Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-23T13:11:40.665Z Has data issue: false hasContentIssue false

2 - Ontogeny of the mammalian ovary

from Section 2 - Life cycle

Published online by Cambridge University Press:  05 October 2013

By
Anne Grete Byskov  and
Claus Yding Andersen
Edited by
Alan Trounson ,
Roger Gosden  and
Ursula Eichenlaub-Ritter
Anne Grete Byskov
Affiliation:
Laboratory of Reproductive Biology, Juliane Marie Center, Rigshospitalet, Copenhagen, Denmark
Claus Yding Andersen
Affiliation:
Laboratory of Reproductive Biology, Juliane Marie Centre, University Hospital of Copenhagen, and Faculty of Health Science, University of Copenhagen, Copenhagen, Denmark
Alan Trounson
Affiliation:
California Institute for Regenerative Medicine
Roger Gosden
Affiliation:
Center for Reproductive Medicine and Infertility, Cornell University, New York
Ursula Eichenlaub-Ritter
Affiliation:
Universität Bielefeld, Germany
Get access

Summary

Introduction

Mammalian ovarian formation and differentiation takes place early in life, often before birth, but the ovary is not ready to fulfill its main purpose, that is, to ovulate a mature oocyte, until puberty. During early fetal development the germ cells populate the gonadal areas in close association with the mesonephros. The following developmental pattern of the ovary differs greatly among species, but one parameter is a must for all: each germ cell differentiates to an oocyte and becomes together with granulosa cells enclosed in a follicular entity. The pool of follicles is final and determines the length of the future reproductive lifespan. The finely tuned interaction between germ cells and somatic cells early in life is therefore crucial.

Origin and migration of primordial germ cells (PGCs) from the epiblast to the gonadal anlage: role of the autonomic nervous system

The classic concept of gonadal formation is that the PGCs arise in the proximal part of the yolk sac, the proximal epiblast [1], and migrate a relatively long distance within the hindgut that grows towards the area where the gonads will develop, around somite 16 [2]. Then the PGCs leave the hindgut and move towards the developing gonads at the ventral part of the mesonephros. Thus, the PGCs are first guided by the hindgut and thereafter by other mechanisms to the gonadal anlage. The importance of the hindgut for PGC movement was shown in Sox17-null mouse embryos in which the hindgut does not expand and the PGCs become immobilized in the hindgut [3].

Type
Chapter
Information
Biology and Pathology of the Oocyte
Role in Fertility, Medicine and Nuclear Reprograming
 , pp. 12 - 23
Publisher: Cambridge University Press
Print publication year: 2013

