Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-05-01T22:06:07.031Z Has data issue: false hasContentIssue false

Chapter 4 - Physiology of the Female Reproductive System

from Section 1 - Physiology of Reproduction

Published online by Cambridge University Press:  05 March 2021

Eliezer Girsh
Affiliation:
Barzilai Medical Center, Ashkelon
Get access

Summary

The physiological importance of the female reproductive system is the production of offspring. The female produces gametes that can be fertilized by the male gamete to form the first cell of the offspring. The sequence of events is tightly dependent on the proper functionality of the endocrine system.

Much of the endocrine system is governed by rhythms, some of which are intrinsic, while others are influenced by the environment. Rhythms that are longer than 24 hours, the infradian rhythms, include the seasonal breeding patterns in some animals and the female menstrual cycle. Circadian or 24-hour rhythms include the sleep–wake cycle and the increase in gonadotropin secretion seen at night in adolescents. Finally, cycles of less than 24 hour, the ultradian cycles, include the pulsatile release of luteinizing hormone (LH), follicle-stimulating hormone (FSH), growth hormone, and prolactin.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2021

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

Gottsch, ML, Cunningham, MJ, Smith, JT, et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145:40734077.Google Scholar
Moreno, I, Codoñer, FM, Vilella, F, et al. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am. J. Obstet. Gynecol. 2016; 215:684703.Google Scholar
Ravel, J, Gajer, P, Abdo, Z, et al. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U. S. A. 2011; 108(Suppl. 1):46804687.Google Scholar
Gougeon, A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev. 1996; 17:121155.Google Scholar
Ng, EH, Yeung, WS, Fong, DY, Ho, PC. Effects of age on hormonal and ultrasound markers of ovarian reserve in Chinese women with proven fertility. Hum. Reprod. 2003; 18:21692174.Google Scholar
Dierich, A, Sairam, MR, Monaco, L, et al. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. U. S. A. 1998; 95:1361213617.Google Scholar
Jayaprakasan, K, Hilwah, N, Kendall, NR, et al. Does 3D ultrasound offer any advantage in the pretreatment assessment of ovarian reserve and prediction of outcome after assisted reproduction treatment? Hum. Reprod. 2007; 22:19321941.CrossRefGoogle ScholarPubMed
Kumar, TR, Wang, Y, Lu, N, Matzuk, MM. Follicle stimulating hormone is required for ovarian follicle maturation but not for male fertility. Nat. Genet. 1997; 15:201204.Google Scholar
Matthews, CH, Borgato, S, Beck-Peccoz, P, et al. Primary amenorrhoea and infertility due to a mutation in the beta-subunit of follicle-stimulating hormone. Nat. Genet. 1993; 5:8386.Google Scholar
Eppig, J. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001; 122:829838.Google Scholar
Kidder, GM, Mhawi, AA. Gap junctions and ovarian folliculogenesis. Reproduction 2002; 123:613620.CrossRefGoogle ScholarPubMed
Eppig, JJ, Wigglesworth, K, Pendola, FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc. Natl. Acad. Sci. U. S. A. 2002; 99:28902894.Google Scholar
Vitt, UA, Hayashi, M, Klein, C, Hsueh, AJW. 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. 2000; 62:370377.Google Scholar
Parrott, JA, Skinner, MK. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 1999; 140:42624271.Google Scholar
Nilsson, E, Parrott, JA, Skinner, MK. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol. Cell. Endocrinol. 2001; 25:123130.Google Scholar
Dissen, GA, Garcia-Rudaz, C, Ojeda, SR. Role of neurotrophic factors in early ovarian development. Semin. Reprod. Med. 2009; 27:2431.CrossRefGoogle ScholarPubMed
Nilsson, E, Dole, G, Skinner, MK. Neurotrophin NT3 promotes ovarian primordial to primary follicle transition. Reproduction 2009; 138:697707.Google Scholar
