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Expression of manganese superoxide dismutase mRNA in reproductive organs during the ovulatory process and the estrous cycle of the rat

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Abstract

Expression of managanese superoxide dismutase (Mn-SOD) mRNA during the pregnant mare serum gonadotrophin (PMSG)/human chorionic gonadotrophin (HCG)-induced ovulatory process, and during the estrous cycle was examined in rat female reproductive organs. Mn-SOD mRNA levels in theca interna cells markedly increased in PMSG-primed rats and high levels of the transcripts were maintained after HCG injection. The PMSG-enhanced expression of Mn-SOD mRNA in follicular epithelial cells increased concomitantly with luteinization of these cells. The levels of Mn-SOD mRNA remained high and became equivalent in both granulosa and theca lutein cells 24 h after HCG injection. Neither luteinization nor the expression of Mn-SOD mRNA was observed in the epithelial cells of unovulated follicles. Luteal bodies had formed 3 days after HCG injection, and the same level of Mn-SOD mRNA expression continued in lutein cells, but not in stromal cells. During the estrous cycle, Mn-SOD mRNA was localized to theca interna cells on proestrus, to the epithelial cells of luteinizing follicles on estrus, and to newly formed luteal bodies on diestrus. The epithelial cells in the oviduct did not express Mn-SOD mRNA throughout the ovulatory process or the estrous cycle. Expression of Mn-SOD mRNA in the luminal epithelial cells of the uterus increased after PMSG injection, reaching a maximum after 24 h, and became relatively negative 3 days after HCG injection when corpora lutea had formed in the ovary. During the estrous cycle, uterine epithelial cells and leukocytes showed marked increases in Mn-SOD mRNA expression on estrus and on proestrus, respectively. Expression in the vaginal epithelium became apparent 3 days after HCG injection and continued for at least 12 days after HCG injection. The expression was localized to the superficial layer of the epithelium. During the estrous cycle, expression occurs in the basal layer on proestrus and estrus, transferring to the superficial layer on diestrus day 1, and expression stops on diestrus day 2. The relationship between the expression of Mn-SOD mRNA and hormone-induced metabolic changes, including steroidogenesis, is discussed.

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References

  • Agrawal P, Laloraya MM (1977) Induction of peroxidase in corpora lutea of rat ovary by lutropin. Biochem J 166:205–208

    PubMed  Google Scholar 

  • Armstrong DT (1981) Prostaglandins and follicular functions. J Reprod Fertil 62:283–291

    PubMed  Google Scholar 

  • Espey LL (1980) Ovulation as an inflammatory reaction — a hypothesis. Biol Reprod 22:73–106

    PubMed  Google Scholar 

  • Hesla JS, Miyazaki T, Dasko LM, Wallach EE, Dharmarajan AM (1992) Superoxide dismutase activity, lipid peroxide production and corpus luteum steroidogenesis during natural luteolysis and regression induced by oestradiol deprivation of the ovary in pseudopregnant rabbits. J Reprod Fertil 95:915–924

    PubMed  Google Scholar 

  • Hsueh AJW, Adashi EY, Jones PBC, Welsh TH Jr (1984) Hormonal regulation of the differentiation of cultured ovariant granulosa cells. Endocr Rev 5:76–127

    PubMed  Google Scholar 

  • Iwamasa J, Sibata S, Tanaka N, Matsuura K, Okamura H (1992) The relationship between ovarian progesterone and proteolytic enzyme activity during ovulation in the gonadotropi-treated immature rat. Biol Reprod 46:309–313

    PubMed  Google Scholar 

  • Kitai H, Kobayashi Y, Santulli R, Wright KH, Wallach EE (1985) The relationship between prostaglandins and histamine in the ovulatory process as determined with the in vitro perfused rabbit ovary. Fertil Steri 43:646–651

    Google Scholar 

  • Kobayashi M, Nakano R, Ooshima A (1990) Immunohistochemical localization of pituitary gonadotrophins and gonadal steroids confirms the ‘two-cell, two-gonadotrophin’ hypothesis of steroidogenesis in the human ovary. J Endocrinol 126:483–488

