Maturation of the Follicular Microenvironment

  • Cecilia L. Schmidt


Over the past decade, the orchestration of the menstrual cycle, formerly attributed to the hypothalamic-pituitary axis, has been properly ascribed to the dominant follicle. It is the microenvironment of the follicle destined to ovulate that determines the circulating hormonal milieu and impinges upon the fate of the selected oocyte. The purpose of this chapter is to survey the factors basic to follicular development and achievement of dominance in the spontaneous menstrual cycle. Understanding these events is mandatory to those who attempt hormonal manipulation of the ovarian cycle to ensure oocyte retrieval for in vitro fertilization.


Granulosa Cell Corpus Luteum Follicular Fluid Zona Pellucida Antral Follicle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Amsterdam, A., Lindner, H.R., and Groschei-Stewart, U., 1977, Localization of actin and myosin in the rat oocyte and follicular wall by immunofluorescence, Anat. Rec., 187:311.PubMedCrossRefGoogle Scholar
  2. Baca, M. and Zamboni, L., 1967, The fine structure of human follicular oocytes, J. Ultrastruct. Res., 19:354.PubMedCrossRefGoogle Scholar
  3. Baker, T.G., 1972, Oogenesis and ovulation, in: “Reproduction in Mammals. I. Germ Cells and Fertilization,” C.R. Austin and R.V. Short, eds., Cambridge University Press, Oxford.Google Scholar
  4. Baker, T.G., and Franchi, L.L., 1967, The fine structure of oogonia and oocytes in human ovaries, J. Cell. Sci., 2:213.PubMedGoogle Scholar
  5. Balmaceda, J.P., Asch, R.H., Fernandez, E.O., Valenzuela, G., Eddy, C.A., and Pauerstein, C.J., 1979, Prostaglandin production by rhesus monkey corpora lutea in vitro, Fertil. Steril., 31:214.PubMedGoogle Scholar
  6. Balmaceda, J., Valenzuela, G., Eddy, C.A., and Asch, R.H., 1980, Prostaglandin production by rhesus monkey corpora lutea in vitro: effects of estrogen administration, Int. J. Gynaecol. Obstet., 18:15.PubMedGoogle Scholar
  7. Balmaceda, J. P., Valenzuela, G., Eddy, C.A., and Asch, R.H., 1981, Effects of hCG on prostaglandin synthesis and function of corpus luteum, Obstet. Gynecol., 57:505.PubMedGoogle Scholar
  8. Brailly, S., Gougeon, A., Milgrom, E., Bomsel-Helmreich, O., and Papiernik, E., 1981, Androgens and progestins in the human ovarian follicle: differences in the evolution of preovulatory, healthy nonovulatory, and atretic follicles, J. Clin. Endocrinol. Metab., 53:128.PubMedCrossRefGoogle Scholar
  9. Channing, C.P., Anderson, L.D., and Batta, S.K., 1978, Follicular growth and development, Clin. Obstet. Gynaecol., 5:375.PubMedGoogle Scholar
  10. Channing, C.P., Anderson, L.D., Hoover, D.J., Kolena, J., Osteen, K.G., Pomerantz, S.H., and Tanabe, 1982, The role of nonsteroidal regulators in control of oocyte and follicular maturation, Recent Prog. Horm. Res., 38:331.PubMedGoogle Scholar
  11. Chiquoine, A.D., 1960, The development of the zona pellucida ofthe mammalian ovum, Am. J. Anat., 106:149.PubMedCrossRefGoogle Scholar
  12. Crowley, W.F., and McArthur, J.W., 1980, Stimulation of the normal menstrual cycle in Kallman’s syndrome by pulsatile administration of luteinizing hormone-releasing hormone (LHRH), J. Clin. Endocrinol. Metab., 51:173.PubMedCrossRefGoogle Scholar
  13. Csapo, A.I., Pulkkinen, M.O., and Wiest, W.G., 1973, Effects of luteectomy and progesterone replacement therapy in early pregnant patients, Am. J. Obstet. Gynecol., 115:759.PubMedGoogle Scholar