Abir, R, Fisch, B, Jin, S, et al. Presence of NGF and its receptors in ovaries from human fetuses and adults. Mol. Hum. Reprod. 2005; 11:229236.Google Scholar
El-Fouly, MA, Cook, B, Nekola, M, Nalbandov, AV. Role of the ovum in follicular luteinization. Endocrinology 1970; 87:286293.Google Scholar
Nekola, MV, Nalbandov, AV. Morphological changes of rat follicular cells as influenced by oocytes. Biol. Reprod. 1971; 4:154160.Google Scholar
Weenen, C, Laven, JSE, von Bergh, ARM, et al. Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol. Hum. Reprod. 2004; 10:7783.Google Scholar
Jeppesen, JV, Anderson, RA, Kelsey, TW, et al. Which follicles make the most anti-Müllerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol. Hum. Reprod. 2013; 19:519527.Google Scholar
Amsterdam, A, Koch, Y, Lieberman, ME, Lindner, HR. Distribution of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat. J. Cell. Biol. 1975; 67:894900.CrossRefGoogle ScholarPubMed
Lawrence, TS, Dekel, N, Beers, WH. Binding of human chorionic gonadotropin by rat cumuli oophori and granulosa cells: a comparative study. Endocrinology 1980; 106:11141118.Google Scholar
Chen, L, Russell, PT, Larsen, WJ. Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol. Reprod. Dev. 1993; 34:8793.Google Scholar
Peng, XR, Hsueh, AJ, LaPolt, PS, Bjersing, L, Ny, T. Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 1991; 129:32003207.Google Scholar
Gougeon, A. Rate of follicular growth in the human ovary. In: Rolland, R, Van Hall, EV, Hillier, SG, McNatty, KP, Schoemaker, JS, eds., Follicular Maturation and Ovulation. Amsterdam: Excerpta Medica. 1982; 155163.Google Scholar
McNatty, KP, Hillier, SG, van den Boogaard, AMJ, et al. Follicular development during the luteal phase of the human menstrual cycle. J. Clin. Endocrinol. Metab. 1983; 56:10221031.Google Scholar
Pache, TD, Wladimiroff, JW, de Jong, FH, Hop, WC, Fauser, BCJM. Growth patterns of non dominant ovarian follicles during the normal menstrual cycle. Fertil. Steril. 1990; 54:638642.Google Scholar
Gougeon, A, Lefèvre, B. Evolution of the diameters of the largest healthy and atretic follicles during the human menstrual cycle. J. Reprod. Fert. 1983; 69:497502.CrossRefGoogle ScholarPubMed
Kobayashi, M, Nakano, R, Ooshima, A. Immunocytochemical localization of pituitary gonadotrophins and gonadal steroids confirms the ‘two-cell, two-gonadotrophin’ hypothesis of steroidogenesis in the human ovary. J. Endocrinol. 1990; 126:483488.Google Scholar
Soules, MR, Steiner, RA, Clifton, DK, et al. Progesterone modulation of pulsatile luteinizing hormone secretion in normal women. J. Clin. Endocrinol. Metab. 1984; 58:378383.Google Scholar
Crowley, WF, McArthur, JW. Simulations of the normal menstrual cycle in Kallmann’s syndrome by pulsatile administration of luteinizing hormone-releasing hormone (LHRH). J. Clin. Endocrinol. Metab. 1980; 51:173175.Google Scholar
Solovyeva, EV, Hayashi, M, Margi, K, et al. Growth differentiation factor-9 stimulates rat theca-interstitial cell androgen biosynthesis. Biol. Reprod. 2000; 63:12141218.Google Scholar
Dunlop, CE, Anderson, RA. The regulation and assessment of follicular growth. Scand. J. Clin. Lab. Invest. Suppl. 2014; 244:1317.Google Scholar
Donez, J, Squifflet, J, Jadoul, P, et al. Pregnancy and live birth after autotransplantation of frozen-thawed ovarian tissue in a patient with metastatic disease undergoing chemotherapy and hematopoietic stem cell transplantation. Fertil. Steril. 1987; 2011:e1-e4.Google Scholar
Choi, J. Smitz, J. Luteinizing hormone and human chorionic gonadotropin: origins of difference. Mol. Cell. Endocrinol. 2014; 383:203213.Google Scholar
Casarini, L, Lispi, M, Longobardi, S, et al. LH and hCG action on the same receptor results in quantitatively and qualitatively different intracellular signaling. PLoS One 2012; 7, e46682.Google Scholar
