivo. Cell Tissue Res 235:565–573
Chiras DD, Greenwald GS (1977) An autoradiographic study of longterm follicular development in the cycle hamster. Anat Rec 188:331–337
Engle ET (1927) A quantitative study of follicular atresia in the mouse. Am J Anat 39:187–203
Gillet JY (1971) La microvascularisation de l'ovaire. Gyn Obst (Paris) 70:251–272
Goodman AL, Nixon WE, Johnson DK, Hodgen GD (1977) Regulation of folliculogenesis in the cyclic rhesus monkey: Selection of the dominant follicle. Endocrinology 100:155–161
Gosden RG, Laing SC, Flurkey K, Finch CE (1983) Graafian follicle growth and replacement in anovulatory ovaries of ageing C57BL/6J mice. J Reprod Fert 69:453–462
Greenwald GS (1974) Role of follicle-stimulating hormone and luteinizing hormone in follicular development and ovulation. In: Greep RO, Aswood EB, Knobil E, Sawyer WH, Geiger SR (eds) Handbook of physiology Vol IV. American Physiological Society Washington, Baltimore Waverly Press pp 293–323
Groen-Klevant AC (1981) An autoradiographic study of follicle growth in the ovaries of cyclic rats. Acta Endocrinol 96:377–381
Harper MJK (1961) The time of ovulation in the rabbit following the injection of luteinizing hormone. J Endocrinol 22:147–152
Hay MF, Cran DG, Moor RM (1976) Structural changes occurring during atresia in sheep ovarian follicles. Cell Tissue Res 169:515–529
Hill M, White WE (1933) The growth and regression of follicles in the oestrous rabbit. J Physiol 80:174–178
Hirshfield AN, Midgley AR Jr (1978a) Morphometric analysis of follicular development in the rat. Biol Reprod 19:597–605
Hirshfield AN, Midgley AR Jr (1978b) The role of FSH in the selection of large ovarian follicles in the rat. Biol Reprod 19:606–611
Ingram DL (1962) Atresia. In: Zuckerman S, Mandl AM, Eckstein P (eds) The ovary Vol. I Academic Press New York pp 247–273
Kaur P, Guraya SS (1983) Follicular growth and kinetics during the estrous cycle, pregnancy and postpartum in the Indian mole rat (Bandicota bengalensis). Am J Anat 166:469–482
Lane ChE, Davis FR (1939) The ovary of the adult rat. Anat Rec 73:429–442
Mandl AM, Zuckerman S (1952) Cyclical changes in the number of medium and large follicles in the adult rat ovary. J Endocrinol 8:341–346
Mori H, Matsumoto K (1970) On the histogenesis of the ovarian interstitial gland in rabbits. I. Primary interstitial gland. Am J Anat 129:289–306
Mori H, Matsumoto K (1973) Development of the secondary interstitial gland in the rabbit ovary. J Anat 116:417–430
Myers HI, Young WC, Dempsey EW (1936) Graafian follicle development throughout the reproductive cycle in the guinea pig, with special reference to changes during oestrus (sexual receptivity). Anat Rec 65:381–401
Pedersen T (1970a) Determination of follicle growth rate in the ovary of the immature mouse. J Reprod Fert 21:81–93
Pedersen T (1970b) Follicle kinetics in the ovary of the cyclic mouse. Acta Endocrinol 64:304–323
Peters H, Levy E (1966) Cell dynamics of the ovarian cycle. J Reprod Fert 11:227–236
Peters H, Byskov AG, Himelstein-Braw R, Faber M (1975) Follicular growth. The basic event in the mouse and human ovary. J Reprod Fert 45:559–566
Richards JS (1980) Maturation of ovarian follicles: Actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol Rev 60:51–89
Schmidt IG (1942) Mitotic proliferation in the ovary of the normal mature guinea pig treated with colchicine. Am J Anat 71:245–270
Schwartz NB (1974) The role of FSH and LH and of their antibodies on follicle growth and on ovulation. Biol Reprod 10:236–272
Spanel-Borowski K (1981) Morphological investigations on follicular atresia in canine ovaries. Cell Tissue Res 214:155–168
Spanel-Borowski K, Trepel F, Schick P, Pilgrim Ch (1981) Aspects of cellular proliferation during follicular atresia in the dog ovary. Cell Tissue Res 219:173–183
Thielen R (1953) Blutgefäße und Follikelepithel in ihrer funktionellen Bedeutung für die Bildung des Liquor in den Ovarialfollikeln. Ann Univ Sarav Med 2:127–142
Turnbull KE, Braden AWH, Mattner PE (1977) The pattern of follicular growth and atresia in the ovine ovary. Aust J Biol Sci 30:229–241
Watzka M (1957) Weibliche Genitalorgane. Das Ovarium. In: Handbuch der mikroskopischen Anatomie des Menschen (begründet von W.v. Möllendorff, fortgeführt von W. Bargmann), Bd VII/3, Springer, Berlin Göttingen Heidelberg pp 1–178
Zerega GD di, Hodgen GD (1980) The primate ovarian cycle: Suppression of human menopausal gonadotropin-induced follicular growth in the presence of the dominant follicle. J Clin Endocrinol Metab 50:819–825
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Kranzfelder, D., Korr, H., Mestwerdt, W. et al. Follicle growth in the ovary of the rabbit after ovulation-inducing application of human chorionic gonadotropin. Cell Tissue Res. 238, 611–620 (1984). https://doi.org/10.1007/BF00219879
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DOI: https://doi.org/10.1007/BF00219879