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.
Similar content being viewed by others
References
Boyd JD, Hamilton WJ (1970) The human placenta. Heffer and Sons Ltd, Cambridge
Bulmer JN, Johnson PM (1985) Antigen expression by trophoblast populations in the human placenta and their possible immunobiological relevance. Plancenta 6:127–140
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 31:134–137
Corner GW (1923) The problem of embryonic pathology in mammals, with observations upon intra-uterine mortality in the pig. Am J Anat 31:523–545
Enders AC, Hendrickx AG (1980) Morphological basis of implantation in the rhesus monkey. Prog Reprod Biol 7:270–283
Enders AC, Schlafke S (1971) Penetration of the uterine epithelium during implantation in the rabbit. Am J Anat 132:219–240
Enders AC, Schlafke S (1972) Implantation in the ferret: epithelial penetration. Am J Anat 133:291–326
Enders AC, Schlafke S (1981) Differentiation of the blastocyst of the rhesus monkey. Am J Anat 162:1–21
Enders AC, Hendrickx AG, Schlafke S (1983) Implantation in the rhesus monkey: Initial penetration of endometrium. Am J Anat 167:275–298
Exalto N, Rollang R, Eskes TKAB, Vooij GP (1983) Urogenital III Early pregnancy. Boehringer Ingelheim Int. GmbH, pp 5–41
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 27:31–41
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 49–66
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 6:191–202
Hearn JP (1983) The marmoset monkey (Callithrix jacchus). In: Reproduction in New World Primates. Hearn JP (ed) MTP Press Lancaster, pp 181–215
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 29:127–156
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 31:65–84
Hertig AT, Rock J, Adams EC (1956) A description of 34 human ova within the first 17 days of development. Am J Anat 98:435–494
Hill JP (1932) The developmental history of the primates. Philos Trans R Soc Lond [Biol] 221:45–178
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 69:613–621
Houston ML (1971) Placenta In: Embryology of the Baboon. AG Hendrickx (ed) University of Chicago Press, Chicago
Hsi B-L, Yeh C-JG, Faulk WP (1984) Class I antigens of the major histocompatability complex on cytotrophoblast of human chorion laeve. Immunology 52:621–629
Kurman RJ, Colleen SM, Hao-Chia C (1984) Intermediate trophoblast: A distinctive form of trophoblast with specific morphological, biological and functional features. Placenta 5:349–370
Lind T, McFadyen IR (1986) Human pregnancy failure. Lancet I, pp 91–92
Luckett WP (1978) Origin and differentiation of the yolk sac and extraembryonic mesoderm in presomite human and rhesus monkey embryos. Am J Anat 152:59–98
Mollenhauer HH (1964) Plastic embedding mixture for use in electron microscopy. Stain Technol 39:111–114
Moore HDM, Gems S, Hearn JP (1985) Early implantation stages in the marmoset monkey (Callithrix jacchus). Am J Anat 172:265–278
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 531
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 207–233
Redman CWG, McMichael AJ, Stirrats GM, Sunderland CA, Ting A (1984) Class I major histocompatibility complex antigens on human extravillous trophoblast. Immunology 52:457–468
Reinius S, Fritz GR, Knobil E (1973) Ultrastructure and endocrinological correlates of an early implantation site in the rhesus monkey. J Reprod Fertil 32:171–173
Reynold ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212
Sharma V, Riddle A, Ford N, Mason B, Campbell S (1986) Pregnancy failure in in vitro fertilisation. Lancel I, p 1391
Smith CA, Monaghan P, Neville AM (1984) Basal clear cells of the normal human breast. Virchows Arch [A] 402:319–329
Stempak JG, Ward RT (1964) An improved staining method for electron microscopy. J Cell Biol 22:697–701
Summers PM (1986) Personal communication
Terzakis JA (1963) The ultrastructure of normal human first trimester placenta. J Ultrastruct Res 9:268–284
Tighe JR, Garrod PR, Curran RC (1967) The trophoblast of human chorionic villus. J Pathol Bacteriol 93:559–567
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 27:1–66
Wynn RM (1972) Cytotrophoblast specializations: An ultrastructural study of the human placenta. Am J Obstet Gynecol 114:339–353
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Smith, C.A., Moore, H.D.M. & Hearn, J.P. The ultrastructure of early implantation in the marmoset monkey (Callithrix jacchus). Anat Embryol 175, 399–410 (1987). https://doi.org/10.1007/BF00309853
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00309853