Skip to main content Accessibility help
×
Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-28T01:34:26.954Z Has data issue: false hasContentIssue false

2 - Mechanisms of Follicular Development: The Role of Gonadotrophins

from PART I - PHYSIOLOGY OF REPRODUCTION

Published online by Cambridge University Press:  04 August 2010

Botros R. M. B. Rizk
Affiliation:
University of South Alabama
Juan A. Garcia-Velasco
Affiliation:
Rey Juan Carlos University School of Medicine,
Hassan N. Sallam
Affiliation:
University of Alexandria School of Medicine
Antonis Makrigiannakis
Affiliation:
University of Crete
Get access

Summary

INTRODUCTION

Folliculogenesis in women is a dynamic and uninterrupted process from fetal life until menopause. Following pubertal maturation of the reproductive axis, all types of follicles from the primordial to the preovulatory stage are present in the human ovary. Over the past twenty years, it has become clear that these follicles represent sequential forms of the developmental process classified into eight categories, based on the size and the number of the granulosa cells (Gougeon, 1986). For example, class 1 corresponds to a secondary preantral follicle and class 8 to a large preovulatory follicle.

Folliculogenesis is a lengthy process (Figure 2.1). Based on the calculation of the doubling time of granulosa cells, it is estimated that the time spent from the primordial to the preovulatory stage is approximately one year (Gougeon, 1986). However, maturation of a follicle from class 1 to class 8 is achieved within eighty-five days (Gougeon, 1986). At the beginning, proliferation of the granulosa cells on several layers takes place and the primordial follicle becomes preantral. Following this, the theca interna develops and the antral cavity is formed. The rate at which follicles leave the primordial pool is not known. However, it seems that the departure follows an ordered sequence, so that follicles formed first leave the pool earlier (Hirshfield, 1991).

It remains unclear which factors are responsible for the initiation of maturation of a primordial follicle or what is the trigger for the passage of a follicle from the preantral to the antral stage (Figure 2.1).

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adashi, E.Y. (1998) The IGF family and folliculogenesis. J. Reprod. Immunol. 39, 13–19.CrossRefGoogle ScholarPubMed
Adashi, E.Y. and Hsueh, A.J. (1982) Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa cells. J. Biol. Chem. 257, 6077–83.Google ScholarPubMed
Alexandris, E., Milingos, S., Kollios, G., Seferiadis, K., Lolis, D. and Messinis, I.E. (1997) Changes in gonadotrophin response to gonadotrophin releasing hormone in normal women following bilateral ovariectomy. Clin. Endocrinol. (Oxf.) 47, 721–6.CrossRefGoogle ScholarPubMed
Baird, D.T. (1983) Factors regulating the growth of the preovulatory follicle in the sheep and human. J. Reprod. Fertil. 69, 343–52.CrossRefGoogle ScholarPubMed
Baird, D.T. (2001) Is there a place for different isoforms of FSH in clinical medicine? IV. The clinician's point of view. Hum. Reprod. 16, 1316–18.CrossRefGoogle Scholar
Baker, S.J. and Spears, N. (1999) The role of intra-ovarian interactions in the regulation of follicle dominance. Hum. Reprod. Update 5, 153–65.CrossRefGoogle ScholarPubMed
Barreca, A., Del Monte, P., Ponzani, P., Artini, P.G., Genazzani, A.R. and Minuto, F. (1996) Intrafollicular insulin-like growth factor-II levels in normally ovulating women and in patients with polycystic ovary syndrome. Fertil. Steril. 65, 739–45.CrossRefGoogle ScholarPubMed
Beckers, N.G., Macklon, N.S., Devroey, P., Platteau, P., Boerrigter, P.J. and Fauser, B.C. (2003) First live birth after ovarian stimulation using a chimeric long-acting human recombinant follicle-stimulating hormone (FSH) agonist (recFSH-CTP) for in vitro fertilization. Fertil. Steril. 79, 621–3.CrossRefGoogle ScholarPubMed
Bergh, C., Olsson, J.H. and Hillensjo, T. (1991) Effect of insulin-like growth factor I on steroidogenesis in cultured human granulosa cells. Acta. Endocrinol. (Copenh). 125, 177–85.Google ScholarPubMed
Billig, H., Furuta, I. and Hsueh, A.J. (1993) Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 133, 2204–12.CrossRefGoogle ScholarPubMed
Brown, J.B., Evans, J.H., Adey, F.D. and Taft, H.P. (1969) Factors involved in the induction of fertile ovulation with human gonadotrophins. J. Obstet. Gynaecol. Br. Commonw. 76, 289–307.CrossRefGoogle ScholarPubMed
Bukovsky, A., Caudle, M.R., Keenan, J.A., Wimalasena, J., Foster, J.S. and Meter, S.E. (1995a) Quantitative evaluation of the cell cycle-related retinoblastoma protein and localization of Thy-1 differentiation protein and macrophages during follicular development and atresia, and in human corpora lutea. Biol. Reprod. 52, 776–92.CrossRefGoogle ScholarPubMed
