Abstract
Superoxide (O2−), hydrogen peroxide (H2O2), and lipid peroxides are generated in luteal tissue during natural and prostaglandin-induced regression in the rat, and this response is associated with reversible depletion of ascorbic acid. Reactive oxygen species immediately uncouple the luteinizing hormone receptor from adenylate cyclase and inhibit steroidogenesis by interrupting transmitochondrial cholesterol transport. The cellular origin of oxygen radicals in regressing corpora lutea is predominately from resident and infiltrated leukocytes, notably neutrophils. Reactive oxygen species are also produced within the follicle at ovulation and, like the corpus luteum, leukocytes are the major source of these products. Antioxidants block the resumption of meiosis, whereas the generation of reactive oxygen induces oocyte maturation in the follicle. Although oxygen radicals may serve important physiologic roles within the ovary, the cyclic production of these damaging agents over years may lead to an increased cumulative risk of ovarian pathology that would probably be exacerbated under conditions of reduced antioxidant status.
Article PDF
Avoid common mistakes on your manuscript.
References
Matzuk MM, Dionne L, Guo Q, Kumar TR, Lebovitz RM. Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 1998;139:4008–11.
Kolodecik TR, Aten RF, Behrman HR. Ascorbic acid-dependent cytoprotection of ovarian cells by leukocyte and nonleukocyte peroxidases. Biochem Pharmacol 1998;55:1497–503.
Musicki B, Kodaman PH, Aten RF, Behrman HR. Endocrine regulation of ascorbic acid transport and secretion in luteal cells. Biol Reprod 1996;54:399–406.
Behrman HR, Preston SL, Aten RF, Rinaudo P, Zreik TG. Hormone induction of ascorbic acid transport in immature granulosa cells. Endocrinology 1996;137:4316–21.
Aten RF, Duarte KM, Behrman HR. Regulation of ovarian antioxidant vitamins, reduced glutathione, and lipid peroxidation by luteinizing hormone and prostaglandin F2α. Biol Reprod 1992;46:401–7.
Guarnaccia MM, Takami M, Jones EE, Preston SL, Behrman HR. LH depletes ascorbic acid in preovulatory rat follicles. Fertil Steril 2000;74:959–63.
Aten RF, Kolodecik TR, Behrman HR. Ovarian vitamin E accumulation: Evidence for a role of lipoproteins. Endocrinology 1994;135:533–9.
Riley JCM, Behrman HR. In vivo generation of hydrogen peroxide in the rat corpus luteum during luteolysis. Endocrinology 1991;128:1749–53.
Sawada M, Carlson JC. Rapid plasma membrane changes in superoxide radical formation, fluidity, and phospholipase A2 activity in the corpus luteum of the rat during induction of luteolysis. Endocrinology 1991;128:2992–8.
Aten RF, Kolodecik TR, Rossi MJ, Debusscher C, Behrman HR. Prostaglandin F2a treatment in vivo, but not in vitro, stimulates protein kinase C-activated superoxide production by nonsteroidogenic cells of the rat corpus luteum. Biol Reprod 1998;59:1069–76.
Margolin Y, Behrman HR. Xanthine oxidase and dehydrogenase activities in rat ovarian tissues. Am J Physiol 1992;262:E173–8.
Pepperell JR, Wolcott K, Behrman HR. Luteolytic effect of neutrophils in rat luteal cells. Endocrinology 1992;130:1001–8.
Wang F, Riley JCM, Behrman HR. Immunosuppressive glucocorticoid blocks extrauterine luteolysins in the rat. Biol Reprod 1993;49:66–75.
Behrman HR, Preston SL. Luteolytic actions of peroxide in rat ovarian cells. Endocrinology 1989;124:2895–900.
Margolin Y, Aten RF, Behrman HR. Antigonadotropic and antisteroidogenic actions of peroxide in rat granulosa cells. Endocrinology 1990;127:245–50.
Gatzuli E, Aten RF, Behrman HR. Inhibition of gonadotropin action and progesterone synthesis by xanthine oxidase in rat luteal cells. Endocrinology 1991;128:2253–8.
Endo T, Aten RF, Leykin L, Behrman HR. Hydrogen peroxide evokes antisteroidogenic and antigonadotropic actions in human granulosa lutein cells. J Clin Endocrinol Metab 1993;76:337–42.
Musicki B, Behrman HR. Metal chelators reverse the action of hydrogen peroxide in rat luteal cells. Mol Cell Endocrinol 1993;92:215–20.
Soodak LK, Macdonald GJ, Behrman HR. Luteolysis is linked to LH-induced depletion of ATP in vivo. Endocrinology 1988;122:187–93.
Behrman HR, Aten RF. Evidence that hydrogen peroxide blocks hormone-sensitive cholestrol transport into mitochondria of rat luteal cells. Endocrinology 1991;128:2958–66.
Musicki B, Aten RF, Behrman HR. Inhibition of protein synthesis and hormone-sensitive steroidogenesis in response to hydrogen peroxide in rat luteal cells. Endocrinology 1994;134:588–95.
Stocco DM, Wells J, Clark BJ. The effects of hydrogen peroxide on steroidogenesis in mouse Leydig tumor cells. Endocrinology 1993;133:2827–32.
Takami M, Preston SL, Toyloy VA, Behrman HR. Antioxidants reversibly inhibit the spontaneous resumption of meiosis. Am J Physiol 1999;276:E684–8.
Takami M, Preston SL, Behrman HR. Eicosatetranoic and eicosatrynoic acids, lipoxygenase inhibitors, block meiosis via antioxidant action. Am J Cell Physiol 2000;278:C646–50.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by grants NICHD-10718 and NICHD-35663 from the NIH.
Rights and permissions
This article is published under an open access license. Please check the 'Copyright Information' section either on this page or in the PDF for details of this license and what re-use is permitted. If your intended use exceeds what is permitted by the license or if you are unable to locate the licence and re-use information, please contact the Rights and Permissions team.
About this article
Cite this article
Behrman, H.R., Kodaman, P.H., Preston, S.L. et al. Oxidative Stress and the Ovary. Reprod. Sci. 8 (Suppl 1), S40–S42 (2001). https://doi.org/10.1177/1071557601008001S13
Published:
Issue Date:
DOI: https://doi.org/10.1177/1071557601008001S13