Skip to main content Accessibility help
  • Cited by 1
  • Print publication year: 2013
  • Online publication date: August 2013

Chapter 1 - The normal human ovary part I: reproductive and endocrine functions

Related content

Powered by UNSILO


1. Fritz MA, Speroff L. Clinical Gynecologic Endocrinology and Infertility. 8th edition. Philadelphia: Lippincott, Williams and Wilkins; 2011.
2. Oktem O, Urman B. Understanding follicle growth in vivo. Hum Reprod. 2010;25(12):2944–54.
3. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev. 2000;21(2):200–14.
4. Richards JS, Pangas SA. The ovary: basic biology and clinical implications. J Clin Invest. 2010;120(4):963–72.
5. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction. 2006;132(2):191–206.
6. Mais V, Kazer RR, Cetel NS, et al. The dependency of folliculogenesis and corpus luteum function on pulsatile gonadotropin secretion in cycling women using a gonadotropin-releasing hormone antagonist as a probe. J Clin Endocrinol Metab. 1986;62(6):1250–5.
7. Trombly DJ, Woodruff TK, Mayo KE. Roles for transforming growth factor beta superfamily proteins in early folliculogenesis. Semin Reprod Med. 2009;27(1):14–23.
8. Visser JA, Themmen AP. Anti-Müllerian hormone and folliculogenesis. Mol Cell Endocrinol. 2005;234(1–2):81–6.
9. van Rooij IA, Broekmans FJ, Scheffer GJ, et al. Serum antimullerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: a longitudinal study. Fertil Steril. 2005;83(4):979–87.
10. Pangas SA, Jorgez CJ, Tran M, et al. Intraovarian activins are required for female fertility. Mol Endocrinol. 2007;21(10):2458–71.
11. Zhao J, Taverne MA, van der Weijden GC, et al. Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II. Biol Reprod. 2001;65(3):967–77.
12. Smitz J, Cortvrindt R. Inhibin A and B secretion in mouse preantral follicle culture. Hum Reprod. 1998;13(4):927–35.
13. Alak BM, Coskun S, Friedman CI, et al. Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertil Steril. 1998;70(6):1126–30.
14. Giudice LC. Insulin-like growth factors and ovarian follicular development. Endo Rev. 1992;13:641–69.
15. el-Roely A, Chen X, Roberts VJ, et al. 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. 1993;77(5):1411–18.
16. Dor J, Ben-Shlomo I, Lunenfeld B, et al. Insulin-like growth factor-I (IGF-I) may not be essential for ovarian follicular development: evidence from IGF-I deficiency. J Clin Endocrinol Metab. 1992;74(3):539–42.
17. Palter SF, Tavares AB, Hourvitz A, Veldhuis JD, Adashi AY. Are estrogens of import to primate/human ovarian folliculogenesis? Endocr Rev. 2001;22:389–424.
18. Fowler PA, Anderson RA, Saunders PT, et al. Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary. J Clin Endocrinol Metab. 2011;96:1754–62.
19. Ben-Chetrit A, Gotlieb L, Wong PY, et al. Ovarian response to recombinant human follicle-stimulating hormone in luteinizing hormone-depleted women: examination of the two cell, two gonadotropin theory. Fertil Steril. 1996;65(4):711–17.
20. Karnitis VJ, Townson DH, Friedman CI, et al. Recombinant human follicle-stimulating hormone stimulates multiple follicular growth, but minimal estrogen production in gonadotropin-releasing hormone antagonist-treated monkeys: examining the role of luteinizing hormone in follicular development and steroidogenesis. J Clin Endocrinol Metab. 1994;79(1):91–7.
21. Rabinovici J, Blankstein J, Goldman B, et al. 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. 1989;68(3):693–7.
22. Robker RL, Akison LK, Russell DL. Control of oocyte release by progesterone receptor-regulated gene expression. Nucl Recept Signal. 2009;7:e012.
23. Tena-Sempere M. Kisspeptin signaling in the brain: recent developments and future challenges. Mol Cell Endocrinol. 2010;314(2):164–9.
24. Roa J, Aguilar E, Dieguez C, et al. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front Neuroendocrinol. 2008;29(1):48–69.
25. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev. 2009;30(6):713–43.
26. Roa J, Castellano JM, Navarro VM, et al. Kisspeptins and the control of gonadotropin secretion in male and female rodents. Peptides. 2009;30(1):57–66.
