Germ and somatic cell interactions during gonadal morphogenesis

  • Horacio Merchant-Larios
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 2)


The extragonadal origin of primordial germ cells (PGCs) is now accepted unanimously (1). From the point of view of gonadal morphogenesis, interaction between germ and somatic cell lines is viewed as the interaction between two cell types differing in the time and place of their appearance. The gonad is different from other organs which have been studied as models of morphogenesis (2). The fundamental difference between gonadal morphogenesis and that of other organs is that, although the basic morphogenetic processes (localized cell division, cell movements, programmed cell death, modifications in the extracellular matrix, and cellular differentiation) take place in the gonad, these processes can be affected by the presence of ‘foreign’ cells, i.e., the PGCs. A series of interactions between germ and somatic cell lines can be established for each stage of gonadal morphogenesis. This chapter will describe somatic cell interactions and the roles played by PGCs in the two principal morphogenetic stages through which the gonad passes during its development: an undifferentiated stage and sexual differentiation.


Germ Cell Somatic Cell Basal Lamina Gonadal Development Primordial Germ Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Nieuwkoop PD, Sutasurya LA: Primordial germ cells in the chordates. Embryogenesis and Phylogenesis, Cambridge, Cambridge University Press, 1979.Google Scholar
  2. 2.
    Wolpert L: Positional information and pattern formation. Curr Top Dev Biol (6): 183–224, 1971.PubMedCrossRefGoogle Scholar
  3. 3.
    Mossman HW, Duke KL: The Mammalian Ovary, Madison, University of Wisconsin Press, 1973.Google Scholar
  4. 4.
    Swartz WJ: Effect of steroids on definitive localization of primordial germ cells in the chick embryo. Am J Anat (142): 499–513, 1975.PubMedCrossRefGoogle Scholar
  5. 5.
    Dubois R, Cumminge D: Chimiotactisme et organization biologique. Etude de l’installation de le lingnée germinale dans les ébauches gonadal somatic cells. The most plausible origin would be that of a ‘gonadal blastema’ formed by the condensation of gonadiques chez Tembryon de poulet. Ann Biol (13): 241–258, 1974.Google Scholar
  6. 6.
    Didier E, Fargeix N, Bergaud Y: Age-dependent control exerted by the somatic part of the gonad upon gonocyte proliferation in the chick embryo. Dev Biol (77): 488–493, 1980.PubMedCrossRefGoogle Scholar
  7. 7.
    Mintz B, Russell ES: Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool (134): 207–238, 1957.PubMedCrossRefGoogle Scholar
  8. 8.
    Zamboni L, Bezard J, Mauleon P: The role of the mesonephros in the development of the sheep fetal ovary. Ann Biol Anim Bioch Biophys (19): 1153–1178, 1979.CrossRefGoogle Scholar
  9. 9.
    Upadhay S, Luciano JM, Zamboni L: The role of mesonephros in the development of the mouse testis and its excurrent pathways. In: Development and function of reproductive organs-V workshop on development and function of reproductive organs. Copenhagen, July 6–9, 1981. Byskov AG, Peters H (eds), Amsterdam, Excerpta Medica, 1981, pp 18–27.Google Scholar
  10. 10.
    Wartenberg H: The influence of the mesonephric blastema on gonadal development and sexual differentiation. Copenhagen, July 6–9, 1981. Byskov AG, Peters H (eds), Amsterdam, Excerpta Medica, 1981, pp 3–12.Google Scholar
  11. 11.
    Deanesly R: Follicle formation in guinea-pigs and rabbits: a comparative study with notes on the rete ovarii. J Reprod Fert (45): 371–374, 1975.CrossRefGoogle Scholar
  12. 12.
    Dang DC, Fouquet JP: Differentiation of the fetal gonad of Macaca Fascicularis with special reference to the testis. Ann Biol Anim Bioch Biophys (19): 1197–1209, 1979.CrossRefGoogle Scholar
  13. 13.
    Merchant-Larios H: Origin of the somatic cells in the rat gonad: an autoradiographic approach. Ann Biol Anim Bioch Biophys (19): 1219–1229, 1979.CrossRefGoogle Scholar
  14. 14.
    Yamada T: Cellular and subcellular events in wolffian lens regeneration. In: Current topics in developmental biology. Moscona AA, Monroy A (eds), New York, Academic Press, pp 247–283, 1967.Google Scholar
  15. 15.
