Cyclic changes in ciliation of the oviductal epithelium in the pig‐tailed macaque (Macaca nemestrina)

Abstract

Many of the cilia in the oviducts of rhesus monkeys are formed in the follicular phase of the menstrual cycle, and lost in the subsequent luteal phase (Brenner, '69a). This striking phenomenon has rarely been observed in other species, and its occurrence in human oviducts is a point of dispute. This study was designed to determine whether cyclic shedding and renewal of oviductal cilia occur in a primate species other than the rhesus monkey and to reveal the surface characteristics of the oviductal mucosa in a subhuman primate. Oviducts were removed from Macaca nemestrina females a t three specific times during the menstrual cycle and examined by scanning electron microscopy. The fimbriae appeared to be extensively ciliated a t midcycle but only sparsely ciliated in the early follicular and late luteal phases. Early in the cycle, large numbers of cells were seen in the process of ciliogenesis, but in the late luteal phase there were signs of ciliary degeneration and shedding. The ampullar epithelium showed similar though less dramatic changes, and the isthmus little change. Long-term ovariectomy caused almost complete deciliation of the fimbrial and ampullar epithelium, but treatment of ovariectomized animals with estrogen for only a few days restored the epithelium to normal. Despite the high degree of variability in the mucosa, it was clear that the oviducts of M. nemestrina, like those of the rhesus monkey, undergo cyclic ciliogenesis and deciliation. The surface features of the oviductal lining in M. nemestrina are described here for the first time.One of the most remarkable discoveries about the mammalian oviduct in recent years has been the finding that, in the rhesus monkey, oviductal cilia are regularly produced and shed with each menstrual cycle (Brenner, '67, '69a,b). Large numbers of cilia are formed during the early part of the follicular phase, creating a richly ciliated epithelium by midcycle when ovulation occurs. During the late luteal phase, extensive atrophy and deciliation occur. These changes are most marked a t the fimbriated end. In the ampulla and isthmus the epithelial cells undergo cyclic hypertrophy and atrophy, but ciliogenesis and deciliation occur only rarely.Changes of this nature are obviously important to document in view of fimbrial function. In many mammals, including the monkey, it is the cilia of the fimbriae that are primarily responsible for the pickup and first phase of transport of ova (Blandau, '73; Odor and Blandau, '73). The importance of a richly ciliated epithelium a t midcycle is obvious, but the functional significance, if any, of cyclic ciliogenesis and deciliation is not yet clear.Apart from a brief mention of similar cyclic changes in the oviducts of cynomolgus monkeys, M. fascicularis (Brenner et al., '73), there have been no reports on the extent to which this phenomenon occurs among other subhuman primates. Yet this would seem to be an important area for investigation, since studies on human oviducts have already produced conflicting data on this issue....

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

“…In agreement with our data, studies in the cow (Abe and Taneaki, 1993), baboon , and monkey (Rumery et al, 1978;Odor et al, 1980Odor et al, , 1983Brenner and Slayden, 1994) support the hypothesis that the epithelial cells of the isthmus are more resistant to the anti-estrogen effects of progesterone than either the fimbria or ampulla. With the exception of the monkey (Rumery et al, 1978;Odor et al, 1980Odor et al, , 1983Brenner and Slayden, 1994), there are few studies that have systematically compared fine structural differences in all three segments throughout the reproductive cycle or early pregnancy. The data presented here are the first to provide a detailed report of alterations in the isthmus oviduct of the pregnant animal for comparison to the ampulla (Murray, 1995) and fimbria (Murray, 1996) obtained at identical reproductive stages.…”

“…Stage-and steroid hormone-specific regional variations in oviduct cytology have been reported in the human (Verhage et al, 1979;Crow et al, 1994), baboon , monkey (Rumery et al, 1978;Odor et al, 1983;Brenner and Slayden, 1994), mouse (Kapur and Johnson, 1988), rat (Abe, 1994), hamster (Abe and Oikawa, 1991), cow (Eriksen et al, 1994;Abe and Taneaki, 1993), goat (Abe et al, 1993b), and rabbit (Jansen and Bajpai, 1982). In agreement with our data, studies in the cow (Abe and Taneaki, 1993), baboon , and monkey (Rumery et al, 1978;Odor et al, 1980Odor et al, , 1983Brenner and Slayden, 1994) support the hypothesis that the epithelial cells of the isthmus are more resistant to the anti-estrogen effects of progesterone than either the fimbria or ampulla.…”

“…These data are important in further establishing the unique responsiveness of the oviduct as ovarian hormones fluctuate. 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.…”

Scanning electron microscopy of reproductive epithelia in the female musk shrew, Suncus murinus

“…Further, fimbrial ciliation of primates is apparently more sensitive to plasma estrogen-progesterone levels than in other oviducal regions (Rumery et al, 1978;Brenner, 1969). Since Suncus is a reflex ovulator, oviducal ciliation might be extensive even without estrogen treatment.…”

“…[ Rumery et al, 1978) and after exogenous hormonal treatment (Brenner, 1967;Odor et al, 1981Odor et al, , 1983. These changes include ciliogenesis, secretory processes, and changes in cell shape and composition.…”