27. Whitlock KE. Origin and development of GnRH neurons. Trends Endocrinol Metab. 2005;16(4):145–51.
28. Marshall JC, Dalkin AC, Haisenleder DJ, et al. Gonadotropin-releasing hormone pulses: regulators of gonadotropin synthesis and ovulatory cycles. Recent Prog Horm Res. 1991;47:155–87.
29. Filicori M, Santoro N, Merriam GR, et al. Characterization of the physiological pattern of episodic gonadotropin secretion throughout the human menstrual cycle. J Clin Endocrinol Metab. 1986;62(6):1136–44.
30. Ottowitz WE, Dougherty DD, Fischman AJ, et al. [18F]2-fluoro-2-deoxy-D-glucose positron emission tomography demonstration of estrogen negative and positive feedback on luteinizing hormone secretion in women. J Clin Endocrinol Metab. 2008;93(8):3208–14.
31. Chappel SC, Resko JA, Norman RL, et al. Studies in rhesus monkeys on the site where estrogen inhibits gonadotropins: delivery of 17 beta-estradiol to the hypothalamus and pituitary gland. J Clin Endocrinol Metab. 1981;52(1):1–8.
32. Wildt L, Hutchison JS, Marshall G, et al. On the site of action of progesterone in the blockade of the estradiol-induced gonadotropin discharge in the rhesus monkey. Endocrinology. 1981;109(4):1293–4.
33. Wetsel WC, Valença MM, Merchenthaler I, et al. Intrinsic pulsatile secretory activity of immortalized luteinizing hormone-releasing hormone-secreting neurons. Proc Natl Acad Sci U S A. 1992;89(9):4149–53.
34. Winters SJ, Moore JP. Paracrine control of gonadotrophs. Semin Reprod Med. 2007;25(5):379–87.
35. Richards JS, Fitzpatrick SL, Clemens JW, et al. Ovarian cell differentiation: a cascade of multiple hormones, cellular signals, and regulated genes. Recent Prog Horm Res. 1995;50:223–54.
36. Deroo BJ, Rodriguez KF, Couse JF, et al. Estrogen receptor beta is required for optimal cAMP production in mouse granulosa cells. Mol Endocrinol. 2009;23(7):955–65.
37. Parakh TN, Hernandez JA, Grammer JC, et al. Follicle-stimulating hormone/cAMP regulation of aromatase gene expression requires beta-catenin. Proc Natl Acad Sci USA. 2006;103(33):12435–40.
38. Van Wagenen G, Simpson ME. Embryology of the Ovary and Testes in “Homo sapiens and Macaca mulatta.” New Haven, CN: Yale University Press; 1965.
39. Tomizuka K, Horikoshi K, Kitada R, et al. R-spondin1 plays an essential role in ovarian development through positively regulating Wnt-4 signaling. Hum Mol Genet. 2008;17(9):1278–91.
40. Ottolenghi C, Pelosi E, Tran J, et al. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet. 2007;16(23):2795–804.
41. Ying Y, Qi X, Zhao GQ. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci USA. 2001;98(14):7858–62.
42. Ohinata Y, Ohta H, Shigeta M, et al. A signaling principle for the specification of the germ cell lineage in mice. Cell. 2009;137(3):571–84.
43. Saitou M, Barton SC, Surani MA. A molecular programme for the specification of germ cell fate in mice. Nature. 2002;418(6895):293–300.
44. Thomas FH, Vanderhyden BC. Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod Biol Endocrinol. 2006;4:19.
45. Baker TG. A quantitative and cytological study of germ cells in human ovaries. Proc R Soc Lond B Biol Sci. 1963;158:417–33.
46. De Pol A, Vaccina F, Forabosco A, et al. Apoptosis of germ cells during human prenatal oogenesis. Hum Reprod. 1997;12(10):2235–41.
47. Pangas SA, Rajkovic A. Transcriptional regulation of early oogenesis: in search of masters. Hum Reprod Update. 2006;12(1):65–76.
48. Maheshwari A, Fowler PA. Primordial follicular assembly in humans – revisited. Zygote. 2008;16(4):285–96.
49. Baltus AE, Menke DB, Hu YC, et al. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet. 2006;38(12):1430–4.
50. Kezele P, Nilsson E, Skinner MK. Cell–cell interactions in primordial follicle assembly and development. Front Biosci. 2002;7:d1990–6.
