Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-17T22:19:25.112Z Has data issue: false hasContentIssue false
  • English
  • Français

Post-natal oogenesis: a concept for controversy that intensified during the last decade

Published online by Cambridge University Press:  20 December 2013

Yashar Esmaeilian ,
Arzu Atalay  and
Esra Erdemli
Yashar Esmaeilian*
Affiliation:
Biotechnology Institute, University of Ankara, Ankara 06500, Turkey. Biotechnology Institute, University of Ankara, Ankara, Turkey.
Arzu Atalay
Affiliation:
Biotechnology Institute, University of Ankara, Ankara, Turkey.
Esra Erdemli
Affiliation:
Department of Histology and Embryology, School of Medicine, University of Ankara, Ankara, Turkey.
*
All correspondence to: Yashar Esmaeilian. Biotechnology Institute, University of Ankara, Ankara 06500, Turkey. Tel: +90 312 222 5816. Fax: +90 312 222 5872. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

For decades, scientists have considered that female mammals are born with a lifetime reserve of oocytes in the ovary, irrevocably fated to decline after birth. However, controversy in the matter of the possible presence of oocytes and granulosa cells that originate from stem cells in the adult mammalian ovaries has been expanded. The restricted supply of oocytes in adult female mammals has been disputed in recent years by supporters of neo-oogenesis, who claim that germline stem cells (GSCs) exist in the ovarian surface epithelium (OSE) or the bone marrow (BM). Differentiation of ovarian stem cells (OSCs) into oocytes, fibroblast-like cells, granulosa phenotype, neural and mesenchymal type cells and generation of germ cells from OSCs under the contribution of an OSC niche that consists of immune system-related cells and hormonal signalling has been claimed. Although these arguments have met with intense suspicion, their confirmation would necessitate the revision of the current classic knowledge of female reproductive biology.

Keywords

Germline stem cellOocyteOogenesisOvarian stem cellOvary
Type
Review
Information
Zygote , Volume 23 , Issue 3 , June 2015 , pp. 315 - 326
Copyright
Copyright © Cambridge University Press 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

Allen, E. (1923). Ovogenesis during sexual maturity. Am. J. Anat. 31, 439–81.CrossRefGoogle Scholar
Allen, E. & Creadick, R.N. (1937). Ovogenesis during sexual maturity. The first stage, mitoses in the germinal epithelium, as shown by the colchicine technique. Anat. Rev. 69, 191–5.CrossRefGoogle Scholar
Anderson, L.D. & Hirshfield, A.N. (1992). An overview of follicular development in the ovary: from embryo to the fertilized ovum in vitro . Maryland State Med. J. 41, 614–20.Google Scholar
Anderson, E.L., Baltus, A.E., Roepers-Gajadien, H.L., Hassold, T.J., de Rooij, D.G., van Pelt, A.M.M. & Page, D.C. (2008). Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc. Natl. Acad. Sci. USA 105, 14976–80.CrossRefGoogle ScholarPubMed
Artem'eva, N. (1961). Regenerative capacity of rat ovary after compensatory hypertrophy. Biull. Eksp. Biol. Med. 51, 76–81. [In Russian]CrossRefGoogle Scholar
Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N. & Lovell-Badge, R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Gene Dev. 17, 126–40.CrossRefGoogle ScholarPubMed