Bukovsky, A., Caudle, M.R., Keenan, J.A., Wimalasena, J., Foster, J.S., Upadhyaya, N.B. and Meter, S.E. (1995b) Expression of cell cycle regulatory proteins (p53, pRb) in the human female genital tract. J. Assist. Reprod. Genet. 12, 123–31.CrossRefGoogle ScholarPubMed
Campbell, B.K. (1999) The modulation of gonadotrophic hormone action on the ovary by paracrine and autocrine factors. Anat. Histol. Embryol. 28, 247–51.CrossRefGoogle ScholarPubMed
Carabatsos, M.J., Elvin, J., Matzuk, M.M. and Albertini, D.F. (1998) Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev. Biol. 204, 373–84.CrossRefGoogle ScholarPubMed
Carlsson, I.B., Scott, J.E., Visser, J.A., Ritvos, O., Themmen, A.P. and Hovatta, O. (2006) Anti-Mullerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum. Reprod. 21, 2223–7.CrossRefGoogle ScholarPubMed
Conover, C.A., Oxvig, C., Overgaard, M.T., Christiansen, M. and Giudice, L.C. (1999) Evidence that the insulin-like growth factor binding protein-4 protease in human ovarian follicular fluid is pregnancy associated plasma protein-A. J. Clin. Endocrinol. Metab. 84, 4742–5.CrossRefGoogle ScholarPubMed
Cortvrindt, R., Hu, Y. and Smitz, J. (1998) Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone-supplemented mouse preantral follicle culture. Hum. Reprod. 13, 1292–302.CrossRefGoogle ScholarPubMed
Couse, J.F., Yates, M.M., Deroo, B.J. and Korach, K.S. (2005) Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 146, 3247–62.CrossRefGoogle ScholarPubMed
Dafopoulos, K.C., Kotsovassilis, C.P., Milingos, S.D., Kallitsaris, A.T., Georgadakis, G.S., Sotiros, P.G. and Messinis, I.E. (2004) Changes in pituitary sensitivity to GnRH in estrogen-treated post-menopausal women: evidence that gonadotrophin surge attenuating factor plays a physiological role. Hum. Reprod. 19, 1985–92.CrossRefGoogle Scholar
Kretser, D.M., Hedger, M.P., Loveland, K.L. and Phillips, D.J. (2002) Inhibins, activins and follistatin in reproduction. Hum. Reprod. Update 8, 529–41.CrossRefGoogle ScholarPubMed
Di Blasio, A.M., Vigano, P. and Ferrari, A. (1994) Insulin-like growth factor-II stimulates human granulosa-luteal cell proliferation in vitro. Fertil. Steril. 61, 483–7.CrossRefGoogle ScholarPubMed
Di Pasquale, E., Beck-Peccoz, P. and Persani, L. (2004) Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am. J. Hum. Genet. 75, 106–11.CrossRefGoogle ScholarPubMed
Dissen, G.A., Romero, C., Hirshfield, A.N. and Ojeda, S.R. (2001) Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142, 2078–86.CrossRefGoogle ScholarPubMed
Dor, J., Ben-Shlomo, I., Lunenfeld, B., Pariente, C., Levran, D., Karasik, A., Seppala, M. and Mashiach, S. (1992) Insulin-like growth factor-I (IGF-I) may not be essential for ovarian follicular development: evidence from IGF-I deficiency. J. Clin. Endocrinol. Metab. 74, 539–42.Google Scholar
Dorrington, J.H. and Armstrong, D.T. (1979) Effects of FSH on gonadal functions. Recent Prog. Horm. Res. 35, 301–42.Google ScholarPubMed
Dube, J.L., Wang, P., Elvin, J., Lyons, K.M., Celeste, A.J. and Matzuk, M.M. (1998) The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 12, 1809–17.CrossRefGoogle ScholarPubMed
Duijkers, I.J., Klipping, C., Boerrigter, P.J., Machielsen, C.S., Bie, J.J., and Voortman, G. (2002) Single dose pharmacokinetics and effects on follicular growth and serum hormones of a long-acting recombinant FSH preparation (FSH-CTP) in healthy pituitary-suppressed females. Hum. Reprod. 17, 1987–93.CrossRefGoogle ScholarPubMed
Eden, J.A., Jones, J., Carter, G.D. and Alaghband-Zadeh, J. (1990) Follicular fluid concentrations of insulin-like growth factor 1, epidermal growth factor, transforming growth factor-alpha and sex-steroids in volume matched normal and polycystic human follicles. Clin. Endocrinol. (Oxf). 32, 395–405.CrossRefGoogle ScholarPubMed
El-Roeiy, A., Chen, X., Roberts, V.J., LeRoith, D., Roberts, C.T. Jr. and Yen, S.S. (1993) Expression of insulin-like growth factor-I (IGF-I) and IGF-II and the IGF-I, IGF-II, and insulin receptor genes and localization of the gene products in the human ovary. J. Clin. Endocrinol. Metab. 77, 1411–18.Google ScholarPubMed
Emmen, J.M., Couse, J.F., Elmore, S.A., Yates, M.M., Kissling, G.E. and Korach, K.S. (2005) In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER){alpha} and ER{beta} null mice indicate a role for ER{beta} in follicular maturation. Endocrinology 146, 2817–26.CrossRefGoogle ScholarPubMed
Erickson, G.F. and Shimasaki, S. (2000) The role of the oocyte in folliculogenesis. Trends Endocrinol. Metab. 11, 193–8.CrossRefGoogle ScholarPubMed
Erickson, G.F. and Shimasaki, S. (2001) The physiology of folliculogenesis: the role of novel growth factors. Fertil. Steril. 76, 943–9.CrossRefGoogle ScholarPubMed
Erickson, G.F., Magoffin, D.A., Dyer, C.A. and Hofeditz, C. (1985) The ovarian androgen producing cells: a review of structure/function relationships. Endocr. Rev. 6, 371–99.CrossRefGoogle ScholarPubMed
