Ovulation in the Absence of the Ovarian Surface Epithelium in the Primate1

Abstract

The ovarian surface epithelium (OSE) has a prominent role in ovarian cancer in women, but no studies have been conducted to evaluate its role in normal ovarian function. Data from other species suggest the OSE is needed for ovulation. We have tested whether the OSE is needed for follicle rupture, a necessary step in ovulation, using the nonhuman primate, rhesus macaque. The OSE was removed in two different short-term protocols spanning a single periovulatory interval--one protocol used a cytology brush to remove the OSE only from the follicle apex, and one used mild detergent to remove the entire OSE--and in one long-term protocol spanning 6 wk (two periovulatory intervals) that removed the entire OSE with detergent. Serum levels of estrogen and progesterone (E and P) were monitored, and sectioned ovaries were examined for evidence of successful OSE removal and follicle rupture. In the short-term protocols, removal of the OSE over the follicle apex did not prevent follicle rupture (n = 4 ovaries), but removal of the entire OSE using detergent did in four of six cases. In the long-term protocol, when ovaries were collected after the second periovulatory interval, all the ovaries (n = 5) showed evidence of follicle rupture. In all the protocols, E and P production appeared unaffected. Detergent penetrated up to 40 microm into the ovary. This may have transiently disrupted the stroma and caused follicle rupture failure. We conclude that the primate OSE is not essential for ovulation and perhaps can be removed without lasting consequence.

The fimbria/ovarian surface junction

“…Considering that tumours often take decades until they manifest (Beerenwinkel et al, 2007), FE cells that have repopulated ruptured ovarian surface epithelia might thus be the culprits for later tumour development in some cases. Ovulation itself which, at least in primates, does not require the OSE (Wright et al, 2010), may further contribute to ovarian carcinogenesis via free radicals in the follicular fluid and via inflammatory mediators released in response to follicular rupture and during tissue repair (Murdoch and Martinchick, 2004). This is in complete agreement with epidemiological data showing that women who have used ovulation-inhibiting oral contraceptives over a number of years bear a reduced risk of developing ovarian cancer (Ory, 1987;Beral et al, 2007).…”

Mechanism for the Decision of Ovarian Surface Epithelial Stem Cells to Undergo Neo-Oogenesis or Ovarian Tumorigenesis

“…Studies have found almost 90% of ovarian cancer originates from the ovarian surface epithelium (mesothelium) that invaginates into the underlying stroma resulting in inclusion cysts that eventually undergo malignant transformation [25][26][27]29] . As a result, Wright et al [30] think that if the OSE is removed, the risk for developing ovarian cancer can be greatly reduced, [31] used a rhesus monkey model to extend observation time to 6 months and 12 months after removal of the OSE and obtained similar results. This study provides a new strategy for preventing ovarian cancer.…”

Dynamics of the primate ovarian surface epithelium during the ovulatory menstrual cycle

“…Fixed ovaries were paraffin embedded and cut into 5 mm sections as described previously (Wright et al, 2010) for hematoxylin and eosin (H&E) or immunohistochemical (IHC) staining. H&E labeled sections were used to examine OSE morphological characteristics: height, lateral density and presence or absence of an apical projection.…”