Wide, L, Bakos, O. More basic forms of both human follicle-stimulating hormone and luteinizing hormone in serum at midcycle compared with the follicular or luteal phase. J. Clin. Endocrinol. Metab. 1993; 76:885889.Google Scholar
McNatty, KP. Ovarian follicular development from the onset of luteal regression in humans and sheep. In: Rolland, R, Van Hall, EV, Hillier, SG, McNatty, KP, Schoemaker, JS, eds., Follicular Maturation and Ovulation. Amsterdam: Excerpta Medica. 1982; 118.Google Scholar
Liu, L, Kong, N, Xia, G, Zhang, M. Molecular control of oocyte meiotic arrest and resumption. Reprod. Fertil. Dev. 2013; 25:463471.Google Scholar
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; 18:28132824.Google Scholar
Meduri, G, Charnaux, N, Driancourt, MA, et al. Follicle-stimulating hormone receptors in oocytes? J. Clin. Endocrinol. Metab. 2002; 87:22662276.Google Scholar
Patsoula, E, Loutradis, D, Drakakis, P, et al. Messenger RNA expression for the follicle-stimulating hormone receptor and luteinizing hormone receptor in human oocytes and pre-implantation-stage embryos. Fertil. Steril. 2003; 79:11871193.Google Scholar
Otsuka, F, Shimasaki, S. A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc. Natl. Acad. Sci. U. S. A. 2002; 99:80608065.Google Scholar
Lefievre, L, Conner, SJ, Salpekar, A, et al. Four zona pellucida glycoproteins are expressed in the human. Hum. Reprod. 2004; 19:15801586.Google Scholar
Motta, PM, Makabe, S, Naguro, T, Correr, S. Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy. Arch. Histol. Cytol. 1994; 57:369394.Google Scholar
Bergh, C, Olsson, JH, Selleskog, U, Hillensjo, T. Steroid production in cultured thecal cell obtained from human ovarian follicles. Hum. Reprod. 1993; 8:519524.CrossRefGoogle ScholarPubMed
Gilling-Smith, C, Franks, S. Ovarian function in assisted reproduction. In: Leung, PC, Adashi, EY, eds., The Ovary, 2nd ed. San Diego: Elsevier Academic Press. 2004; 473488.Google Scholar
Gougeon, A. Steroid 3β-ol-dehydrogenase activity in the largest healthy and atretic follicles in the human ovary during the menstrual cycle. Ann. Biol. Anim. Biochim. Biophys. 1977; 17:10871094.Google Scholar
Curtis, EM. Normal ovarian histology in infancy and childhood. Obstet. Gynecol. 1962; 19:444454.Google Scholar
Dekel, N, David, MP, Yedwab, GA, Kraicer, PF. Follicular development during late pregnancy. Int. J. Fertil. 1977; 22:2429.Google Scholar
Bloom, W, Fawcett, DW. A Textbook of Histology, 10th ed. Philadelphia: Saunders. 1975.Google Scholar
Amsterdam, A, Rotmensch, S. Structure-function relationships during granulosa cell differentiation. Endocr. Rev. 1987; 8:309337.Google Scholar
Hillier, SG, Yong, EL, Illingworth, PJ, et al. Effect of recombinant inhibin on androgen synthesis in cultured human thecal cells. Mol. Cell. Endocrinol. 1991; 75:R1R6.Google Scholar
Roberts, VJ, Barth, S, El-Roeiy, A, Yen, SSC. Expression of inhibin/activin subunits and follistatin messenger ribonucleic acids and proteins in ovarian follicles and the corpus luteum during the human menstrual cycle. J. Clin. Endocrinol. Metab. 1993; 77:14021410.Google Scholar
Sasano, H, Okamoto, M, Mason, JI, et al. Immunolocalization of aromatase, 17ɑ-hydroxylase and side-chain cleavage cytochrome P-450 in the human ovary. J. Reprod. Fertil. 1989; 85:163169.Google Scholar
Hernandez, ER, Hurwitz, A, Vera, A, et al. Expression of the genes encoding the insulin-like growth factors and their receptors in the human ovary. J. Clin. Endocrinol. Metab. 1992; 74:419425.Google ScholarPubMed
Salas, C, Julio-Pieper, M, Valladares, M, et al. Nerve growth factor-dependent activation of trkA receptors in the human ovary results in synthesis of follicle-stimulating hormone receptors and estrogen secretion. J. Clin. Endocrinol. Metab. 2006; 91:23962403.Google Scholar