Fauser, B.C. and Heusden, A.M. (1997) Manipulation of human ovarian function: physiological concepts and clinical consequences. Endocr. Rev. 18, 71–106.Google ScholarPubMed
Findlay, J.K., Drummond, A.E., Britt, K.L., Dyson, M., Wreford, N.G., Robertson, D.M., Groome, N.P., Jones, M.E. and Simpson, E.R. (2000) The roles of activins, inhibins and estrogen in early committed follicles. Mol. Cell. Endocrinol. 163, 81–7.CrossRefGoogle ScholarPubMed
Geisthovel, F., Moretti-Rojas, I., Asch, R.H. and Rojas, F.J. (1989) Expression of insulin-like growth factor-II (IGF-II) messenger ribonucleic acid (mRNA), but not IGF-I mRNA, in human preovulatory granulosa cells. Hum. Reprod. 4, 899–902.CrossRefGoogle Scholar
Glister, C., Groome, N.P. and Knight, P.G. (2006) Bovine follicle development is associated with divergent changes in activin-A, inhibin-A and follistatin and the relative abundance of different follistatin isoforms in follicular fluid. J. Endocrinol. 188, 215–25.CrossRefGoogle ScholarPubMed
Gosden, R.G., Huntley, J.F., Douglas, A., Inglis, L. and Miller, H.R. (1993) Quantitative and cytochemical studies of mast cell proteases in rat ovaries and uteri in various reproductive states. J. Reprod. Fertil. 98, 577–82.CrossRefGoogle ScholarPubMed
Gougeon, A. (1986) Dynamics of follicular growth in the human: a model from preliminary results. Hum. Reprod. 1, 81–7.CrossRefGoogle ScholarPubMed
Gougeon, A. and Lefevre, B. (1983) Evolution of the diameters of the largest healthy and atretic follicles during the human menstrual cycle. J. Reprod. Fertil. 69, 497–502.CrossRefGoogle ScholarPubMed
Gougeon, A. and Testart, J. (1990) Influence of human menopausal gonadotropin on the recruitment of human ovarian follicles. Fertil. Steril. 54, 848–52.CrossRefGoogle ScholarPubMed
Groome, N.P., Illingworth, P.J., O'Brien, M., Pai, R., Rodger, F.E., Mather, J.P. and McNeilly, A.S. (1996) Measurement of dimeric inhibin B throughout the human menstrual cycle. J. Clin. Endocrinol. Metab. 81, 1401–5.Google ScholarPubMed
Grunwald, K., Feldmann, K., Melsheimer, P., Rabe, T., Neulen, J. and Runnebaum, B. (1998) Aneuploidy in human granulosa lutein cells obtained from gonadotrophin-stimulated follicles and its relation to intrafollicular hormone concentrations. Hum. Reprod. 13, 2679–87.CrossRefGoogle ScholarPubMed
Hayashi, M., McGee, E.A., Min, G., Klein, C., Rose, U.M., Duin, M. and Hsueh, A.J. (1999) Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236–44.CrossRefGoogle ScholarPubMed
Hernandez, E.R., Resnick, C.E., Svoboda, M.E., Wyk, J.J., Payne, D.W. and Adashi, E.Y. (1988) Somatomedin-C/insulin-like growth factor I as an enhancer of androgen biosynthesis by cultured rat ovarian cells. Endocrinology 122, 1603–12.CrossRefGoogle ScholarPubMed
Hild-Petito, S., Stouffer, R.L. and Brenner, R.M. (1988) Immunocytochemical localization of estradiol and progesterone receptors in the monkey ovary throughout the menstrual cycle. Endocrinology 123, 2896–905.CrossRefGoogle ScholarPubMed
Hillier, S.G. (1994) Current concepts of the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Hum. Reprod. 9, 188–91.CrossRefGoogle ScholarPubMed
Hillier, S.G. (2001) Gonadotropic control of ovarian follicular growth and development. Mol. Cell. Endocrinol. 179, 39–46.CrossRefGoogle ScholarPubMed
Hillier, S.G. and Tetsuka, M. (1997) Role of androgens in follicle maturation and atresia. Baillieres Clin. Obstet. Gynaecol. 11, 249–60.CrossRefGoogle ScholarPubMed
Hillier, S.G., Whitelaw, P.F. and Smyth, C.D. (1994) Follicular oestrogen synthesis: the ‘two-cell, two-gonadotrophin’ model revisited. Mol. Cell. Endocrinol. 100, 51–4.CrossRefGoogle ScholarPubMed
Hirshfield, A.N. (1991) Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43–101.CrossRefGoogle ScholarPubMed
Hohmann, F.P., Laven, J.S., Jong, F.H., Eijkemans, M.J. and Fauser, B.C. (2001) Low-dose exogenous FSH initiated during the early, mid or late follicular phase can induce multiple dominant follicle development. Hum. Reprod. 16, 846–54.CrossRefGoogle ScholarPubMed
Hohmann, F.P., Laven, J.S., Jong, F.H. and Fauser, B.C. (2005) Relationship between inhibin A and B, estradiol and follicle growth dynamics during ovarian stimulation in normo-ovulatory women. Eur. J. Endocrinol. 152, 395–401.CrossRefGoogle Scholar
Hourvitz, A., Widger, A.E., Filho, F.L., Chang, R.J., Adashi, E.Y. and Erickson, G.F. (2000) Pregnancy-associated plasma protein-A gene expression in human ovaries is restricted to healthy follicles and corpora lutea. J. Clin. Endocrinol. Metab. 85, 4916–20.CrossRefGoogle ScholarPubMed
Hsu, S.Y., Kubo, M., Chun, S.Y., Haluska, F.G., Housman, D.E. and Hsueh, A.J. (1995) Wilms tumor protein WT1 as an ovarian transcription factor: decreases in expression during follicle development and repression of inhibin-alpha gene promoter. Mol. Endocrinol. 9, 1356–66.Google ScholarPubMed
