Human ovarian follicular development: From activation of resting follicles to preovulatory maturation

Gougeon, A.

doi:10.1016/j.ando.2010.02.021

Cited by 257Reproductive Biology and FertilityOvarian function and disordersReproductive Physiology in Livestock

Human ovarian follicular development: From activation of resting follicles to preovulatory maturation

Gougeon, A.·2010·Annales d'Endocrinologie

DOI 10.1016/j.ando.2010.02.021

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Abstract

By integrating morphometrical and endocrinological data, as well as biological effects of various molecules synthesized by the human follicle, we propose a dynamic view of the follicle growth within the human ovary. Folliculogenesis starts with entry of resting follicles into the growth phase, a process where the kit system plays a key role. Several months are required for a new growing follicle to reach the preantral stage (0.15mm), then 70 additional days to reach the size of 2mm. Early growing follicle growth is regulated by subtle interactions between follicle-stimulating hormone (FSH) and local factors produced by theca and granulosa cells (GCs), as well as the oocyte. From the time they enter the selectable stage during the late luteal phase, follicles become sensitive to cyclic changes of FSH in terms of granulosa cell proliferation. During the early follicular phase, the early selected follicle grows very quickly and estradiol is present in the follicular fluid. However, the total steroid production remains moderate. From the mid-follicular phase, the preovulatory follicle synthesizes high quantities of estradiol, then after the mid-cycle gonadotropin surge, very large amounts of progesterone. At this stage of development, the responsiveness of the follicle to gonadotropins is maximum, especially to luteinizing hormone (LH) that triggers granulosa wall dissociation and cumulus expansion as well as oocyte nuclear maturation. Thus, as the follicle develops, its responsiveness to gonadotropins progressively increases under the control of local factors acting in an autocrine/paracrine fashion.

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FSHB encodes the beta polypeptide of FSH, a glycoprotein hormone that plays a central role in ovarian folliculogenesis.
“FSHB encodes the beta polypeptide of FSH, a glycoprotein hormone that plays a central role in ovarian folliculogenesis46.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [46]
FSH and LH play central roles in regulating follicle development in the ovary, influencing oestradiol release during the proliferative phase of the cycle and contributing to a role for estradiol in endometriosis risk.
“They both play central roles in regulating follicle development in the ovary, influencing oestradiol release during the proliferative phase of the cycle46 and contributing to a role for estradiol in endometriosis risk.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [46]