  14. diZerega, G.S., and Hodgen, G.D., 1982, The interovarian progesterone gradient: a spatial and temporal regulator of folliculogenesis in the primate ovarian cycle, J. Clin. Endocrinol. Metab., 54:495.PubMedCrossRefGoogle Scholar
  15. diZerega, G.S., Lynch, A., and Hodgen, G.D., 1981, Initiation of asymmetrical ovarian estradiol secretion in the primateovarian cycle after luteectomy, Endocrinol., 108:1233.CrossRefGoogle Scholar
  16. diZerega, G.S., Marut, E.L., Turner, C.K., and Hodgen, G.D., 1980a, Asymmetrical ovarian function during recruitment and selection of the dominant follicle in the menstrual cycle of the rhesus monkey, J. Clin. Endocrinol. Metab., 51:698.PubMedCrossRefGoogle Scholar
  17. diZerega, G.S., Nixon, W.E., and Hodgen, G.D., 1980b, Intercycle serum FSH elevations: significance in recruitment and selection of the dominant follicle and assessment of corpus luteum normalcy, J. Clin. Endocrinol. Metab., 50:1046.CrossRefGoogle Scholar
  18. Edman, C.D., 1983, Testicular regression syndrome, Semin. Re prod. Endocrinol., 1:129.CrossRefGoogle Scholar
  19. Edwards, R.G., and Steptoe, P.C., 1975, Induction of follicular growth, ovulation and luteinization in the human ovary, J. Reprod. Fert., Suppl. 22:121.Google Scholar
  20. Edwards, R.G., Steptoe, P.C., Fowler, R.E., and Baillie, J., 1980, Observations on preovulatory human ovarian follicles and their aspirates, Br. J. Obstet. Gynaecol., 87:769.PubMedCrossRefGoogle Scholar
  21. Eppig, J.J., 1979, FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles, Nature, London, 281:483.CrossRefGoogle Scholar
  22. Eppig, J.J., 1980, Role of serum in FSH stimulated cumulus expansion by mouse oocyte-cumulus cell complexes in vitro, Biol. Reprod., 22:629.PubMedGoogle Scholar
  23. Erickson, G.F., Hsueh, A.J.W., Quigley, M.E., Rebar, R.W., and Yen, S.S.C., 1979, Functional studies of aromatase activity in human granulosa cells from normal and polycystic ovaries, J Clin. Endocrinol. Metab., 49:514.PubMedCrossRefGoogle Scholar
  24. Garcia, J.E., Jones, G.S., and Wright, G.L., 1981, Prediction of the time of ovulation, Fertil. Steril., 36:308.PubMedGoogle Scholar
  25. Goldsmith, L.T., Grob, H.S., Scherer, K.J., Surve, A., Steinetz, B.G., and Weiss, G., 1981, Placental control of ovarian immunoreactive relaxin secretion in the pregnant rat, Endocrinol., 109:548.CrossRefGoogle Scholar
  26. Goodman, A.L., and Hodgen, G.D., 1977, Systemic versus intraovarian progesterone replacement after luteectomy in rhesus monkeys: differential patterns of gonadotropins and follicle growth, J. Clin. Endocrinol. Metab., 45:837.PubMedCrossRefGoogle Scholar
  27. Goodman, A.L., and Hodgen, G.D., 1979, Between-ovary interaction in the regulation of follicle growth, corpus luteum function, and gonadotropin secretion in the primate ovarian cycle. II. Effects of luteectomy and hemiovariectomy during the luteal phase in cynomolgus monkeys, Endocrinol., 104:1310.CrossRefGoogle Scholar
  28. Grady, R.R., Savoy-Moore, R.T., and Schwartz, N.B., 1981, Selective suppression of follicle-stimulating hormone by folliculostatin: a proposed ovarian hormone, in: “Bioregulators of Reproduction,” G. Jagiello and H.J. Vogel, eds., Academic Press, Inc., New York.Google Scholar
  29. Haseltine, F.P., 1983, Defects in H-Y antigen expression and related gonadal failure, Semin. Reprod. Endocrinol., 1:113.CrossRefGoogle Scholar
