Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria

Free Radical Biology and Medicine

Volumn 49, Issue 4, 2010, Pages 674-681

  Miyamoto, Kaori ^a   Sato, Eisuke F ^a   Kasahara, Emiko ^a   Jikumaru, Mika ^a   Hiramoto, Keiichi ^a   Tabata, Hisae ^a   Katsuragi, Miyuki ^a   Odo, Satoshi ^b   Utsumi, Kozo ^c   Inoue, Masayasu ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Lonza Japan Ltd   (Japan)

^c OKAYAMA UNIVERSITY   (Japan)

Author keywords

Aging; Carnitine; Free radicals; Mitochondria; Oocyte; Ovulation; Oxidative stress

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; CARNITINE; CATALASE; CHORIONIC GONADOTROPIN; COPPER ZINC SUPEROXIDE DISMUTASE; ESTROGEN; EXTRACELLULAR SUPEROXIDE DISMUTASE; GLUTATHIONE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; NUCLEAR RESPIRATORY FACTOR 1; PROGESTERONE; PROSTAGLANDIN F2 ALPHA; SERIC GONADOTROPIN; THIOL;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL COUNT; CELL CULTURE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION; GENE EXPRESSION; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OOCYTE; OOCYTE MATURATION; OVARY FUNCTION; OVULATION; OXIDATIVE STRESS; PRIORITY JOURNAL; ZYGOTE;

ANIMALS; CHORIONIC GONADOTROPIN; DINOPROST; FEMALE; GONADOTROPINS, EQUINE; HUMANS; MICE; MICE, INBRED ICR; MITOCHONDRIA; OOCYTES; OVARY; OVULATION INDUCTION; OXIDATIVE STRESS;

MUS; RODENTIA;

EID: 77954533119     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.05.025     Document Type: Article

References (46)