51. Fortune JE, Cushman RA, Wahl CM, et al. The primordial to primary follicle transition. Mol Cell Endocrinol. 2000;163(1–2):53–60.
52. Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update. 2005;11(5):461–71.
53. Reddy P, Zheng W, Liu K. Mechanisms maintaining the dormancy and survival of mammalian primordial follicles. Trends Endocrinol Metab. 2010;21(2):96–103.
54. Hansen KR, Knowlton NS, Thyer AC, et al. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod. 2008;23(3):699–708.
55. John GB, Gallardo TD, Shirley LJ, et al. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol. 2008;321(1):197–204.
56. Reddy P, Adhikari D, Zheng W, et al. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum Mol Genet. 2009;18(15):2813–24.
57. Cantley LC. The phosphoinositide 3-kinase pathway. Science. 2002;296(5573):1655–7.
58. Engelman JA, Luo J, Cantley LC. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet. 2006;7(8):606–19.
59. Vanhaesebroeck B, Ali K, Bilancio A, et al. Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem Sci. 2005;30(4):194–204.
60. Oktem O, Oktay K. The ovary: anatomy and function throughout human life. Ann N Y Acad Sci. 2008;1127:1–9.
61. Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update. 2005;11(5):461–71.
62. Gougeon A, Ecochard R, Thalabard JC. Age-related changes of the population of human ovarian follicles: increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biol Reprod. 1994;50(3):653–63.
63. Baker TG, Scrimgeour JB. Development of the gonad in normal and anencephalic human fetuses. J Reprod Fertil. 1980;60(1):193–9.
64. Halpin DM, Jones A, Fink G, Charlton HM. Postnatal ovarian follicle development in hypogonadal (hpg) and normal mice and associated changes in the hypothalamic-pituitary axis. J Reprod Fertil. 1986;77:287–96.
65. Shimasaki S, Moore RK, Otsuka F, et al. The bone morphogenetic protein system in mammalian reproduction. Endocr Rev. 2004;25(1):72–101.
66. Nilsson EE, Skinner MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod. 2003;69(4):1265–72.
67. Hreinsson JG, Scott JE, Rasmussen C, et al. Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J Clin Endocrinol Metab. 2002;87(1):316–21.
68. Hanrahan JP, Gregan SM, Mulsant P, et al. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod. 2004;70(4):900–9.
69. Salmon NA, Handyside AH, Joyce IM. Oocyte regulation of anti-Müllerian hormone expression in granulosa cells during ovarian follicle development in mice. Dev Biol. 2004;266(1):201–8.
70. Parrott JA, Skinner MK. Thecal cell–granulosa cell interactions involve a positive feedback loop among keratinocyte growth factor, hepatocyte growth factor, and Kit ligand during ovarian follicular development. Endocrinology. 1998;139(5):2240–5.
71. 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(3):1018–24.
72. 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(1–2):19–25.
73. Zou K, Yuan Z, Yang Z, et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol. 2009;11(5):631–6.
74. Woods DC, Tilly JL. The next (re)generation of ovarian biology and fertility in women: is current science tomorrow’s practice? Fertil Steril. 2012;98(1):3–10.
75. Findlay JK, Drummond AE, Dyson ML, et al. Recruitment and development of the follicle; the roles of the transforming growth factor-beta superfamily. Mol Cell Endocrinol. 2002;191(1):35–43.
76. Juengel JL, McNatty KP. The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum Reprod Update. 2005;11(2):143–60.
77. Visser JA, Themmen AP. Anti-Müllerian hormone and folliculogenesis. Mol Cell Endocrinol. 2005;234(1–2):81–6.
78. Goldenberg RL, Powell RD, Rosen SW, et al. Ovarian morphology in women with anosmia and hypogonadotropic hypogonadism. Am J Obstet Gynecol. 1976;126(1):91–4.
79. Oktay K, Briggs D, Gosden RG. Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab. 1997;82(11):3748–51.
80. Nakai Y, Plant TM, Hess DL, et al. On the sites of the negative and positive feedback actions of estradiol in the control of gonadotropin secretion in the rhesus monkey. Endocrinology. 1978;102(4):1008–14.
81. Marshall JC, Dalkin AC, Haisenleder DJ, et al. Gonadotropin-releasing hormone pulses: regulators of gonadotropin synthesis and ovulatory cycles. Recent Prog Horm Res. 1991;47:155–87.
