Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-19T19:34:13.162Z Has data issue: false hasContentIssue false
  • English
  • Français

Primordial follicular assembly in humans – revisited

Published online by Cambridge University Press:  01 November 2008

A. Maheshwari  and
P. A. Fowler
A. Maheshwari*
Affiliation:
University of Aberdeen, Aberdeen Maternity hospital, Aberdeen AB25 2ZL, Scotland, UK.
P. A. Fowler
Affiliation:
Centre for Reproductive Endocrinology and Medicine, Institute of Medical Sciences, University of Aberdeen, Aberdeen AB25 2ZD, Scotland, UK.
*
All correspondence to: A. Maheshwari. University of Aberdeen, Aberdeen Maternity hospital, Aberdeen AB25 2ZL, Scotland, UK. Tel: +44 1224 554976. e-mail: Abha.maheshwari@abdn.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Recent interest in the initial phases of ovarian follicular formation and development has lead to a number of publications in this area, most of which address the autocrine and paracrine factors involved in primordial follicle activation to primary follicle. Primordial follicle assembly (first step in follicle formation) determines the lifetime supply of primordial follicles and remains a poorly understood phenomenon. Despite a number of recent articles that are concentrating on immuno-histochemistry, basic steps in the process are not clear. Hence, we feel it is time to take a step back and see what is available in the literature and identify the gaps in which future research about primordial follicle assembly in humans needs to be directed.

Keywords

Fetal ovaryFolliculogenesisHumanOvaryPrimordial follicle assembly
Type
Research Article
Information
Zygote , Volume 16 , Issue 4 , November 2008 , pp. 285 - 296
Copyright
Copyright © Cambridge University Press 2008

