Epithelial Lining of the Sheep Ampulla Oviduct Undergoes Pregnancy-Associated Morphological Changes in Secretory Status and Cell Height1

Abstract

The biosynthetic activity of the sheep ampulla oviduct changes during the first few days of pregnancy. An estrogen (E2)-dependent glycoprotein (M(r) 90,000-92,000) is expressed, synthesized, and released when fertilization and embryo development occur in the oviduct. The objective of the present study was to determine whether the secretory epithelial lining of the ampulla, the cellular source of the E2-dependent protein, undergoes morphological alterations during early pregnancy is a contemporaneous manner. Ampulla oviducts obtained from ovariectomized (ovx), estrous (Day 0), and pregnant (Days 1.5, 2, 3, 4, 6, and 16) ewes were analyzed with light and electron microscopy. The mean cell height of epithelial cells from estrus and from Days 1.5, 2, and 3 of pregnancy was significantly (p < 0.05) higher than in ovx animals. A significant reduction in cell height was observed at Day 4 of pregnancy, and this value remained unchanged at Day 6 and Day 16. Ciliated and nonciliated cells were present in the ampulla at all stages examined, with ciliated cells constituting the major cell type. Consistent with previous results, the nonciliated cells obtained from ovx ewes were synthetically inactive and at estrus were characterized by well-developed secretory organelles, including abundant amounts of secretory granules containing the E2-dependent glycoprotein. Extensive microvilli and cytoplasmic blebs protruding into the oviduct lumen distinguished the apical surface of secretory epithelial cells until Day 3. At Day 1.5 the secretory cells contained dilated cisternae of rough endoplasmic reticulum and enlarged Golgi, which were progressively diminished with increasing stages of pregnancy. Exocytosis, fusion of secretory granules, and a reduction in their electron density were seen until Days 3-4. By Day 4 and Day 6, fewer granules were observed in the ampulla cytoplasm and few, if any, were present by Day 16. Increases in the amount of heterochromatin were seen in nuclei at Day 6 and Day 16. Extrusion of epithelial cells into the oviduct-lumen was evident at Day 16 of pregnancy. These data show that 1) the secretory epithelium of the sheep ampulla oviduct undergoes morphological alterations in protein-synthesizing organelles and apical specializations that vary with the stage of pregnancy, 2) the secretory product contained in lamellar granules is released by the process of exocytosis until Days 3-4, and 3) cell death appears to occur at Day 16 by shedding of epithelial cells into the oviduct lumen.

Morphological features of epithelial cells in the sheep isthmus oviduct during early pregnancy

“…In ovariectomized, estrous and pregnant ewes, the lumen of the isthmus oviduct was relatively narrow and the mucosal folds less extensive compared to the fimbria (Murray, 1996) and ampulla (Murray, 1995). This is consistent with reports in other species (Abe and Oikawa, 1991;Jansen, 1995).…”

“…By contrast to the ampulla and fimbria, the secretory protein patterns of the isthmus do not exhibit any remarkable variations at estrus or during the first few days of pregnancy (Murray, 1993). Recently, we have shown that the secretory organelles in nonciliated epithelial cells of the ampulla and fimbria sheep oviduct undergo region-specific structural changes that account for the protein synthetic alterations in early pregnancy (Murray, 1995(Murray, , 1996. Whether the apparent lack of pregnancy-associated biosynthetic changes in the isthmus is correlated with a cytologically static secretory epithelium is not known.…”

“…The structural alterations in the isthmus can then be compared to those in fimbria and ampulla, segments which have been well characterized morphologically in several mammals (Verhage et al, 1979;Rumery et al, 1978;Odor et al, 1980Odor et al, , 1983Brenner and Slayden, 1994;Verhage et al, 1990) including the sheep (Murray, 1995(Murray, , 1996. Therefore, the objectives of the present study were a) to define the structural alterations of the isthmus oviduct of the sheep at estrus and during the first few weeks of pregnancy (days 2, 3, 4, 6, and 16) to ascertain whether the isthmus oviduct undergoes pregnancyassociated, cytological modifications that are distinct from the ampulla (Murray, 1995) and fimbria (Murray, 1996); and b) to determine whether the absence of significant protein synthetic capacity as assessed biochemically in the isthmus at estrus and during pregnancy (Murray, 1993;DeSouza and Murray, 1995) can be accounted for by a stationary secretory epithelium. In addition, in order for cytological comparison to a state devoid of ovarian steroid influence, oviducts were also obtained from long-term ovariectomized ewes.…”

Microenvironnement tubaire: rôle dans la maturation des ovocytes canins in vivo et in vitro

“…Chez la brebis en anoestrus, les cellules de l'oviducte sont majoritairement indifférenciées (Murray 1995). Sous imprégnation oestrogénique en début de phase folliculaire, la proportion de cellules ciliées augmente, alors que sous l'effet de la progestérone, les cellules se dédifférencient et leur proportion diminue.…”

Comparison of mRNA for IGFs and their binding proteins in the oviduct during the peri-oestrous period between dairy heifers and lactating cows

“…The morphology and activity of the epithelium change during the oestrous cycle (Yaniz et al 2000). Secretory activity increases during the peri-ovulatory period and early luteal phase under the influence of oestrogen (Murray 1995, Buhi et al 2000 but decreases during the luteal phase and pregnancy when there is a prevailing high-progesterone concentration (Nayak et al 1976). Oviductal fluid can enhance sperm survival (Boilard et al 2004) and fertilisation and provides an environment rich in 'embryotrophic factors' capable of enhancing embryo development (Leese 1988, Lai et al 1996.…”