Copper/Zinc superoxide dismutase insufficiency impairs progesterone secretion and fertility in female mice

Biology of Reproduction

Volumn 86, Issue 1, 2012, Pages

  Noda, Yoshihiro ^a   Ota, Kuniaki ^b   Shirasawa, Takuji ^c   Shimizu, Takahiko ^a  

^a TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^b TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Corpus luteum; CuZn SOD (SOD1); Progesterone

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; ESTRADIOL; FOLLITROPIN; HYPOPHYSIS HORMONE; LUTEINIZING HORMONE; PROGESTERONE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATROPHY; CONTROLLED STUDY; CORPUS LUTEUM; CYTOPLASM; EMBRYO TRANSFER; FEMALE; FEMALE FERTILITY; FERTILIZATION IN VITRO; HISTOCHEMISTRY; HORMONE METABOLISM; HORMONE SYNTHESIS; LUTEAL CELL; MOUSE; MUTANT; NONHUMAN; OOCYTE; PHYSIOLOGY; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROGESTERONE RELEASE; PROTEIN LOCALIZATION; SPONTANEOUS ABORTION; SUPEROVULATION; VASCULARIZATION; WILD TYPE; ANIMAL; BODY WEIGHT; EMBRYO DEVELOPMENT; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; OVARY; PREGNANCY;

MUS;

ANIMALS; BODY WEIGHT; CORPUS LUTEUM; EMBRYO TRANSFER; EMBRYONIC DEVELOPMENT; FEMALE; FERTILITY; FERTILIZATION IN VITRO; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MICE; MICE, KNOCKOUT; OVARY; OVUM; PREGNANCY; PROGESTERONE; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84856284134     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.092999     Document Type: Article

References (35)