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Androgens and Progestins in the Human Ovarian Follicle: Differences in the Evolution of Preovulatory, Healthy Nonovulatory, and Atretic Follicles*
Brailly, S., Gougeon, A., Milgröm, E., Bomsel‐Helmreich, O., & Papiernik, E. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-53-1-128 · Cited by 123 · see citing works
Self-citation
Hormonal regulation of follicle-stimulating hormone receptor messenger ribonucleic acid levels in cultured rat granulosa cells.
Tilly, J. L., LaPolt, P. S., & Hsueh, A. J. W. (1992) · Endocrinology · doi:10.1210/endo.130.3.1311235 · Cited by 122 · see citing works
Platelet-derived growth factor modulates the primordial to primary follicle transition
Nilsson, E. E., Detzel, C., & Skinner, M. K. (2006) · Reproduction · doi:10.1530/rep.1.00978 · Cited by 122 · see citing works
Keratinocyte Growth Factor Acts as a Mesenchymal Factor That Promotes Ovarian Primordial to Primary Follicle Transition
Kezele, P. R., Nilsson, E. E., & Skinner, M. K. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.043117 · Cited by 121 · see citing works
Effects of epidermal growth factor and insulin-like growth factor I on the levels of mRNA encoding aromatase cytochrome P-450 of human ovarian granulosa cells
Steinkampf, M. P., Mendelson, C. R., & Simpson, E. R. (1988) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(88)90199-2 · Cited by 120 · see citing works
In Vitro Development of Growing Oocytes from Fetal Mouse Oocytes: Stage-Specific Regulation by Stem Cell Factor and Granulosa Cells
Klinger, F. G., & Felici, M. D. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0592 · Cited by 120 · see citing works
Anti-Müllerian hormone initiates growth of human primordial follicles in vitro
Schmidt, K. L. T., Kryger‐Baggesen, N., Byskov, A. G., & Andersen, C. Y. (2005) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2004.12.010 · Cited by 117 · see citing works
Evolution of the diameters of the largest healthy and atretic follicles during the human menstrual cycle
Gougeon, A., & Lefèvre, B. (1983) · Reproduction · doi:10.1530/jrf.0.0690497 · Cited by 117 · see citing works
Self-citation
Mesenchymal-epithelial interactions in the ovarian follicle involve keratinocyte and hepatocyte growth factor production by thecal cells and their action on granulosa cells
Parrott, J. A., Vigne, J. L., Chu, B. Z., & Skinner, M. K. (1994) · Endocrinology · doi:10.1210/endo.135.2.8033804 · Cited by 117 · see citing works
Importance of the IGF system in early folliculogenesis
Monget, P., & Bondy, C. A. (2000) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(99)00244-0 · Cited by 113 · see citing works
Luteinzing Hormone Activity in Menotropins Optimizes Folliculogenesis and Treatment in Controlled Ovarian Stimulation
Filicori, M., Cognigni, G. E., Taraborrelli, S., Spettoli, D., Ciampaglia, W., de Fatis, C. T., Pocognoli, P., Cantelli, B., & Boschi, S. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.1.7108 · Cited by 107 · see citing works
EGF-like factor epiregulin and amphiregulin expression is regulated by gonadotropins/cAMP in human ovarian follicular cells
Freimann, S., Ben‐Ami, I., Dantes, A., Ron‐El, R., & Amsterdam, A. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.09.129 · Cited by 103 · see citing works
Activin from Secondary Follicles Causes Small Preantral Follicles to Remain Dormant at the Resting Stage
Mizunuma, H., Liu, X., Andoh, K., Abe, Y., Kobayashi, J., 山田, 清., Yokota, H., Ibuki, Y., & Hasegawa, Y. (1999) · Endocrinology · doi:10.1210/endo.140.1.6409 · Cited by 97 · see citing works
