Skip to main content
Log in

Development of the ovarian surface and associated germ cells in the human fetus

A correlated study by scanning and transmission electron microscopy

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The ovarian surface and associated germ cells have been studied in human fetuses from 12 weeks of age until near term, using light, TEM and SEM techniques. The surface epithelium and related cords proliferate extensively, especially at midterm. The cords in the ovarian cortex appear to be linked with ingrowths from the surface epithelium, and both structures have a common basal lamina. Germ cells are always interspersed among the somatic cells of the surface epithelium and associated cords. These results indicate that both the proliferating cords and surface epithelium may contribute to the formation of early follicles. Furthermore, the occurrence, of elements having some of the features of primitive steroidogenic cells in the regions of cordsurface epithelium continuity, suggests that both structures (surface epithelium and cords) contribute somatic cells, which in addition to becoming granulosa cells, might also contribute to the provision of primitive interstitial cells.

Gonocytes tend to migrate through the developing ovarian tissue towards the surface where they become extruded into the peritoneal cavity. This phenomenon might contribute to the reduction in the number of germ cells at birth and parallels the atretic processes within the ovary.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson E, Lee G, Letourneau R, Albertini DF, Meller SM (1976) Cytological observation on the ovarian epithelium in mammals during the reproductive cycle. J Morphol 150:135–166

    Google Scholar 

  • Beck W (1980) Postnatal development of the ovarian surface epithelium. Anat Anz 147:424–436

    Google Scholar 

  • Bjersing L (1977) Ovarian histochemistry. In: Zuckerman S, Weir JB (eds) The Ovary. Academic Press, New York London, pp 303–391

    Google Scholar 

  • Blandau RJ, White BJ, Rumery RE (1963) Observations on the movements of the living primordial germ cells in the mouse. Fertil Steril 14:482–489

    Google Scholar 

  • Byskov AG (1978) The anatomy and ultrastructure of the rete system in the fetal mouse ovary. Biol Reprod 19:720–735

    Google Scholar 

  • Byskov AG (1980) Sexual differentiation of the mammalian ovary. In: Motta PM, Hafez ESE (eds) Biology of the ovary. Martinus Nijihoff, The Hague Boston London, pp 3–15

    Google Scholar 

  • Byskov AG, Lintern-Moore SM (1973) Follicle formation in the immature mouse ovary. The role of rete ovarii. J Anat 116:207–217

    Google Scholar 

  • Byskov AG, Rasmussen G (1973) Ultrastructural studies of the developing follicle. In: Peters H (ed) The development and maturation of the ovary and its function. Excerpta Medica, Amsterdam, pp 55–62

    Google Scholar 

  • Byskov AG, Skakkebaek NE, Stafanger G, Peters H (1977) Influences of ovarian surface epithelium and rete ovarii on follicle formation. J Anat 123:77–86

    Google Scholar 

  • Cajander S (1976) Structural analysis of rabbit ovarian follicles after mating with special reference to the overlying surface epithelium. Cell Tissue Res 173:437–449

    Google Scholar 

  • Cherney DD, Motta PM, Didio LJA (1973) Ovarian villi in rabbits studies with light, scanning and transmission electron microscopy. J de Microsc (Paris) 17:37–40

    Google Scholar 

  • Ferronha MH, David-Ferreira JF (1980) Uptake and transport of an exogenous protein (HRP) by the hamster ovary surface epithelium. J Submicrosc Cytol 12:61–71

    Google Scholar 

  • Gillman J (1948) The development of the gonads in man, with a consideration of the role of fetal endocrines and the histogenesis of ovarian tumors. Contrib Embryol Carnegie Inst 32:81–131

    Google Scholar 

  • Gondos B (1969) Ultrastructure of the germinal epithelium during oogenesis in the rabbit. J Exp Zool 72:465–480

    Google Scholar 

  • Gondos B (1975) Surface epithelium of the developing ovary. Possible correlation with ovarian neoplasia. Am J Pathol 81:303–320

    Google Scholar 

  • Gondos B (1978) Oogonia and oocytes in mammals. In: Jones RE (ed) The vertebrate Ovary. Plenum Press, New York, pp 83–120