  30. Himelstein-Braw, R., Byskov, A.G., Peters, H., and Faber, M., 1976, Follicular atresia in the infant human ovary, J. Reprod. Fertil., 46:55.PubMedCrossRefGoogle Scholar
  31. Hodgen, G.D., Goodman, A.L., Stouffer, R.L., Williams, R.F., diZerega, G.S., Kreitman, O.L., Marut, E.L., and Schenken, R.S., 1983, Selection and maturation of the dominant follicle and its ovum in the menstrual cycle, in: “Fertilization of the Human Egg In Vitro,” H.M. Beier and H.R. Lindner, eds., Springer-Verlag, Berlin.Google Scholar
  32. Ingram, D.L., 1962, Atresia, in: “The Ovary,” S. Zuckerman, A.M. Mandi and P. Eckstein, eds., Academic Press, London.Google Scholar
  33. Jewelwicz, R., Dyrenfurth, I., Warren, M., Joshi, U., and Vande Wiele, R.L., 1973, Factors involved in the maintenance and regression of the corpus luteum of women, in: “Le Corps jaune. Rapporteurs generaux,” R. Denamur, ed., Masson, Paris.Google Scholar
  34. Karsch, F.J., and Sutton, G.P., 1976, An intra-ovarian site for the luteolytic action of estrogen in the rhesus monkey, Endocrinol., 98:553.CrossRefGoogle Scholar
  35. Knobil, E., 1980, The neuroendocrine control of the menstrual cycle, Recent Prog. Horm. Res., 36:53.PubMedGoogle Scholar
  36. LeMaire, W.J., Leidner, R., and Marsh, J.M., 1975, Pre and post ovulatory changes in the concentration of prostaglandins in rat Graafian follicles, Prostaglandins, 9:221.PubMedCrossRefGoogle Scholar
  37. Leyendecker, G., Wildt, L., and Hansmann, M., 1980, Pregnancies following chronic intermittent (pulsatile) administration of Gn-RH by means of a portable pump (“Zyklomat”)-a new approach to the treatment of infertility in hypothalamic amenorrhea, JClin. Endocrinol. Metab., 51:1214.PubMedCrossRefGoogle Scholar
  38. Lintern-Moore, S., Peters, H., Moore, G.P.M., and Faber, M., 1974, Follicular development in the infant human ovary, J. Reprod. Fertil., 39:53.PubMedCrossRefGoogle Scholar
  39. Lunenfeld, B.I., Ben-Aderet, N., Michael, R.B., Griistein, S., Kraiem, Z., Potashek, G., Shalit, A., Tikotzky, D., and Rofehh, C., 1977, Correlation of hormonal profile and ovarian morphological features during the preovulatory peroid in the human, in: “Endocrinology of the Ovary,” R. Scholler, ed., Editions Sepe, Paris.Google Scholar
  40. McNatty, K.P., Baird, D.T., Bolton, A., Chambers, P., Corker, C.S., and McLean, H., 1976, Concentrations of oestrogens and androgens in human ovarian venous plasma and follicular fluid throughout the menstrual cycle, J. Endocrinol., 71:77.PubMedCrossRefGoogle Scholar
  41. McNatty, K.P., Hillier, S.G., van der Boogaard, A.M.J., Trimbos-Kemper, T.C.M., Reichert, L.E., and van Hall, E.V., 1983, Follicular development during luteal phase of the human menstrual cycle, J. Clin. Endocrinol. Metab., 56:1022.PubMedCrossRefGoogle Scholar
  42. McNatty, K.P., Makris, A., DeGrazia, C., Osathanondh, R., and Ryan, K.J., 1979, The production of progesterone, androgens, and estrogens by granulosa cells, thecal tissue, and stromal tissue from human ovaries in vitro, J. Clin. Endocrinol. Metab., 49:687.PubMedCrossRefGoogle Scholar
  43. McNatty, K.P., Sawers, R.S., and McNeilly, A.S., 1974, A possible role for prolactin in control of steroid secretion by the human Graafian follicle, Nature, London, 250:653.CrossRefGoogle Scholar
  44. Marut, E.L., Williams, R.F., Cowan, B.D., Lynch, A., Lerner, S.P., and Hodgen, G.D., 1981, Pulsatile pituitary gonadotropin secretion during maturation of the dominant follicle in monkeys: estrogen positive feedback enhances the biological activity of LH, Endocrinol., 109:2270.CrossRefGoogle Scholar