Bao, S., Leitch, H.G., Gillich, A., Nichols, J., Tang, F., Kim, S., Lee, C., Zwaka, T., Li, X. & Surani, M.A. (2012). The germ cell determinant blimp1 is not required for derivation of pluripotent stem cells. Cell Stem Cell 11, 110–7.CrossRefGoogle Scholar
Bazer, F.W. (2004). Strong science challenges conventional wisdom: new perspectives on ovarian biology. Reprod. Biol. Endocrinol. 2, 28.CrossRefGoogle ScholarPubMed
Begum, S., Papaioannou, V.E. & Gosden, R.G. (2008). The oocyte population is not renewed in transplanted or irradiated adult ovaries. Hum. Reprod. 23, 2326–30.CrossRefGoogle ScholarPubMed
Bhartiya, D., Sriraman, K., Gunjal, P. & Modak, H. (2012). Gonadotropin treatment augments postnatal oogenesis and primordial follicle assembly in adult mouse ovaries. J. Ovarian Res. 5, 32.CrossRefGoogle ScholarPubMed
Borum, K. (1961). Oogenesis in the mouse. A study of the meiotic prophase. Exp. Cell. Res. 24, 495–507.CrossRefGoogle Scholar
Bristol-Gould, S.K., Kreeger, P.K., Selkirk, C.G., Kilen, S.M., Mayo, K.E., Shea, L.D. & Woodruff, T.K. (2006). Fate of the initial follicle pool: empirical and mathematical evidence supporting its sufficiency for adult fertility. Dev. Biol. 298, 149–54.CrossRefGoogle ScholarPubMed
Bukovsky, A. (2006). Immune system involvement in the regulation of ovarian function and augmentation of cancer. Microsc. Res. Tech. 69, 482–500.CrossRefGoogle ScholarPubMed
Bukovsky, A. (2011a). Immune maintenance of self in morphostasis of distinct tissues, tumour growth and regenerative medicine. Scand. J. Immunol. 73, 159–89.CrossRefGoogle ScholarPubMed
Bukovsky, A. (2011b). Ovarian stem cell niche and follicular renewal in mammals. Anat. Rec. 294, 1284–306.CrossRefGoogle ScholarPubMed
Bukovsky, A. & Caudle, M.R. (2012). Immunoregulation of follicular renewal, selection, POF, and menopause in vivo, vs. neo-oogenesis in vitro, POF and ovarian infertility treatment, and a clinical trial. Reprod. Biol. Endocrinol. 10, 97.CrossRefGoogle ScholarPubMed
Bukovsky, A., Keenan, J.A., Caudle, M.R., Wimalasena, J., Upadhyaya, N.B. & Vanmeter, S.E. (1995). Immunohistochemical studies of the adult human ovary-possible contribution of immune and epithelial factors to folliculogenesis. Am. J. Reprod. Immunol. 33, 323–40.CrossRefGoogle ScholarPubMed
Bukovsky, A., Caudle, M.R., Svetlikova, M. & Upadhyaya, N.B. (2004). Origin of germ cells and formation of new primary follicles in adult human ovaries. Reprod. Biol. Endocrinol. 2, 20.CrossRefGoogle ScholarPubMed
Bukovsky, A., Svetlikova, M. & Caudle, M.R. (2005). Oogenesis in cultures derived from adult human ovaries. Reprod. Biol. Endocrinol. 3, 17.CrossRefGoogle ScholarPubMed
Bukovsky, A., Ayala, M.E., Dominguez, R., Svetlikova, M. & Selleck-White, R. (2007). Bone marrow derived cells and alternative pathways of oogenesis in adult rodents. Cell Cycle 6, 2306–9.CrossRefGoogle ScholarPubMed
Bukovsky, A., Caudle, M.R., Virant-Klun, I., Gupta, S.K., Dominguez, R., Svetlikova, M. & Xu, F. (2009). Immune physiology and oogenesis in fetal and adult humans, ovarian infertility, and totipotency of adult ovarian stem cells. Birth Defects Res. Part C. 87, 64–89.CrossRefGoogle ScholarPubMed
Bunster, E. & Mayer, R.K. (2005). An improved method of parabiosis. Anat Rec. 57, 339–43.CrossRefGoogle Scholar
Burkl, W. & Schiechl, H. (1978). The growth of follicles in the rat ovary under the influence of busulphan and endoxan. Cell Tissue Res. 186, 351–9.CrossRefGoogle ScholarPubMed