    Franchi LL, Mandl Am, Zuckerman S: The development of the ovary and the process of oogenesis. In: The ovary I. Zuckerman S (ed), New York, Academic Press, 1962, pp 1–88.Google Scholar
  16. 16.
    Merchant-Larios H, Villaplando I: Ultrastructural events during early gonadal development in Rana pipiens and Xenopus Laevis. Anat Rec (199): 349–360, 1981.PubMedCrossRefGoogle Scholar
  17. 17.
    Witschi E: Biochemistry of sex differentiation in vertebrate embryos. In: The biochemistry of animal development, Weber R (ed), New York, Academic Press, 1967, pp 193–225.Google Scholar
  18. 18.
    Vannini E: Organogénèse des gonades et déterminisme du sexe chez les amphibiens et les amniotes. Arch Anat Micr Exp (39): 295–313, 1952.Google Scholar
  19. 19.
    Humphrey RR: The development and sex differentiation of the gonad in the wood frog (Rana sylvatica) Following extirpation or orthotopic implantation of the intermediate segment and adjacent mesoderm. J Exp Zool (65): 243–269, 1933.CrossRefGoogle Scholar
  20. 20.
    Cambar R, Mesnage J: L’agénésie expérimentale du mésonéphros n’ influence pas le développement de la glande génitale chez les Amphibiens Anoures. C R Acad Sci Paris (257): 4021–4023, 1963.PubMedGoogle Scholar
  21. 21.
    Bishop-Calamé S: Etude expérimentale de Y organogénèse du système uro-génitale de l’embryon de poulet. Arch Anat Micr Morph Exp (55) (Supp. # 2): 215, 1966.PubMedGoogle Scholar
  22. 22.
    Reyss-Brion M, Popova L, Merchant-Larios H: Unpublished observations.Google Scholar
  23. 23.
    Bernfield MR, Cohn RH, Banerjee SB: Glucosaminoglycans and epithelial organ formation. Am Zool (13): 1067–1083, 1973.Google Scholar
  24. 24.
    Kelley RO, Bluemink JG: An ultrastructual analysis of cell and matrix differentiation during early limb development in Xenopus laevis. Dev Biol (37): 1–17, 1974.PubMedCrossRefGoogle Scholar
  25. 25.
    Cutler LS, Chaudhry AP: Intercellular contacts at the epithelial-mesenchymal interface during the prenatal development of the rat submandibular gland. Dev Biol (33): 229–240, 1973.PubMedCrossRefGoogle Scholar
  26. 26.
    Merchant-Larios H: Ultrastructural events in horse gonadal morphogenesis. J Reprod Fert (27 supp): 479–485, 1979.Google Scholar
  27. 27.
    Peters H, McNatty PJ: The ovary: a correlation of structure and function in mammals, London, Granada Publishing, 1980.Google Scholar
  28. 28.
    Ohno S: Life history of female germ cells in mammals. Proc. 2nd int conf on congenital malformations. New York, Int Med Congr Ltd, 1963, pp 36–42.Google Scholar
  29. 29.
    Carr DH, Haggar RA, Har AG: Germ cells in the ovaries of XO female infants. Am J Clin Pathol (49): 521–526, 1968.PubMedGoogle Scholar
  30. 30.
    Burgoyne PS: The role of the sex chromosomes in mammalian germ cell differentiation. Ann Biol anim Bioch Biophys (18): 317–325, 1978.CrossRefGoogle Scholar
  31. 31.
    Mystkowska ET, Tarkowski AK: Behaviour of germ cells and sexual differentiation in late embryonic and early postnatal mouse chimaeras. J Embyol Exp Morph (23): 395–405, 1970.Google Scholar
  32. 32.
    McLaren A, Chandley AC, Kofman-Alfaro A: A study of meiotic germ cells in the gonads of foetal mouse chimaeras. J Embryol Exp Morph (27): 515–524, 1972.PubMedGoogle Scholar
  33. 33.
    Byskov AG, Saxen L: Induction of meiosis in fetal mouse testis in vitro. Dev Biol (52): 193–200, 1976.PubMedCrossRefGoogle Scholar
  34. 34.
    O WS, Baker TG: Germinal and somatic cell interrelationships in gonadal sex differentiation. Ann Biol Anim Bioch Biophys (18): 351–357, 1978.CrossRefGoogle Scholar
  35. 35.
    Tsafriri A, Pomerantz SH, Channing CP: Inhibition of ovocyte maturation by porcine follicular fluid: partial characterization of the inhibitor. Biol Reprod (14): 511–516, 1976.PubMedCrossRefGoogle Scholar
  36. 36.
    Dufaure PH: Recherches descriptives et expérimentales sur les modalités et facteurs du développement de l’appareil génital chez le lézard vivipare (Lacerte vivipare). Arch Anat Micr Morph Exp. (55, supp): 437–537, 1966.Google Scholar
  37. 37.
    Watchel SS, Ohno S, Koo GC, Boyse EA: Possible role for H-Y antigen in the primary determination of sex. Nature (257): 235–236, 1975.CrossRefGoogle Scholar
  38. 38.
    Gillman J: 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 Washington (32): 81–83, 1948.Google Scholar