Shima, K, Kitayama, S, Nakano, R. Gonadotropin binding sites in human ovarian follicles and corpora lutea during the menstrual cycle. Obstet. Gynecol. 1987; 69:800806.Google Scholar
McNatty, KP, Makris, A, DeGrazia, C, Osathanondh, R, Rayan, 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; 49:687699.Google Scholar
McNatty, KP, Smith, DM, Makris, A, Osathanondh, R, Ryan, KJ. The microenvironment of the human antral follicle: interrelationship 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. 1979; 49:851860.Google Scholar
Hillier, SG. Intrafollicular paracrine function of ovarian androgen. J. Steroid. Biochem. 1987; 27:351357.Google Scholar
Zeleznik, AJ, Schuler, HM, Reichert, LE. Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle. Endocrinology 1981; 109:356362.Google Scholar
Wulff, C, Wiegand, SJ, Saunders, PT, Scobie, GA, Fraser, HM. Angiogenesis during follicular development in the primate and its inhibition by treatment with truncated Flt-1-Fc (vascular endothelial growth factor Trap[A40]). Endocrinology 2001; 142:32443254.Google Scholar
Pauerstein, CJ, Eddy, CA, Croxatto, HD, et al. Temporal relationships of estrogen, progesterone, and luteinizing hormone levels to ovulation in women and infra-human primates. Am. J. Obstet. Gynecol. 1978; 130:876886.Google Scholar
Park, SJ, Goldsmith, LT, Skurnick, JH, Wojtczuk, A, Weiss, G. Characteristics of the urinary luteinizing hormone surge in young ovulatory women. Fertil. Steril. 2007; 88:684690.Google Scholar
Direito, A, Bailly, S, Mariani, A, Ecochard, R. Relationships between the luteinizing hormone surge and other characteristics of the menstrual cycle in normally ovulating women. Fertil. Steril. 2012; 99:279285.Google Scholar
Alliende, ME. Luteinizing hormone surge in normally ovulating women. Fertil. Steril. 2013; 99:e14e15.Google Scholar
Yussman, MA, Taymor, MI, Miyata, J, Pheteplace, C. Serum levels of follicle-stimulating hormone, luteinizing hormone, and plasma progestins correlated with human ovulation. Fertil. Steril. 1970; 21:119125.Google Scholar
Kerin, J. Ovulation detection in the human. Clin. Reprod. Fertil. 1982; 1:2754.Google Scholar
Richards, JS, Russell, DL, Ochsner, S, Espey, LL. Ovulation: new dimensions and new regulators of the inflammatory-like response. Ann. Rev. Physiol. 2002; 64:6992.Google Scholar
Okamura, H, Okazaki, T, Nakajima, A. Effects of electrical stimulation on human ovarian contractility. Obstet. Gynecol. 1975; 45:557561.Google Scholar
Okamura, H, Takenaka, A, Yajima, Y, Nishimura, T. Ovulatory changes in the wall at the apex of the human Graafian follicle. J. Reprod. Fertil. 1980; 58:153155.Google Scholar
Duffy, DM. Novel contraceptive targets to inhibit ovulation: the prostaglandin E2 pathway. Hum. Reprod. Update 2015; 21:652670.Google Scholar
Priddy, AR, Killick, SR, Elstein, M, et al. Ovarian follicular fluid eicosanoid concentrations during the pre-ovulatory period in humans. Prostaglandins 1989; 38:197202.Google Scholar
Duffy, DM, Stouffer, RL. The ovulatory gonadotrophin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle. Mol. Hum. Reprod. 2001; 7:731739.Google Scholar
Tjugum, J, Norström, A, Dennefors, B, Lundin, S. Oxytocin in human follicular fluid and its possible role in the ovulatory process as studied in vitro. Hum. Reprod. 1986; 1:283286.Google Scholar
Meidan, R, Altstein, M, Girsh, E. Biosynthesis and release of oxytocin by granulosa cells derived from preovulatory bovine follicles: effects of forskolin and insulin-like growth factor-I. Biol. Reprod. 1992; 46:715720.Google Scholar
Horka, P, Malickova, K, Jarosova, R, et al. Matrix metalloproteinases in serum and the follicular fluid of women treated by in vitro fertilization. J. Assist. Reprod. Genet. 2012; 29:12071212.Google Scholar
Hernandez-Gonzalez, I, Gonzalez-Robayna, I, Shimada, M, et al. Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process? Mol. Endocrinol. 2006; 20:13001321.Google Scholar