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

Wylie, CC.The biology of primordial germ cells. Eur Urol 1993; 23(1): 62–6.CrossRefGoogle ScholarPubMed
Witschi, E.Migration of the germ cells of human embryos from the yolk sac to the primitive gonadal folds. Contrib Embryol 1948; 209: 67–80.Google Scholar
Hara, K, Kanai-Azuma, M, Uemura, M, et al. Evidence for crucial role of hindgut expansion in directing proper migration of primordial germ cells in mouse early embryogenesis. Dev Biol 2009; 330(2): 427–39.CrossRefGoogle ScholarPubMed
Freeman, B.The active migration of germ cells in the embryos of mice and men is a myth. Reproduction 2003; 125(5): 635–43.CrossRefGoogle ScholarPubMed
Saitou, M, Payer, B, O’Carroll, D, Ohinata, Y, Surani, MA.Blimp1 and the emergence of the germ line during development in the mouse. Cell Cycle 2005; 4(12): 1736–40.CrossRefGoogle ScholarPubMed
Nichols, J, Smith, A.The origin and identity of embryonic stem cells. Development 2011; 138(1):3–8.CrossRefGoogle ScholarPubMed
West, JA, Viswanathan, SR, Yabuuchi, A, et al. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 2009; 460(7257): 909–13.CrossRefGoogle ScholarPubMed
Gillich, A, Bao, S, Grabole, N, et al. Epiblast stem cell-based system reveals reprogramming synergy of germline factors. Cell Stem Cell 2012; 10(4): 425–39.CrossRefGoogle ScholarPubMed
Dolci, S, Williams, DE, Ernst, MK, et al. Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 1991; 352(6338):809–11.CrossRefGoogle ScholarPubMed
Laird, DJ, Altshuler-Keylin, S, Kissner, MD, Zhou, X, Anderson, KV.Ror2 enhances polarity and directional migration of primordial germ cells. PLoS Genet 2011; 7(12): e1002428.CrossRefGoogle ScholarPubMed
Koshimizu, U, Watanabe, M, Nakatsuji, N.Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Dev Biol 1995; 168(2): 683–5.CrossRefGoogle ScholarPubMed
Luoh, SW, Bain, PA, Polakiewicz, RD, et al. Zfx mutation results in small animal size and reduced germ cell number in male and female mice. Development 1997; 124(11): 2275–84.Google ScholarPubMed
Richardson, BE, Lehmann, R.Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 2010; 11(1): 37–49.CrossRefGoogle ScholarPubMed
Møllgård, K, Jespersen, A, Lutterodt, MC, et al. Human primordial germ cells migrate along nerve fibers and Schwann cells from the dorsal hind gut mesentery to the gonadal ridge. Mol Hum Reprod 2010; 16(9): 621–31.CrossRefGoogle ScholarPubMed
Dees, WL, Hiney, JK, McArthur, NH, et al. Origin and ontogeny of mammalian ovarian neurons. Endocrinology 2006; 147(8): 3789–96.CrossRefGoogle ScholarPubMed
Renault, AD, Lehmann, R.Follow the fatty brick road: lipid signaling in cell migration. Curr Opin Genet Dev 2006; 16(4): 348–54.CrossRefGoogle ScholarPubMed
Byskov, AG, Hoyer, PE, Yding AC, , et al. No evidence for the presence of oogonia in the human ovary after their final clearance during the first two years of life. Hum Reprod 2011; 26(8): 2129–39.CrossRefGoogle ScholarPubMed
Hoyer, PE, Byskov, AG, Mollgard, K.Stem cell factor and c-Kit in human primordial germ cells and fetal ovaries. Mol Cell Endocrinol 2005; 234(1–2): 1–10.CrossRefGoogle ScholarPubMed
Pesce, M, Canipari, R, Ferri, GL, Siracusa, G, De Felici, M.Pituitary adenylate cyclase-activating polypeptide (PACAP) stimulates adenylate cyclase and promotes proliferation of mouse primordial germ cells. Development 1996; 122(1): 215–21.Google ScholarPubMed
Zamboni, L, Bézard, J, Mauléon, P.The role of mesonephros in the development of the sheep fetal ovary. Ann Biol Anim Biochim Biophys 1979; 19(4B): 1153–78.CrossRefGoogle Scholar
Byskov, AG.The anatomy and ultrastructure of the rete system in the fetal mouse ovary. Biol Reprod 1978; 19(4): 720–35.CrossRefGoogle ScholarPubMed
Juengel, JL, Sawyer, HR, Smith, PR, et al. Origins of follicular cells and ontogeny of steroidogenesis in ovine fetal ovaries. Mol Cell Endocrinol 2002; 191(1): 1–10.CrossRefGoogle ScholarPubMed
Byskov, AG, Høyer, PE.Embryology of mammalian gonads and ducts. In: Knobil, E, Neill, JD, eds. The Physiology of Reproduction, 2nd edn. New York: Raven Press, Ltd. 1994; 487–540.Google Scholar