Huang, E.J., Manova, K., Packer, A.I., Sanchez, S., Bachvarova, R.F. and Besmer, P. (1993) The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev. Biol. 157, 100–9.CrossRefGoogle ScholarPubMed
Hugues, J.N., Soussis, J., Calderon, I., Balasch, J., Anderson, R.A. and Romeu, A. (2005) Recombinant LH Study Group. Does the addition of recombinant LH in WHO group II anovulatory women over-responding to FSH treatment reduce the number of developing follicles? A dose-finding study. Hum. Reprod. 20, 629–35.CrossRefGoogle Scholar
Hussein, M.R. (2005) Apoptosis in the ovary: molecular mechanisms. Hum. Reprod. Update 11, 162–77.CrossRefGoogle ScholarPubMed
Iwai, T., Nanbu, Y., Iwai, M., Taii, S., Fujii, S. and Mori, T. (1990) Immunohistochemical localization of oestrogen receptors and progesterone receptors in the human ovary throughout the menstrual cycle. Virchows Arch A. Pathol. Anat. Histopathol. 417, 369–75.CrossRefGoogle ScholarPubMed
Judd, S., Terry, A., Petrucco, M. and White, G. (1992) The source of pulsatile secretion of progesterone during the human follicular phase. J. Clin. Endocrinol. Metab. 74, 299–305.Google ScholarPubMed
Kamada, S., Kubota, T., Taguchi, M., Ho, W.R., Sakamoto, S. and Aso, T. (1992) Effects of insulin-like growth factor-II on proliferation and differentiation of ovarian granulosa cells. Horm. Res. 37, 141–9.CrossRefGoogle ScholarPubMed
Kerketze, K., Blaschuk, O.W. and Farookhi, R. (1996) Cellular heterogeneity in the membrana granulosa of developing rat follicles: assessment by flow cytometry and lectin binding. Endocrinology 137, 3089–100.CrossRefGoogle ScholarPubMed
Klein, N.A., Houmard, B.S., Hansen, K.R., Woodruff, T.K., Sluss, P.M., Bremner, W.J. and Soules, M.R. (2004) Age-related analysis of inhibin A, inhibin B, and activin A relative to the intercycle monotropic follicle-stimulating hormone rise in normal ovulatory women. J. Clin. Endocrinol. Metab. 89, 2977–81.CrossRefGoogle ScholarPubMed
Knight, P.G. and Glister, C. (2003) Local roles of TGF-beta superfamily members in the control of ovarian follicle development. Anim. Reprod. Sci. 78, 165–83.CrossRefGoogle ScholarPubMed
Knight, P.G. and Glister, C. (2006) TGF-beta superfamily members and ovarian follicle development. Reproduction 32, 191–206.CrossRefGoogle Scholar
Lawrence, J.B., Oxvig, C., Overgaard, M.T., Sottrup-Jensen, L., Gleich, G.J., Hays, L.G., Yates, J.R., 3rd and Conover, C.A. (1999) The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proc. Natl. Acad. Sci. U. S. A. 96, 3149–53.CrossRefGoogle ScholarPubMed
Leroy, I., d'Acremont, M., Brailly-Tabard, S., Frydman, R., Mouzon, J. and Bouchard, P. (1994) A single injection of a gonadotropin-releasing hormone (GnRH) antagonist (Cetrorelix) postpones the luteinizing hormone (LH) surge: further evidence for the role of GnRH during the LH surge. Fertil. Steril. 62, 461–7.CrossRefGoogle ScholarPubMed
Lolis, D.E., Tsolas, O. and Messinis, I.E. (1995) The follicle-stimulating hormone threshold level for follicle maturation in superovulated cycles. Fertil. Steril. 63, 1272–7.CrossRefGoogle ScholarPubMed
Loumaye, E., Engrand, P., Shoham, Z., Hillier, S.G. and Baird, D.T. (2003) Clinical evidence for an LH ‘ceiling’ effect induced by administration of recombinant human LH during the late follicular phase of stimulated cycles in World Health Organization type I and type II anovulation. Hum. Reprod. 18, 314–22.CrossRefGoogle Scholar
MacNatty, K.P., Hunter, W.M., MacNeilly, A.S. and Sawers, R.S. (1975) Changes in the concentration of pituitary and steroid hormones in the follicular fluid of human graafian follicles throughout the menstrual cycle. J. Endocrinol. 64, 555–71.CrossRefGoogle Scholar
Magoffin, D.A. and Weitsman, S.R. (1994) Insulin-like growth factor-I regulation of luteinizing hormone (LH) receptor messenger ribonucleic acid expression and LH-stimulated signal transduction in rat ovarian theca-interstitial cells. Biol. Reprod. 51, 766–75.CrossRefGoogle ScholarPubMed
Mais, V., Cetel, N.S., Muse, K.N., Quigley, M.E., Reid, R.L. and Yen, S.S. (1987) Hormonal dynamics during luteal-follicular transition. J. Clin. Endocrinol. Metab. 64, 1109–14.CrossRefGoogle ScholarPubMed
Marrone, B.L. and Crissman, H.A. (1988) Characterization of granulosa cell subpopulations from avian preovulatory follicles by multiparameter flow cytometry. Endocrinology 122, 651–8.CrossRefGoogle ScholarPubMed
Mason, H.D., Willis, D.S., Holly, J.M. and Franks, S. (1994) Insulin preincubation enhances insulin-like growth factor-II (IGF-II) action on steroidogenesis in human granulosa cells. J. Clin. Endocrinol. Metab. 78, 1265–7.Google ScholarPubMed
Mason, H.D., Cwyfan-Hughes, S.C., Heinrich, G., Franks, S. and Holly, J.M. (1996) Insulin-like growth factor (IGF) I and II, IGF-binding proteins, and IGF-binding protein proteases are produced by theca and stroma of normal and polycystic human ovaries. J. Clin. Endocrinol. Metab. 81, 276–84.Google ScholarPubMed