Edson, MA, Nagaraja, AK, Matzuk, MM. The mammalian ovary from genesis to revelation. Endocr. Rev. 2009; 30:624712.Google Scholar
Gershon, E, Plaks, V, Dekel, N. Gap junctions in the ovary: expression, localization and function. Mol. Cell. Endocrinol. 2008; 282:1825.Google Scholar
Freimann, S, Ben-Ami, I, Dantes, A, Ron-El, R, Amsterdam, A. EGF-like factor epiregulin and amphiregulin expression is regulated by gonadotropins/cAMP in human ovarian follicular cells. Biochem. Biophys. Res. Commun. 2004; 324:829834.Google Scholar
Park, JY, Su, YQ, Ariga, M, et al. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004; 303:682684.Google Scholar
Hizaki, H, Segi, E, Sugimoto, Y, et al. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc. Natl. Acad. Sci. U. S. A. 1999; 96:1050110506.Google Scholar
Gueripel, X, Brun, V, Gougeon, A. 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 expansion. Biol. Reprod. 2006; 75:836843.Google Scholar
Elvin, JA, Yan, C, Matzuk, MM. Oocyte-expressed TGF-beta superfamily members in female fertility. Mol. Cell. Endocrinol. 2000; 159:15.Google Scholar
Maruo, T, Katayama, K, Barnea, ER, Mochizuki, M. A role for thyroid hormone in the induction of ovulation and corpus luteum function. Horm. Res. 1992; 37 (Suppl. 1):1218.Google Scholar
Chaffkin, LM, Luciano, AA, Peluso, JJ. Progesterone as an autocrine/paracrine regulator of human granulosa cell proliferation. J. Clin. Endocrinol. Metab. 1992; 75:14041408.Google Scholar
Sasano, H, Mori, T, Sasano, N, Nagura, H, Mason, JI. Immunolocalization of 3beta-hydroxysteroid dehydrogenase in human ovary. J. Reprod. Fertil. 1990; 89:743751.Google Scholar
Brezinka, C. 3D ultrasound imaging of the human corpus luteum. Reprod. Biol. 2014; 14:110114.CrossRefGoogle ScholarPubMed
Jokubkiene, L, Sladkevičius, P, Rovas, L, Valentin, L. Assessment of changes in volume and vascularity of the ovaries during the normal menstrual cycle using three dimentional power Doppler ultrasound. Hum. Reprod. 2006; 21:26612668.Google Scholar
Stouffer, RL, Bishop, CV, Bogan, RL, Xu, F, Hennebold, JD. Endocrine and local control of the primate corpus luteum. Reprod. Biol. 2013; 13:259271.Google Scholar
Nishimori, K, Dunkel, L, Hsueh, A, Yamoto, M, Nakano, R. Expression of luteinizing hormone and chorionic gonadotropin receptor messenger ribonucleic acid in human corpora lutea during menstrual cycle and pregnancy. J. Clin. Endocrinol. Metab. 1995; 80:14441448.Google Scholar
Crisp, TM, Dessouky, DA, Denys, FR. The fine structure of the human corpus luteum of early pregnancy and during the progestational phase of menstrual cycle. Am. J. Anat. 1970; 127:3769.Google Scholar
Meidan, R, Girsh, E, Blum, O, Aberdam, E. In vitro differentiation of bovine theca and granulosa cells into small and large luteal-like cells: morphological and functional characteristics. Biol. Reprod. 1990; 43:913921.Google Scholar
Sanders, SL, Stouffer, RL. Localization of steroidogenic enzymes in macaque luteal tissue during the menstrual cycle and simulated early pregnancy: immunohistochemical evidence supporting the two-cell model for estrogen production in the primate corpus luteum. Biol. Reprod. 1997; 56:10771087.Google Scholar
Reynolds, L, Redmer, D. Growth and development of the corpus luteum. J. Reprod. Fertil. Suppl. 1999; 54:181191.Google Scholar
Robinson, RS, Woad, KJ, Hammond, AJ, et al. Angiogenesis and vascular function in the ovary. Reproduction 2009; 138:869881.Google Scholar
Ferrara, N, Chen, H, Davis-Smyth, T, et al. Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat. Med. 1998; 4:336340.Google Scholar
Wulff, C, Dickson, SE, Duncan, WC, Fraser, HM. Angiogenesis in the human corpus luteum: simulated early pregnancy by hCG treatment is associated with both angiogenesis and vessel stabilization. Hum. Reprod. 2001; 16:25152524.Google Scholar
Forsythe, JA, Jiang, BH, Iyer, NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 1996; 16:46044613.Google Scholar