82. Mais V, Kazer RR, Cetel NS, et al. The dependency of folliculogenesis and corpus luteum function on pulsatile gonadotropin secretion in cycling women using a gonadotropin-releasing hormone antagonist as a probe. J Clin Endocrinol Metab. 1986;62(6):1250–5.
83. Yen SS, Lein A. The apparent paradox of the negative and positive feedback control system on gonadotropin secretion. Am J Obstet Gynecol. 1976;126(7):942–54.
84. Hoff JD, Quigley ME, Yen SS. Hormonal dynamics at midcycle: a reevaluation. J Clin Endocrinol Metab. 1983;57(4):792–6.
85. Ferin M, Rosenblatt H, Carmel PW, et al. Estrogen-induced gonadotropin surges in female rhesus monkeys after pituitary stalk section. Endocrinology. 1979;104(1):50–2.
86. Herbison, AE. Multimodel influence of estrogen upon gonadotropin-re;easing neurons. Endocr Rev. 1998;19:302–38.
87. Hrabovszky E, Shughrue PJ, Merchenthaler I, et al. Detection of estrogen receptor-β messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology. 2000;141:3506–9.
88. Abraham IM, Han S-K, Todman MG, Kroach KS, Herbison AE. Estrogen receptor β mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci. 2003;23(13):5771–7.
89. Radovick S, Ticknor CM, Nakayama Y, et al. Evidence for direct estrogen regulation of the human gonadotropin-releasing hormone gene. Clin Invest. 1991;88:1649–55.
90. Urban RJ, Veldhuis JD, Dufau ML. Estrogen regulates the gonadotropin-releasing hormone-stimulated secretion of biologically active luteinizing hormone. J Clin Endocrinol Metab. 1991;72(3):660–8.
91. Evans NP, Dahl GE, Mauger D, Karsch FJ. Estradiol induces both qualitative and quantitative changes in the pattern of gonadotropin-releasing hormone secretion during the presurge period in the ewe. Endocrinology. 1995;136:1603–9.
92. Liu JH, Yen SS. Induction of midcycle gonadotropin surge by ovarian steroids in women: a critical evaluation. J Clin Endocrinol Metab. 1983;57(4):797–802.
93. Waring DW, Turgeon JL. A pathway for luteinizing hormone releasing-hormone self-potentiation: cross-talk with the progesterone receptor. Endocrinology. 1992;130:3275–82.
94. Wildt L, Hutchison JS, Marshall G, et al. On the site of action of progesterone in the blockade of the estradiol-induced gonadotropin discharge in the rhesus monkey. Endocrinology. 1981;109(4):1293–4.
95. Plant TM. Hypothalamic control of the pituitary-gonadal axis in higher primates: key advances over the last two decades. J Neuroendocrinol. 2008;20:719–26.
96. Kaplan SL, Grumbach MM, Aubert ML. The ontogenesis of pituitary hormones and hypothalamic factors in the human fetus: maturation of central nervous system regulation of anterior pituitary function. Recent Prog Horm Res. 1976;32:161–243.
97. Kaplan SL, Grumbach MM. Pituitary and placental gonadotrophins and sex steroids in the human and sub-human primate fetus. Clin Endocrinol Metab. 1978;7(3):487–511.
98. Winter JS, Hughes IA, Reyes FI, et al. Pituitary-gonadal relations in infancy: 2. Patterns of serum gonadal steroid concentrations in man from birth to two years of age. J Clin Endocrinol Metab. 1976;42(4):679–86.
99. Burger HG, Yamada Y, Bangah ML, McCloud PI, Warne GL. Serum gonadotropin, sex steroid, and immunoreactive inhibin levels in the first two years of life. J Clin Endocrinol Metab. 1991;72(3):682–6.
100. Wildt L, Marshall G, Knobil E. Experimental induction of puberty in the infantile female rhesus monkey. Science. 1980;207(4437):1373–5.
101. Conte FA, Grumbach MM, Kaplan SL. A diphasic pattern of gonadotropin secretion in patients with the syndrome of gonadal dysgenesis. J Clin Endocrinol Metab. 1975;40(4):670–4.
102. Mitsushima D, Hei DL, Terasawa E. Gamma-aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc Natl Acad Sci USA. 1994;91(1):395–9.