Localization of Androgen Receptor in the Follicle and Corpus Luteum of the Primate Ovary during the Menstrual Cycle1
Hild-Petito, S. A., West, N. B., Brenner, R., & Stouffer, R. L. (1991) · Biology of Reproduction · doi:10.1095/biolreprod44.3.561 · Cited by 96 · see citing works
Hormonal regulation of early follicle development in the rat ovary
Hsueh, A. J. W., McGee, E. A., Hayashi, M., & Hsu, S. Y. (2000) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(99)00245-2 · Cited by 96 · see citing works
Growth Differentiation Factor-9 Stimulates Rat Theca-Interstitial Cell Androgen Biosynthesis1
Solovyeva, E. V., Hayashi, M., Margi, K., Barkats, C., Klein, C., Amsterdam, A., Hsueh, A. J. W., & TSAFRIRI, A. (2000) · Biology of Reproduction · doi:10.1095/biolreprod63.4.1214 · Cited by 95 · see citing works
Morphologic and functional determinants of primordial and primary follicles in the monkey ovary
Gougeon, A., & Busso, D. (2000) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(00)00220-3 · Cited by 93 · see citing works
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Pregnancy: The expression of c-kit protein in human adult and fetal tissues
Horie, K., Fujita, J., Takakura, K., Kanzaki, H., Suginami, H., Iwai, M., Nakayama, H., & Mori, T. (1993) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137967 · Cited by 92 · see citing works
Reproductive Defects in γ-Glutamyl Transpeptidase-Deficient Mice1
Kumar, T. R., Wiseman, A. L., Kala, G., Kala, S. V., Matzuk, M. M., & Lieberman, M. W. (2000) · Endocrinology · doi:10.1210/endo.141.11.7760 · Cited by 90 · see citing works
Cyclic changes in ovarian morphology during the menstrual cycle in Macaca mulatta
Koering, M. J. (1969) · American Journal of Anatomy · doi:10.1002/aja.1001260107 · Cited by 88 · see citing works
Nerve Growth Factor-Dependent Activation of trkA Receptors in the Human Ovary Results in Synthesis of Follicle-Stimulating Hormone Receptors and Estrogen Secretion
Salas, C., Julio‐Pieper, M., Valladares, M., Pommer, R., Vega, M., Mastronardi, C. A., Kerr, B., Ojeda, S. R., Lara, H. E., & Romero, C. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1925 · Cited by 85 · see citing works
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 Cells1
Magoffin, D. A., & Weitsman, S. R. (1994) · Biology of Reproduction · doi:10.1095/biolreprod51.4.766 · Cited by 85 · see citing works
Gonadotropin binding sites in human ovarian follicles and corpora lutea during the menstrual cycle.
Shima, K., Kitayama, S., & Nakano, R. (1987) · PubMed · Cited by 84 · see citing works
Oocyte Bone Morphogenetic Protein 15, but not Growth Differentiation Factor 9, Is Increased During Gonadotropin-Induced Follicular Development in the Immature Mouse and Is Associated with Cumulus Oophorus Expansion1
Guéripel, X., Brun, V., & Gougeon, A. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.106.055574 · Cited by 84 · see citing works
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Does 3D ultrasound offer any advantage in the pretreatment assessment of ovarian reserve and prediction of outcome after assisted reproduction treatment?
Jayaprakasan, K., Hilwah, N., Kendall, N. R., Hopkisson, J. F., Campbell, B. K., Johnson, I. R., & Raine‐Fenning, N. (2007) · Human Reproduction · doi:10.1093/humrep/dem104 · Cited by 84 · see citing works
Presence of NGF and its receptors in ovaries from human fetuses and adults
Abir, R., Fisch, B., Jin, S., Barnnet, M., Ben‐Haroush, A., Felz, C., Kessler‐Icekson, G., Feldberg, D., Nitke, S., & Ao, A. (2005) · Molecular Human Reproduction · doi:10.1093/molehr/gah164 · Cited by 82 · see citing works