Fraser, HM, Duncan, WC. Regulation and manipulation of angiogenesis in the ovary and endometrium. Reprod. Fertil. Dev. 2009; 21:277392.Google Scholar
Spencer, TE, Bazer, FW. Conceptus signals for establishment and maintenance of pregnancy. Reprod. Biol. Endocrinol. 2004; 2:49.Google Scholar
Horton, EW, Poyser, NL. Uterine luteolytic hormone: a physiological role of prostaglandin F2α. Physiol. Rev. 1976; 56:595651.Google Scholar
Miyamoto, A, Shirasuna, K, Shimizu, T, Bollwein, H, Schams, D. Regulation of corpus luteum development and maintenance: specific roles of angiogenesis and action of prostaglandin F2α. Soc. Reprod. Fertil. Suppl. 2010; 67:289304.Google Scholar
Best, CL, Pudney, J, Welch, WR, Burger, N, Hill, JA. Localization and characterization of white blood cell populations within the human ovary throughout the menstrual cycle and menopause. Hum. Reprod. 1996; 11:790797.Google Scholar
Townson, DH, Liptak, AR. Chemokines in the corpus luteum: implications of leukocyte chemotaxis. Reprod. Biol. Endocrinol. 2003; 1:94.Google Scholar
Girsh, E, Milvae, RA, Wang, W, Meidan, R. Effect of endothelin-1 on bovine luteal cell function: role in prostaglandin F2a-induced antisteroidogenic action. Endocrinology 1996; 137:13061312.Google Scholar
Wulff, C, Wilson, H, Largue, P, et al. Angiogenesis in the human corpus luteum: localization and changes in angiopoietins, tie-2, and vascular endothelial growth factor messenger ribonucleic acid. J. Clin. Endocrinol. Metab. 2000; 85:43024309.Google Scholar
Zalman, Y, Klipper, E, Farberov, S, et al. Regulation of angiogenesis-related prostaglandin F2α-induced genes in the bovine corpus luteum. Biol. Reprod. 2012; 86:92.Google Scholar
Farberov, S, Meidan, R. Thrombospondin-1 affects bovine luteal function via transforming growth factor β1-dependent and independent actions. Biol. Reprod. 2016; 94:25.Google Scholar
Yadav, VK, Lakshmi, G, Medhamurthy, R. Prostaglandin F2α-mediated activation of apoptotic signaling cascades in the corpus luteum during apoptosis: involvement of caspase-activated DNase. J. Biol. Chem. 2005; 280:1035710367.Google Scholar
Duncan, WC, McNeilly, AS, Fraser, HM, Illingworth, PJ. Luteinizing hormone receptor in the human corpus luteum: lack of down regulation during maternal recognition of pregnancy. Hum. Reprod. 1996; 11:22912297.Google Scholar
Jabbour, HN, Kelly, RW, Fraser, HM, Critchley, HO. Endocrine regulation of menstruation. Endocr. Rev. 2006; 27:1746.Google Scholar
Nagaoka, SI, Hassold, TJ, Hunt, PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 2012; 13:493504.Google Scholar
Huang, L, Tong, X, Luo, L, et al. Mutation analysis of the TUBB8 gene in nine infertile women with oocyte maturation arrest. RBM Online 2017; 35:305310.Google Scholar
American College of Obstetricians and Gynecologists. ACOG Committee Opinion. Age-related fertility decline. Obstet. Gynecol. 2008; 112:409411.Google Scholar
Ziebe, S, Devroey, P. Assisted reproductive technologies are an integrated part of national strategies addressing demographic and reproductive challenges. Hum. Reprod. Update. 2008; 14:583592.Google Scholar
Menken, J, Trussell, J, Larsen, U. Age and infertility. Science 1986; 233:13891394.Google Scholar
Faddy, MJ, Gosden, RG, Gougeon, A, Richardson, SJ, Nelson, JF. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum. Reprod. 1992; 7:13421346.Google Scholar
Rosen, MP, Johnstone, E, McCulloch, CE, et al. A characterization of the relationship of ovarian reserve markers with age. Fertil. Steril. 2012; 97:238243.Google Scholar
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; 23:699708.Google Scholar
Wang, YA, Dean, J, Badgery-Parker, T, Sullivan, EA. Assisted Reproduction Technology in Australia and New Zealand 2006. Sydney: AIHW National Peritnatal Statistics Unit. 2008.Google Scholar