103. Mitsushima D, Marzban F, Luchansky LL, et al. Role of glutamic acid decarboxylase in the prepubertal inhibition of the luteinizing hormone-releasing hormone release in female rhesus monkeys. J Neurosci. 1996;16(8):2563–73.
104. Pau KY, Berria M, Hess DL, et al. Hypothalamic site-dependent effects of neuropeptide Y on gonadotropin-releasing hormone secretion in rhesus macaques. J Neuroendocrinol. 1995;7(1):63–7.
105. El Majdoubi M, Sahu A, Ramaswamy S, et al. Neuropeptide Y: a hypothalamic brake restraining the onset of puberty in primates. Proc Natl Acad Sci U S A. 2000;97(11):6179–84.
106. Gore AC, Mitsushima D, Terasawa E. A possible role of neuropeptide Y in the control of the onset of puberty in female rhesus monkeys. Neuroendocrinology. 1993;58(1):23–34.
107. Braun DW. Excitatory amino acids: evidence for a role in the control of reproduction and anterior pituitary hormone secretion. Endocr Rev. 1997;18:678–700.
108. Frisch R, Revelle R. Variation in body weights and the age of the adolescent growth spurt among Latin American and Asian populations, in relation to calorie supplies. Hum Biol. 1969;41(2):185–212.
109. Frisch RE, Revelle R, Cook S. Components of weight at menarche and the initiation of the adolescent growth spurt in girls: estimated total water, lean body weight and fat. Hum Biol. 1973;45(3):469–83.
110. Roemmich JN, Rogol AD. Role of leptin during childhood growth and development. Endocrinol Metab Clin North Am. 1999;28(4):749–64.
111. Farooqi IS, Jebb SA, Langmack G, et al. Effects of recombinant leptin therapy in a child with congenital leptin deficiency. N Engl J Med. 1999;341(12):879–84.
112. Ahima RS. Body fat, leptin and hypothalamic amenorrhea. N Eng J Med. 2004;351:959–62.
113. Farooqi IS. Leptin and the onset of puberty: insights from rodent and human genetics. Semin Reprod Med. 2002;20(2):139–44.
114. Apter D, Bützow TL, Laughlin GA, et al. Gonadotropin-releasing hormone pulse generator activity during pubertal transition in girls: pulsatile and diurnal patterns of circulating gonadotropins. J Clin Endocrinol Metab. 1993;76(4):940–9.
115. Mitamura R, Yano K, Suzuki N, et al. Diurnal rhythms of luteinizing hormone, follicle-stimulating hormone, testosterone, and estradiol secretion before the onset of female puberty in short children. J Clin Endocrinol Metab. 2000;85(3):1074–80.
116. Oerter KE, Uriarte MM, Rose SR, et al. Gonadotropin secretory dynamics during puberty in normal girls and boys. J Clin Endocrinol Metab. 1990;71(5):1251–8.
117. Legro RS, Lin HM, Demers LM, et al. Rapid maturation of the reproductive axis during perimenarche independent of body composition. J Clin Endocrinol Metab. 2000;85(3):1021–5.
118. Sehested A, Juul AA, Andersson AM, et al. Serum inhibin A and inhibin B in healthy prepubertal, pubertal, and adolescent girls and adult women: relation to age, stage of puberty, menstrual cycle, follicle-stimulating hormone, luteinizing hormone, and estradiol levels. J Clin Endocrinol Metab. 2000;85(4):1634–40.
119. Andersen CY. Characteristics of human follicular fluid associated with successful conception after in vitro fertilization. J Clin Endocrinol Metab. 1993;77(5):1227–34.
120. Erickson GF, Magoffin DA, Dyer CA, et al. The ovarian androgen producing cells: a review of structure/function relationships. Endocr Rev. 1985;6(3):371–99.
121. Eppig JJ, Chesnel F, Hirao Y, et al. Oocyte control of granulosa cell development: how and why. Hum Reprod. 1997;12(11 Suppl):127–32.
122. Schipper I, Hop WC, Fauser BC. 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. 1998;83(4):1292–8.
123. Gore MA, Nayudu PL, Vlaisavljevic V. Attaining dominance in vivo: distinguishing dominant from challenger follicles in humans. Hum Reprod. 1997;12(12):2741–7.