Role of Neurotrophic Factors in Early Ovarian Development
Dissen, G. A., Garcia‐Rudaz, C., & Ojeda, S. R. (2009) · Seminars in Reproductive Medicine · doi:10.1055/s-0028-1108007 · Cited by 80 · see citing works
A Comparative Study on Transforming Growth Factor-β and Activin A for Preantral Follicles from Adult, Immature, and Diethylstilbestrol-Primed Immature Mice
Liu, X., Andoh, K., Abe, Y., Kobayashi, J., 山田, 清., Mizunuma, H., & Ibuki, Y. (1999) · Endocrinology · doi:10.1210/endo.140.6.6827 · Cited by 78 · see citing works
Interaction of Extracellular Matrix and Activin-A in the Initiation of Follicle Growth in the Mouse Ovary1
Oktay, K., Karlikaya, G., Akman, O. H., Ojakian, G. K., & Oktay, M. H. (2000) · Biology of Reproduction · doi:10.1095/biolreprod63.2.457 · Cited by 77 · see citing works
Immunolocalization of 3β-hydroxysteroid dehydrogenase in human ovary
Sasano, H., Mori, T., Sasano, N., Nagura, H., & Mason, J. I. (1990) · Reproduction · doi:10.1530/jrf.0.0890743 · Cited by 73 · see citing works
Messenger RNA expression for the follicle-stimulating hormone receptor and luteinizing hormone receptor in human oocytes and preimplantation-stage embryos
Patsoula, E., Loutradis, D., Drakakis, P., Michala, L., Bletsa, R., & Michalas, S. S. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00071-2 · Cited by 70 · see citing works
FOXL2 mutations lead to different ovarian phenotypes in BPES patients: Case Report
Méduri, G., Bachelot, A., Duflos-Cohade, C., Bständig, B., Poirot, C., Genestie, C., Veitia, R. A., Baere, E. B. W. D., & Touraine, P. A. (2009) · Human Reproduction · doi:10.1093/humrep/dep355 · Cited by 68 · see citing works
INHIBITION OF OESTRADIOL PRODUCTION BY EPIDERMAL GROWTH FACTOR IN HUMAN GRANULOSA CELLS OF NORMAL AND POLYCYSTIC OVARIES
Mason, H. D., Margara, R. A., Winston, R. M. L., Beard, R. W., Reed, M. J., & Franks, S. (1990) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1990.tb03888.x · Cited by 65 · see citing works
Paradoxical Action of Activin A on Folliculogenesis in Immature and Adult Mice
Yokota, H., 山田, 清., Liu, X., Kobayashi, J., Abe, Y., Mizunuma, H., & Ibuki, Y. (1997) · Endocrinology · doi:10.1210/endo.138.11.5526 · Cited by 65 · see citing works
Classification of small type B/C follicles as primordial follicles in mature rats
Meredith, S., Dudenhoeffer, G., & Jackson, K. S. (2000) · Reproduction · doi:10.1530/jrf.0.1190043 · Cited by 65 · see citing works
Immunohistochemical localization of pituitary gonadotrophins and gonadal steroids confirms the 'two-cell, two-gonadotrophin' hypothesis of steroidogenesis in the human ovary
Kobayashi, M., Nakano, R., & Ooshima, A. (1990) · Journal of Endocrinology · doi:10.1677/joe.0.1260483 · Cited by 64 · see citing works
Epidermal Growth Factor and Transforming Growth Factor-β Modulation of Follicle-Stimulating Hormone-Induced Deoxyribonucleic Acid Synthesis in Hamster Preantral and Early Antral Follicles1
Roy, S. K. (1993) · Biology of Reproduction · doi:10.1095/biolreprod48.3.552 · Cited by 64 · see citing works
Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses
Ben‐Haroush, A., Abir, R., Ao, A., Jin, S., Kessler‐Icekson, G., Feldberg, D., & Fisch, B. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.05.018 · Cited by 64 · see citing works
Pregnancy-Associated Plasma Protein-A Gene Expression in Human Ovaries Is Restricted to Healthy Follicles and Corpora Lutea
Hourvitz, A., Widger, A. E., Filho, F. L. T., Chang, R. J., Adashi, E. Y., & Erickson, G. F. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.12.7169 · Cited by 62 · see citing works