Fitzgerald, O, Paul, RC, Harris, K, Chambers, GM. Assisted Reproductive Technology in Australia and New Zealand 2016. Sydney: National Perinatal Epidemiology and Statistics Unit, the Univeristy of New South Wales Sydney. 2018.Google Scholar
Gilbert, WM, Nesbitt, TS, Danielsen, B. Childbearing beyond age 40: pregnancy outcome in 24,032 cases. Obstet. Gynecol. 1999; 93:914.Google Scholar
Meng, L, Jan, SZ, Hamer, G, et al. Preantral follicular atresia occurs mainly through autophagy, while antral follicles degenerate mostly through apoptosis. Biol. Reprod. 2018; 99:853863.Google Scholar
Baker, TG. A quantitative and cytological study of germ cells in human ovaries. Proc. R. Soc. Lond. B. Biol. Sci. 1963;158:417433.Google Scholar
Richardson, SJ, Senikas, V, Nelson, JF. Follicular depletion during the menopausal transition: evidence for accelerated loss and ultimate exhaustion. J. Clin. Endocrinol. Metab. 1987; 65:12311237.Google Scholar
Murray, A, Schoemaker, MJ, Bennett, CE, et al. Population-based estimates of the prevalence of FMR1 expansion mutations in women with early menopause and primary ovarian insufficiency. Genet. Med. 2014; 16:1924.Google Scholar
Broekmans, FJ, Soules, MR, Fauser, BC. Ovarian aging: mechanisms and clinical consequences. Endocr. Rev. 2009; 30:465493.Google Scholar
Johnson, NP, Bagrie, EM, Coomarasamy, A, et al. Ovarian reserve tests for predicting fertility outcomes for assisted reproductive technology: the International Systematic Collaboration of Ovarian Reserve Evaluation protocol for a systematic review of ovarian reserve test accuracy. BJOG 2006; 113:14721480.Google Scholar
te Velde, ER, Pearson, PL. The variability of female reproductive ageing. Hum. Reprod. Update 2002; 8:141154.Google Scholar
Klein, NA, Battaglia, DE, Miller, PB, et al. Ovarian follicular development and the follicular fluid hormones and growth factors in normal women of advanced reproductive age. J. Clin. Endocrinol. Metab. 1996; 81:19461951.Google Scholar
Burger, HG, Hale, GE, Dennerstein, L, Robertson, DM. Cycle and hormone changes during perimenopause: the key role of ovarian function. Menopause 2008; 15:603612.Google Scholar
Klein, NA, Battaglia, DE, Fujimoto, VY, et al. Reproductive aging: accelerated ovarian follicular development associated with a monotropic follicle-stimulating hormone rise in normal older women. J. Clin. Endocrinol. Metab. 1996; 81:10381045.Google Scholar
Rossmanith, WG. Gonadotropin secretion during aging in women. Exp. Gerontology 1995; 30:369381.Google Scholar
de Bruin, JP, Bovenhuis, H, van Noord, PA, et al. The role of genetic factors in age at natural menopause. Hum. Reprod. 2001; 16:20142018.Google Scholar
van Asselt, KM, Kok, HS, Pearson, PL, et al. Heritability of menopausal age in mothers and daughters. Fertil. Steril. 2004; 82:13481351.Google Scholar
Kalmbach, KH, Antunes, DM, Kohlrausch, F, Keefe, DL. Telomeres and female reproductive aging. Semin. Reprod. Med. 2015; 33:389395.Google Scholar
Keefe, DL, Marquard, K, Liu, L. The telomere theory of reproductive senescence in women. Curr. Opin. Obstet. Gynecol. 2006; 18:280285.Google Scholar
Keefe, DL. Telomeres, reproductive aging, and genomic instability during early development. Reprod. Sci. 2016; 23:16121615.Google Scholar
Westhoff, C, Murphy, P, Heller, D. Predictors of ovarian follicle number. Fertil. Steril. 2000; 74:624628.Google Scholar
Stock, D, Knight, JA, Raboud, J, et al. Rotating night shift work and menopausal age. Hum. Reprod. 2019; 34:539548.Google Scholar
Pellestor, F, Andreo, B, Arnal, F, Humeau, C, Demaille, J. Maternal aging and chromosomal abnormalities: new data drawn from in vitro unfertilized human oocytes. Hum. Genet. 2003; 112:195203.Google Scholar
Alberman, E, Creasy, M, Elleott, M, Spicier, C. Maternal factors associated with fetal chromosomal anomalies in spontaneous abortions. Br. J. Obstet. Gynecol. 1976; 83:621627.Google Scholar