Byskov, A.G., Hoyer, P.E., Andersen, C.Y., Kristensen, S.G., Jespersen, A. & Mollgard, K. (2011). No evidence for the presence of oogonia in the human ovary after their final clearance during the first two years of life. Hum. Reprod. 26, 2129–39.CrossRefGoogle ScholarPubMed
Cauffman, G., Van de Velde, H., Liebaers, I. & Van Steirteghem, A. (2005). Oct-4 mRNA and protein expression during human preimplantation development. Mol. Hum. Reprod. 11, 173–81.CrossRefGoogle ScholarPubMed
Crone, M., Levy, E. & Peters, H. (1965). The duration of the premeiotic DNA synthesis in mouse oocytes. Exp. Cell Res. 39, 678–88.CrossRefGoogle ScholarPubMed
Eggan, K., Jurga, S., Gosden, R., Min, I. M. & Wagers, A. J. (2006). Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature 441, 1109–14.CrossRefGoogle ScholarPubMed
Esmaeilian, Y., Gur Dedeoglu, B., Atalay, A. & Erdemli, E. (2012). Investigation of stem cells in adult and prepubertal mouse ovaries. Adv. Biosci. Biotechnol. 3, 936–44.CrossRefGoogle Scholar
Faddy, M.J. (2000). Follicle dynamics during ovarian ageing. Mol. Cell. Endocrinol. 163, 43–8.CrossRefGoogle ScholarPubMed
Faddy, M. & Gosden, R. (2009). Let's not ignore the statistics. Biol. Reprod. 81, 231–2.Google Scholar
Faddy, M.J., Jones, E.C. & Edwards, R.G. (1976). An analytical model for ovarian follicle dynamics. J. Exp. Zool. 197, 173–85.CrossRefGoogle ScholarPubMed
Faddy, M.J., Telfer, E. & Gosden, R.G. (1987). The kinetics of pre-antral follicle development in ovaries of CBA/Ca mice during the first 14 weeks of life. Cell Tissue Kinet. 20, 551–60.Google ScholarPubMed
Franchi, L.L., Mandl, A.M. & Zuckerman, S. (1962). The development of the ovary and the process of oogenesis. In The Ovary (ed. Zuckerman, S.), pp. 1–88. London: Academic Press.Google Scholar
Ghadami, M., El-Demerdash, E., Zhang, D., Salama, S.A., Binhazim, A.A., Archibong, A.E., Chen, X.L., Ballard, B.R., Sairam, M.R. & Al-Hendy, A. (2012). Bone marrow transplantation restores follicular maturation and steroid hormones production in a mouse model for primary ovarian failure. PLoS One 7, e32462.CrossRefGoogle Scholar
Gong, S.P., Lee, S.T., Lee, E.J., Kim, D.Y., Lee, G., Chi, S.G., Ryu, B.K., Lee, C.H., Yum, K.E., Lee, H.J., Han, J.Y., Tilly, J.L. & Lim, J.M. (2010). Embryonic stem cell-like cells established by culture of adult ovarian cells in mice. Fertil. Steril. 93, 2594-U153.CrossRefGoogle ScholarPubMed
Gosden, R.G. (2004). Germline stem cells in the postnatal ovary: is the ovary more like a testis? Hum. Reprod. Update 10, 193–5.CrossRefGoogle Scholar
Gougeon, A. & Notarianni, E. (2011). There is no neo-oogenesis in the adult mammalian ovary. J. Turkish German Gynecol. Assoc. 12, 270–3.CrossRefGoogle ScholarPubMed
Hemsworth, B. & Jackson, H. (1963). Effect of busulphan on the developing ovary in the rat. J. Reprod. Fertil. 6, 229–33.CrossRefGoogle ScholarPubMed
Honda, A., Hirose, M., Hara, K., Matoba, S., Inoue, K., Miki, H., Hiura, H., Kanatsu-Shinohara, M., Kanai, Y., Kono, T., Shinohara, T. & Ogura, A. (2007). Isolation, characterization, and in vitro and in vivo differentiation of putative thecal stem cells. Proc. Natl. Acad. Sci. USA 104, 12389–94.CrossRefGoogle ScholarPubMed
