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.
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
Beck W (1980) Postnatal development of the ovarian surface epithelium. Anat Anz 147:424–436
Bjersing L (1977) Ovarian histochemistry. In: Zuckerman S, Weir JB (eds) The Ovary. Academic Press, New York London, pp 303–391
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
Byskov AG (1978) The anatomy and ultrastructure of the rete system in the fetal mouse ovary. Biol Reprod 19:720–735
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
Byskov AG, Lintern-Moore SM (1973) Follicle formation in the immature mouse ovary. The role of rete ovarii. J Anat 116:207–217
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
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
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
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
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
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
Gondos B (1969) Ultrastructure of the germinal epithelium during oogenesis in the rabbit. J Exp Zool 72:465–480
Gondos B (1975) Surface epithelium of the developing ovary. Possible correlation with ovarian neoplasia. Am J Pathol 81:303–320
Gondos B (1978) Oogonia and oocytes in mammals. In: Jones RE (ed) The vertebrate Ovary. Plenum Press, New York, pp 83–120
Gondos B, Bhiraleus P, Hobel CJ (1971) Ultrastructural observations on germ cells in human fetal ovaries. Am J Obstet Gynecol 110:644–652
Guraya SS (1977) Recent advances in the morphology, histochemistry and biochemistry of the developing mammalian ovary. Int Rev Cytol 51:49–131
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
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
Hafez ESE, Makabe S, Motta PM (1980) Surface ultrastructure of functional and nonfunctional human ovaries. Int J Fertil 25:94–99
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
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
Jeppesen TH (1975) Surface epithelium of the fetal guinea-pig ovary: A light and electron microscopic study. Anat Rec 183:499–516
Jones EC (1978) The vertebrate ovary. Comparative biology and evolution. Plenum Press, New York London
Jones EC, Krohn PL (1961) The relationship between age, number of oocytes and fertility in virgin and multiparous mice. J Endocrinol 21:469–495
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
Merchant-Larios H (1975) Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study. Dev Biol 44:1–21
Merchant-Larios H (1978) Ovarian differentiation. In: Jones RE (ed) The vertebrate Ovary. Plenum Press, New York, pp 47–81
Merchant-Larios H (1979) Origin of the somatic cells in the rat gonad: an autoradiographic approach. Ann Biol Anim Biochim Biophys 19:1219–1229
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
Mossman HW, Duke KL (1973) Comparative morphology of the mammalian ovary. University of Wisconsin Press, Madison W
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
Motta PM, Hafez ESE (1980) Biology of the Ovary. Martinus Nijhoff Publ, The Hague Boston London
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
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
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
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
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
Nilsson O, Munshi SF (1973) Scanning electron microscopy of mouse follicles at ovulation. J Submicrosc Cytol 5:1–6
Papadaky L, Beilby JOW (1971) The fine structure of the surface epithelium of the human ovary. J Cell Sci 8:445–465
Pelliniemi JL (1975) Ultrastructure of the indifferent gonad in male and female pig embryos. Tissue Cell 8:163–174
Peters H (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinol (Kbh) 62:98–116
Peters H (1978) Folliculogenesis in mammals. In: Jones RE (ed) The Vertebrate Ovary. Plenum Press, New York, pp 121–144
Quattropani SL (1975) Microscopy of ovarian cords and mesothelium in the fetal monkey (Macaca arctoides) and fetal human. Anat Rec 181:454a
Rawson JM, Espey L (1977) Concentration of electron dense granules in the rabbit ovarian surface epithelium during ovulation. Biol Reprod 17:561–566
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
Van Blerkom J, Motta PM (1979) The cellular Basis of Mammalian Reproduction. Urban & Schwarzenberg, Baltimore Munich
Van Wagenen G, Simpson ME (1965) Embryology of the ovary and testis. Homo Sapiens and Macaca mulatta. Yale Univ Press, New Haven
Waldeyer W (1870) Eierstock und Ei. Engleman, Leipzig
Watson ML (1958) Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol 4:175–177
Weakley BS (1969) Differentiation of the surface epithelium of the hamster ovary. An electron microscopic study. J Anat 105:129–147
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
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
Zamboni L, Merchant H (1973) The fine morphology of mouse primordial germ cells in estragonadal locations. Am J Anat 137:299–336
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
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
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
Zuckerman S, Weir BJ (eds) (1977) The ovary, 2nd ed. Academic Press, New York London
Author information
Authors and Affiliations
Rights 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
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00214779