124. Welt CK, Pagan YL, Smith PC, et al. Control of follicle-stimulating hormone by estradiol and the inhibins: critical role of estradiol at the hypothalamus during the luteal-follicular transition. J Clin Endocrinol Metab. 2003;88(4):1766–71.
125. Chikazawa K, Araki S, Tamada T. Morphological and endocrinological studies on follicular development during the human menstrual cycle. J Clin Endocrinol Metab. 1986;62(2):305–13.
126. Rivier C, Rivier J, Vale W. Inhibin-mediated feedback control of follicle-stimulating hormone secretion in the female rat. Science. 1986;234(4773):205–8.
127. Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Müllerian hormone. Reproduction. 2002;124(5):601–9.
128. Filicori M, Cognigni GE, Tabarelli C, et al. Stimulation and growth of antral ovarian follicles by selective LH activity administration in women. J Clin Endocrinol Metab. 2002;87(3):1156–61.
129. Sawetawan C, Carr BR, McGee E, et al. Inhibin and activin differentially regulate androgen production and 17 alpha-hydroxylase expression in human ovarian thecal-like tumor cells. J Endocrinol. 1996;148(2):213–21.
130. Magoffin DA. Regulation of differentiated functions in ovarian theca cells. Semin Reprod Endocrinol. 1991;9:321.
131. Lockwood GM, Muttukrishna S, Ledger WL. Inhibins and activins in human ovulation, conception and pregnancy. Hum Reprod Update. 1998;4(3):284–95.
132. Andersen CY, Byskov AG, Estradiol and regulation of anti-Müllerian hormone, inhibin-A, and inhibin-B secretion: analysis of small antral and preovulatory human follicles’ fluid. J Clin Endocrinol Metab. 2006;91:4064–9.
133. Filicori M, Cognigni GE, Ciampaglia W. Effects of LH on oocyte yield and developmental competence. Hum Reprod. 2003;18(6):1357–8; author reply 1358–60.
134. Suzuki T, Sasano H, Takaya R, et al. Cyclic changes of vasculature and vascular phenotypes in normal human ovaries. Hum Reprod. 1998;13(4):953–9.
135. Chaffkin LM, Luciano AA, Peluso JJ. Progesterone as an autocrine/paracrine regulator of human granulosa cell proliferation. J Clin Endocrinol Metab. 1992;75:1404–8.
136. Temporal relationships between ovulation and defined changes in the concentration of plasma estradiol-17 beta, luteinizing hormone, follicle-stimulating hormone, and progesterone. I. Probit analysis. World Health Organization, Task Force on Methods for the Determination of the Fertile Period, Special Programme of Research, Development and Research Training in Human Reproduction. Am J Obstet Gynecol. 1980;138(4):383–90.
137. Fritz MA, McLachlan RI, Cohen NL, et al. Onset and characteristics of the midcycle surge in bioactive and immunoactive luteinizing hormone secretion in normal women: influence of physiological variations in periovulatory ovarian steroid hormone secretion. J Clin Endocrinol Metab. 1992;75(2):489–93.
138. Fan HY, Liu Z, Shimada M, et al. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science. 2009;324(5929):938–41.
139. Liu JH, Yen SS. Induction of midcycle gonadotropin surge by ovarian steroids in women: a critical evaluation. J Clin Endocrinol Metab. 1983;57(4):797–802.
140. Collins RL, Hodgen GD. Blockade of the spontaneous midcycle gonadotropin surge in monkeys by RU 486: a progesterone antagonist or agonist? J Clin Endocrinol Metab. 1986;63(6):1270–6.
141. Peng X-R. Regulation of the fibrinolytic system during gonadotropin induction of ovulation in mice with inactivation of the genes encoding tPA, uPA or PAI-1. Fibrinolysis. 1994;8:101.
142. Jones PB, Vernon MW, Muse KN, et al. Plasminogen activator and plasminogen activator inhibitor in human preovulatory follicular fluid. J Clin Endocrinol Metab. 1989;68(6):1039–45.
143. Lösel R, Wehling M. Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol. 2003;4(1):46–56.
144. Zhu Y, Bond J, Thomas P. Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc Natl Acad Sci U S A. 2003;100(5):2237–42.
145. Mehlmann LM, Saeki Y, Tanaka S, et al. The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science. 2004;306(5703):1947–50.
146. Markosyan N, Duffy DM. Prostaglandin E2 acts via multiple receptors to regulate plasminogen-dependent proteolysis in the primate periovulatory follicle. Endocrinology. 2009;150(1):435–44.