Hu, Y., Bai, Y., Chu, Z., Wang, J., Wang, L., Yu, M., Lian, Z. & Hua, J. (2012). GSK3 inhibitor-BIO regulates proliferation of female germline stem cells from the postnatal mouse ovary. Cell Prolif. 45, 287–98.CrossRefGoogle ScholarPubMed
Hubner, K., Fuhrmann, G., Christenson, L.K., Kehler, J., Reinbold, R., De La Fuente, R., Wood, J., Strauss, J.F., Boiani, M. 3rd & Scholer, H.R. (2003). Derivation of oocytes from mouse embryonic stem cells. Science 300, 1251–6.CrossRefGoogle ScholarPubMed
Hummitzsch, K., Irving-Rodgers, H.F., Hatzirodos, N., Bonner, W., Sabatier, L., Reinhardt, D.P., Sado, Y., Ninomiya, Y., Wilhelm, D. & Rodgers, R.J. (2013). A new model of development of the mammalian ovary and follicles. PLoS One 8, e55578.CrossRefGoogle ScholarPubMed
Imudia, A.N., Wang, N., Tanaka, Y., White, Y.A., Woods, D.C. & Tilly, J.L. (2013). Comparative gene expression profiling of adult mouse ovary-derived oogonial stem cells supports a distinct cellular identity. Fertil. Steril. 100, 1451–1458.CrossRefGoogle ScholarPubMed
Ioannou, J.M. (1967). Oogenesis in adult prosimians. J. Embryol. Exp. Morphol. 17, 139–45.Google ScholarPubMed
Jiang, Y., Zhao, J., Qi, H.-J., Li, X.-L., Zhang, S.-R., Song, D.W., Yu, C.-Y. & Gao, J.-G. (2013). Accelerated ovarian aging in mice by treatment of busulfan and cyclophosphamide. J. Zhejiang. Univ. Sci. B. 14, 318–24.CrossRefGoogle ScholarPubMed
Johnson, J., Canning, J., Kaneko, T., Pru, J.K. & Tilly, J.L. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145–50.CrossRefGoogle ScholarPubMed
Johnson, J., Bagley, J., Skaznik-Wikiel, M., Lee, H.J., Adams, G.B., Niikura, Y., Tschudy, K.S., Tilly, J.C., Cortes, M.L., Forkert, R., Spitzer, T., Iacomini, J., Scadden, D.T. & Tilly, J.L. (2005a). Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 122, 303–15.CrossRefGoogle ScholarPubMed
Johnson, J., Skaznik-Wikiel, M., Lee, H.J., Niikura, Y., Tilly, J.C. & Tilly, J.L. (2005b). Setting the record straight on data supporting postnatal oogenesis in female mammals. Cell Cycle 4, 1471–7.Google ScholarPubMed
Kerr, J.B., Duckett, R., Myers, M., Britt, K.L., Mladenovska, T. & Findlay, J.K. (2006). Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 132, 95–109.CrossRefGoogle ScholarPubMed
Kerr, J.B., Brogan, L., Myers, M., Hutt, K.J., Mladenovska, T., Ricardo, S., Hamza, K., Scott, C.L., Strasser, A. & Findlay, J.K. (2012). The primordial follicle reserve is not renewed after chemical or gamma-irradiation mediated depletion. Reproduction 143, 469–76.CrossRefGoogle ScholarPubMed
Kim, J.M., Liu, H.L., Tazaki, M., Nagata, M. & Aoki, F. (2003). Changes in histone acetylation during mouse oocyte meiosis. J. Cell Biol. 162, 37–46.CrossRefGoogle ScholarPubMed
Kingery, H.M. (1917). Oogenesis in the white mouse. J. Morphol. 30, 261–315.CrossRefGoogle Scholar
Kossowska-Tomaszczuk, K., De Geyter, C., De Geyter, M., Martin, I., Holzgreve, W., Scherberich, A. & Zhang, H. (2009). The multipotency of luteinizing granulosa cells collected from mature ovarian follicles. Stem Cells 27, 210–9.CrossRefGoogle ScholarPubMed
Lee, H.J., Sakamoto, H., Luo, H., Skaznik-Wikiel, M.E., Friel, A.M., Niikura, T., Tilly, J.C., Niikura, Y., Klein, R., Styer, A.K., Zukerberg, L.R., Tilly, J.L. & Rueda, B.R. (2007a). Loss of CABLES1, a cyclin-dependent kinase-interacting protein that inhibits cell cycle progression, results in germline expansion at the expense of oocyte quality in adult female mice. Cell Cycle 6, 2678–84.CrossRefGoogle ScholarPubMed