  45. Mossman, H.W., and Duke, K.L., 1973, “Comparative Morphology of the Mammalian Ovary,” University of Wisconsin Press, Madison.Google Scholar
  46. Nakano, R., Yamoto, M., and Iwasaki, M., 1981, Effects of oestrogen and prostaglandin F2 on luteinizing hormone receptors in human corpora lutea, J. Endocrinol., 88:401.PubMedCrossRefGoogle Scholar
  47. O’Grady, J.P., Caldwell, B.V., Auletta, F.J., and Speroff, L., 1972, The effects of an inhibition of prostaglandin synthesis (indomethacin) on ovulation, pregnancy, and pseudopregnancy in the rabbit, Prostaglandins, 1:97.PubMedCrossRefGoogle Scholar
  48. Pauerstein, C.J., Eddy, C.A., Croxatto, H.D., Hess, R., Siler-Khodr, T.M., and Croxatto, H.B., 1978, Temporal relationships of estrogen, progesterone, and luteinizing hormone levels to ovulation in women and infrahuman primates, Am. J. Obstet. Gynecol., 130:876.PubMedGoogle Scholar
  49. Peters, H., and McNatty, K.P., 1980, Corpus luteum function, in: “The Ovary,” University of California Press, Los Angeles.Google Scholar
  50. Peters, H., Himelstein-Braw, R., and Faber, M., 1976, The normal development of the ovary in childhood, Acta. Endo., 82:617.Google Scholar
  51. Polhemus, D.W., 1953, Ovarian maturation and cyst formation in children, Pediatrics, 1:588.Google Scholar
  52. Potter, E.L., 1961, “Pathology of the Fetus and the Newborn,” Yearbook Publishers, Chicago.Google Scholar
  53. Quagliarello, J., Goldsmith, L., Steinetz, B., Lustig, D.S., and Weiss, G., 1980, Induction of relaxin secretion in nonpregnant women by human chorionic gonadotropin, J. Clin. Endocrinol. Metab., 51:74.PubMedCrossRefGoogle Scholar
  54. Quagliarello, J., Szlachter, N., Steinetz, B.G., Goldsmith, L.T., and Weiss, G., 1979, Serial relaxin concentrations in human pregnancy, Am. J. Obstet. Gynecol., 135:43.PubMedGoogle Scholar
  55. Quigley, M.M., Kendall, J.Z., and Wilbourn, S.D., 1982, Application of a rapid serum RIA for LH in a clinical human in vitro fertilization (IVF) Program, Endocrinol., 110:411.Google Scholar
  56. Rebar, R.W., 1983, Premature menopause, Semin. Reprod. Endocrinol., 1:169.CrossRefGoogle Scholar
  57. Richards, J.S., 1979, Hormonal control of ovarian follicular development: a 1978 perspective, Recent Prog. Horm. Res., 35:343.Google Scholar
  58. Richards, J.S., and Midgley, A.R. Jr., 1976, Protein hormone action: a key to understanding ovarian follicular and luteal cell development, Biol. Reprod., 14:82.PubMedCrossRefGoogle Scholar
  59. Ross, G.T., and Lipsett, M.B., 1978, Hormonal correlates of normal and abnormal follicle growth and atresia after puberty in humans and other primates. Clin. Endocrinol. Metab., 7:561.PubMedCrossRefGoogle Scholar
  60. Ross, G.T., Cargille, C.M., Lipsett, M.B., Rayford, P.L., Marshall, J.R., Strott, C.A., and Rodbard, D., 1970, Pituitary and gonadal hormones in women during spontaneous and induced ovulatory cycles, Recent Prog. Horm. Res., 26:1.PubMedGoogle Scholar
  61. Ryan, K.J., Petro, Z., and Kaiser, J., 1968, Steroid formation by isolated and recombined ovarian granulosa and thecal cells, J. Clin. Endocrinol. Metab., 28:355.PubMedCrossRefGoogle Scholar
  62. Sarosi, P., Schmidt, C.L., Essig, M., Steinetz, B.G., and Weiss, G., 1983, The effect of relaxin and progesterone on rat uterine contractions, Am. J. Obstet. Gynecol., 145:402.PubMedGoogle Scholar