  39. 39.
    Ohno S, Nagai Y, Ciccarese S, Iwata H: Testis organizing H-Y antigen and the primary sex-determining mechanism of mammals. Rec Progr Horm Res (35): 449–476, 1979.PubMedGoogle Scholar
  40. 40.
    Zenzes MT, Wolf U, Gunther E, Engel W: Studies on the function of H- Y antigen: dissociation and reorganization experiments on rat gonadal tissue. Cytogenet Cell Genet (20): 365–372, 1978.PubMedCrossRefGoogle Scholar
  41. 41.
    Ohno S, Nagai Y, Ciccarese S: Testicular cells lysostripped of H-Y antigen organize ovarian folliclelike aggregates. Cytogenet Cells Genet (20): 351–364, 1978.CrossRefGoogle Scholar
  42. 42.
    Nagai Y, Ciccarese S, Ohno S: The identification of human H-Y antigen and testicular transformation induced by its interaction with the receptor site of bovine fetal ovarian cells. Differentiation (13): 155–164, 1979.PubMedCrossRefGoogle Scholar
  43. 43.
    Müller U, Zenzes MT, Wolf U, Engel W, Weniger JP: Appearance of H-W (H-Y) antigen in the gonads of oestradiol sex-reversed male chicken embryos. Nature (280): 142–144, 1979.PubMedCrossRefGoogle Scholar
  44. 44.
    Wachtel SS, Bresler PA, Koide SS: Does H-Y antigen induce the heterogametic ovary? Cell (20): 859–864, 1980.PubMedCrossRefGoogle Scholar
  45. 45.
    Bounoure L: Sur le développement sexuel des glandes génitales de la grenouille en l’absence des gonocytes. Arch Anat Micr Morph Exp (39): 247–256, 1950.Google Scholar
  46. 46.
    Padoa E: I differenziamiento sesualle dele gonadi di Rana esculenta rese stenli dall’irradiamento con ultravioletto delle indivise. Boll Zool (31): 811–825, 1964.CrossRefGoogle Scholar
  47. 47.
    Simon D: Organogénese et différentiation sexuelle des glandes génitales de l’embryon de poulet en l’absence totale des cellules germinales. C R Acad Sci Paris (251): 449–451, 1960.PubMedGoogle Scholar
  48. 48.
    Mc Carrey JR, Abbot UK: Chick gonad differentiation following excision of primordial germ cells. Dev Biol (66): 256–265, 1978.PubMedCrossRefGoogle Scholar
  49. 49.
    Merchant H: Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study. Dev Biol (44): 1–21, 1975.PubMedCrossRefGoogle Scholar
  50. 50.
    Merchant-Larios H: The roles of germ cells in the morphogenesis and cytodifferentiation of the rat ovary. In: Progress in differentiation research. Müller-Bérat N Company (ed), Amsterdam, North Holland publishing 1976, pp 453–462.Google Scholar
  51. 51.
    Ohno S, Matsunaga T: The role of H-Y plasma membrane antigen in the evolution of the chromosomal sex determining mechanism. In: Levels of genetic control in development. Subtelney S, Abbot UK (eds), New York, Alan R Liss Inc, 1981, pp 235–246.Google Scholar
  52. 52.
    Merchant-Larios H, Centeno B: Morphogenesis of the ovary from the sterile W/W mouse. In: Advances in the morphology of cells and tissues. Acosta Vidrio E, Galina MA (eds), New York, Alan R Liss Inc, 1981, pp 383–392.Google Scholar
  53. 53.
    Benirschke K, Brownhill LE, Beath MM: Somatic chromosomes of the horse, the donkey and their hybrids, the mule and the hinney. J Reprod Fert (4): 319–326, 1962.CrossRefGoogle Scholar
  54. 54.
    Singh RP, Carr DH: The anatomy and histology of XO human embryos and fetuses. Anat Rec (155): 369–384, 1966.PubMedCrossRefGoogle Scholar
  55. 55.
    Froland A, Lykke A, Zachau-Christiansen B: Ovarian dysgenesis (Turner’s dyndrome) in the newborn. Acta Path Microbiol Scand (57): 21, 1963.CrossRefGoogle Scholar
  56. 56.
    Jones WH,ScottWW: Turner’s syndrome and other conditions with streak gonads. In: Hermaphroditism, genital anomalies and related endocrine disorders. JonesHW,ScottWW (eds), Baltimore, the Williams and Wilkins Co, 1971, pp 76–96Google Scholar
  57. 57.
    Fortune JE, Armstrong DT: Androgen production by theca and granulosa isolated from proestrus rat follicles. Endrocrinology (100): 1341–1347, 1977.CrossRefGoogle Scholar

Copyright information

© Martinus Nijhoff Publishers, Boston, The Hague, Dordrecht, Lancaster 1984

Authors and Affiliations

  • Horacio Merchant-Larios
    • 1
  1. 1.Instituto de Investigaciones BiomédicasUniversidad Nacional Autónoma de México Ciudad UniversitariaMéxico, D.FMexico

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