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

Abir, R., Orvieto, R., Dicker, D., Zukerman, ?., Barnett, M. & Fisch, B. (2002). Preliminary studies on apoptosis in human fetal ovaries. Fertil. Steril. 78, 259–64.CrossRefGoogle ScholarPubMed
Abir, R., Fisch, B., Jin, S., Barnnet, M., Kesler-Icekson, G. & Ao, A. (2004). Expression of stem cell factor and its receptor in human fetal and adult ovaries. Fertil. Steril. 82 (Suppl 3)1235–43.CrossRefGoogle ScholarPubMed
Anderson, R.A., Robinson, L.L., Brooks, J., Spears, N. (2002). Neurotropins and their receptors are expressed in the human fetal ovary. J. Clin. Endocrinol. Metab. 87, 890–7.CrossRefGoogle ScholarPubMed
Baker, T.G. (1963). A quantitative and cytologic study of germ cells in human ovaries. Proc. R. Soc. Lond. B Biol. Sci. 158, 417–33.Google ScholarPubMed
Baker, T.G. & Franchi, L.L. (1967). The fine structure of oogonia and oocytes in human ovaries. J. Cell. Sci. 2, 213–24.CrossRefGoogle ScholarPubMed
Bayne, R.A.L., Martins da Silva, S.J. & Anderson, R.A. (2004). Increased expression of the FIGLA transcription factor is associated with primordial follicle formation in the human fetal ovary. Mol. Hum. Reprod. 10, 373–81.CrossRefGoogle ScholarPubMed
Bendsen, E., Byskov, A.G., Andersen, C.Y. & Westergaard, L.G. (2006). Number of germ cells and somatic cells in human fetal ovaries during the first weeks after sex differentiation. Hum. Reprod. 21, 30–5.CrossRefGoogle ScholarPubMed
Britt, K.L., Saunders, P.K., McPherson, S.J., Misso, M.L., Simpson, E.R. & Findlay, J.K. (2004). Estrogen actions on follicle formation and early follicle development. Biol. Reprod. 71, 1712–23.CrossRefGoogle ScholarPubMed
Byskov, A.G. (1986). Differentiation of mammalian embryonic gonad. Physiol. Rev. 66, 71–117.CrossRefGoogle ScholarPubMed
De Pol, A., Vaccina, F., Forabosco, A., Cavazzuti, E. & Marzona, L. (1997). Apoptosis of germ cells during human prenatal oogenesis. Hum. Reprod. 12, 2235–41.CrossRefGoogle ScholarPubMed
Donovan, P.J. (1998). The germ cell – the mother of all stem cells. Int. J. Dev. Biol. 42, 1043–50.Google ScholarPubMed
Fowler, P.A., Evans, L.W., Groome, N.P., Templeton, A. & Knight, P.G. (1998). Pro-alphaC and follistatin during pregnancy – a longitudinal study of maternal serum inhibin-A, inhibin-B, activin-A, activin-AB. Hum. Reprod. 13, 3530–6.CrossRefGoogle ScholarPubMed
Fulton, N., Martins da Silva, S.J., Bayne, R.A.L. & Anderson, R.A. (2005). Germ cell proliferation and apoptosis in the developing human ovary. Endocrinol. Metab. 90, 4664–70.CrossRefGoogle ScholarPubMed
Gondos, B. & Hobel, C.J. (1973). Interstitial cells in the human fetal ovary. Endocrinology 93, 736–9.CrossRefGoogle ScholarPubMed
Gondos, B. & Zamboni, L. (1969). Ovarian development: the functional importance of germ cell interconnections. Fertil. Steril. 20, 176–89.CrossRefGoogle ScholarPubMed
Gondos, B., Bhiraleus, P. & Hobel, C.J. (1971). Ultrastructural observations on germ cells in human fetal ovaries. Am. J. Obstet. Gynecol. 110, 644–52.CrossRefGoogle ScholarPubMed
Gondos, B., Westergaard, L. & Byskov, A.G. (1986). Initiation of oogenesis in the human fetal ovary: ultrastructural and squash preparation study. Am. J. Obstet. Gynecol. 155, 189–95.CrossRefGoogle ScholarPubMed
Gumienny, T.L, Lambie, E., Hartwieg, E., Horvitz, H.R. & Hengartner, M.O. (1999). Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126, 1011–22.CrossRefGoogle ScholarPubMed
Hartley, P.S, Bayne, R.A.L, Robinson, L.L.L, Fulton, N. & Anderson, R.A. (2002). Developmental changes in expression of myeloid cell leukemia-1 in human germ cells during oogenesis and early folliculogenesis. J. Clin. Endocrinol. Metab. 87, 3417–27.CrossRefGoogle ScholarPubMed
Hirshfield, A.N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43–101.CrossRefGoogle ScholarPubMed
Hoyer, P.E, Byskov, A.G. & Mollgard, K. (2005). Stem cell factor and c-Kit in human primordial germ cells and fetal ovaries. Mol. Cell. Endocrinol. 234, 1–10.CrossRefGoogle ScholarPubMed
Hussein, M.R. (2005). Apoptosis in the ovary: molecular mechanisms. Hum. Reprod. Update 11, 162–78.CrossRefGoogle ScholarPubMed
Kaivooja, N., Jeffery, L.A., Ritvos, O. & Mottershead, D. (2006). SMAD signalling in the ovary. Reprod. Biol. Endocrinol. 4, 21–33.CrossRefGoogle ScholarPubMed
Kezele, P. & Skinner, M.K. (2003). Regulation of primordial follicle assembly and development by estrogens and progesterones: endocrine model of follicle assembly. Endocrinology 144, 3329–37.CrossRefGoogle ScholarPubMed
Kezele, P.R, Ague, J.M., Nilsson, E. & Skinner, M.K. (2005). Alterations in ovarian transcriptome during primordial follicle assembly and development. Biol. Reprod. 72, 241–55.CrossRefGoogle ScholarPubMed
Kim, M.R. & Tilly, J.L. (2004). Current concepts in Bcl-2 family member regulation of female germ cell development and survival. Biochimica et Biophysica Acta 1644, 205–10.CrossRefGoogle ScholarPubMed
Klinkert, E.R, Broekmans, F.J, Looman, C.W., Habbema, J.D. & te Velde, E.R. (2005). Expected poor responders on the basis of an antral follicle count do not benefit from a higher starting dose of gonadotrophins in IVF treatment: a randomized controlled trial. Hum. Reprod. 20, 611–5.CrossRefGoogle Scholar