1. Armstrong D.T. Prostaglandins and follicular functions. J. Reprod. Fertil. 1981, 62:283-291.
2. Kitai H., Kobayashi Y., Santulli R., Wright K.H., Wallach E.E. The relationship between prostaglandins and histamine in the ovulatory process as determined with the in vitro perfused rabbit ovary. Fertil. Steril. 1985, 43:646-651.
3. Yoshimura Y., Espey L., Hosoi Y., Adachi T., Atlas S.J., Ghodgaonkar R.B., Dubin N.H., Wallach E.E. The effects of bradykinin on ovulation and prostaglandin production by the perfused rabbit ovary. Endocrinology 1988, 122:2540-2546.
4. Espey L.L., Stein V.I., Dumitrescu J. Survey of antiinflammatory agents and related drugs as inhibitors of ovulation in the rabbit. Fertil. Steril. 1982, 38:238-247.
5. Laloraya M., Pradeep K.G., Laloraya M.M. Changes in the levels of superoxide anion radical and superoxide dismutase during the estrous cycle of Rattus norvegicus and induction of superoxide dismutase in rat ovary by lutropin. Biochem. Biophys. Res. Commun. 1988, 157:146-153.
6. Sato E.F., Kobuchi H., Edashige K., Takahashi M., Yoshioka T., Utsumi K., Inoue M. Dynamic aspects of ovarian superoxide dismutase isozymes during the ovulatory process in the rat. FEBS Lett. 1992, 303:121-125.
7. Wang Z., Tamura K., Yoshie M., Tamura H., Imakawa K., Kogo H. Prostaglandin F2alpha-induced functional regression of the corpus luteum and apoptosis in rodents. J. Pharmacol. Sci. 2003, 92:19-27.
8. Minegishi K., Tanaka M., Nishimura O., Tanigaki S., Miyakoshi K., Ishimoto H., Yoshimura Y. Reactive oxygen species mediate leukocyte-endothelium interactions in prostaglandin F2alpha-induced luteolysis in rats. Am. J. Physiol. Endocrinol. Metab. 2002, 283:E1308-E1315.
9. 2) accumulation in the epidermis of patients with vitiligo and its successful removal by a UVB-activated pseudocatalase. J. Invest. Dermatol. Symp. Proc. 1999, 4:91-96.
10. Yang H.W., Hwang K.J., Kwon H.C., Kim H.S., Choi K.W., Oh K.S. Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum. Reprod. 1998, 13:998-1002.
11. Van Blerkom J., Antczak M., Schrader R. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum. Reprod. 1997, 12:1047-1055.
12. Liu L., Keefe D.L. Cytoplasm mediates both development and oxidation-induced apoptotic cell death in mouse zygotes. Biol. Reprod. 2000, 62:1828-1834.
13. Eichenlaub-Ritter U., Boll I. Nocodazole sensitivity, age-related aneuploidy, and alterations in the cell cycle during maturation of mouse oocytes. Cytogenet. Cell Genet. 1989, 52:170-176.
14. Jikumaru M., Hiramoto K., Honma T., Sato E.F., Sekiyama A., Inoue M. Effect of starvation on the survival of male and female mice. Physiol. Chem. Phys. Med. NMR 2007, 39:247-257.
15. Park A.M., Li Q., Nagata K., Tamura T., Shimono K., Sato E.F., Inoue M. Oxygen tension regulates reactive oxygen generation and mutation of Helicobacter pylori. Free Radic. Biol. Med. 2004, 36:1126-1133.
16. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 1969, 27:502-522.
17. Banwell K.M., Lane M., Russell D.L., Kind K.L., Thompson J.G. Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum. Reprod. 2007, 22:2768-2775.
18. Sumanasekera W.K., Zhao L., Ivanova M., Morgan D.D., Noisin E.L., Keynton R.S., Klinge C.M. Effect of estradiol and dihydrotestosterone on hypergravity-induced MAPK signaling and occludin expression in human umbilical vein endothelial cells. Cell Tissue Res. 2006, 324:243-253.
19. Toyokuni S., Tanaka T., Hattori Y., Nishiyama Y., Yoshida A., Uchida K., Hiai H., Ochi H., Osawa T. Quantitative immunohistochemical determination of 8-hydroxy-2'-deoxyguanosine by a monoclonal antibody N45.1: its application to ferric nitrilotriacetate-induced renal carcinogenesis model. Lab. Invest. 1997, 76:365-374.
20. Chang B., Nishikawa M., Sato E., Utsumi K., Inoue M. L-Carnitine inhibits cisplatin-induced injury of the kidney and small intestine. Arch. Biochem. Biophys. 2002, 405:55-64.
21. Chang B., Nishikawa M., Nishiguchi S., Inoue M. L-Carnitine inhibits hepatocarcinogenesis via protection of mitochondria. Int. J. Cancer 2005, 113:719-729.
22. Furuno T., Kanno T., Arita K., Asami M., Utsumi T., Doi Y., Inoue M., Utsumi K. Roles of long chain fatty acids and carnitine in mitochondrial membrane permeability transition. Biochem. Pharmacol. 2001, 62:1037-1046.
23. Uchida K., Kawakishi S. Site-specific oxidation of angiotensin I by copper(II) and L-ascorbate: conversion of histidine residues to 2-imidazolones. Arch. Biochem. Biophys. 1990, 283:20-26.