    Google Scholar 

  • Gondos B, Bhiraleus P, Hobel CJ (1971) Ultrastructural observations on germ cells in human fetal ovaries. Am J Obstet Gynecol 110:644–652

    Google Scholar 

  • Guraya SS (1977) Recent advances in the morphology, histochemistry and biochemistry of the developing mammalian ovary. Int Rev Cytol 51:49–131

    Google Scholar 

  • Guraya SS, Motta PM (1980) Interstitial cells and related structures. In: Motta PM, Hafez ESE (eds) Biology of the Ovary. Martinus Nijhoff Publ, The Hague Boston London, pp 68–85

    Google Scholar 

  • Haffen K (1977) Sexual differentiation of the ovary. In: Zuckerman S, Weir JB (eds) The ovary, 2nd edn: Vol I. Academic Press, New York, pp 69–112

    Google Scholar 

  • Hafez ESE, Makabe S, Motta PM (1980) Surface ultrastructure of functional and nonfunctional human ovaries. Int J Fertil 25:94–99

    Google Scholar 

  • Hiura M, Fujita H (1977) Electron microscopic observations on the elimination of the oocyte through the peritoneal epithelium in the neonatal mouse ovary. Cell Tissue Res 182:73–79

    Google Scholar 

  • Hoyer PE (1980) Histoenzymology of the human ovary: dehydrogenases directly involved in steroidogenesis. In: Motta PM, Hafez ESE (eds) Biology of the ovary. Martinus Nijihoff Publ, The Hague Boston London, pp 52–67

    Google Scholar 

  • Jeppesen TH (1975) Surface epithelium of the fetal guinea-pig ovary: A light and electron microscopic study. Anat Rec 183:499–516

    Google Scholar 

  • Jones EC (1978) The vertebrate ovary. Comparative biology and evolution. Plenum Press, New York London

    Google Scholar 

  • Jones EC, Krohn PL (1961) The relationship between age, number of oocytes and fertility in virgin and multiparous mice. J Endocrinol 21:469–495

    Google Scholar 

  • Kölliker A (1898) Über die Markkanäle und Markstränge in den Eierstöcken junger Hündinnen. Verh Anat Ges

  • Luft JA (1961) Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9:409–414

    Article  CAS  PubMed  Google Scholar 

  • Merchant-Larios H (1975) Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study. Dev Biol 44:1–21

    Google Scholar 

  • Merchant-Larios H (1978) Ovarian differentiation. In: Jones RE (ed) The vertebrate Ovary. Plenum Press, New York, pp 47–81

    Google Scholar 

  • Merchant-Larios H (1979) Origin of the somatic cells in the rat gonad: an autoradiographic approach. Ann Biol Anim Biochim Biophys 19:1219–1229

    Google Scholar 

  • Mori H, Matsumoto K (1970) On the histogenesis of the ovarian interstitial gland in rabbits. I. Primary interstitial gland. Am J Anat 129:289–306

    Google Scholar 

  • Mossman HW, Duke KL (1973) Comparative morphology of the mammalian ovary. University of Wisconsin Press, Madison W

    Google Scholar 

  • Motta PM (1974) Superficial epithelium and surface invaginations in the cortex of mature rabbit ovaries. A note on the histogenesis of the interstitial cells. Fertil Steril 25:336–347

    Google Scholar 

  • Motta PM, Hafez ESE (1980) Biology of the Ovary. Martinus Nijhoff Publ, The Hague Boston London

    Google Scholar 

  • Motta PM, Makabe S (1981) Morphodynamic changes of the mammalian ovary in normal and some pathological conditions. A scanning electron microscopic study. In: Fujita I, Tanaka K, Tokunagagn J (eds) SEM in Cell Biology and Medicine. Biomed Res Suppl, pp 105–121

  • Motta PM, Van Blerkom J (1975) A scanning electron microscopic study of the luteo-follicular complex. II. Events leading to ovulation. Am J Anat 143:241–264

    Google Scholar 

  • Motta PM, Van Blerkom J (1979) Morphodinamic aspects of the ovarian superficial epithelium as revealed by transmission, scanning and high voltage electron microscopy. Ann Biol Anim Biochim Biophys 19:1259–1265