Lee, H.J., Selesniemi, K., Niikura, Y., Niikura, T., Klein, R., Dombkowski, D.M. & Tilly, J.L. (2007b). Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure. J. Clin. Oncol. 25, 3198–204.CrossRefGoogle Scholar
Lee, Y.-M., Kumar, B.M., Lee, J.-H., Lee, W.-J., Kim, T.-H., Lee, S.-L., Ock, S.-A., Jeon, B.-G., Park, B.-W. & Rho, G.-J. (2013). Characterisation and differentiation of porcine ovarian theca-derived multipotent stem cells. Vet. J. 197, 761–768.CrossRefGoogle ScholarPubMed
Lei, L. & Spradling, A.C. (2013). Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. Proc. Natl. Acad. Sci. U.S.A. 110, 8585–90.CrossRefGoogle ScholarPubMed
Liu, Y.F., Wu, C., Lyu, Q.F., Yang, D.Z., Albertini, D.F., Keefe, D.L. & Liu, L. (2007). Germline stem cells and neo-oogenesis in the adult human ovary. Dev. Biol. 306, 112–20.CrossRefGoogle ScholarPubMed
McLaren, A. (1984). Meiosis and differentiation of mouse germ cells. Symp. Soc. Exp. Biol. 38, 7–23.Google ScholarPubMed
Meirow, D., Lewis, H., Nugent, D. & Epstein, M. (1999). Subclinical depletion of primordial follicular reserve in mice treated with cyclophosphamide: clinical importance and proposed accurate investigative tool. Hum. Reprod. 14, 1903–7.CrossRefGoogle ScholarPubMed
Morita, Y., Manganaro, T.F., Tao, X.J., Martimbeau, S., Donahoe, P.K. & Tilly, J.L. (1999). Requirement for phosphatidylinositol-3′-kinase in cytokine-mediated germ cell survival during fetal oogenesis in the mouse. Endocrinology. 140, 941–9.CrossRefGoogle ScholarPubMed
Nagano, M.C. (2003). Homing efficiency and proliferation kinetics of male germ line stem cells following transplantation in mice. Biol. Reprod. 69, 701–7.CrossRefGoogle ScholarPubMed
Niikura, Y., Niikura, T. & Tilly, J.L. (2009). Aged mouse ovaries possess rare premeiotic germ cells that can generate oocytes following transplantation into a young host environment. Aging 1, 971–8.CrossRefGoogle Scholar
Niikura, Y., Niikura, T., Wang, N., Satirapod, C. & Tilly, J.L. (2010). Systemic signals in aged males exert potent rejuvenating effects on the ovarian follicle reserve in mammalian females. Aging 2, 999–1003.CrossRefGoogle ScholarPubMed
Notarianni, E. (2011). Reinterpretation of evidence advanced for neo-oogenesis in mammals, in terms of a finite oocyte reserve. J. Ovarian Res. 4, 1.CrossRefGoogle ScholarPubMed
Oh, H., Bradfute, S.B., Gallardo, T.D., Nakamura, T., Gaussin, V., Mishina, Y., Pocius, J., Michael, L.H., Behringer, R.R., Garry, D.J., Entman, M.L. & Schneider, M.D. (2003). Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. USA 100, 12313–8.CrossRefGoogle ScholarPubMed
Oktem, O. & Oktay, K. (2009). Current knowledge in the renewal capability of germ cells in the adult ovary. Birth Defects Res. C. 87, 90–5.CrossRefGoogle ScholarPubMed
Pacchiarotti, J., Maki, C., Ramos, T., Marh, J., Howerton, K., Wong, J., Pham, J., Anorve, S., Chow, Y.C. & Izadyar, F. (2010). Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation 79, 159–70.CrossRefGoogle ScholarPubMed
Pansky, B. & Mossman, H.W. (1953). The regenerative capacity of the rabbit ovary. Anat. Rec. 116, 19–51.CrossRefGoogle ScholarPubMed
Parte, S., Bhartiya, D., Telang, J., Daithankar, V., Salvi, V., Zaveri, K. & Hinduja, I. (2011 ). Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells Dev. 20, 1451–64.CrossRefGoogle ScholarPubMed