Mason, H.D., Cwyfan-Hughes, S., Holly, J.M. and Franks, S. (1998) Potent inhibition of human ovarian steroidogenesis by insulin-like growth factor binding protein-4 (IGFBP-4). J. Clin. Endocrinol. Metab. 83, 284–7.CrossRefGoogle Scholar
Matthews, C.H., Borgato, S., Beck-Peccoz, P., Adams, M., Tone, Y., Gambino, G., Casagrande, S., Tedeschini, G., Benedetti, A. and Chatterjee, V.K. (1993) Primary amenorrhoea and infertility due to a mutation in the beta-subunit of follicle-stimulating hormone. Nat. Genet. 5, 83–6.CrossRefGoogle ScholarPubMed
May, J.V., Frost, J.P. and Bridge, A.J. (1990) Regulation of granulosa cell proliferation: facilitative roles of platelet-derived growth factor and low density lipoprotein. Endocrinology 126, 2896–905.CrossRefGoogle ScholarPubMed
Mazerbourg, S., Bondy, C.A., Zhou, J. and Monget, P. (2003) The insulin-like growth factor system: a key determinant role in the growth and selection of ovarian follicles? A comparative species study. Reprod. Domest. Anim. 38, 247–58.CrossRefGoogle ScholarPubMed
McGee, E.A. and Hsueh, A.J. (2000) Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 21, 200–14.Google ScholarPubMed
McGee, E., Spears, N., Minami, S., Hsu, S.Y., Chun, S.Y., Billig, H. and Hsueh, A.J. (1997) Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3, 5-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinology 138, 2417–24.CrossRefGoogle ScholarPubMed
McGee, E.A., Smith, R., Spears, N., Nachtigal, M.W., Ingraham, H. and Hsueh, A.J. (2001) Mullerian inhibitory substance induces growth of rat preantral ovarian follicles. Biol. Reprod. 64, 293–8.CrossRefGoogle ScholarPubMed
McGrath, S.A., Esquela, A.F. and Lee, S.J. (1995) Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 9, 131–6.Google ScholarPubMed
McNatty, K.P. and Baird, D.T. (1978) Relationship between follicle-stimulating hormone, androstenedione and oestradiol in human follicular fluid. J. Endocrinol. 76, 527–31.CrossRefGoogle ScholarPubMed
McNatty, K.P., Smith, D.M., Makris, A., Osathanondh, R. and Ryan, K.J. (1979a) The microenvironment of the human antral follicle: interrelationships among the steroid levels in antral fluid, the population of granulosa cells, and the status of the oocyte in vivo and in vitro. J. Clin. Endocrinol. Metab. 49, 851–60.CrossRefGoogle ScholarPubMed
McNatty, K.P., Makris, A., Reinhold, V.N., Grazia, C., Osathanondh, R. and Ryan, K.J. (1979b) Metabolism of androstenedione by human ovarian tissues in vitro with particular reference to reductase and aromatase activity. Steroids 34, 429–43.CrossRefGoogle ScholarPubMed
McNatty, K.P., Makris, A., DeGrazia, C., Osathanondh, R. and Ryan, K.J. (1979c) 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, 687–99.CrossRefGoogle ScholarPubMed
McNatty, K.P., Juengel, J.L., Reader, K.L., Lun, S., Myllymaa, S., Lawrence, S.B., Western, A., Meerasahib, M.F., Mottershead, D.G., Groome, N.P., Ritvos, O. and Laitinen, M.P.E. (2005) Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129, 473–80.CrossRefGoogle ScholarPubMed
Messinis, I.E. (1989) Drugs used in in vitro fertilisation procedures. Drugs 38, 148–59.CrossRefGoogle ScholarPubMed
Messinis, I.E. (2006) Ovarian feedback, mechanism of action and possible clinical implications. Hum. Reprod. Update 12, 557–71.CrossRefGoogle ScholarPubMed
Messinis, I.E. and Templeton, A. (1986) Urinary oestrogen levels and follicle ultrasound measurements in clomiphene induced cycles with an endogenous luteinizing hormone surge. Br. J. Obstet. Gynaecol. 93, 43–9.CrossRefGoogle ScholarPubMed
Messinis, I.E. and Templeton, A.A. (1987) Endocrine and follicle characteristics of cycles with and without endogenous luteinizing hormone surges during superovulation induction with pulsatile follicle-stimulating hormone. Hum. Reprod. 2, 11–16.CrossRefGoogle ScholarPubMed
Messinis, I.E. and Templeton, A.A. (1988a) The endocrine consequences of multiple folliculogenesis. J. Reprod. Fertil. Suppl. 36, 27–37.Google ScholarPubMed
Messinis, I.E. and Templeton, A. (1988b) Blockage of the positive feedback effect of oestradiol during prolonged administration of clomiphene citrate to normal women. Clin. Endocrinol. (Oxf). 29, 509–16.CrossRefGoogle ScholarPubMed
Messinis, I.E. and Templeton, A.A. (1990a) Effects of supraphysiological concentrations of progesterone on the characteristics of the oestradiol-induced gonadotrophin surge in women. J. Reprod. Fertil. 88, 513–19.CrossRefGoogle ScholarPubMed
Messinis, I.E. and Templeton, A.A. (1990b) The importance of follicle-stimulating hormone increase for folliculogenesis. Hum. Reprod. 5, 153–6.CrossRefGoogle ScholarPubMed
