Skip to main content
Log in

Effect of androgen substrates on the steroidogenic pattern of cumulus cells: Correlation with cumulus culture morphology

  • Andrology
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Background: In previous studies, higher progesterone secretion was observed in mature versus immature cumulusoocyte complexes. In mature cumulus mass that become homogeneously spread in culture (type C/D) progesterone secretion was higher than in partially (type B) or totally (type A) aggregated morphology. In sharp contrast, estradiol-17β secretion was significantly higher in type A than type C/D cumulus.

Purpose: Our purpose was to assess whether the decreased estradiol-17β level in type C/D cumulus culture is caused by deficiency of substrates.

Methods: The different cumulus types were incubated with or without 10−7 M dehydroepiandrosterone, 4-androstane-3, 17-dione, or testosterone. The levels of estradiol-17β, testosterone, and progesterone, were measured after 24 hr of culture.

Results: The addition of dehydroepiandrosterone or 4-androstane-3,17-dione significantly increased the estradiol-17β levels in all types of cumulus cells, whereas the addition of testosterone was less effective. In all types of cumulus cells the testosterone levels increased significantly on adding these androgen substrates. In the type C/D cumulus, the testosterone increased to lower levels compared to type A cumulus cells. In the presence of these androgens progesterone secretion is significantly reduced in type A cumulus cells. In type C/D cumulus cells, however, progesterone levels were significantly higher than in type A. The estradiol-17β/testosterone and progesterone/estradiol-17β ratios, which partially resemble the degree of aromatase activity and the degree of selectivity for progesterone secretion, respectively, were higher in type C/D than in type A cumulus cells.

Conclusions: In type C/D cumulus the significant increase in estradiol-17β secretion in the presence of various androgens suggests that, under basal conditions, androgen is less available for estradiol-17β biosynthesis compared to type A cumulus. Furthermore, the higher progesterone secretion in type C/D cumulus may suggest that the follicles yielding type C/D cumulus cells are more mature than the follicles yielding type A cumulus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Eppig JJ: FSH stimulates hyaluronic acid synthesis by oocytecumulus cell complexes from mouse preovulatory follicles. Nature 1979;281:483–484

    Article  PubMed  CAS  Google Scholar 

  2. Larsen WJ, Wert SE, Brunner GD: A dramatic loss of cumulus cell gap junctions is correlated with germinal vesicle breakdown in rat oocytes. Dev Biol 1986;113:517–521

    Article  PubMed  CAS  Google Scholar 

  3. Bar-Ami S: Increasing progesterone secretion and 3β-hydroxysteroid dehydrogenase activity of human cumulus cells and granulosa-lutein cells concurrent with successful fertilization of the corresponding oocyte. J Steroid Biochem Mol Biol 1994;51:299–305

    Article  PubMed  CAS  Google Scholar 

  4. Simonetti S, Veeck LL, Jones HW Jr: Correlation of follicular fluid volume with oocyte morphology from follicles stimulated by human menopausal gonadotropin. Fertil Steril 1985;44:177–180

    PubMed  CAS  Google Scholar 

  5. Moor RM, Trounson AO: Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and their subsequent developmental capacity. J Reprod Fertil 1977;49:101–109

    Article  PubMed  CAS  Google Scholar 

  6. Tsuji K, Sowa M, Nakano R: Relationship between human oocyte maturation and different follicular sizes. Biol Reprod 1985;32:413–417

    Article  PubMed  CAS  Google Scholar 

  7. Bar-Ami S, Gitay-Goren H, Brandes JM: Different morphological and steroidogenic patterns in oocyte/cumulus-corona cell complexes aspirated at in vitro fertilization. Biol Reprod 1989;41:761–770

    Article  PubMed  CAS  Google Scholar 

  8. Testart J, Frydman R, De Mouzon J, Lassalle B, Belaisch JC: A study of factors affecting the success of human fertilization in vitro I. Influence of ovarian stimulation upon the number and condition of oocytes collected. Biol Reprod 1983;28:415–424

    Article  PubMed  CAS  Google Scholar 

  9. Diamond MP, Rogers BJ, Vaughn WK, Wentz AC: Effect of the number of inseminating sperm and the follicular stimulation protocol on in vitro fertilization of human oocytes in male factor and non-male factor couples. Fertil Steril 1985;44:499–503

