When the Y chromosome of a Mus musculus domesticus mouse strain is placed onto the C57BL/6J (B6) inbred genetic background, the XY (B6.YDOM) progeny develop ovaries or ovotestes, but not normal testes, during fetal life. At puberty, while some of the hermaphroditic males become fertile, none of the XY sex-reversed females produce litters. We have previously demonstrated that the eggs ovulated from the B6.YDOM ovary undergo fertilization efficiently, but cannot develop beyond the 2-cell stage either in vivo or in vitro. In the present study, we collected oocytes directly from the XY ovary, and examined their maturation, fertilization, and embryonic development in vitro. The results show that the juvenile XY ovary yielded far more fertilizable oocytes by direct collection and in vitro maturation than through in vivo ovulation, but the majority of fertilized eggs failed to reach the blastocyst stage. Hence, developmental incompetence of oocytes in the XY ovary appears to be programmed during oocyte differentiation or growth. Nonetheless, in vitro matured oocytes showed a higher potential of embryonic development than the ovulated eggs, suggesting that fertility of the XY female may be impaired by multiple factors. We hypothesized that poor responsiveness of the XY ovary to gonadotropins, as we have previously demonstrated in testosterone production, may impair follicular development or proper recruitment of oocytes for ovulation. In the present study, we compared 125I-hCG binding in XX and XY ovaries, but did not find a significant difference. Hence, LH activity appears to be impaired after receptor binding in the XY ovary. On the other hand, the pattern of 125I-hCG binding indicated that the majority of antral follicles in the XY ovary failed to undergo normal preovulatory phases, which may explain the lower developmental capacity of eggs after ovulation.
The mouse XX gonadal primordium develops seminiferous-like tubules after transplantation into the renal subcapsular site of the adult male or female mouse. We examined the ontogeny of Sertoli cell differentiation in XX gonadal grafts by immunocytochemical staining and organ culture bioassay for Müllerian Inhibiting Substance (MIS). During normal in situ development of the XY gonad, MIS staining was first detected in fetal Sertoli cells at 12 days of gestation (d.g.) and remained intense until 4 days postpartum (d.pp.), after which it gradually diminished with progressive testicular development. In the normal in situ XX gonad, MIS was detected in granulosa cells of growing follicles at 7 d.pp. and thereafter. When the XX gonad at 12 d.g. was grafted beneath the renal capsule, a few testicular cords composed of MIS-positive cells appeared on Day 7 post-transplantation (equivalent to 19 d.g.), much earlier than the normal appearance of MIS production in the intact XX ovary. The ovarian region containing germ cells at the meiotic prophase was unstained for MIS in the same sections. The incidence of XX gonadal grafts containing MIS-positive testicular cords and the number of such cords per gonadal graft steadily increased from Day 7 to Day 14 post-transplantation. Germ cells were absent or scarce inside the MIS-positive testicular cords. The MIS bioactivity in both control gonads and gonadal grafts coincided with the immunocytochemical staining for MIS. These results support the hypothesis that XX cells differentiate into Sertoli cells as a consequence of oocyte loss in the gonadal graft.
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