147. Lumsden MA, Kelly RW, Templeton AA, et al. Changes in the concentration of prostaglandins in preovulatory human follicles after administration of hCG. J Reprod Fertil. 1986;77(1):119–24.
148. Wayne CM, Fan HY, Cheng X, et al. Follicle-stimulating hormone induces multiple signaling cascades: evidence that activation of Rous sarcoma oncogene, RAS, and the epidermal growth factor receptor are critical for granulosa cell differentiation. Mol Endocrinol. 2007;21(8):1940–57.
149. Gonzalez-Robayna IJ, Falender AE, Ochsner S, et al. Follicle-stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-induced kinase (Sgk): evidence for A kinase-independent signaling by FSH in granulosa cells. Mol Endocrinol. 2000;14(8):1283–300.
150. Wulff C, Dickson SE, Duncan WC, et al. Angiogenesis in the human corpus luteum: simulated early pregnancy by HCG treatment is associated with both angiogenesis and vessel stabilization. Hum Reprod. 2001;16(12):2515–24.
151. Brannian JD, Shiigi SM, Stouffer RL. Gonadotropin surge increases fluorescent-tagged low-density lipoprotein uptake by macaque granulosa cells from preovulatory follicles. Biol Reprod. 1992;47(3):355–60.
152. Lei ZM, Chegini N, Rao CV. Quantitative cell composition of human and bovine corpora lutea from various reproductive states. Biol Reprod. 1991;44(6):1148–56.
153. Maas S, Jarry H, Teichmann A, et al. Paracrine actions of oxytocin, prostaglandin F2 alpha, and estradiol within the human corpus luteum. J Clin Endocrinol Metab. 1992;74(2):306–12.
154. Hutchison JS, Zeleznik AJ. The rhesus monkey corpus luteum is dependent on pituitary gonadotropin secretion throughout the luteal phase of the menstrual cycle. Endocrinology. 1984;115(5):1780–6.
155. Fraser HM, Lunn SF, Morris KD, et al. Initiation of high dose gonadotrophin-releasing hormone antagonist treatment during the late follicular phase in the macaque abolishes luteal function irrespective of effects upon the luteinizing hormone surge. Hum Reprod. 1997;12(3):430–5.
156. Auletta FJ, Flint AP. Mechanisms controlling corpus luteum function in sheep, cows, nonhuman primates, and women especially in relation to the time of luteolysis. Endocr Rev. 1988;9(1):88–105.
157. Lenton EA, Landgren BM, Sexton L, et al. Normal variation in the length of the follicular phase of the menstrual cycle: effect of chronological age. Br J Obstet Gynaecol. 1984;91(7):681–4.
158. McCracken JA, Custer EE, Lamsa JC. Luteolysis: a neuroendocrine-mediated event. Physiol Rev. 1999;79(2):263–323.
159. Duncan WC, McNeilly AS, Illingworth PJ. The effect of luteal “rescue” on the expression and localization of matrix metalloproteinases and their tissue inhibitors in the human corpus luteum. J Clin Endocrinol Metab. 1998;83(7):2470–8.
160. Vega M, Urrutia L, Iñiguez G, et al. Nitric oxide induces apoptosis in the human corpus luteum in vitro. Mol Hum Reprod. 2000;6(8):681–7.
161. Miceli F, Minici F, Garcia Pardo M, et al. Endothelins enhance prostaglandin (PGE(2) and PGF(2alpha)) biosynthesis and release by human luteal cells: evidence of a new paracrine/autocrine regulation of luteal function. J Clin Endocrinol Metab. 2001;86(2):811–17.
162. Vermesh M, Kletzky OA. Longitudinal evaluation of the luteal phase and its transition into the follicular phase. J Clin Endocrinol Metab. 1987;65(4):653–8.
163. Wunder DM, Bersinger NA, Yared M, et al. Statistically significant changes of antimüllerian hormone and inhibin levels during the physiologic menstrual cycle in reproductive age women. Fertil Steril. 2008;89(4):927–33.
164. Welt CK, Martin KA, Taylor AE, et al. Frequency modulation of follicle-stimulating hormone (FSH) during the luteal-follicular transition: evidence for FSH control of inhibin B in normal women. J Clin Endocrinol Metab. 1997;82(8):2645–52.