    PubMed  Google Scholar 

  • Laloraya M, Kumar GP, Laloraya MM (1988) Changes in the levels of superoxide anion radical and superoxide dismutase during the estrous cycle ofRattus norvegicus and induction of superoxide dismutase in rat ovary by lutropin. Biochem Biophys Res Commun 157:146–153

    PubMed  Google Scholar 

  • Laloraya M, Kumar GP, Laloraya MM (1991) Changes in the superoxide radical and superoxide dismutase levels in the uterus ofRattus norvegicus during the estrous cycle and a possible role for superoxide radical in uterine oedema and cell proliferation at proestrus. Biochem Cell Biol 69:313–316

    PubMed  Google Scholar 

  • LaPolt PS, Tilly JL, Aihara T, Nishimori K, Hsueh AJW (1992) Gonadotropin-induced up- and down-regulation of ovarian follicle-stimulating hormone (FSH) receptor gene expression in immature rats: effects of pregnant mare's serum gonadotropin, human chorionic gonadotropin, and recombinant FSH. Endocrinology 130:1289–1295

    PubMed  Google Scholar 

  • Lee SH (1982) Uterine epithelial and eosinophil estrogen receptors in rats during the estrous cycle. Histochemistry 74:443–452

    PubMed  Google Scholar 

  • Miyazaki T, Sueoka K, Dharmarajan AM, Atlas SJ, Bulkley GB, Wallach EE (1991) Effect of inhibition of oxygen free radical on ovulation and progesterone production by the in vitro perfused rabbit ovary. J Reprod Fertil 91:207–212

    PubMed  Google Scholar 

  • Morissette M, Garcia-Segura LM, Belanger A, DiPaolo T (1992) Changes of rat striatal neuronal membrane morphology and steroid content during the estrous cycle. Neuroscience 49:893–902

    PubMed  Google Scholar 

  • Parlow A (1972) Influence of differences in the persistence of luteinizing hormones in blood on their potency in the ovarian ascorbic acid depletion bioassay. Endocrinology 91:1109–1112

    PubMed  Google Scholar 

  • Sasaki J, Watanabe S, Nomura T, Kanda S, Yamaai T, Koyama E, Noji S, Taniguchi S (1990) Synthesis of actin in the nonciliated bronchiolar epithelial (Clara) cells of perinatal rats demonstrated by electron microscopy and in situ hybridization. Acta Histochem Cytochem 23:453–465

    Google Scholar 

  • Sasaki J, Nomura T, Watanabe S, Kanda S, Sato EF, Takehara Y, Fujii Y (1992) In situ hybridization at light and electron microscopic levels. J Clin Electron Microse 25:338–339

    Google Scholar 

  • Sasaki J, Sato EF, Nomura T, Mori H, Watanabe S, Kanda S, Watanabe H, Utsumi K, Inoue M (1994) Detection of manganese superoxide dismutase mRNA in the theca interna cells of rat ovary during the ovulatory process by in situ hybridization. Histochemistry 102:173–176

    PubMed  Google Scholar 

  • Sato EF, Kobuchi H, Edashige K, Takahashi M, Yoshioka T, Utsumi K, Inoue M (1992) Dynamic aspects of ovarian superoxide dismutase isozymes during the ovulatory process in the rat. FEBS Lett 303:121–125

    PubMed  Google Scholar 

  • Watanabe G, Taya K, Sasamoto S (1990) Dynamics of ovarian inhibin secretion during the oestrous cycle of the rat. J Endocrinol 126:151–157

    PubMed  Google Scholar 

  • Yoshimura Y, Espey L, Hosoi Y, Adachi T, Atlas SJ, Ghodgaonkar RB, Dubin NH, Wallach EE (1988) The effects of bradykinin on ovulation and prostaglandin production by the perfused rabbit ovary. Endocrinology 122:2540–2546

    PubMed  Google Scholar 

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Nomura, T., Sasaki, J., Mori, H. et al. Expression of manganese superoxide dismutase mRNA in reproductive organs during the ovulatory process and the estrous cycle of the rat. Histochem Cell Biol 105, 1–6 (1996). https://doi.org/10.1007/BF01450872

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