Parte, S., Bhartiya, D., Manjramkar, D.D., Chauhan, A. & Joshi, A. (2013). Stimulation of ovarian stem cells by follicle stimulating hormone and basic fibroblast growth factor during cortical tissue culture. J. Ovarian Res. 6, 20.CrossRefGoogle ScholarPubMed
Patel, H., Bhartiya, D., Parte, S., Gunjal, P., Yedurkar, S. & Bhatt, M. (2013). Follicle stimulating hormone modulates ovarian stem cells through alternately spliced receptor variant FSH-R3. J. Ovarian Res. 6, 52.CrossRefGoogle ScholarPubMed
Pearl, R. & Schoppe, W.E. (1921). Studies on the physiology of reproduction in the domestic fowl. J. Exp. Zool. 34, 101–18.CrossRefGoogle Scholar
Pelloux, M., Picon, R., Gangnerau, M. & Darmoul, D. (1988). Effects of busulfan on ovarian folliculogenesis, steroidogenesis and anti-Müllerian activity of rat neonates. Acta Endocrinol. 118, 218–26.Google ScholarPubMed
Pelosi, E., Omari, S., Michel, M., Ding, J., Amano, T., Forabosco, A., Schlessinger, D. & Ottolenghi, C. (2013). Constitutively active Foxo3 in oocytes preserves ovarian reserve in mice. Nat. Commun. 4, 1843.CrossRefGoogle ScholarPubMed
Perez, G.I., Robles, R., Knudson, C.M., Flaws, J.A., Korsmeyer, S.J. & Tilly, J.L. (1999). Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat. Genet. 21, 200–3.CrossRefGoogle ScholarPubMed
Peters, H. (1970). Migration of gonocytes into the mammalian gonad and their differentiation. Philos. Trans. Roy. Soc. Lond. B. Biol. Sci. 259, 91–101.Google ScholarPubMed
Peters, H., Levy, E. & Crone, M. (1962). Deoxyribonucleic acid synthesis in oocytes of mouse embryos. Nature 195, 915–6.CrossRefGoogle ScholarPubMed
Richardson, S.J., Senikas, V. & Nelson, J.F. (1987). Follicular depletion during the menopausal transition: evidence for accelerated loss and ultimate exhaustion. J. Clin. Endocrinol. Metab. 65, 1231–7.CrossRefGoogle ScholarPubMed
Santiquet, N., Vallières, L., Pothier, F., Sirard, M.-A., Robert, C. & Richard, F. (2012). Transplanted bone marrow cells do not provide new oocytes but rescue fertility in female mice following treatment with chemotherapeutic agents. Cell. Reprogram. 14, 123–9.CrossRefGoogle Scholar
Selesniemi, K., Lee, H.J., Niikura, T. & Tilly, J.L. (2009). Young adult donor bone marrow infusions into female mice postpone age-related reproductive failure and improve offspring survival. Aging 1, 49–57.CrossRefGoogle Scholar
Shinoda, G., De Soysa, T.Y., Seligson, M.T., Yabuuchi, A., Fujiwara, Y., Huang, P.Y., Hagan, J.P., Gregory, R.I., Moss, E.G. & Daley, G.Q. (2013). Lin28a regulates germ cell pool size and fertility. Stem Cells. 31, 1001–9.CrossRefGoogle ScholarPubMed
Shirota, M., Soda, S., Katoh, C., Asai, S., Sato, M., Ohta, R., Watanabe, G., Taya, K. & Shirota, K. (2003). Effects of reduction of the number of primordial follicles on follicular development to achieve puberty in female rats. Reproduction. 125, 85–94.CrossRefGoogle ScholarPubMed
Song, S.H., Kumar, B.M., Kang, E.J., Lee, Y.M., Kim, T.H., Ock, S.A., Lee, S.L., Jeon, B.G. & Rho, G.J. (2011). Characterization of porcine multipotent stem/stromal cells derived from skin, adipose, and ovarian tissues and their differentiation in vitro into putative oocyte-like cells. Stem Cells Dev. 20, 1359–70.CrossRefGoogle ScholarPubMed
