Implantation in the rhesus monkey: Initial penetration of endometrium

Allen C. Enders, Andrew G Hendrickx, Sandra Schlafke

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Abstract

A series of peri‐implantation stages of the rhesus monkey has been collected; these range from preimplantation blastocysts through initial implantation to early villus formation. The three earliest postimplantation specimens encompass the stages of penetration into and through the uterine luminal epithelium and into endometrial blood vessels. The day of pregnancy was established by radioimmunoassay of estrogen (E) levels to determine the prevulatory E peak, and in each instance the embryo was examined to determine the extent of development. The conceptus collected on day 9.5 of pregnancy was the earliest implantation stage; it ballooned above a depression in the endometrium to which it was firmly attached. A column of syncytial trophoblast penetrated into the uterine epithelium to the basal lamina of the latter. The syncytial trophoblast shared junctional complexes with the uterine epithelial cells to which it was apposed at the margin of the site of epithelial penetration. Basal to the apical junction complexes, processes of syncytium indented uterine epithelial cells. Several epithelial cells had been partially isolated and surrounded by flanges of syncytial trophoblast. In the next specimen, at 10.0 days after ovulation, the uterine epithelium had initiated the epithelial plaque reaction. The trophoblast had extended along the residual basal lamina of the uterine epithelium and into the neck of an adjacent uterine gland. Cytotrophoblast was abundant in the central region of the implantation site, and was intermixed with syncytium which formed the majority of the peripheral trophoblast. In several places clefts had formed in the syncytial trophoblast; these clefts were lined with microvilli, had intermicrovillous caveolae, and consequently more closely resemble the trophoblast that eventually lines the intervillous spaces than the trophoblast involved in initial invasion. In the day‐10.5 specimen, in addition to prelacunar clefts, lacunae containing maternal blood were present for the first time. The basal lamina was penetrated in many places, and syncytial trophoblast was interposed between maternal endothelial cells of the underlying vessels. It was concluded that syncytial trophoblast is the first tissue to penetrate the uterine luminal epithelium; that the basal lamina of the uterine luminal epithelium, but not the basal lamina of endothelium, constitutes a temporary barrier to trophoblast penetration; that invasion is accomplished with less destruction of maternal tissue than previously suggested; and that the rapid superficial growth of the placenta is made possible by the early tapping of the endometrial vessels.

Original languageEnglish (US)
Pages (from-to)275-298
Number of pages24
JournalAmerican Journal of Anatomy
Volume167
Issue number3
DOIs
StatePublished - 1983

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Trophoblasts
Endometrium
Macaca mulatta
Basement Membrane
Epithelium
Epithelial Cells
Mothers
Giant Cells
Caveolae
Pregnancy
Blastocyst
Microvilli
Ovulation
Placenta
Endothelium
Radioimmunoassay
Blood Vessels
Estrogens
Neck
Embryonic Structures

ASJC Scopus subject areas

  • Anatomy

Cite this

Implantation in the rhesus monkey : Initial penetration of endometrium. / Enders, Allen C.; Hendrickx, Andrew G; Schlafke, Sandra.

In: American Journal of Anatomy, Vol. 167, No. 3, 1983, p. 275-298.

Research output: Contribution to journalArticle

Enders, Allen C. ; Hendrickx, Andrew G ; Schlafke, Sandra. / Implantation in the rhesus monkey : Initial penetration of endometrium. In: American Journal of Anatomy. 1983 ; Vol. 167, No. 3. pp. 275-298.
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