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Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka.

ABSTRACT: Identification of the hydrolytic enzymes involved in follicle rupture during vertebrate ovulation remains a central challenge for research in reproductive biology. Here, we report a previously uncharacterized approach to this problem by using an in vitro ovulation system in the medaka, Oryzias latipes, which is a small freshwater teleost. We found that follicle rupture in the medaka ovary involves the cooperation of at least three matrix metalloproteinases (MMPs), together with the tissue inhibitor of metalloproteinase-2b protein. We determined the discrete roles of each of these proteins during follicle rupture. Our results indicated that gelatinase A induces the hydrolysis of type IV collagen constituting the basement membrane, membrane-type 2 MMP degrades type I collagen present in the theca cell layer, and MT1-MMP and the tissue inhibitor of metalloproteinase-2b are involved in the production and regulation of gelatinase A. These findings will help clarify the mechanism of follicle wall degradation during ovulation in mammalian species.

SUBMITTER: Ogiwara K

PROVIDER: S-EPMC1150835 | biostudies-literature | 2005 Jun

REPOSITORIES: biostudies-literature

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Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka.

Ogiwara Katsueki K Takano Naoharu N Shinohara Masakazu M Murakami Masahiro M Takahashi Takayuki T

Proceedings of the National Academy of Sciences of the United States of America 20050607 24

Identification of the hydrolytic enzymes involved in follicle rupture during vertebrate ovulation remains a central challenge for research in reproductive biology. Here, we report a previously uncharacterized approach to this problem by using an in vitro ovulation system in the medaka, Oryzias latipes, which is a small freshwater teleost. We found that follicle rupture in the medaka ovary involves the cooperation of at least three matrix metalloproteinases (MMPs), together with the tissue inhibi ...[more]

PMID: 15941829

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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.

Dataset Information

Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka.

Publications

Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka.

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