Postnatal development of the ovarian bursa of the golden hamster (Mesocricetus auratus): Its complete closure and morphogenesis of lymphatic stomata

Abstract

The golden hamster ovarian bursa was studied by light and electron microscopy to clarify the process of its complete closure and the development of lymphatics that leads to morphogenesis of stomata. The results were as follows. 1) The bursa completely closed at 9 days of age primarily due to development of the mesotubarium superius. 2) With the closure, the ovary and bursa became closely apposed, and most of the original bursal cavity disappeared. 3) Between 9 and 12 days of age U-shaped folds of the bursal mesothelium began to invade the connective tissue of the bursa. 4) Widening of the internal angle of the U-shaped folds contributed to reappearance of the bursal cavity, and thus separation of the bursa from the ovary. It also contributed to future geometrical proximity of lymphatics to the cavity of the bursa. 5) The separation of the bursa from the ovary began as early as 12 days of age in the cephalic half of the bursa. It occurred remarkably late in the caudal half. Juxtaposition of the window portion of the bursa to the ovary remained in some adult animals. 6) Development of lymphatics in the cephalic half of the bursa was divided into two stages, before and after days 21-24 of life. In the first stage, lymphatics grew in the submesothelial connective tissue, and the framework of lymphatics was formed. In the second stage, lymphatics extended small branches to form the submesothelial plexus or lymphatic lacuna. 7) Intercellular junctions between contiguous lymphatic endothelial cells were mostly tight and desmosomelike. Open junctions were, if they occurred at all, rare. (8) A smooth-surfaced area lined with the lymphatic endothelium was found in the bursa on day 27 of life, before the initiation of ovulation. Valvelike stomal orifices were absent before the initiation of ovulation and extremely rare even after the first ovulation. They were commonly present in the bursae after the fourth ovulation, however. The process of complete closure of the ovarian bursa is very complex and may be related to the later development of the bursal mesothelium and lymphatics. Some liplike stomal orifices are of purely developmental origin. However, all valvelike stomal orifices are assumed to be formed as a result of damage to the bursal mesothelium, as well as to the submesothelial connective tissue and lymphatics, by repetition of ovulation. It is possible that liplike stomal orifices may be formed in the process of repairing the damage.

Peritoneal lymphatic stomata of the diaphragm in the mouse: Process of their formation

“…The proposed morphogenesis of the lymphatic stomata supports the idea, as described by Leak and Rahil (1978), that lymphatic stomata are formed when the cell margins of several lymphatic endothelial cells span the submesothelial connective tissue to form intercellular junctions with cell margins of several neighboring mesothelial cells lining the peritoneal surface of the diaphragm. However, we found slightly different morphogenesis of the lymphatic stoma in the diaphragm compared with that in the ovarian bursa of the golden hamster affected by ovulation (Shinohara et al, 1987). Shinohara et al described that during the reparative period after ovulation, which damages the bursal mesothelium, submesothelial lymphatics, and connective tissue, the lymphatic endothelial cells may grow more rapidly to the bursal surface, forming the lymphatic stomata.…”

“…The lymphatic stomata in the diaphragms of mice, rats, and golden hamsters, however, first appear at birth or a few days after birth, and their number increases exponentially as the animal grows (Nakatani et al, 1996). Moreover, the stomata in the ovarian bursa of golden hamsters are first observed on day 27 after birth, before the initiation of ovulation, and they become abundant after the start of ovulation (Shinohara et al, 1987). To our knowledge, there is only one paper concerning the process of formation of such a unique lymphatic stomata, by Shinohara et al (1987) who studied the morphogenesis of lymphatic stomata of the ovarian bursa.…”

“…Moreover, the stomata in the ovarian bursa of golden hamsters are first observed on day 27 after birth, before the initiation of ovulation, and they become abundant after the start of ovulation (Shinohara et al, 1987). To our knowledge, there is only one paper concerning the process of formation of such a unique lymphatic stomata, by Shinohara et al (1987) who studied the morphogenesis of lymphatic stomata of the ovarian bursa. We are not aware of any studies on the morphogenesis of the stomata of the diaphragm.…”

Hormonal Regulation of Ovarian Bursa Fluid in Mice and Involvement of Aquaporins

“…It has been demonstrated in murine species, the formation of ovarian bursa began after the postnatal day 9 and its complete formation progressed gradually after first ovulation [3]. The clear structural arrangement of ovarian bursa and its close relationship with ovary have been utilized for cell/tissue transplantation, drug/reagent delivery in ovarian functional studies, which have been proven to be successful [4], [5], [6], [7].…”

Ultrastructure and Estrogen Regulation of the Lymphatic Stomata of Ovarian Bursa in Mice

“…The ultrastructure and morphogenesis of lymphatic stomata have been studied on ovarian bursa (Shinohara et al, 1985(Shinohara et al, , 1986(Shinohara et al, , 1987; however, little is known about the regulation of the lymphatic stomata on ovarian bursa. Following the first description in the golden hamster, the lymphatic stomata were found in the ovarian bursa of European beaver and guinea pig, and they also existed in human ovary epithelium (Shinohara et al, 1985;Dobroszynska and Janiszewska, 1998;Sui and Li, 2001a,b).…”