Implantation in the marmoset monkey: Expansion of the early implantation site

Abstract

This study was initiated to examine the early stages of trophoblast adhesion and invasion during implantation in the marmoset. Seven implantation sites were found in the uteri of four marmosets taken between days 13 and 15 of gestation. Three implantation sites in two uteri were examined in detail by electron microscopy. Between days 13 and 15, the marmoset implantation site expanded peripherally by adding areas where syncytial trophoblast penetrated between uterine luminal epithelial cells. Such penetrating masses often bridged openings of endometrial glands, shared junctional complexes with the uterine epithelial cells between which they are infiltrating, and subsequently reached the residual basal lamina of the uterine luminal epithelium. Centripetal to the peripheral region was an intermediate region in which syncytial trophoblast overlay individual clusters of epithelial cells and rested along the basal lamina. In this region there was some evidence of fusion of syncytial trophoblast with uterine epithelial cells. In the central region of the implantation site near the inner cell mass and amnion the trophoblast formed elaborate lamellipodia in relation to the basal lamina. In one of the three specimens examined with electron microscopy there were two foci where trophoblast penetrated through the basal lamina. It was also in the central region that trophoblast penetrated farthest into the uterine glands. The gland cells closest to trophoblast were less closely associated and lost their columnar shape, forming large round cells similar to the epithelial plaque cells of other primates. Where two blastocysts implanted on the same side of the uterus a conjoint membrane was formed which in regions consisted solely of syncytial trophoblast with two basal surfaces and two basal laminas. The prolonged period of time when the implantation site expands within the plane of the uterine epithelium (trophoblastic plate stage) and the peripheral to central sequence in extent of development make this primate a particularly useful animal for studies of trophoblast adhesion to and penetration of the uterine luminal epithelium.

Immunoneutralization of vascular endothelial growth factor inhibits pregnancy establishment in the rhesus monkey (Macaca mulatta)

“…We believe that the observed differences in the results of pregnancy outcome after anti-VEGF Mab administration between marmosets and rhesus monkeys arise from the difference in the process of blastocyst implantation in these species. In the marmoset, there is a prolonged period of time when the implantation site expands in the plane of uterine epithelium (trophoblast plate stage) with fusion of syncytiotrophoblast with uterine epithelial cells, but even at day 31 after ovulation syncytiotrophoblast cells do not breach maternal blood vessels; uterine blood vessels are invaded only around days 45-60 of gestation by trophoblast cells expressing FLT-1 (Enders & Lopata 1999, Wulff et al 2002, Rowe et al 2003. In contrast, in the macaque and the baboon, soon after embryo attachment, there is invasion of maternal blood vessels around days 12 of gestation by trophoblast cells similar to the human (Enders & Schlafke 1986).…”

Characteristics of the uterine luminal surface epithelium at preovulatory and preimplantation stages in the marmoset monkey

“…Collectively, the early embryonic stages without attachment are referred to as preimplantation stages. Day 11 of pregnancy has been estimated to correspond to 1 day before marmoset blastocyst implantation (Smith et al, 1987;Enders and Lopata, 1999) and is also referred to as peri-implantation. Uteri were excised only when an animal had undergone the maximum number of laparotomies (n ϭ 6) approved by the Royal Women's Hospital and University of Melbourne Animal Experimentation Ethics Committees.…”

“…Overall, this study provides an insight into the basic cellular make-up of the uterine luminal surface epithelium in a primate at preovulation, days 4 -8 of pregnancy and day 11 of pregnancy for the first time. Because day 11 of pregnancy is 1 day before blastocyst attachment in the marmoset monkey (Smith et al, 1987;Enders and Lopata, 1999), features of the uterine luminal epithelium at pre-and peri-implantation stages are elucidated in this study.…”

Angiogenesis and microvascular development in the marmoset (Callithrix jacchus) endometrium during early pregnancy

“…Implantation in the marmoset occurs on day 12 after ovulation and previous studies have described the morphological and ultra-structural changes involved (Enders & Lopata 1999, Enders 2000, Niklaus et al 2001). We have recently described the changes in gene expression of vascular endothelial growth factor (VEGF) and angiopoietin families and their receptors during early pregnancy in this species (Rowe et al 2002(Rowe et al , 2003.…”