24. Hino K., Nishikawa M., Sato E., Inoue M. L-Carnitine inhibits hypoglycemia-induced brain damage in the rat. Brain Res. 2005, 1053:77-87.
25. Sasaki J., Sato E.F., Nomura T., Mori H., Watanabe S., Kanda S., Watanabe H., Utsumi K., Inoue M. Detection of manganese superoxide dismutase mRNA in the theca interna cells of rat ovary during the ovulatory process by in situ hybridization. Histochemistry 1994, 102:173-176.
26. Staiger K., Staiger H., Weigert C., Haas C., Haring H.U., Kellerer M. Saturated, but not unsaturated, fatty acids induce apoptosis of human coronary artery endothelial cells via nuclear factor-kappaB activation. Diabetes 2006, 55:3121-3126.
27. Rachek L.I., Musiyenko S.I., LeDoux S.P., Wilson G.L. Palmitate induced mitochondrial deoxyribonucleic acid damage and apoptosis in l6 rat skeletal muscle cells. Endocrinology 2007, 148:293-299.
28. Malhi H., Bronk S.F., Werneburg N.W., Gores G.J. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J. Biol. Chem. 2006, 281:12093-12101.
29. Inoue M., Sato E.F., Nishikawa M., Park A.M., Kira Y., Imada I., Utsumi K. Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr. Med. Chem. 2003, 10:2495-2505.
30. Cotter M.A., Thomas J., Cassidy P., Robinette K., Jenkins N., Florell S.R., Leachman S., Samlowski W.E., Grossman D. N-acetylcysteine protects melanocytes against oxidative stress/damage and delays onset of ultraviolet-induced melanoma in mice. Clin. Cancer Res. 2007, 13:5952-5958.
31. Wang Y., Kashiba M., Kasahara E., Tsuchiya M., Sato E.F., Utsumi K., Inoue M. Metabolic cooperation of ascorbic acid and glutathione in normal and vitamin C-deficient ODS rats. Physiol. Chem. Phys. Med. NMR 2001, 33:29-39.
32. Miranda S., Foncea R., Guerrero J., Leighton F. Oxidative stress and upregulation of mitochondrial biogenesis genes in mitochondrial DNA-depleted HeLa cells. Biochem. Biophys. Res. Commun. 1999, 258:44-49.
33. Jeng J.Y., Yeh T.S., Lee J.W., Lin S.H., Fong T.H., Hsieh R.H. Maintenance of mitochondrial DNA copy number and expression is essential for preservation of mitochondrial function and cell growth. J. Cell. Biochem. 2008, 103:347-357.
34. Davis A.F., Ropp P.A., Clayton D.A., Copeland W.C. Mitochondrial DNA polymerase gamma is expressed and translated in the absence of mitochondrial DNA maintenance and replication. Nucleic Acids Res. 1996, 24:2753-2759.
35. Larsson N.G., Oldfors A., Holme E., Clayton D.A. Low levels of mitochondrial transcription factor A in mitochondrial DNA depletion. Biochem. Biophys. Res. Commun. 1994, 200:1374-1381.
36. Suliman H.B., Carraway M.S., Welty-Wolf K.E., Whorton A.R., Piantadosi C.A. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. J. Biol. Chem. 2003, 278:41510-41518.
37. Mattingly K.A., Ivanova M.M., Riggs K.A., Wickramasinghe N.S., Barch M.J., Klinge C.M. Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol. Endocrinol. 2008, 22:609-622.
38. Silva J.P., Kohler M., Graff C., Oldfors A., Magnuson M.A., Berggren P.O., Larsson N.G. Impaired insulin secretion and beta-cell loss in tissue-specific knockout mice with mitochondrial diabetes. Nat. Genet. 2000, 26:336-340.
39. Larsson N.G., Wang J., Wilhelmsson H., Oldfors A., Rustin P., Lewandoski M., Barsh G.S., Clayton D.A. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 1998, 18:231-236.
40. Nishi Y., Takeshita T., Sato K., Araki T. Change of the mitochondrial distribution in mouse ooplasm during in vitro maturation. J. Nippon Med. Sch. 2003, 70:408-415.
41. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 1998, 93:1147-1158.
42. Nangaku M., Sato-Yoshitake R., Okada Y., Noda Y., Takemura R., Yamazaki H., Hirokawa N. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 1994, 79:1209-1220.
43. Zuelke K.A., Jones D.P., Perreault S.D. Glutathione oxidation is associated with altered microtubule function and disrupted fertilization in mature hamster oocytes. Biol. Reprod. 1997, 57:1413-1419.
44. Tarin J.J. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 1996, 2:717-724.
45. Muller D.M., Seim H., Kiess W., Loster H., Richter T. Effects of oral L-carnitine supplementation on in vivo long-chain fatty acid oxidation in healthy adults. Metabolism 2002, 51:1389-1391.
46. Borum P.R. Carnitine and lipid metabolism. Bol. Asoc. Med. P. R. 1991, 83:134-135.