Follicle development during the normal menstrual cycle
Macklon, N., & Fauser, B. C. J. M. (1998) · Maturitas · doi:10.1016/s0378-5122(98)00072-3 · Cited by 62 · see citing works
Expression of c-kit ligand messenger ribonucleic acids in human ovaries and regulation of their steady state levels by gonadotropins in cultured granulosa-luteal cells
Laitinen, M. V., Rutanen, E. ‐., & Ritvos, O. (1995) · Endocrinology · doi:10.1210/endo.136.10.7545103 · Cited by 60 · see citing works
Epidermal growth factor (EGF) in human preovulatory follicles
Westergaard, L. G., & Anhdersen, C. Y. (1989) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136883 · Cited by 57 · see citing works
Progesterone as an autocrine/paracrine regulator of human granulosa cell proliferation.
Chaffkin, L. M., Luciano, A. A., & Peluso, J. J. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.75.6.1464640 · Cited by 56 · see citing works
Epidermal growth factor antagonizes ovarian theca-interstitial cytodifferentiation
Erickson, G. F., & Case, E. (1983) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(83)90031-x · Cited by 52 · see citing works
Interaction between activin A and cAMP in the induction of FSH receptor in cultured rat granulosa cells
Nakamura, M., Nakamura, K., Igarashi, S., Tano, M., Miyamoto, K., Ibuki, Y., & Minegishi, T. (1995) · Journal of Endocrinology · doi:10.1677/joe.0.1470103 · Cited by 52 · see citing works
Immunohistochemical localization of basic fibroblast growth factor (bFGF) during folliculogenesis in the human ovary
Yamamoto, S., Konishi, I., Nanbu, K., Komatsu, T., Mandai, M., Kuroda, H., Matsushita, K., & Mori, T. (1997) · Gynecological Endocrinology · doi:10.3109/09513599709152538 · Cited by 52 · see citing works
Potent Inhibition of Human Ovarian Steroidogenesis by Insulin-Like Growth Factor Binding Protein-4 (IGFBP-4)
Mason, H. D., Cwyfan-Hughes, S. C., Holly, J. M. P., & Franks, S. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.1.4630 · Cited by 51 · see citing works
Influence of human menopausal gonadotropin on the recruitment of human ovarian follicles
Gougeon, A., & Testart, J. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53944-2 · Cited by 48 · see citing works
Self-citation
Neurotrophin NT3 promotes ovarian primordial to primary follicle transition
Nilsson, E. E., Dole, G., & Skinner, M. K. (2009) · Reproduction · doi:10.1530/rep-09-0179 · Cited by 46 · see citing works
Hepatocyte growth factor and stem cell factor involvement in paracrine interplays of theca and granulosa cells in the human ovary
Ito, M., Harada, T., Tanikawa, M., Fujii, A., Shiota, G., & Terakawa, N. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01747-2 · Cited by 42 · see citing works
Classification of small type B/C follicles as primordial follicles in mature rats
Meredith, S., Dudenhoeffer, G., & Jackson, K. (2000) · Reproduction · doi:10.1530/reprod/119.1.43 · Cited by 42 · see citing works
Effect of insulin-like growth factor-I on cholesterol side-chain cleavage cytochrome P450 messenger ribonucleic acid expression in ovarian theca-interstitial cells stimulated to differentiate in vitro
Magoffin, D. A., & Weitsman, S. R. (1993) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(93)90093-y · Cited by 41 · see citing works
Fallen arches, or how the vertebrate got its head.
Fishman, M. C., & Kirby, M. L. (1998) · Journal of Clinical Investigation · doi:10.1172/jci4143 · Cited by 40 · see citing works
Hepatocyte growth factor promotes cell proliferation and inhibits progesterone secretion via PKA and MAPK pathways in a human granulosa cell line