Wrobel, KH, Suss, F.The significance of rudimentary nephrostomial tubules for the origin of the vertebrate gonad. Anat Embryol (Berl) 2000; 201(4): 273–90.CrossRefGoogle ScholarPubMed
Koopman, P, Gubbay, J, Vivian, N, Goodfellow, P, Lovell-Badge, R.Male development of chromosomally female mice transgenic for Sry. Nature 1991; 351(6322): 117–21.CrossRefGoogle ScholarPubMed
Vidal, VP, Chaboissier, MC, de Rooij, DG, Schedl, A.Sox9 induces testis development in XX transgenic mice. Nat Genet 2001; 28(3): 216–17.CrossRefGoogle ScholarPubMed
Vainio, S, Heikkila, M, Kispert, A, Chin, N, McMahon, AP.Female development in mammals is regulated by Wnt-4 signalling. Nature 1999; 397(6718): 405–9.CrossRefGoogle ScholarPubMed
Gondos, B, Zamboni, L.Ovarian development: the functional importance of germ cell interconnections. Fertil Steril 1969; 20(1): 176–89.CrossRefGoogle ScholarPubMed
Pepling, ME, Spradling, AC.Female mouse germ cells form synchronously dividing cysts. Development 1998; 125(17): 3323–8.Google ScholarPubMed
Childs, AJ, Cowan, G, Kinnel, HL, Anderson, RA, Saunders, PT. Retinoic acid signalling and the control of meiotic entry in the human fetal gonad. PLoS One 2011; 6(6): 1–6.CrossRefGoogle ScholarPubMed
Chen, Y, Jefferson, WN, Newbold, RR, Padilla-Banks, E, Pepling, ME.Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007; 148(8): 3580–90.CrossRefGoogle ScholarPubMed
Byskov, AG.Does the rete ovarii act as a trigger for the onset of meiosis?Nature 1974; 252(5482): 396–7.CrossRefGoogle ScholarPubMed
Byskov, AG, Grinsted, J.Feminizing effect of mesonephros on cultured differentiating mouse gonads and ducts. Science 1981; 212(4496): 817–18.CrossRefGoogle ScholarPubMed
Menke, DB, Koubova, J, Page, DC.Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev Biol 2003; 262(2): 303–12.CrossRefGoogle Scholar
Koubova, J, Menke, DB, Zhou, Q, et al. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci USA 2006; 103(8): 2474–9.CrossRefGoogle ScholarPubMed
Bendsen, E, Byskov, AG, Andersen, CY, Westergaard, LG.Number of germ cells and somatic cells in human fetal ovaries during the first weeks after sex differentiation. Hum Reprod 2006; 21: 30–5.CrossRefGoogle ScholarPubMed
Byskov, AG.The meiosis inducing interaction between germ cells and rete cells in the fetal mouse gonad. Ann Biol Anim Biochim Biophys 1978; 18(2): 327–34.CrossRefGoogle Scholar
Byskov, AG, Andersen, CY, Nordholm, L, et al. Chemical structure of sterols that activate oocyte meiosis. Nature 1995; 374(6522): 559–62.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Le Bouffant, R, Souquet, B, Duval, N, et al. Msx1 and Msx2 promote meiosis initiation. Development 2011; 138(24): 5393–402.CrossRefGoogle ScholarPubMed
Naillat, F, Prunskaite-Hyyrylainen, R, Pietila, I, et al. Wnt4/5a signalling coordinates cell adhesion and entry into meiosis during presumptive ovarian follicle development. Hum Mol Genet 2010; 19(8): 1539–50.CrossRefGoogle ScholarPubMed
Byskov, AG.Regulation of meiosis in mammals. Ann Biol Anim Biochim Biophys 1979; 19(4B): 1251–61.CrossRefGoogle Scholar
Byskov, AG.Differentiation of mammalian embryonic gonad. Physiol Rev 1986; 66(1): 71–117.CrossRefGoogle ScholarPubMed
George, FW, Wilson, JD.Sex determination and differentiation. In: Knobil, E, Neill, JD, eds. The Physiology of Reproduction. New York: Raven Press Ltd., 1988; 3–25.Google Scholar
Lun, S, Smith, P, Lundy, T, et al. Steroid contents of and steroidogenesis in vitro by the developing gonad and mesonephros around sexual differentiation in fetal sheep. J Reprod Fertil 1998; 114(1): 131–9.CrossRefGoogle ScholarPubMed
Bowles, J, Koopman, P.Retinoic acid, meiosis and germ cell fate in mammals. Development 2007; 134(19): 3401–11.CrossRefGoogle ScholarPubMed
Baker, TG.A quantitative and cytological study of germ cells in human ovaries. Philos Trans R Soc Lond B 1963; 158: 417–33.Google ScholarPubMed
Tingen, C, Kim, A, Woodruff, TK.The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 2009; 15(12): 795–803.CrossRefGoogle ScholarPubMed
