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Semaphorin 3E-Plexin-D1 pathway regulates ovulation, granulosa cell luteinization, and ovarian angiogenesis in mice

ABSTRACT: Ovulation is induced by the luteinizing hormone surge and accompanied by granulosa cell luteinization and ovarian angiogenesis. Sema3E-Plexin-D1 pathway regulates angiogenesis in other tissues, but its role in the ovary was unknown. We report herein that the expression of Sema3E and its receptor, Plexin-D1, is dynamically regulated in the mouse ovary downstream of the LH surge. This regulation is mediated by CCAAT/enhancer-binding proteins α and β through modulating chromatin accessibility. Intraovarian injection of recombinant Sema3E results in reduced ovulation, impaired corpus luteum formation, and aberrant ovarian angiogenesis. These in vivo physiological abnormalities are consistent with altered expression of genes regulating these processes, and with data from in vitro cultured granulosa cells and/or ovarian stromal tissues treated with Sema3E or Plexin-D1 neutralizing antibody. Our findings shed light on the important role of Sema3E-Plexin-D1 pathway in the ovary, pinpointing it as a potential therapeutic target for fertility and infertility management.

ORGANISM(S): Mus musculus

PROVIDER: GSE262209 | GEO | 2025/08/01

REPOSITORIES: GEO

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Project description:Ovulation refers to the process when the ovarian surface-facing wall of a preovulatory follicle ruptures and releases the cumulus oocyte complex (COC) into the oviduct or fallopian tube in response to hormonal cues. In parallel, the unruptured wall of the follicle within the ovary transitions to becoming a progesterone-producing corpus luteum. Ovulation is essential for fertilization and eventual pregnancy. Disruption of ovulation, whether purposefully through contraceptive intervention or idiopathically in cases of anovulatory infertility, has translational implications for human health. Importantly, key processes of ovulation, including follicle rupture and luteinization, are recapitulated in models of ex vivo ovulation despite the absence of an intact hypothalamic-pituitary-gonadal axis and intra-ovarian cues. In our study, we used an ex vivo ovulation model to identify functional and molecular differences between distinct regions of the follicle wall, which we refer to as the ruptured and unruptured sides. We observed that the unruptured side of the follicle wall exhibits hallmarks of luteinization after ovulation while the ruptured side exhibits signs of cell death. RNA-sequencing of these specific follicle regions revealed 2,099 differentially expressed genes between follicle sides without hCG exposure and 1,673 between follicle sides 12 hours post-hCG, which were further validated in vivo. We found enriched pathways that recapitulate known ovulation biology, including oxidative stress on the ruptured side and angiogenesis on the unruptured side. We also identified previously unappreciated pathways that may play an important role in ovulation, such as amino acid transport and Jag-Notch signaling on the ruptured side, as well as metal ion processing and IL-11 signaling on the unruptured side. Ultimately our studies demonstrate that our ex vivo model recapitulates known in vivo ovarian biology, identifies pathways that may be novel regulators of ovulation and luteinization, and may have future translational applications for the study of ovulatory disorders and the development of novel non-hormonal contraceptives.

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Semaphorin 3E-Plexin-D1 pathway regulates ovulation, granulosa cell luteinization, and ovarian angiogenesis in mice

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