Taniguchi, F., Harada, T., Deura, I., Iwabe, T., Tsukihara, S., & Terakawa, N. (2004) · Molecular Reproduction and Development · doi:10.1002/mrd.20076 · Cited by 39 · see citing works
Evidence for the presence of hepatocyte growth factor expression in human ovarian follicles
Osuga, Y. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.8.703 · Cited by 30 · see citing works
Somatostatin Inhibits Stem Cell Factor Messenger RNA Expression by Sertoli Cells and Stem Cell Factor-Induced DNA Synthesis in Isolated Seminiferous Tubules1
Goddard, I., Bauer, Š., Gougeon, A., Lopez, F., Giannetti, N., Susini, C., Benahmed, M., & Krantic, S. M. (2001) · Biology of Reproduction · doi:10.1095/biolreprod65.6.1732 · Cited by 26 · see citing works
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Production of transforming growth factor-alpha by normal and polycystic ovaries
Mason, H. D., Carr, L., LEAKE, R. E., & Franks, S. (1995) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.80.7.7608254 · Cited by 25 · see citing works
Steroid production in cultured thecal cells obtained from human ovarian follicles
Bergh, C., Olsson, J., Selleskog, U., & Hillensjø, T. (1993) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138087 · Cited by 25 · see citing works
Kit Ligand and the Somatostatin Receptor Antagonist, BIM-23627, Stimulate in Vitro Resting Follicle Growth in the Neonatal Mouse Ovary
Gougeon, A., Delangle, A., Arouche, N., Stridsberg, M., Gotteland, J. P., & Loumaye, E. (2010) · Endocrinology · doi:10.1210/en.2009-0762 · Cited by 22 · see citing works
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Immunological detection of the oestradiol receptor protein in cell lines derived from the lymphatic system and the haematopoietic system: variability of specific hormone binding in vitro
Jakob, F. J., Tony, H. P., Schneider, D., & Thole, H. H. (1992) · Journal of Endocrinology · doi:10.1677/joe.0.1340397 · Cited by 19 · see citing works
Inhibitory action of somatostatin-14 on hormone-stimulated cyclic adenosine monophosphate induction in porcine granulosa and luteal cells
Rajkumar, K., Kerr, D. E., Kirkwood, R. N., & Laarveld, B. (1992) · Journal of Endocrinology · doi:10.1677/joe.0.1340297 · Cited by 15 · see citing works
Steroid concentrations in fluid from human ovarian antral follicles during pregnancy
Westergaard, L. G., McNatty, K. P., & Christensen, I. J. (1985) · Journal of Endocrinology · doi:10.1677/joe.0.1070133 · Cited by 14 · see citing works
Keratinocyte growth factor and its receptor in human ovaries from fetuses, girls and women
Abir, R., Fisch, B., Zhang, X. Y., Felz, C., Kessler‐Icekson, G., Krissi, H., Nitke, S., & Ao, A. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan080 · Cited by 9 · see citing works
Steroid 3β-ol-dehydrogenase activity in the largest healthy and atretic follicles in the human ovary during the menstrual cycle
Gougeon, A., & GUILLOU, M. (1977) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:19770816 · Cited by 8 · see citing works
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Follicular atresia in relation to oocyte morphology in non-pregnant and pregnant women
Westergaard, L. G. (1985) · Reproduction · doi:10.1530/jrf.0.0740113 · Cited by 8 · see citing works
Evidence for the Presence Keratinocyte Growth Factor(KGF) in Human Ovarian Follicles.
Osuga, Y., Koga, K., Tsutsumi, O., Yano, T., Kugu, K., Momoeda, M., Okagaki, R., Suenaga, A., Fujiwara, T., Fujimoto, A., et al. (2001) · Endocrine Journal · doi:10.1507/endocrj.48.161 · Cited by 7 · see citing works

