Anatomy and Embryology

, Volume 175, Issue 3, pp 399–410 | Cite as

The ultrastructure of early implantation in the marmoset monkey (Callithrix jacchus)

  • Caroline A. Smith
  • H. D. M. Moore
  • J. P. Hearn
Article

Summary

The ultrastructural morphology of the initial stages of implantation in the marmoset monkey (Callithrix jacchus) was studied in pregnant monkeys at known time intervals after ovulation. The earliest samples, obtained 13 days after ovulation, displayed both cytotrophoblast and syncytiotrophoblast. The cytotrophoblast was restricted to the blastocoel, whilst syncytiotrophoblast intruded to the endometrial basal lamina. At later stages, days 16 and 19 after ovulation, both cytotrophoblast and syncytiotrophoblast had extended laterally around the uterus, and the syncytiotrophoblast also extended deeper into the maternal tissnes. The mesoderm layer was first discernible at 19 days after ovulation. At 23 days after ovulation the syncytiotrophoblast surrounded the maternal blood vessels entirely. In this study syncytiotrophoblast was not observed to breach the maternal blood vessels, even at 31 days after ovulation. Early cytotrophoblast columns could be seen at 31 days after ovulation. The endothelial cells lining the maternal blood vessels displayed hypertrophy from the earliest stages (day 13) onwards, although a true decidual response was only observed in samples of 23 and 31 days after ovulation.