Messinis, I.E., Koutsoyiannis, D., Milingos, S., Tsahalina, E., Seferiadis, K., Lolis, D. and Templeton, A.A. (1993) Changes in pituitary response to GnRH during the luteal-follicular transition of the human menstrual cycle. Clin. Endocrinol. (Oxf). 38, 159–63.CrossRefGoogle ScholarPubMed
Messinis, I.E., Lolis, D., Zikopoulos, K., Tsahalina, E., Seferiadis, K. and Templeton, A.A. (1994) Effect of an increase in FSH on the production of gonadotrophin-surge-attenuating factor in women. J. Reprod. Fertil. 101, 689–95.CrossRefGoogle ScholarPubMed
Minegishi, T., Hirakawa, T., Kishi, H., Abe, K., Abe, Y., Mizutani, T. and Miyamoto, K. (2000) A role of insulin-like growth factor I for follicle-stimulating hormone receptor expression in rat granulosa cells. Biol. Reprod. 62, 325–33.CrossRefGoogle ScholarPubMed
Miro, F. and Hillier, S.G. (1996) Modulation of granulosa cell deoxyribonucleic acid synthesis and differentiation by activin. Endocrinology 137, 464–8.CrossRefGoogle ScholarPubMed
Molskness, T.A., Woodruff, T.K., Hess, D.L., Dahl, K.D. and Stouffer, R.L. (1996) Recombinant human inhibin-A administered early in the menstrual cycle alters concurrent pituitary and follicular, plus subsequent luteal, function in rhesus monkeys. J. Clin. Endocrinol. Metab. 81, 4002–6.Google ScholarPubMed
Moore, R.K. and Shimasaki, S. (2005) Molecular biology and physiological role of the oocyte factor, BMP-15. Mol. Cell. Endocrinol. 234, 67–73.CrossRefGoogle ScholarPubMed
Mullis, P.E., Yoshimura, N., Kuhlmann, B., Lippuner, K., Jaeger, P. and Harada, H. (1997) Aromatase deficiency in a female who is compound heterozygote for two new point mutations in the P450arom gene: impact of estrogens on hypergonadotropic hypogonadism, multicystic ovaries, and bone densitometry in childhood. J. Clin. Endocrinol. Metab. 82, 1739–45.Google Scholar
Nahum, R., Thong, K.J. and Hillier, S.G. (1995) Metabolic regulation of androgen production by human thecal cells in vitro. Hum. Reprod. 10, 75–81.CrossRefGoogle ScholarPubMed
Nakatani, A., Shimasaki, S., Depaolo, L.V., Erickson, G.F. and Ling, N. (1991) Cyclic changes in follistatin messenger ribonucleic acid and its protein in the rat ovary during the estrous cycle. Endocrinology 129, 603–11.CrossRefGoogle ScholarPubMed
Nilsson, E.E., Detzel, C. and Skinner, M.K. (2006) Platelet-derived growth factor modulates the primordial to primary follicle transition. Reproduction 31, 1007–15.CrossRefGoogle Scholar
Otsuka, F., Yao, Z., Lee, T., Yamamoto, S., Erickson, G.F. and Shimasaki, S. (2000) Bone morphogenetic protein-15. Identification of target cells and biological functions. J. Biol. Chem. 275, 39523–8.CrossRefGoogle ScholarPubMed
Pelletier, G. and El-Alfy, M. (2000) Immunocytochemical localization of estrogen receptors alpha and beta in the human reproductive organs. J. Clin. Endocrinol. Metab. 85, 4835–40.Google ScholarPubMed
Perez, G.I., Robles, R., Knudson, C.M., Flaws, J.A., Korsmeyer, S.J. and Tilly, J.L. (1999) Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat. Genet. 21, 200–3.CrossRefGoogle ScholarPubMed
Peters, H., Byskov, A.G. and Grinsted, J. (1978) Follicular growth in fetal and prepubertal ovaries of humans and other primates. J. Clin. Endocrinol. Metab. 7, 469–85.CrossRefGoogle ScholarPubMed
Piontkewitz, Y., Sundfeldt, K. and Hedin, L. (1997) The expression of c-myc during follicular growth and luteal formation in the rat ovary in vivo. J. Endocrinol. 152, 395–406.CrossRefGoogle ScholarPubMed
Piquette, G.N., LaPolt, P.S., Oikawa, M. and Hsueh, A.J. (1991) Regulation of luteinizing hormone receptor messenger ribonucleic acid levels by gonadotropins, growth factors, and gonadotropin-releasing hormone in cultured rat granulosa cells. Endocrinology 128, 2449–56.CrossRefGoogle ScholarPubMed
Rabin, D., Spitz, I., Bercovici, B., Bell, J., Laufer, A., Benveniste, R. and Polishuk, W. (1972) Isolated deficiency of follicle-stimulating hormone. Clinical and laboratory features. N. Engl. J. Med. 287, 1313–17.CrossRefGoogle ScholarPubMed
Rabinovici, J., Blankstein, J., Goldman, B., Rudak, E., Dor, Y., Pariente, C., Geier, A., Lunenfeld, B. and Mashiach, S. (1989) In vitro fertilization and primary embryonic cleavage are possible in 17 alpha-hydroxylase deficiency despite extremely low intrafollicular 17 beta-estradiol. J. Clin. Endocrinol. Metab. 68, 693–7.CrossRefGoogle ScholarPubMed
Rae, M.T. and Hillier, S.G. (2005) Steroid signalling in the ovarian surface epithelium. Trends Endocrinol. Metab. 16, 327–33.CrossRefGoogle ScholarPubMed
Reilly, C.M., Cannady, W.E., Mahesh, V.B., Stopper, V.S., Sevilla, L.M. and Mills, T.M. (1996) Duration of estrogen exposure prior to follicle-stimulating hormone stimulation is critical to granulosa cell growth and differentiation in rats. Biol. Reprod. 54, 1336–42.CrossRefGoogle ScholarPubMed
Richards, J.S. (1994) Hormonal control of gene expression in the ovary. Endocr. Rev. 15, 725–51.CrossRefGoogle ScholarPubMed