  63. Sherman, B.M., West, J.H., and Korenman, S.G., 1976, The menopausal transition: analyses of LH, FSH, estradiol and progesterone concentrations during menstrual cycles of older women. J. Clin. Endocrinol. Metab., 42:629.PubMedCrossRefGoogle Scholar
  64. Sotrel, G. Helvacioglu, A., Dowers, S., Scommmegna, S., and Auletta, F.J., 1981, Mechanisms of luteolysis: effect of estradiol and prostaglandin F2 on corpus luteum luteinizing hormone/human chorionic gonadotropin receptors and cyclic nucleotides in the rhesus monkey, Am. J. Obstet. Gynecol., 139:134.PubMedGoogle Scholar
  65. Speroff, L., Glass, R.H., and Kase, N.G., 1983, Regulation of the menstrual cycle, in: “Clinical Gynecologic Endocrinology and Infertility,” Williams and Wilkins, Baltimore.Google Scholar
  66. Steptoe, P.C., and Edwards, R.G., 1970, Laparoscopic recovery of preovulatory human oocytes after priming of ovaries with gonadotropins, Lancet, 1:683.PubMedCrossRefGoogle Scholar
  67. Stoufer, R.L., Nixon, W.E., and Hodgen, G.D., 1977, Estrogen inhibition of basal and gonadotropin-stimulated progesterone production by rhesus monkey luteal cells in vitro, Endocrinol., 101:1157.CrossRefGoogle Scholar
  68. Strickland, S., and Beers, W.H., 1976, Studies on the role of plasminogen activator in ovulation, J. Biol. Chem., 251:5694.PubMedGoogle Scholar
  69. Testart, J., Tbebault, A., and Frydman, R., 1982, Timing of ovulation and oocyte maturity after LH surge in women, in: “In Vitro Fertilization and Embryo Transfer,” E.S.E. Hafez and K. Semm, eds., M.T.P. Press Ltd., Lancaster.Google Scholar
  70. Tsafriri, A., and Channing, C.P., 1975, An inhibitory influence of granulosa cells and follicular fluid upon porcine oocyte meiosis in vitro, Endocrinol., 96:922.CrossRefGoogle Scholar
  71. Tsafriri, A., Kocb, Y., and Lindner, H.R., 1973, Ovulation rate and serum LH levels in rats treated witb indometbacin or prostaglandin E2, Prostaglandins, 3:461.PubMedCrossRefGoogle Scholar
  72. Van Wagener, G., and Simpson, M.E., 1965, “Embryology of tbe Ovary and Testis: Homo sapiens and macaca mulatta”, Yale University Press, New Haven.Google Scholar
  73. Wassarman, P.M., 1983, Oogenesis: synthetic events in tbe developing mammalian egg, in: “Mecbanism and Control of Animal Fertilization,” J.F. Hartmann, ed., Academic Press, New York.Google Scholar
  74. Williams, M.T., Rotb, M.S., Marsb, J.M., and LeMaire, W.J., 1979, Inhibition of buman chorionic gonadotropin-induced progesterone synthesis by estradiol in isolated human luteal cells, J. Clin. Endocrinol. Metab., 48:437.PubMedCrossRefGoogle Scholar
  75. Williams, R.F., Turner, C.K., and Hodgen, G.D., 1982, The late pubertal cascade in perimenarchial monkeys: onset of asymmetrical ovarian estradiol secretion and bioassayable LH release, J. Clin. Endocrinol. Metab., 55:660.PubMedCrossRefGoogle Scholar
  76. Wramsby, H., Kullander, S., Liedholm, P., Rannevik, G., Sundstrom, P., and Thorell, J., 1981, The success rate of in vitro fertilization of human oocytes in relation to the concentrations of different hormones in follicular fluid and peripheral plasma, Fertil. Steril., 36:448.PubMedGoogle Scholar
  77. Zamboni, L., 1972, Comparative studies on the ultrastructure of mammalian oocytes, in: “Oogenesis,” J.D. Biggers and A.W. Schuetz, eds., University Park Press, Baltimore.Google Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Cecilia L. Schmidt

There are no affiliations available

Personalised recommendations