From Primary Follicle to Ovulation
Abstract
Folliculogenesis is a very complex process not clearly understood yet. Contributions of many hormones, growth factors, regulatory proteins and different types of cells make this process more confusing. However, important milestones of understanding female reproductive life are hidden in this process. Investigations on this issue may yield important data which may enable us to improve assisted reproduction techniques or prevent/treat ovarian failure.
We aimed to summarize new aspects of this issue and proposed new hypotheses in the light of recent literature.
References
Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005;5:461-71.
Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL. et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008;5863:611-3.
De Baere E, Beysen D, Oley C, Lorenz B, Cocquet J, De Sutter P, Devriendt K, Dixon M, Fellous M, Fryns JP. et al. FOXL2 and BPES: mutational hotspots, phenotypic variability, and revision of the genotype-phenotype correlation. Am J Hum Genet 2003;2:478-87.
Oktem O, Oktay K. The ovary: anatomy and function throughout human life. Ann NY Acad Sci 2008;1127:1-9.
Oktay K, Newton H, Mullan J, Gosden RG. Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone. Hum Reprod 1998; 13:1133-8.
Schipper I, Hop WC, Frauser BC. The follicle stimulating hormone (FSH) treshold/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 1998;83:1292-8.
Rankin T, Familari M, Lee E, Ginsberg A, Dwyer N, Blanchette-Mackie J, Drago J, Westphal H, Dean J. Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development 1996;9:2903-10.
Ackert CL, Gittens JE, O’Brien MJ,Eppig JJ, Kidder GM. Intercelluler communication via connexin43 gap junction is required for ovarian folliculogenesis in the mouse. Dev Biol 2001;233:258-70.
Granot I, Dekel N. Developmental expression and regulation of the gap junction protein and transcription in rat ovaries. Mol reprod Dev 1997;47:231-9.
Khan-Dawood FS. Oxytocin in intercellular communication in the corpus luteum. Seminars Reprod Endocrinol 1998;15:395-407.
O’Brien MJ, Pendola JK, Eppig JJ. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod 2003;5:1682-6.
Oktay K, Briggs D, Gosden RG. Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab 1997;11:3748-51.
Lee WS, Otsuka F, Moore RK, Shimasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod 2001; 4:994-9.
Nilsson EE, Skinner MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod 2003;4:1265-72.
Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996;6600:531-5.
Carabatsos MJ, Elvin J, Matzuk MM, Albertini DF. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol 1998;2:373-84.
Nilsson EE, Kezele P, Skinner MK. Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol Cell Endocrinol 2002;188:65-73.
Nilsson EE, Skinner MK. Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Mol Cell Endocrinol 2004;214:19-25.
Nilsson EE, Skinner MK.Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol Reprod 2002;67:1018-24.
Kezele PR, Nilsson EE, Skinner MK. Insulin but not insulin-like growth factor-1 promotes the primordial to primary follicle transition. Mol Cell Endocrinol 2002;192:37–43.
Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 2004;5687:1157-9.
John GB, Gallardo TD, Shirley LJ, Castrillon DH. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 2008;1:197–204.
Hall JE. Neuroendocrine control of the menstrual cycle. In: Strauss JF III, Barbieri RL, editors. Yen and Jaffe’s Reproductive Endocrinology: Physiology, Pathophysiology, and Clinical Management. 5th ed. Philadelphia: Elsevier Saunders; 2004.
Hodges CA, Ilagan Ajennings D, et al. Experimental evidence that changes in oocyte growth influence meiotic chromosome segregation. Hum Reprod 2022;17: 1171-80.
Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006;2:191-206.
Goldenberg RL, Powell RD, Rosen SW, Marshall JR, Ross GT. Ovarian morphology in women with anosmia and hypogonadotropic hypogonadism. Am J Obstet Gynecol 1976;1:91-4.
McGee E, Spears N, Minami S, Hsu SY, Chun SY, Billig H, Hsueh AJ. 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 1997;6:2417-24
Oktem O, Urman B. Understanding follicle growth in vivo. Hum Reprod 2010;25:2944-54.