Richards, J.S., Russell, D.L., Robker, L., Dajee, M. and Alliston, T.N. (1998) Molecular mechanisms of ovulation and luteinization. Mol. Cell. Endocrinol. 145, 47–54.CrossRefGoogle ScholarPubMed
Rivera, G.M. and Fortune, J.E. (2003) Proteolysis of insulin-like growth factor binding proteins -4 and -5 in bovine follicular fluid: implications for ovarian follicular selection and dominance. Endocrinology 144, 2977–87.CrossRefGoogle ScholarPubMed
Rizk, B. (Ed.). 2008 Ultrasonography in reproductive medicine and infertilityCambridge: United Kingdom, Cambridge University Press (in press).Google Scholar
Rolaki, A., Drakakis, P., Millingos, S., Loutradis, D. and Makrigiannakis, A. (2005) Novel trends in follicular development, atresia and corpus luteum regression: a role for apoptosis. Reprod. Biomed. Online 11, 93–103.CrossRefGoogle ScholarPubMed
Roy, S.K., Wang, S.C. and Greenwald, G.S. (1987) Radioreceptor and autoradiographic analysis of FSH, hCG and prolactin binding sites in primary to antral hamster follicles during the periovulatory period. J. Reprod. Fertil. 79, 307–13.CrossRefGoogle ScholarPubMed
Salha, O. and Balen, A.H. (2000) New concepts in superovulation strategies for assisted conception treatments. Curr. Opin. Obstet. Gynecol. 12, 201–6.CrossRefGoogle ScholarPubMed
Sasson, R. and Amsterdam, A. (2002) Stimulation of apoptosis in human granulosa cells from in vitro fertilization patients and its prevention by dexamethasone: involvement of cell contact and bcl-2 expression. J. Clin. Endocrinol. Metab. 87, 3441–51.CrossRefGoogle ScholarPubMed
Schipper, I., Hop, W.C. and Fauser, B.C. (1998) The follicle-stimulating hormone (FSH) threshold/window concept examined by different interventions with exogenous FSH during the follicular phase of the normal menstrual cycle: duration, rather than magnitude, of FSH increase affects follicle development. J. Clin. Endocrinol. Metab. 83, 1292–8.Google ScholarPubMed
Schoot, D.C., Coelingh Bennink, H.J., Mannaerts, B.M., Lamberts, S.W., Bouchard, P. and Fauser, B.C. (1992) Human recombinant follicle-stimulating hormone induces growth of preovulatory follicles without concomitant increase in androgen and estrogen biosynthesis in a woman with isolated gonadotropin deficiency. J. Clin. Endocrinol. Metab. 74, 1471–3.Google Scholar
Scobie, G.A., Macpherson, S., Millar, M.R., Groome, N.P., Romana, P.G. and Saunders, P.T. (2002) Human oestrogen receptors: differential expression of ER alpha and beta and the identification of ER beta variants. Steroids 67, 985–92.CrossRefGoogle ScholarPubMed
Smyth, C.D., Miro, F., Whitelaw, P.F., Howles, C.M. and Hillier, S.G. (1993) Ovarian thecal/interstitial androgen synthesis is enhanced by a follicle-stimulating hormone-stimulated paracrine mechanism. Endocrinology 133, 1532–8.CrossRefGoogle ScholarPubMed
Spicer, L.J. (2004) Proteolytic degradation of insulin-like growth factor binding proteins by ovarian follicles: a control mechanism for selection of dominant follicles. Biol. Reprod. 70, 1223–30.CrossRefGoogle ScholarPubMed
Sullivan, M.W., Stewart-Akers, A., Krasnow, J.S., Berga, S.L. and Zeleznik, A.J. (1999) Ovarian responses in women to recombinant follicle-stimulating hormone and luteinizing hormone (LH): a role for LH in the final stages of follicular maturation. J. Clin. Endocrinol. Metab. 84, 228–32.Google ScholarPubMed
Templeton, A., Messinis, I.E. and Baird, D.T. (1986) Characteristics of ovarian follicles in spontaneous and stimulated cycles in which there was an endogenous luteinizing hormone surge. Fertil. Steril. 46, 1113–17.CrossRefGoogle ScholarPubMed
Tetsuka, M. and Hillier, S.G. (1996) Androgen receptor gene expression in rat granulosa cells: the role of follicle-stimulating hormone and steroid hormones. Endocrinology 137, 4392–7.CrossRefGoogle ScholarPubMed
Tetsuka, M., Whitelaw, P.F., Bremner, W.J., Millar, M.R., Smyth, C.D. and Hillier, S.G. (1995) Developmental regulation of androgen receptor in rat ovary. J. Endocrinol. 145, 535–43.CrossRefGoogle ScholarPubMed
Touraine, P., Beau, I., Gougeon, A., Meduri, G., Desroches, A., Pichard, C., Detoeuf, M., Paniel, B., Prieur, M., Zorn, J.R., Milgrom, E., Kuttenn, F. and Misrahi, M. (1999) New natural inactivating mutations of the follicle-stimulating hormone receptor: correlations between receptor function and phenotype. Mol. Endocrinol. 13, 1844–54.CrossRefGoogle ScholarPubMed
Dessel, H.J., Schipper, I., Pache, T.D., Geldorp, H., Jong, F.H. and Fauser, B.C. (1996a) Normal human follicle development: an evaluation of correlations with oestradiol, androstenedione and progesterone levels in individual follicles. Clin. Endocrinol. (Oxf). 44, 191–8.CrossRefGoogle ScholarPubMed
Dessel, H.J., Chandrasekher, Y., Yap, O.W., Lee, P.D., Hintz, R.L., Faessen, G.H., Braat, D.D., Fauser, B.C. and Giudice, L.C. (1996b) Serum and follicular fluid levels of insulin-like growth factor I (IGF-I), IGF-II, and IGF-binding protein-1 and -3 during the normal menstrual cycle. J. Clin. Endocrinol. Metab. 81, 1224–31.Google Scholar