Xu, B, Hua, J, Zhang, Y, et al. Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries. PLoS One 2011; 6(1): e16046.Google ScholarPubMed
Monget, P, Bobe, J, Gougeon, A, et al. The ovarian reserve in mammals: a functional and evolutionary perspective. Mol Cell Endocrinol 2012; 356(1–2): 2–12.CrossRefGoogle ScholarPubMed
Witschi, E.Embryogenesis of the adrenal and the reproductive glands. Horm Res 1951; 6: 1.Google Scholar
Burns, RK.Role of hormones in the differentiation of sex. In: Young, WC, ed. Sex and Internal Secretions, 3rd edn. Baltimore: The Williams and Wilkins Co. 1961; 76–158.Google Scholar
Byskov, AG, Skakkebaek, NE, Stafanger, G, Peters, H.Influence of ovarian surface epithelium and rete ovarii on follicle formation. J Anat 1977; 123(1): 77–86.Google ScholarPubMed
Mork, L, Tang, H, Batchvarov, I, Capel, B.Mouse germ cell clusters form by aggregation as well as clonal divisions. Mech Dev 2012; 128(11–12): 591–6.CrossRefGoogle ScholarPubMed
Byskov, AG, Hoyer, PE, Yding, AC, et al. No evidence for the presence of oogonia in the human ovary after their final clearance during the first two years of life. Hum Reprod 2011; 26(8): 2129–39.CrossRefGoogle ScholarPubMed
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(6): 1754–62.CrossRefGoogle ScholarPubMed
Pepling, ME.Follicular assembly: mechanisms of action. Reproduction 2012; 143(2): 139–49.CrossRefGoogle ScholarPubMed
Baker, TG.A quantitative and cytological study of oogenesis in the rhesus monkey. J Anat 1966; 100(4): 761–76.Google ScholarPubMed
Mamsen, LS, Lutterodt, MC, Andersen, EW, Byskov, AG, Andersen, CY.Germ cell numbers in human embryonic and fetal gonads during the first two trimesters of pregnancy: analysis of six published studies. Hum Reprod 2011; 26(8): 2140–5.CrossRefGoogle ScholarPubMed
Fowler, PA, Flannigan, S, Mathers, A, et al. Gene expression analysis of human fetal ovarian primordial follicle formation. J Clin Endocrinol Metab 2009; 94(4): 1427–35.CrossRefGoogle ScholarPubMed
Childs, AJ, Kinnell, HL, Collins, CS, et al. BMP signaling in the human fetal ovary is developmentally regulated and promotes primordial germ cell apoptosis. Stem Cells 2010; 28: 1368–78.CrossRefGoogle ScholarPubMed
Byskov, AG, Rasmussen, G.Ultrastructural studies of the developing follicle. In: Peters, H, ed. International Congress Series 267. Amsterdam: Excerpta Medica. 1973; 55–62.Google Scholar
Motta, PM, Makabe, S.Elimination of germ cells during differentiation of the human ovary: an electron microscopic study. Eur J Obstet Gynecol Reprod Biol 1986; 22(5–6): 271–86.CrossRefGoogle Scholar
Johnson, J, Canning, J, Kaneko, T, Pru, JK, Tilly, JL.Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004; 428(6979): 145–50.CrossRefGoogle ScholarPubMed
Byskov, AG, Faddy, MJ, Lemmen, JG, Andersen, CY.Eggs forever?Differentiation 2005; 73(9–10): 438–46.CrossRefGoogle ScholarPubMed
Virant-Klun, I, Zech, N, Rozman, P, et al. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation 2008; 76(8): 843–56.CrossRefGoogle ScholarPubMed
White, YA, Woods, DC, Takai, Y, et al. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med 2012; 18(3):413–21.CrossRefGoogle ScholarPubMed
Zhang, H, Zheng, W, Shen, Y, et al. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc Natl Acad Sci USA 2012; 109(31): 12580–5.CrossRefGoogle ScholarPubMed
Telfer, EE, Albertini, DF.The quest for human ovarian stem cells. Nat Med 2012; 18(3): 353–4.CrossRefGoogle ScholarPubMed
Oatley, J, Hunt, PA.Of mice and (wo)men: purified oogonial stem cells from mouse and human ovaries. Biol Reprod 2012; 86(6): 196.CrossRefGoogle ScholarPubMed
Liu, CF, Liu, C, Yao, HH.Building pathways for ovary organogenesis in the mouse embryo. Curr Top Dev Biol 2010; 90: 263–90.CrossRefGoogle ScholarPubMed
Lechowska, A, Bilinski, S, Choi, Y, et al. Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown. J Assist Reprod Genet 2011; 28(7): 583–9.CrossRefGoogle ScholarPubMed
Wallace, WH, Kelsey, TW.Human ovarian reserve from conception to the menopause. PLoS One 2010; 5(1): e8772.CrossRefGoogle ScholarPubMed

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
×