    PubMed  CAS  Google Scholar 

  10. Veeck LL, Wortham JWE Jr, Witmyer J, Sandow BA, Acosta AA, Garcia JE, Jones GS, Jones HW Jr: Maturation and fertilization of morphologically immature human oocytes in a program of in vitro fertilization. Fertil Steril 1983;39:594–602

    PubMed  CAS  Google Scholar 

  11. Trounson A, Wood C, Kausche A:In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients. Fertil Steril 1994;62:353–362

    PubMed  CAS  Google Scholar 

  12. Gitay-Goren H, Brandes JM, Bar-Ami S: Altered steroidogenic pattern of human granulosa-lutein cells in relation to cumulus cell culture morphology. J Steroid Biochem 1990;36:457–464

    Article  PubMed  CAS  Google Scholar 

  13. Barkey RJ, Ben-Shachar D, Amit T, Youdim, MBH: Increased hepatic and reduced prostatic prolactin (PRL) binding in iron deficiency and during neuroleptic treatment: Correlation with changes in serum PRL and testosterone. Eur J Pharmacol 1985;109:193–200

    Article  PubMed  CAS  Google Scholar 

  14. McNatty KP, Moore-Smith D, Makris A, Osathanondh R, Ryan KJ: Steroidogenesis by the human oocyte-cumulus cell complex in vitro. Steroids 1980;35:643–651

    Article  PubMed  CAS  Google Scholar 

  15. Laufer N, DeCherney AH, Haseltine FP, Behrman HR: Steroid secretion by the human egg-corona-cumulus complex in culture. J Clin Endocrinol Metab 1984;58:1153–1157

    PubMed  CAS  Google Scholar 

  16. Hillensjö T, Sjögren A, Strander B, Andino N: Steroid secretion by cumulus cells isolated from human preovulatory follicles. Acta Endocrinol (Copenh) 1985;108:407–413

    Google Scholar 

  17. Goldschmit D, Kraicer P, Orly J: Periovulatory expression of cholesterol side-chain cleavage cytochrome P-450 in cumulus cells. Endocrinology 1989;124:369–378

    PubMed  CAS  Google Scholar 

  18. Oda T, Yoshimura Y, Takahara Y, Hara T, Yoshimura S, Izumi Y, Aoki R, Natori M, Ohno T: Oocyte fertilizability and hormonal environment of human preovulatory follicles in hyperstimulated cycles in an in vitro fertilization program: Are mature preovulatory follicles undergoing atresia? Acta Obst Gyn Jap 1990;42:73–78

    CAS  Google Scholar 

  19. Bar-Ami S, Khoury C: Effect of cell-plating density on the steroidogenic activity of human cumulus cells. J Reprod Fertil 1994;101:729–735

    Article  PubMed  CAS  Google Scholar 

  20. Horie K, Takakura K, Fujiwara H, Suginami H, Liao S, Mori T: Immunohistochemical localization of androgen receptor in the human ovary throughout the menstrual cycle in relation to oestrogen and progesterone receptor expression. Hum Reprod 1992;7:184–190

    PubMed  CAS  Google Scholar 

  21. Schürenkämper P, Lisse K: Effects of cyproterone on the steroid biosynthesis in the human ovaryin vitro. Endokrinologie 1982;80:281–286

    PubMed  Google Scholar 

  22. Bernhisel MA, Holman JF, Haney AF, Schomberg DW: Estrogen and progesterone production by granulosa cell monolayers derived from in vitro fertilization procedures: Lack of evidence for modulation by androgen. J Clin Endocrinol Metab 1987;64:1251–1256

    PubMed  CAS  Google Scholar 

  23. Harlow CR, Hillier SG, Hodges JK: Androgen modulation of follicle-stimulating hormone-induced granulosa cell steroidogenesis in the primate ovary. Endocrinology 1986;119:1403–1405

    PubMed  CAS  Google Scholar 

  24. Schreiber JR, Nakamura K, Schmit V, Weinstein DB: Androgen and FSH synergistically stimulate lipoprotein degradation and utilization by ovary granulosa cells. Steroids 1984;43:25–42