Stimpfel, M., Skutella, T., Cvjeticanin, B., Meznaric, M., Dovc, P., Novakovic, S., Cerkovnik, P., Vrtacnik-Bokal, E. & Virant-Klun, I. (2013). Isolation, characterization and differentiation of cells expressing pluripotent/multipotent markers from adult human ovaries. Cell Tissue Res. 354, 593–607.CrossRefGoogle ScholarPubMed
Szilvassy, S.J., Ragland, P.L., Miller, C.L. & Eaves, C.J. (2003). The marrow homing efficiency of murine hematopoietic stem cells remains constant during ontogeny. Exp. Hematol. 31, 331–8.CrossRefGoogle ScholarPubMed
Szotek, P.P., Chang, H.L., Brennand, K., Fujino, A., Pieretti-Vanmarcke, R., Lo Celso, C., Dombkowski, D., Preffer, F., Cohen, K.S., Teixeira, J. & Donahoe, P.K. (2008). Normal ovarian surface epithelial label-retaining cells exhibit stem/progenitor cell characteristics. Proc. Natl. Acad. Sci. U.S.A. 105, 12469–73.CrossRefGoogle ScholarPubMed
Tilly, J.L. (2001). Commuting the death sentence: how oocytes strive to survive. Nat. Rev. Mol. Cell Biol. 2, 838–48.CrossRefGoogle ScholarPubMed
Torrente, Y., Camirand, G., Pisati, F., Belicchi, M., Rossi, B., Colombo, F., El Fahime, M., Caron, N.J., Issekutz, A.C., Constantin, G., Tremblay, J.P. & Bresolin, N. (2003). Identification of a putative pathway for the muscle homing of stem cells in a muscular dystrophy model. J. Cell Biol. 162, 511–20.CrossRefGoogle Scholar
Vermandevaneck, G.J. (1956). Neo-ovogenesis in the adult monkey-consequences of atresia of ovocytes. Anat. Rec. 125, 207–24.CrossRefGoogle Scholar
Virant-Klun, I., Zech, N., Rozman, P., Vogler, A., Cvjeticanin, B., Klemenc, P., Malicev, E. & Meden-Vrtovec, H. (2008). Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation 76, 843–56.CrossRefGoogle ScholarPubMed
Virant-Klun, I., Rozman, P., Cvjeticanin, B., Vrtacnik-Bokal, E., Novakovic, S., Rulicke, T., Dovc, P. & Meden-Vrtovec, H. (2009). Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev. 18, 137–49.CrossRefGoogle ScholarPubMed
Virant-Klun, I., Skutella, T., Cvjeticanin, B., Stimpfel, M. & Sinkovec, J. (2011a). Serous papillary adenocarcinoma possibly related to the presence of primitive oocyte-like cells in the adult ovarian surface epithelium: a case report. J. Ovarian Res. 4, 13.CrossRefGoogle Scholar
Virant-Klun, I., Skutella, T., Stimpfel, M. & Sinkovec, J. (2011b). Ovarian surface epithelium in patients with severe ovarian infertility: a potential source of cells expressing markers of pluripotent/multipotent stem cells. J. Biomed. Biotechnol. 2011, 381928.CrossRefGoogle ScholarPubMed
Virant-Klun, I., Stimpfel, M. & Skutella, T. (2011c). Ovarian pluripotent/multipotent stem cells and in vitro oogenesis in mammals. Histol. Histopathol. 26, 1071–1082.Google ScholarPubMed
Virant-Klun, I., Skutella, T., Hren, M., Gruden, K., Cvjeticanin, B., Vogler, A. & Sinkovec, J. (2013a). Isolation of small SSEA-4-positive putative stem cells from the ovarian surface epithelium of adult human ovaries by two different methods. Biomed. Res. Int. 2013, 690415.CrossRefGoogle ScholarPubMed
Virant-Klun, I., Skutella, T., Kubista, M., Vogler, A., Sinkovec, J. & Meden-Vrtovec, H. (2013b). Expression of pluripotency and oocyte-related genes in single putative stem cells from human adult ovarian surface epithelium cultured in vitro in the presence of follicular fluid. Biomed. Res. Int. 2013, 861460.CrossRefGoogle ScholarPubMed