1. Findlay JK. Angiogenesis in reproductive tissues. J Endocrinol 1986; 111:357-366.
2. Sugino N, Okuda K. Species-related differences in the mechanism of apoptosis during structural luteolysis. J Reprod Dev 2007; 53:977-986.
3. Haas DM, Ramsey PS. Progestogen for preventing miscarriage. Cochrane Database Syst Rev 2008; 16. CD003511.
4. Agarwal A, Allamaneni SS, Said TM. Chemiluminescence technique for measuring reactive oxygen species. Reprod Biomed Online 2004; 9:466-468.
5. Simsek M, Naziroglu M, Simsek H, Cay M, Aksakal M, Kumru S. Blood plasma levels of lipoperoxides, glutathione peroxidase, beta carotene, vitamin A and E in women with habitual abortion. Cell Biochem Funct 1998; 16:227-231.
6. Sane AS, Chokshi SA, Mishra VV, Barad DP, Shah VC, Nagpal S. Serum lipoperoxides in induced and spontaneous abortions. Gynecol Obstet Invest 1991; 31:172-175.
7. Lagod L, Paszkowski T, Sikorski R, Rola R. The antioxidant-prooxidant balance in pregnancy complicated by spontaneous abortion. Ginekol Pol 2001; 72:1073-1078.
8. Suzuki T, Sugino N, Fukaya T, Sugiyama S, Uda T, Takaya R, Yajima A, Sasano H. Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertil Steril 1999; 72:720-726.
9. Wallace DC, Melov S. Radicals r'aging. Nat Genet 1998; 19:105-106.
10. Okado-Matsumoto A, Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 2001; 276:38388-38393.
11. Imamura Y, Noda S, Hashizume K, Shinoda K, Yamaguchi M, Uchiyama S, Shimizu T, Mizushima Y, Shirasawa T, Tsubota K. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: a model of age-related macular degeneration. Proc Natl Acad Sci U S A 2006; 103:11282-11287.
12. Uchiyama S, Shimizu T, Shirasawa T. CuZn-SOD deficiency causes ApoB degradation and induces hepatic lipid accumulation by impaired lipoprotein secretion in mice. J Biol Chem 2006; 281:31713-31719.
13. Murakami K, Inagaki J, Saito M, Ikeda Y, Tsuda C, Noda Y, Kawakami S, Shirasawa T, Shimizu T. Skin atrophy in cytoplasmic SOD-deficient mice and its complete recovery using a vitamin C derivative. Biochem Biophys Res Commun 2009; 382:457-461.
14. Elchuri S, Oberley TD, Qi W, Eisenstein RS, Jackson Roberts L, Van Remmen H, Epstein CJ, Huang TT. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 2005; 24:367-380.
15. Iuchi Y, Okada F, Onuma K, Onoda T, Asao H, Kobayashi M, Fujii J. Elevated oxidative stress in erythrocytes due to a SOD1 deficiency causes anaemia and triggers autoantibody production. Biochem J 2007; 402:219-227.
16. Muller FL, Song W, Liu Y, Chaudhuri A, Pieke-Dahl S, Strong R, Huang TT, Epstein CJ, Roberts LJ II, Csete M, Faulkner JA, Van Remmen H. Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radic Biol Med 2006; 40:1993-2004.
17. Ho YS, Gargano M, Cao J, Bronson RT, Heimler I, Hutz RJ. Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J Biol Chem 1998; 273:7765-7769.
18. Matzuk MM, Dionne L, Guo Q, Kumar TR, Lebovitz RM. Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 1998; 139:4008-4011.
19. Toyoda Y, Yokoyama M, Hoshi T. Studies on the fertilization of mouse eggs in vitro fertilization of eggs by fresh epididymal sperm [in Japanese]. Jpn J Anim Reprod 1972; 16:147-151.
20. Whitten WK. Nutrient requirements for the culture of preimplantation mouse embryos in vitro. In: Raspa G (ed.), Intrinsic and Extrinsic Factors in Early Mammalian Development. Advances in the Bioscience 1971; 6:129-141.
21. Hinney B, Henze C, Kuhn W, Wuttke W. The corpus luteum insufficiency: a multifactorial disease. J Clin Endocrinol Metab 1996; 81:565-570.
22. Sugino N, Hirosawa-Takamori M, Zhong L, Telleria CM, Shiota K, Gibori G. Hormonal regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase messenger ribonucleic acid in the rat corpus luteum: induction by prolactin and placental lactogens. Biol Reprod 1998; 59:599-605.
23. Sugino N, Takiguchi S, Kashida S, Karube A, Nakamura Y, Kato H. Superoxide dismutase expression in the human corpus luteum during the menstrual cycle and in early pregnancy. Mol Hum Reprod 2000; 6:19-25.
24. El-Far M, El-Sayed IH, El-Motwally AE, Hashem IA, Bakry N. Serum levels of TNF-alpha and antioxidant enzymes and placental TNF-alpha expression in unexplained recurrent spontaneous miscarriage. J Physiol Biochem 2009; 65:175-181.
25. Lim J, Luderer U. Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biol Reprod 2011; 84:775-782.
26. Wong PC, Waggoner D, Subramaniam JR, Tessarollo L, Bartnikas TB, Culotta VC, Price DL, Rothstein J, Gitlin JD. Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase. Proc Natl Acad Sci U S A 2000; 97:2886-2891.
27. Kimura N, Tsunoda S, Iuchi Y, Abe H, Totsukawa K, Fujii J. Intrinsic oxidative stress causes either 2-cell arrest or cell death depending on developmental stage of the embryos from SOD1-deficient mice. Mol Hum Reprod 2010; 16:441-451.
28. Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 1993; 99:673-679.
29. Sugino N, Matsuoka A, Taniguchi K, Tamura H. Angiogenesis in the human corpus luteum. Reprod Med Biol 2008; 7:91-103.
30. Fraser HM, Wilson H, Wulff C, Rudge JS, Wiegand SJ. Administration of vascular endothelial growth factor Trap during the "post-angiogenic" period of the luteal phase causes rapid functional luteolysis and selective endothelial cell death in the marmoset. Reproduction 2006; 132:589-600.
31. Fraser HM, Duncan WC. Vascular morphogenesis in the primate ovary. Angiogenesis 2005; 8:101-116.
32. Fraser HM, Wilson H, Morris KD, Swanston I, Wiegand SJ. Vascular endothelial growth factor Trap suppresses ovarian function at all stages of the luteal phase in the macaque. J Clin Endocrinol Metab 2005; 90:5811-5818.
33. Kashida S, Sugino N, Takiguchi S, Karube A, Takayama H, Yamagata Y, Nakamura Y, Kato H. Regulation and role of vascular endothelial growth factor in the corpus luteum during mid-pregnancy in rats. Biol Reprod 2001; 64:317-323.
34. Groleau J, Dussault S, Haddad P, Turgeon J, Menard C, Chan JS, Rivard A. Essential role of copper-zinc superoxide dismutase for ischemiainduced neovascularization via modulation of bone marrow-derived endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2010; 30:2173-2181.
35. Todorova K, Mazneikova V, Ivanov S, Genova M. The frequency of mild and severe fetal malformations in diabetic women with high values of glycosilated hemoglobin in early pregnancy. Akush Ginekol 2005; 44:3-10.