Volarcik, K, Sheean, L, Goldfarb, J, et al. The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary. Hum. Reprod. 1998; 13:154160.Google Scholar
Yun, Y, Holt, JE, Lane, SI, et al. Reduced ability to recover from spindle disruption and loss of kinetochore spindle assembly checkpoint proteins in oocytes from aged mice. Cell Cycle 2014; 13:19381947.Google Scholar
Hassold, T, Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2001; 2:280291.Google Scholar
Chiang, T, Duncan, FE, Schindler, K, Schultz, RM, Lampson, MA. Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr. Biol. 2010; 20:15221528.Google Scholar
Cheng, JM, Liu, YX. Age-related loss of cohesion: causes and effects. Int. J. Mol. Sci. 2017; 18. doi:10.3390/ijms18071578.Google Scholar
Kuliev, A, Verlinsky, Y. Meiotic and mitotic nondisjunction: lessons from preimplantation genetic diagnosis. Hum. Reprod. Update 2004; 10:401407.Google Scholar
Nagaoka, SI, Hassold, TJ, Hunt, PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 2012; 13:493504.Google Scholar
May-Panloup, P, Boucret, L, Chao de la Barca, JM, et al. Ovarian ageing: the role of mitochondria in oocytes and follicles. Hum. Reprod. Update 2016; 22:725743.Google Scholar
Broekmans, FJ, Faddy, MJ, Scheffer, G, te Velde, ER. Antral follicle counts are related to age at natural fertility loss and age at menopause. Menopause 2004; 11:607614.Google Scholar
Tietze, C. Fertility after discontinuation of intrauterine and oral contraception. Int. J. Fertil. 1968; 13:385389.Google Scholar
Gunby, J, Bissonnette F, , Librach, C, Cowan, L; IVF Directors Group of the Canadian Fertility and Andrology Society. Assisted reproductive technologies (ART) in Canada: 2006 results from the Canadian ART Register. Fertil. Steril. 2010; 93:21892201.Google Scholar
Noci, I, Borri, P, Chieffi, O, et al. Aging of the human endometrium: a basic morphological and immunohistochemical study. Eur. J. Obstet. Gynecol. Reprod. Biol. 1995; 63:181185.Google Scholar
Wang, YA, Farquhar, C, Sullivan, EA. Donor age is a major determinant of success of oocyte donation/recipient programme. Hum. Reprod. 2012; 27:118-125.Google Scholar
Sherman, BM, West, JH, Korenman, SG. The menopausal transition: analysis of LH, FSH, estradiol, and progesterone concentrations during menstrual cycles of older women. J. Clin. Endocrinol. Metab. 1976; 42:629636.Google Scholar
Sabatini, L, Zosmer, A, Hennessy, EM, Tozer, A, Al-Shawaf, T. Relevance of basal serum FSH to IVF outcome varies with patient age. RBM Online 2008; 17:1019.Google Scholar
Broekmans, FJ, de Ziegler, D, Howles, CM, et al. The antral follicle count: practical recommendations for better standardization. Fertil. Steril. 2010; 94:10441051.Google Scholar
Broekmans, FJ, Kwee, J, Hendriks, DJ, Mol, BW, Lambalk, CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum. Reprod. Update 2006; 12:685718.Google Scholar
La Marca, A, Volpe, A. Anti-Mullerian hormone (AMH) in female reproduction: is measurement of circulating AMH a useful tool? Clin. Endocrinol. 2006; 64:603610.Google Scholar
Li, HWR, Yeung, WSB, Lau, EYL, Ho, PC, Ng, EHY. Evaluating the performance of serum antimullerian hormone concentration in predicting the live birth rate of controlled ovarian stimulation and intrauterine insemination. Fertil. Steril. 2010; 94:21772181.Google Scholar
Hehenkamp, WJ, Looman, CW, Themmen, AP, et al. Anti-Mullerian hormone levels in the spontaneous menstrual cycle do not show substantial fluctuation. J. Clin. Endocrinol. Metab. 2006; 91:40574063.Google Scholar
Sowers, MR, Eyvazzadeh, AD, McConnell, D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J. Clin. Endocrinol. Metab. 2008; 93:34783483.Google Scholar
Broekmans, FJ. Testing for ovarian reserve in assisted reproduction programs: the current point of view. Fact Views Vis. Obgin. 2009; 1:7981.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org 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
×