Konishi, I., Fujii, S., Okamura, H., Parmley, T. & Mori, T. (1986). Development of interstitial cells and ovigerous cords in the human fetal ovary: an ultra-structural study. J. Anat. 148, 121–35.Google Scholar
Kurilo, L.F. (1981). Oogenesis in antenatal development in man. Hum. Genet. 57, 86–92.CrossRefGoogle ScholarPubMed
Martins da Silva, S.J., Bayne, R.A.L., Cambray, N., Hartley, P.S., McNeilly, A.S. & Anderson, R.A. (2004). Expression of activin subunits and receptors in the developing human ovary: activin A promotes germ cell survival and proliferation before primordial follicle formation. Develop. Biol. 266, 334–45.CrossRefGoogle ScholarPubMed
McNatty, K.P., Fidler, A.E., Juengel, J.L., Quirke, L.D., Smith, P.R., Heath, D.A., Lundy, T., O'Connell, A. & Tisdall, D.J. (2000). Growth and paracrine factors regulating follicular formation and cellular function. Mol. Cell. Endocrinol. 163, 11–20.CrossRefGoogle ScholarPubMed
Modi, D.N., Sane, S. & Bhartiya, D. (2003). Accelerated germ cell apoptosis in sex chromosome aneuploid fetal human gonads. Mol. Hum. Reprod. 9, 219–25.CrossRefGoogle ScholarPubMed
Modi, D., Bhartiya, D. & Puri, C. (2006). Developmental expression and cellular distribution of Mullerian inhibiting substance in the primate ovary. Reproduction 132, 443–53.CrossRefGoogle ScholarPubMed
Motta, P.M., Nottola, S.A. & Makabe, S. (1997). Natural history of the female germ cell from its origin to full maturation through prenatal ovarian development. Euro. J. Obstet. Gynecol. Reprod. Biol. 75, 5–10.CrossRefGoogle ScholarPubMed
Pepe, G.J., Billiar, R.B. & Albrecht, E.D. (2006). Regulation of baboon fetal ovarian folliculogenesis by estrogen. Mol. Cell. Endocrinol. 247, 41–6.CrossRefGoogle ScholarPubMed
Pepling, M.E. & Spradling, A.C. (2001). Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Develop. Biol. 234, 339–51.CrossRefGoogle ScholarPubMed
Picton, H.M. (2001). Activation of follicle development: the primordial follicle. Theriogenology 55, 1193–210.CrossRefGoogle ScholarPubMed
Pinkerton, J.H.M, McKay, D.G., Adams, E.C. & Hertig, A.T. (1961). Development of the human ovary—a study using histochemical technics. Obstet. Gynecol. 18, 152–81.Google ScholarPubMed
Robinson, L.L.L., Gaskell, T.L., Saunders, T.K. & Anderson, R.A. (2001a). Germ cell specific expression of c-kit in human fetal gonad. Mol. Hum. Reprod. 7, 845–52.CrossRefGoogle ScholarPubMed
Robinson, L.L.L., Sznadjer, N.A., Riley, S.C. & Anderson, R.A. (2001b). Matrix metalloproteinases and tissue inhibitors of metalloproteinases in human fetal testis and ovary. Mol. Hum. Reprod. 7, 641–8.CrossRefGoogle ScholarPubMed
Roy, S.K. & Albee, L. (2000). Requirement for follicle-stimulating hormone action in the formation of primordial follicles during perinatal ovarian development in the hamster. Endocrinology 141, 4449–56.CrossRefGoogle ScholarPubMed
Satoh, M. (1991). Histogenesis and organogenesis of the gonad in human embryos. J. Anat. 177, 85–107.Google ScholarPubMed
Sawyer, H.R., Smith, P., Heath, D.A., Juengel, J.L., Wakefield, S.J. and McNatty, K.P. (2002). Formation of ovarian follicles during fetal development in sheep. Biol. Reprod. 66, 1134–50.CrossRefGoogle ScholarPubMed
Serafica, M.D., Goto, T. & Trounson, A.O. (2005). Transcripts from a human primordial follicle cDNA library. Hum. Reprod. 20, 2074–91.CrossRefGoogle ScholarPubMed
Sforza, C., Vizzotto, L., Ferrario, V.F. & Forabosco, A. (2003). Position of follicles in normal human ovary during definitive histogenesis. Early Hum. Develop. 74, 27–35.CrossRefGoogle ScholarPubMed
Skinner, M.K. (2005). Regulation of primordial follicle assembly and development. Hum. Reprod. Update 11, 461–71.CrossRefGoogle ScholarPubMed
Spears, N., Molinek, M.D., Robinson, L.L., Fulton, N., Cameron, H., Shimoda, K., Telfer, E.E., Anderson, R.A. & Price, D.J. (2003). The role of neurotrophin receptors in female germ-cell survival in mouse and human. Development 130, 5481–91.CrossRefGoogle ScholarPubMed
Stoop, H., Honecker, F., Cools, M., de Krijger, R., Bokemeyer, C. & Looijenga, L.H.J. (2005). Differentation and development of human female germ cells during prenatal gonadogenesis: an immunohistochemical study. Hum. Reprod. 20, 1466–76.CrossRefGoogle Scholar
Vaskivuo, T.E., Anttonen, M., Herva, R., Billig, H., Dorland, M., te Velde, E.R., Stenback, F., Heikinheimo, M. & Tapanainen, J.S. (2001). Survival of human ovarian follicles from fetal to adult life: apoptosis, apoptosis related proteins, and transcription factor GATA-4. J. Clin. Endocrinol. Metab. 86, 3421–9.Google ScholarPubMed
Voutilainen, R. (1992). Differentiation of fetal gonad. Horm. Res. 38 (Suppl 2), 66–71.CrossRefGoogle ScholarPubMed
Wang, J. & Roy, S.K. (2004). Growth differentiation factor-9 and stem cell factor promote primordial follicle formation in the hamster: modulation by follicle-stimulating hormone. Biol. Reprod. 70, 577–85.CrossRefGoogle ScholarPubMed
Wartenberg, H. (1982). Development of the early human ovary and role of the mesonephros in the differentiation of the cortex. Anat. Embryol. 165, 253–80.CrossRefGoogle ScholarPubMed
Yao, H.H.C, Matzuk, M.M., Jorgez, C.J., Menke, D.B., Page, D.C., Swain, A. & Capel, B. (2004). Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev. Dynamics 230, 210–5.CrossRefGoogle ScholarPubMed