Shimasaki S, Zachow RJ, Li D, Kim H, Iemura S, Ueno N, Sampath K, Chang RJ, Erickson GF. A functional bone morphogenetic protein system in the ovary. Proc Natl Acad Sci USA 1999;13:7282-7.
Kezele P, Nilsson EE, Skinner MK. Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol Reprod 2005;5:967-73.
Mc Natty KP, Makris A, DeGrazia C, Osathanondh R, Ryan KJ. The production of progesterone, androgens, and estrogens by granulosa cells, thecal tissue, and stromal tissue from human ovaries in vitro. J Clin Endocrinol Metab 1979;49:687-99.
Speroff L, Fritz MA. Klinik Jinekolojik Endokrinoloji ve İnfertilite. Erk A, Günalp S (Çeviri Editörleri). 7. baskı, Ankara: Güneş Tıp Kitabevi, 2007.
Hild-Petito S, West NB, Brenner RM, Stouffer RL. Localization of androgen receptor in the follicle and corpus luteum of the primate ovary during the menstruel cycle. Biol Reprod 1991;44:561-8.
McNatty KP, Makris A, Reinhold VN, DeGrazia C, Osahanondh R, Ryan KJ. Meatbolism of androstenedione by human ovarian tissues in vitro with particular reference to reductase and aromatase activity. Steroids 1979;34: 429-43.
Visser JA, Themmen AP. Anti-Mullerian hormone and folliculogenesis. Mol Cell Endocrinol 2005;234:81-6.
Rajpert-De Meyts E, Jorgensen N, Graem N, Muller J, Cate RL, Skakkebaek NE. Expression of anti-Mullerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab 1999;10:3836-44.
de Vet A, Laven JS, de Jong FH, Themmen AP, Fauser BC. Antimullerian hormone serum levels: a putative marker for ovarian aging. Fertil Steril 2002;2:357-62.
Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 1999;12:5789-96.
Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, Nachtigal MW, Uilenbroek JT, Grootegoed JA, Themmen AP. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002;3:1076-84.
van Rooij IA, Broekmans FJ, te Velde ER, Fauser BC, Bancsi LF, de Jong FH, Themmen AP. Serum anti-Mullerian hormone levels: a novel measure of ovarian reserve. Hum Reprod 2002;12:3065-71.
Baerwald AR, Adams GP, Pierson RA. Characterization of ovarian follicular wave dynamics in women. Biol Reprod 2003;3:1023-31.
Westergaard L, Christensen Ij, McNatty KP. Steroid levels in ovarian follicular fluid related to follicle size and health status during the normal menstrual cycle in women. Hum Reprod 1986;1:227-32.
European recombinant Human LH Study Group. recombinant Human LH to support Recombinant FSH-induced follicular development in LH- and FSH- deficient anovulatory woman: a dose finding study. J Clin Endocrinol Metab 1998;83: 1507-14.
McNatty KP, Makris A, DeGraziak C, Osahanondh R, Ryan KJ. Steroidogenesis by recombined follicular cells from the human ovary in vitro. J Clin Endocrinol Metab 1980;51: 1286-92.
Hsueh AJ, Dahl KD, Vaughan J, Tucker E, Rivier J, Bardin CW, Vale W. Heterodimers and homodimers of inhibin subunits have different paracrine action in the modulation of luteinizing hormone-stimulated androgen biosynthesis. Proc Natl Acad Sci USA 1987;14:5082-6.
Matzuk MM, Kumar TR, Bradley A. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 1995; 6520:356-60.
Guo Q, Kumar TR, Woodruff T, Hadsell LA, DeMayo FJ, Matzuk MM. Overexpression of mouse follistatin causes reproductive defects in transgenic mice. Mol Endocrinol 1998;1:96-106.
Yamoto M, Minami S, Nakano R, Kobayashi M. Immunohistochemical localization of inhibin/activin subunits in human ovarian follicles during the menstrual cycle. J Clin Endocrinol Metab 1992;5:989-93.