Santbrink, E.J., Hop, W.C., Dessel, T.J., Jong, F.H. and Fauser, B.C. (1995) Decremental follicle-stimulating hormone and dominant follicle development during the normal menstrual cycle. Fertil. Steril. 64, 37–43.Google ScholarPubMed
Wezel, I.L. and Rodgers, R.J. (1996) Morphological characterization of bovine primordial follicles and their environment in vivo. Biol. Reprod. 55, 1003–11.CrossRefGoogle ScholarPubMed
Visser, J.A. and Themmen, A.P. (2005) Anti-Mullerian hormone and folliculogenesis. Mol. Cell. Endocrinol. 234, 81–6.CrossRefGoogle ScholarPubMed
Vitt, U.A., Hayashi, M., Klein, C. and Hsueh, A.J. (2000) Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol. Reprod. 62, 370–7.CrossRefGoogle ScholarPubMed
Wang, H.S. and Chard, T. (1999) IGFs and IGF-binding proteins in the regulation of human ovarian and endometrial function. J. Endocrinol. 161, 1–13.CrossRefGoogle ScholarPubMed
Wang, X.N. and Greenwald, G.S. (1993) Synergistic effects of steroids with FSH on folliculogenesis, steroidogenesis and FSH- and hCG-receptors in hypophysectomized mice. J. Reprod. Fertil. 99, 403–13.CrossRefGoogle ScholarPubMed
Westergaard, L., McNatty, K.P. and Christensen, I.J. (1985) Steroid concentrations in fluid from human ovarian antral follicles during pregnancy. J. Endocrinol. 107, 133–6.CrossRefGoogle ScholarPubMed
Westergaard, L., Christensen, I.J. and McNatty, K.P. (1986) Steroid levels in ovarian follicular fluid related to follicle size and health status during the normal menstrual cycle in women. Hum. Reprod. 1, 227–32.CrossRefGoogle ScholarPubMed
Whitelaw, P.F., Smyth, C.D., Howles, C.M. and Hillier, S.G. (1992) Cell-specific expression of aromatase and LH receptor mRNAs in rat ovary. J. Mol. Endocrinol. 9, 309–12.CrossRefGoogle ScholarPubMed
Whitman, G.F., Boldt, J.P., Martinez, J.E. and Pantazis, C.G. (1991) Flow cytometric analysis of induced human graafian follicles. I. Demonstration and sorting of two luteinized cell populations. Fertil. Steril. 56, 259–64.CrossRefGoogle ScholarPubMed
Wide, L. (1982) Male and female forms of human follicle-stimulating hormone in serum. J. Clin. Endocrinol. Metab. 55, 682–8.CrossRefGoogle ScholarPubMed
Willis, D.S., Watson, H., Mason, H.D., Galea, R., Brincat, M. and Franks, S. (1998) Premature response to luteinizing hormone of granulosa cells from anovulatory women with polycystic ovary syndrome: relevance to mechanism of anovulation. J. Clin. Endocrinol. Metab. 83, 3984–91.Google ScholarPubMed
Yong, E.L., Baird, D.T., Yates, R., Reichert, L.E. Jr. and Hillier, S.G. (1992) Hormonal regulation of the growth and steroidogenic function of human granulosa cells. J. Clin. Endocrinol. Metab. 74, 842–9.CrossRefGoogle ScholarPubMed
Zeleznik, A.J. (1981) Premature elevation of systemic estradiol reduces serum levels of follicle-stimulating hormone and lengthens the follicular phase of the menstrual cycle in rhesus monkeys. Endocrinology 109, 352–5.CrossRefGoogle ScholarPubMed
Zeleznik, A.J. (2001) Follicle selection in primates: “many are called but few are chosen”. Biol. Reprod. 65, 655–9.CrossRefGoogle ScholarPubMed
Zeleznik, A.J. (2004) The physiology of follicle selection. Reprod. Biol. Endocrinol. 2, 31.CrossRefGoogle ScholarPubMed
Zeleznik, A.J. and Hillier, S.G. (1984) The role of gonadotropins in the selection of the preovulatory follicle. Clin. Obstet. Gynecol. 27, 927–40.CrossRefGoogle ScholarPubMed
Zeleznik, A.J. and Kubik, C.J. (1986) Ovarian responses in macaques to pulsatile infusion of follicle-stimulating hormone (FSH) and luteinizing hormone: increased sensitivity of the maturing follicle to FSH. Endocrinology 119, 2025–32.CrossRefGoogle Scholar
Zeleznik, A.J., Hutchinson, J.S. and Schuler, H.M. (1987) Passive immunization with anti-oestradiol antibodies during the luteal phase of the menstrual cycle potentiates the perimenstrual rise in serum gonadotrophin concentrations and stimulates follicular growth in the cynomolgus monkey (Macaca fascicularis). J. Reprod. Fertil. 80, 403–10.CrossRefGoogle Scholar
Zhou, J. and Bondy, C. (1993) Anatomy of the human ovarian insulin-like growth factor system. Biol. Reprod. 48, 467–82.CrossRefGoogle ScholarPubMed
Zimmermann, R.C., Hartman, T., Kavic, S., Pauli, S.A., Bohlen, P., Sauer, M.V. and Kitajewski, J. (2003) Vascular endothelial growth factor receptor 2-mediated angiogenesis is essential for gonadotropin-dependent follicle development. J. Clin. Invest. 112, 659–69.CrossRefGoogle ScholarPubMed
Zoller, L.C. and Weisz, J. (1979) A quantitative cytochemical study of glucose-6-phosphate dehydrogenase and delta 5-3 beta-hydroxysteroid dehydrogenase activity in the membrana granulosa of the ovulable type of follicle of the rat. Histochemistry 62, 125–35.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×