Virant-Klun, I., Stimpfel, M., Cvjeticanin, B., Vrtacnik-Bokal, E. & Skutella, T. (2013c). Small SSEA-4-positive cells from human ovarian cell cultures: related to embryonic stem cells and germinal lineage? J. Ovarian Res. 6, 24.CrossRefGoogle ScholarPubMed
Waldeyer-Hartz, W.V. (1870). Eierstock und Ei. Ein Beitrag zur Anatomie und Entwicklungsgeschichte der Sexualorgane. Leipzig: Engelmann. [In German]Google Scholar
Wallace, W.H.B. & Kelsey, T.W. (2010). Human ovarian reserve from conception to the menopause. PLoS One 5, e8772.CrossRefGoogle Scholar
Wang, N. & Tilly, J.L. (2010). Epigenetic status determines germ cell meiotic commitment in embryonic and postnatal mammalian gonads. Cell Cycle 9, 339–49.CrossRefGoogle ScholarPubMed
White, Y.A., Woods, D.C., Takai, Y., Ishihara, O., Seki, H. & Tilly, J.L. (2012). Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat. Med. 18, 413–21.CrossRefGoogle ScholarPubMed
Whiteside, S.T. & Goodbourn, S. (1993). Signal transduction and nuclear targeting: regulation of transcription factor activity by subcellular localisation. J. Cell Sci. 104, 949–55.CrossRefGoogle ScholarPubMed
Woods, D.C. & Tilly, J.L. (2012). The next (re)generation of ovarian biology and fertility in women: is current science tomorrow's practice? Fertil. Steril. 98, 3–10.CrossRefGoogle ScholarPubMed
Woods, D.C., White, Y.A. & Tilly, J.L. (2013). Purification of oogonial stem cells from adult mouse and human ovaries: an assessment of the literature and a view toward the future. Reprod. Sci. 20, 7–15.CrossRefGoogle Scholar
Wright, D.E., Cheshier, S.H., Wagers, A.J., Randall, T.D., Christensen, J.L. & Weissman, I.L. (2001a). Cyclophosphamide/granulocyte colony-stimulating factor causes selective mobilization of bone marrow hematopoietic stem cells into the blood after M phase of the cell cycle. Blood 97, 2278–85.CrossRefGoogle ScholarPubMed
Wright, D.E., Wagers, A.J., Gulati, A.P., Johnson, F.L. & Weissman, I.L. (2001b). Physiological migration of hematopoietic stem and progenitor cells. Science. 294, 1933–6.CrossRefGoogle ScholarPubMed
Yuan, J., Zhang, D., Wang, L., Liu, M., Mao, J., Yin, Y., Ye, X., Liu, N., Han, J. & Gao, Y. (2013). No evidence for neo-oogenesis may link to ovarian senescence in adult monkey. Stem Cells 31, 2538–2550.CrossRefGoogle ScholarPubMed
Zhang, D., Fouad, H., Zoma, W.D., Salama, S.A., Wentz, M.J. & Al-Hendy, A. (2008). Expression of stem and germ cell markers within nonfollicle structures in adult mouse ovary. Reprod. Sci. 15, 139–46.CrossRefGoogle ScholarPubMed
Zhang, P., Lv, L.X. & Xing, W.J. (2010 ). Early meiotic-specific protein expression in post-natal rat ovaries. Reprod. Domest. Anim. 45, e447–53.CrossRefGoogle ScholarPubMed
Zhang, H., Zheng, W.J., Shen, Y., Adhikari, D., Ueno, H. & Liu, K. (2012). Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc. Natl. Acad. Sci. USA 109, 12580–5.CrossRefGoogle ScholarPubMed
Zou, K., Yuan, Z., Yang, Z., Luo, H., Sun, K., Zhou, L., Xiang, J., Shi, L., Yu, Q. & Zhang, Y. (2009). Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat. Cell Biol. 11, 631–6.CrossRefGoogle ScholarPubMed
Zuckerman, S. (1951). The number of oocytes in the mature ovary. Recent Prog. Horm. Res. 6, 63–109.Google Scholar
Zuckerman, S. & Baker, T.G. (1977). The development of the ovary and the process of oogenesis. In The Ovary vol. 1 (eds Zuckerman, S. & Weir, B.J.), pp. 41–67. New York: Academic Press.Google Scholar