    Article  PubMed  CAS  Google Scholar 

  25. Nimrod A: Studies on the synergistic effect of androgen on the stimulation of progestin secretion by FSH in cultured rat granulosa cells: a search for the mechanism of action. Mol Cell Endocrinol 1977;8:201–211

    Article  PubMed  CAS  Google Scholar 

  26. Azhar S, Khan I, Gibori G: The influence of estradiol on cholesterol processing by the corpus luteum. Biol Reprod 1989;40:961–971

    Article  PubMed  CAS  Google Scholar 

  27. Gougeon A: Dynamics of follicular growth in the human: A model from preliminary results. Hum Reprod 1986;1:81–87

    PubMed  CAS  Google Scholar 

  28. Erickson GF, Yen SSC: New data on follicle cells in polycystic ovaries: A proposed mechanism for the genesis of cystic follicles. Semin Reprod Endocrinol 1984;2:231–250

    Article  Google Scholar 

  29. Mahesh VB, Greenblatt RB: Steroid secretions of the normal and polycystic ovary. Recent Prog Horm Res 1964;20:341–394

    PubMed  CAS  Google Scholar 

  30. McNatty KP, Hillier SG, van den Boogaard AMJ, Trimbos-Kemper TCM, Reichert LE Jr, van Hall EV: Follicular development during the luteal phase of the human menstrual cycle. J Clin Endocrinol Metab 1983;56:1022–1031

    PubMed  CAS  Google Scholar 

  31. Reinthaller A, Deutinger J, Riss P, Müller-Tyl E, Fischl F, Bieglmayer C, Janisch H: Relationship between the steroid and prolactin concentration in follicular fluid and the maturation and fertilization of human oocytes. J Vitro Fert Embryo Transfer 1987;4:228–231

    Article  CAS  Google Scholar 

  32. Iwai T, Nanbu Y, Iwai M, Taii S, Fujii S, Mori T: Immunohistochemical localization of oestrogen receptors and progesterone receptors in the human ovary throughout the menstrual cycle. Virchows Arch A Pathol Anat 1990;417:369–375

    Article  CAS  Google Scholar 

  33. Williams MT, Roth MS, Marsh JM, LeMaire WJ: Inhibition of human chorionic gonadotropin-induced progesterone synthesis by estradiol in isolated human luteal cells. J Clin Endocrinol Metab 1979;48:437–440

    PubMed  CAS  Google Scholar 

  34. Bieszczad RR, McClintock JS, Pepe GJ, Dimino MJ: Progesterone secretion by granulosa cells from different sized follicles of human ovaries after short term incubation. J Clin Endocrinol Metab 1982;55:181–184

    PubMed  CAS  Google Scholar 

  35. McAllister JM, Kerin JFP, Trant JM, Estabrook RW, Mason JI, Waterman MR, Simpson ER: REgulation of cholesterol side-chain cleavage and 17α-hydroxylase/lyase activities in proliferating human theca interna cells in long term monolayer culture. Endocrinology 1989;125:1959–1966

    Article  PubMed  CAS  Google Scholar 

  36. Shimizu A, Hirato K, Hidaka T, Yanaihara T, Nakayama T: Difference of steroidogenesis in human ovary at different stage of cycle. Acta Obst Gyn Jap 1982;34:693–700

    CAS  Google Scholar 

  37. Roldan ERS, Murase T, Shi Q-X: Exocytosis in spermatozoa in response to progesterone and zona pellucida. Science 1994;266:1578–1581

    Article  PubMed  CAS  Google Scholar 

  38. Paltieli Y, Weichselbaum A, Eibschitz I, Ziskind G, Silbermann M: The effect of estrogen and progesterone on the ciliary activity in the human fallopian tubes. J Assist Reprod Genet (Suppl)1995;12:112S

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bar-Ami, S., Regev, A. & Gitay-Goren, H. Effect of androgen substrates on the steroidogenic pattern of cumulus cells: Correlation with cumulus culture morphology. J Assist Reprod Genet 14, 270–276 (1997). https://doi.org/10.1007/BF02765828

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02765828

Key words

Navigation