Key words

Implantation Marmoset Ultrastructure 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Boyd JD, Hamilton WJ (1970) The human placenta. Heffer and Sons Ltd, CambridgeGoogle Scholar
  2. Bulmer JN, Johnson PM (1985) Antigen expression by trophoblast populations in the human placenta and their possible immunobiological relevance. Plancenta 6:127–140Google Scholar
  3. Chartier M, Roger M, Barrat J, Michelon B (1979) Measurement of plasma human chorionic gonadotropin (hCG) and β-hCG activities in the late luteal phase; evidence of the occurrence of spontaneous menstrual abortions in infertile women. Fertil Steril 31:134–137Google Scholar
  4. Corner GW (1923) The problem of embryonic pathology in mammals, with observations upon intra-uterine mortality in the pig. Am J Anat 31:523–545Google Scholar
  5. Enders AC, Hendrickx AG (1980) Morphological basis of implantation in the rhesus monkey. Prog Reprod Biol 7:270–283Google Scholar
  6. Enders AC, Schlafke S (1971) Penetration of the uterine epithelium during implantation in the rabbit. Am J Anat 132:219–240Google Scholar
  7. Enders AC, Schlafke S (1972) Implantation in the ferret: epithelial penetration. Am J Anat 133:291–326Google Scholar
  8. Enders AC, Schlafke S (1981) Differentiation of the blastocyst of the rhesus monkey. Am J Anat 162:1–21Google Scholar
  9. Enders AC, Hendrickx AG, Schlafke S (1983) Implantation in the rhesus monkey: Initial penetration of endometrium. Am J Anat 167:275–298Google Scholar
  10. Exalto N, Rollang R, Eskes TKAB, Vooij GP (1983) Urogenital III Early pregnancy. Boehringer Ingelheim Int. GmbH, pp 5–41Google Scholar
  11. Fisher SJ, Leitch MS, Kantor MS, Basbaum CB, Kramer RH (1985). Degradation of extracellular matrix by the trophoblastic cells of first-trimester human placentas. J Cell Biochem 27:31–41Google Scholar
  12. Hamilton WJ, Boyd JD, Mossman HW (1945) The implantation of the blastocyst and the development of the foetal membranes, placenta and decidua. In: Human embryology. Pub Heffer & Sons Ltd., Cambridge, pp 49–66Google Scholar
  13. Hearn JP, Lunn SF (1975) The reproduction biology of the marmoset monkey (Callithrix jacchus). In: Breeding simians for developmental biology. Laboratory animals handbook. Laboratory Animals Ltd., Sevenoaks 6:191–202Google Scholar
  14. Hearn JP (1983) The marmoset monkey (Callithrix jacchus). In: Reproduction in New World Primates. Hearn JP (ed) MTP Press Lancaster, pp 181–215Google Scholar
  15. Hertig AT, Rock J (1941) Two human ova of the pre-villous stage having an ovulation age of about eleven and twelve days respectively. Carnegie Contrib. Embryol 29:127–156Google Scholar
  16. Hertig AT, Rock J (1945) Two human ova of the pre-villous stage, having a developmental age of about seven and nine days respectively. Carnegie Contrib Embryol 31:65–84Google Scholar
  17. Hertig AT, Rock J, Adams EC (1956) A description of 34 human ova within the first 17 days of development. Am J Anat 98:435–494Google Scholar
  18. Hill JP (1932) The developmental history of the primates. Philos Trans R Soc Lond [Biol] 221:45–178Google Scholar
  19. Hodges JK, Henderson C, Hearn JP (1983) Relationship between ovarian placental steroid production during early pregnancy in the marmoset monkey (Callithrix jacchus). J Reprod Fertil 69:613–621Google Scholar
  20. Houston ML (1971) Placenta In: Embryology of the Baboon. AG Hendrickx (ed) University of Chicago Press, ChicagoGoogle Scholar
  21. Hsi B-L, Yeh C-JG, Faulk WP (1984) Class I antigens of the major histocompatability complex on cytotrophoblast of human chorion laeve. Immunology 52:621–629Google Scholar
  22. Kurman RJ, Colleen SM, Hao-Chia C (1984) Intermediate trophoblast: A distinctive form of trophoblast with specific morphological, biological and functional features. Placenta 5:349–370Google Scholar
  23. Lind T, McFadyen IR (1986) Human pregnancy failure. Lancet I, pp 91–92Google Scholar
  24. Luckett WP (1978) Origin and differentiation of the yolk sac and extraembryonic mesoderm in presomite human and rhesus monkey embryos. Am J Anat 152:59–98Google Scholar
  25. Mollenhauer HH (1964) Plastic embedding mixture for use in electron microscopy. Stain Technol 39:111–114Google Scholar
  26. Moore HDM, Gems S, Hearn JP (1985) Early implantation stages in the marmoset monkey (Callithrix jacchus). Am J Anat 172:265–278Google Scholar
  27. O'Rahilly R (1973) Developmental stages in human embryos Part A: Embryos of the first three weeks (Stages 1–9). Carnegie Inst. Washington Publ, p 531Google Scholar
  28. Owers N, Blandau RJ (1971) Proteolytic activity of the rat and guinea pig blastocyst in vitro. In: Blandau biology of the blastocyst, University of Chicago Press, Chicago, pp 207–233Google Scholar
  29. Redman CWG, McMichael AJ, Stirrats GM, Sunderland CA, Ting A (1984) Class I major histocompatibility complex antigens on human extravillous trophoblast. Immunology 52:457–468Google Scholar
  30. Reinius S, Fritz GR, Knobil E (1973) Ultrastructure and endocrinological correlates of an early implantation site in the rhesus monkey. J Reprod Fertil 32:171–173Google Scholar
  31. Reynold ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212Google Scholar
  32. Sharma V, Riddle A, Ford N, Mason B, Campbell S (1986) Pregnancy failure in in vitro fertilisation. Lancel I, p 1391Google Scholar
  33. Smith CA, Monaghan P, Neville AM (1984) Basal clear cells of the normal human breast. Virchows Arch [A] 402:319–329Google Scholar
  34. Stempak JG, Ward RT (1964) An improved staining method for electron microscopy. J Cell Biol 22:697–701Google Scholar
  35. Summers PM (1986) Personal communicationGoogle Scholar
  36. Terzakis JA (1963) The ultrastructure of normal human first trimester placenta. J Ultrastruct Res 9:268–284Google Scholar
  37. Tighe JR, Garrod PR, Curran RC (1967) The trophoblast of human chorionic villus. J Pathol Bacteriol 93:559–567Google Scholar
  38. Wislocki GB, Streeter GL (1938) On the placentation of the macaque (Macaca mulatta) from the time of implantation until the formation of definitive placenta. Contrib Embryol Carnegie Inst 27:1–66Google Scholar
  39. Wynn RM (1972) Cytotrophoblast specializations: An ultrastructural study of the human placenta. Am J Obstet Gynecol 114:339–353Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • Caroline A. Smith
    • 1
  • H. D. M. Moore
    • 1
  • J. P. Hearn
    • 1
  1. 1.MRC/AFRC Comparative Physiology Research Group, The Institute of ZoologyThe Zoological Society of LondonLondonUnited Kingdom

Personalised recommendations