Changes in the oviducal epithelium during the estrous cycle in the marsupial Monodelphis domestica

Abstract

The Monodelphis oviduct can be divided into four anatomical segments: preampulla (comprising fimbriae and infundibulum), ampulla, isthmus with crypts and uterotubal junction. Ovaries are enclosed in a periovarial sac, the bursa, and in some specimens tubules of an epoophoron could be identified. In both structures non-ciliated cells develop small translucent vesicles, which accumulate in the cell apices and presumably produce fluid as often seen in the bursa and in the tubules of the epooophoron. These vesicles do not stain with Alcian blue or PAS. The same applies also to the non-ciliated cells of the fimbriae. The oviducal epithelium of ampulla and the surface epithelium of the isthmus consisting of ciliated and non-ciliated, secretory cells undergo considerable changes during the estrous cycle. Proestrus shows low numbers of ciliated cells, some are in the process of neo-ciliogenesis, non-ciliated cells carry solitary cilia and few remnant secretory granules from the previous cycle may be found. At estrus the amount of ciliated cells in ampulla and isthmus has increased, most non-cililated cells lost the solitary cilia, developed longer microvilli and formed numerous secretory granules in their cell apices. At postestrus secretory products, often surrounded by membranes, are extruded into the oviducal lumen and contribute towards egg coat formation. First signs of deciliation processes are apparent. Solitary cilia reappear. At metestrus only few secretory cells are left with some secretory material. The lumen is often filled with shed cilia and cell apices. Proliferation of basal bodies within non-secretory cells indicate the formation of new ciliated cells. The non-ciliated epithelial cells of the isthmic crypts form no secretory granules but accumulate a great number of translucent vesicles, which in contrast to the secretory granules do not stain with Alcian blue or PAS.

Fig. 1

Fimbriae and bursa. (a) Semithin section through fimbrial folds at metestrus stage covered by ciliated and non-ciliated cells. ×245. (b) Semithin section through the bursa at estrus stage. Arrowheads, bursa epithelium with ciliated and non-ciliated cells; arrows, serosal epithelium. ×245. (c) Electronmicrograph of fimbrial epithelium at metestrus, depicting only non-ciliated cells. ×6100. (d) Bursa wall, with cuboidal bursal epithelium (arrowhead) and flat serosal epithelium (arrows) at metestrus. ×2300.

Fig. 2

Ampulla at estrus. (a) Scanning electron microscopy. Overview of ampullar folds (arrow). ×560. (b) Folds covered with an epithelium consisting of ciliated and non-ciliated, secretory cells. ×7000. (c) Light microscopical section stained with PAS. Note the intensive positive reaction of the secretory cells in the ampulla (A) and the negative reaction of the fimbrial epithelium (F) where no staining products could be detected. ×145. (d) Semithin section with ampullar epithelium exhibiting non-ciliated, secretory cells, densely packed with secretory granules (arrowheads) at estrus. ×615. (e) Electronmicrograph of secretory cells at estrus, filled with secretory granules often of heterogeneous density (arrows) and highly active Golgi complexes (arrowheads). ×6400.

Fig. 3

Ampulla at post-and metestrus. (a) Semithin section through ampullar epithelium at postestrus stage. The number of secretory active cells (arrowheads) and the amount of secretory granules per cell are reduced. ×500. (b) Scanning electronmicrograph showing postestrus stage with extruded secretory material (arrowheads), partially membrane bound after apocrine secretion. ×3200. (c–g) Electronmicrographs. (c) Non-ciliated cell with apocrine cytoplasmic exocytosis (arrowheads). ×3900. (d) Secretory products in degradation in form of whorls (arrowhead). ×4700. (e) Section through a secretory cell at postestrus still hosting numerous secretory granules, one cell carrying a solitary cilium (arrow). ×8000. (f) Some of the non-ciliated cells show apically numerous translucent small vesicles (arrows) beside few secretory granules. ×6400. (g) Ampullar epithelium at metestrus, occasionally a few remnant secretory granules are left (arrowhead). ×5000.

Fig. 4

Isthmus. (a) Light microscopy: cross section through the isthmus region close to the uterus showing surface epithelium (arrowheads) and crypts (C). ×165. (b) Semithin section through the isthmus region with surface epithelium (arrows) and crypts (arrowheads). ×250. (c–f) Isthmus surface epithelium. (c) Electron microcoscope pictures of isthmus surface epithelium at postestrus stage with ciliated cell (cc) and non-ciliated secretory cells (sc) still containing numerous secretory granules. Degeneration processes (whorls) have started (arrowheads). ×4500. (d) Lumen at metestrus filled with massive deciliation and secretion products (star). Hardly any secretory granules are left in the secretory cells. ×3300. (e) At the same time ciliogenesis has started. Note the multiplication of basal bodies moving to the apical surface (arrowheads). ×6900. (f) Scanning electron microscope: isthmus surface at late metestrus/early proestrus showing numerous non-ciliated cells with solitary cilia (arrows) and ciliated cells exhibiting neo-ciliogenesis at different stages (arrowheads). ×7200.

Fig. 5

Isthmus crypts. (a) Semithin section, invagination of the surface epithelium (arrow) into crypts. Crypt epithelium consists at estrus mainly of secretory cells with bulging apices (arrowheads). ×310. (b) Electron microscopy: crypt cells at estrus. Secretion products exist in numerous translucent vesicles located in bulging cell apices (arrowheads). ×6120. (c) Crypt cells at late postestrus shedding apices and cilia (arrows). Small secretory vesicles can still be found in individual cell apices. Lysosomes and aptotosic cells are typical (arrowheads). ×4200. (d) Crypt at metestrus filled with shed cilia (star), cell with signs of neo-ciliogenesis (arrowhead). ×4300.

Fig. 6

Epoophoron. (a) Cross section (semithin) through epoophoron tubules with narrow lumen and distinct connective tissue layers (arrowheads) surrounding the epithelium. ×450. (b) Semithin sections through tubules with wider lumina lined with ciliated and non-ciliated cells. Both figures are taken from the same animal at metestrus stage. ×300. (c) Electron microscopy: non-ciliated epithelium lining the epoophoron tubules at metestrus, with numerous small vesicles at the cell apices (arrowheads) and secretion product in the lumen (L). ×6900. (d) A ciliated cell of the same tubule. ×6050. (e) A different type of ciliated cell, where cilia sit in deep invaginations with pronounced basal bodies (arrowheads). ×7100.