    Google Scholar 

  • Motta PM, Takeva Z, Bourneva V (1970) A histochemical study of Δ5–3β-hydroxisteroid dehydrogenase activity in the interstitial cells of the mammalian ovary. Experientia 26: 1128–1129

    Google Scholar 

  • Motta PM, Cherney DD, Didio LJ (1971) Scanning and transmission electron microscopy of the ovarian surface in mammals with special reference to ovulation. J Submicrosc Cytol 3:85–100

    Google Scholar 

  • Motta PM, Van Blerkom J, Makabe S (1980) Changes in the surface morphology of ovarian “germinal” epithelium during the reproductive cycle and in some pathological conditions. J Submicrosc Cytol 12:407–425

    Google Scholar 

  • Nilsson O, Munshi SF (1973) Scanning electron microscopy of mouse follicles at ovulation. J Submicrosc Cytol 5:1–6

    Google Scholar 

  • Papadaky L, Beilby JOW (1971) The fine structure of the surface epithelium of the human ovary. J Cell Sci 8:445–465

    Google Scholar 

  • Pelliniemi JL (1975) Ultrastructure of the indifferent gonad in male and female pig embryos. Tissue Cell 8:163–174

    Google Scholar 

  • Peters H (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinol (Kbh) 62:98–116

    Google Scholar 

  • Peters H (1978) Folliculogenesis in mammals. In: Jones RE (ed) The Vertebrate Ovary. Plenum Press, New York, pp 121–144

    Google Scholar 

  • Quattropani SL (1975) Microscopy of ovarian cords and mesothelium in the fetal monkey (Macaca arctoides) and fetal human. Anat Rec 181:454a

    Google Scholar 

  • Rawson JM, Espey L (1977) Concentration of electron dense granules in the rabbit ovarian surface epithelium during ovulation. Biol Reprod 17:561–566

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed  Google Scholar 

  • Van Blerkom J, Motta PM (1979) The cellular Basis of Mammalian Reproduction. Urban & Schwarzenberg, Baltimore Munich

    Google Scholar 

  • Van Wagenen G, Simpson ME (1965) Embryology of the ovary and testis. Homo Sapiens and Macaca mulatta. Yale Univ Press, New Haven

    Google Scholar 

  • Waldeyer W (1870) Eierstock und Ei. Engleman, Leipzig

    Google Scholar 

  • Watson ML (1958) Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol 4:175–177

    Google Scholar 

  • Weakley BS (1969) Differentiation of the surface epithelium of the hamster ovary. An electron microscopic study. J Anat 105:129–147

    Google Scholar 

  • Witschi E (1948) Migration of the germ cells of human embryos from the yolk sac to the primitive gonadal folds. Contr Embr Carnegie Inst Wash 32:67–80

    Google Scholar 

  • Zamboni L (1976) Modulations of follicles cell-oocyte association in sequential stages of mammalian follicle development and maturation. In: Crosignani PG, Mishell DR (eds) Ovulation in the Human. Academic Press, New York, pp 1–30

    Google Scholar 

  • Zamboni L, Merchant H (1973) The fine morphology of mouse primordial germ cells in estragonadal locations. Am J Anat 137:299–336

    Google Scholar 

  • Zamboni L, Bezard J, Mauleon P (1979a) The role of the mesonephros in the development of the sheep fetal ovary. Ann Biol Anim Biochim Biophys 19:1153–1159

    Google Scholar 

  • Zamboni L, Upadhyay S, Bezard J, Luciani JM, Mauleon P (1979b) The role of the mesophros in the development of the mammalian ovary. In: Tozzini RI, Reeves G, Pineda RL (eds) Endocrine physiopathology of the ovary. Elsevier North-Holland, Amsterdam New York, pp 3–42

    Google Scholar 

  • Zuckerman S, Baker TG (1977) The development of the ovary and the process of oogenesis. In: Zuckerman S, Weir JB (eds) The Ovary, Vol I. Academic Press, New York, pp 41–67

    Google Scholar 

  • Zuckerman S, Weir BJ (eds) (1977) The ovary, 2nd ed. Academic Press, New York London

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Motta, P.M., Makabe, S. Development of the ovarian surface and associated germ cells in the human fetus. Cell Tissue Res. 226, 493–510 (1982). https://doi.org/10.1007/BF00214779

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214779

Key words

Navigation