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Ovarian antral folliculogenesis during the human menstrual cycle: A review
Baerwald, A. R., Adams, G. P., & Pierson, R. A. (2012) · Human Reproduction Update · doi:10.1093/humupd/dmr039 · Cited by 487 · see citing works
Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism
Sapkota, Y., Steinthorsdottir, V., Morris, A. P., Fassbender, A., Rahmioglu, N., De Vivo, I., Buring, J. E., Zhang, F., Edwards, T. L., Jones, S., et al. (2017) · Nature Communications · doi:10.1038/ncomms15539 · Cited by 344 · see citing works
The genetic basis of endometriosis and comorbidity with other pain and inflammatory conditions
Rahmioğlu, N., Mortlock, S., Ghiasi, M., Møller, P. L., Stefánsdóttir, L., Galarneau, G., Turman, C., Danning, R., Law, M. H., Sapkota, Y., et al. (2023) · Nature Genetics · doi:10.1038/s41588-023-01323-z · Cited by 311 · see citing works
Autophagy in ovary and polycystic ovary syndrome: role, dispute and future perspective
Kumariya, S., Ubba, V., Jha, R. K., & Gayen, J. R. (2021) · Autophagy · doi:10.1080/15548627.2021.1938914 · Cited by 306 · see citing works
Modeling menopause: The utility of rodents in translational behavioral endocrinology research
Koebele, S. V., & Bimonte‐Nelson, H. A. (2016) · Maturitas · doi:10.1016/j.maturitas.2016.01.015 · Cited by 296 · see citing works
Single-cell reconstruction of follicular remodeling in the human adult ovary
Fan, X., Bialecka, M., Moustakas, I., Lam, E., Torrens-Juaneda, V., Borggreven, N. V., Trouw, L. A., Louwe, L. A., Pilgram, G. S. K., Mei, H., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11036-9 · Cited by 282 · see citing works
Cell Origins of High-Grade Serous Ovarian Cancer
Kim, J., Park, E. Y., Kim, O., Schilder, J. M., Coffey, D., Cho, C., & Bast, R. C. (2018) · Cancers · doi:10.3390/cancers10110433 · Cited by 267 · see citing works
Premature Ovarian Insufficiency: New Perspectives on Genetic Cause and Phenotypic Spectrum
Tucker, E. J., Grover, S. R., Bachelot, A., Touraine, P. A., & Sinclair, A. H. (2016) · Endocrine Reviews · doi:10.1210/er.2016-1047 · Cited by 243 · see citing works
The Ovarian Reserve of Primordial Follicles and the Dynamic Reserve of Antral Growing Follicles: What Is the Link?1
Monniaux, D., Clément, F., Dalbiès-Tran, R., Estienne, A., Fabre, S., Mansanet, C., & Monget, P. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.117077 · Cited by 233 · see citing works
Cytokines in ovarian folliculogenesis, oocyte maturation and luteinisation
Field, S. L., Dasgupta, T., Cummings, M., & Orsi, N. M. (2013) · Molecular Reproduction and Development · doi:10.1002/mrd.22285 · Cited by 214 · see citing works
The Role of Antioxidant Enzymes in the Ovaries
Wang, S., He, G., Chen, M., Zuo, T., Xu, W., & Liu, X. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/4371714 · Cited by 180 · see citing works
Chemotherapy and fertility
Blumenfeld, Z. (2012) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2011.11.008 · Cited by 170 · see citing works
The role of the endocannabinoid system in female reproductive tissues
Walker, O. S., Holloway, A. C., & Raha, S. (2019) · Journal of Ovarian Research · doi:10.1186/s13048-018-0478-9 · Cited by 164 · see citing works
The magnitude of gonadotoxicity of chemotherapy drugs on ovarian follicles and granulosa cells varies depending upon the category of the drugs and the type of granulosa cells
Yüksel, A., Bildik, G., Senbabaoglu, F., Akin, N., Arvas, M., Ünal, F., Kilic, Y., Karanfil, I., Eryılmaz, B., Yilmaz, P., et al. (2015) · Human Reproduction · doi:10.1093/humrep/dev256 · Cited by 137 · see citing works
The use of autologous platelet-rich plasma (PRP) versus no intervention in women with low ovarian reserve undergoing fertility treatment: a non-randomized interventional study
Melo, P., Navarro, C., Jones, C., Coward, K., & Coleman, L. (2020) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-020-01710-z · Cited by 114 · see citing works
Functions of manganese in reproduction
Studer, J. M., Schweer, W., Gabler, N. K., & Ross, J. W. (2022) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2022.106924 · Cited by 106 · see citing works
Epigenetic transgenerational inheritance, gametogenesis and germline development†
Maamar, M. B., Nilsson, E. E., & Skinner, M. K. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab085 · Cited by 85 · see citing works
Natural history of ovarian function including assessment of ovarian reserve and premature ovarian failure
Lew, R. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.05.005 · Cited by 86 · see citing works
The ART of bringing extinction to a freeze – History and future of species conservation, exemplified by rhinos
Hildebrandt, T. B., Hermes, R. E., Göritz, F., Appeltant, R., Colleoni, S., de Mori, B., Diecke, S., Drukker, M., Galli, C., Hayashi, K., et al. (2021) · Theriogenology · doi:10.1016/j.theriogenology.2021.04.006 · Cited by 85 · see citing works
Origin and Evolution of the Neuroendocrine Control of Reproduction in Vertebrates, With Special Focus on Genome and Gene Duplications
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Authors: Gougeon, A.
Affiliations: Inserm (FR)
Corresponding author: Gougeon, A.
Venue: Annales d'Endocrinologie
Publisher: Elsevier BV
Published: 2010-05
Volume: 71
Issue: 3
Pages: 132-143
ISSN: 0003-4266 (ISSN-L)
DOI: 10.1016/j.ando.2010.02.021
OpenAlex: W2120987058
Cited by: 257
References: 144
Citations by year: 2026: 9 · 2025: 25 · 2024: 35 · 2023: 18 · 2022: 24 · 2021: 20 · 2020: 18 · 2019: 15 · 2018: 11 · 2017: 14 · 2016: 8 · 2015: 8 · 2014: 8 · 2013: 12 · 2012: 17
FWCI: 13.62
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Annales d Endocrinologie (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
Keywords: folliculogenesis, follicle activation, KIT signaling, follicle-stimulating hormone, luteinizing hormone, granulosa cell proliferation, estradiol, progesterone, cumulus expansion, oocyte nuclear maturation, follicle selection, autocrine and paracrine regulation, gonadotropins, follicle morphometry
MeSH terms: Aging, Cell Differentiation, Cell Division, Female, Follicle Stimulating Hormone, Ovarian Follicle, Granulosa Cells, Humans, Menstrual Cycle, Oocytes, Ovary, Ovulation, Anti-Mullerian Hormone

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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Human ovarian follicular development: From activation of resting follicles to preovulatory maturation

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