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Pathological Role of Reactive Oxygen Species on Female Reproduction

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Oxidative Stress and Toxicity in Reproductive Biology and Medicine

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1391))

Abstract

Oxidative stress (OS), a clinical predicament characterized by a shift in homeostatic imbalance among prooxidant molecules embracing reactive oxygen species (ROS) and reactive nitrogen species (RNS), along with antioxidant defenses, has been established to play an indispensable part in the pathophysiology of subfertility in both human males and females. ROS are highly reactive oxidizing by-products generated during critical oxygen-consuming processes or aerobic metabolism. A healthy body system has its own course of action to maintain the equilibrium between prooxidants and antioxidants with an efficient defense system to fight against ROS. But when ROS production crosses its threshold, the disturbance in homeostatic balance results in OS. Besides their noxious effects, literature studies have depicted that controlled and adequate ROS concentrations exert physiologic functions, especially that gynecologic OS is an important mediator of conception in females. Yet the impact of ROS on oocytes and reproductive functions still needs a strong attestation for further analysis because the disruption in prooxidant and antioxidant balance leads to abrupt ROS generation initiating multiple reproductive diseases such as polycystic ovary syndrome (PCOS), endometriosis, and unexplained infertility in addition to other impediments in pregnancy such as recurrent pregnancy loss, spontaneous abortion, and preeclampsia. The current article elucidates the skeptical state of affairs created by ROS that influences female fertility.

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References

  • Abuja PM, Albertini R. Methods for monitoring oxidative stress, lipid peroxidation and oxidation resistance of lipoproteins. Clin Chim Acta. 2001;306(1–2):1–17.

    Article  CAS  Google Scholar 

  • Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol. 2012;10(1):1–31.

    Article  Google Scholar 

  • Agarwal A, Gupta S, Sekhon L, Shah R. Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid Redox Signal. 2008;10(8):1375–404.

    Article  CAS  Google Scholar 

  • Aitken R, De Iuliis G. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 2009;16(1):3–13.

    Article  Google Scholar 

  • Aitken RJ, Buckingham DW, Carreras A, Irvine DS. Superoxide dismutase in human sperm suspensions: relationship with cellular composition, oxidative stress, and sperm function. Free Radic Biol Med. 1996;21(4):495–504.

    Article  CAS  Google Scholar 

  • Alam H, et al. Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology. 2009;150(2):915–28.

    Article  CAS  Google Scholar 

  • Aouache R, Biquard L, Vaiman D, Miralles F. Oxidative stress in preeclampsia and placental diseases. Int J Mol Sci. 2018;19(5):1496.

    Article  Google Scholar 

  • Araki M, Fukumatsu Y, Katabuchi H, Shultz LD, Takahashi K, Okamura H. Follicular development and ovulation in macrophage colony-stimulating factor-deficient mice homozygous for the osteopetrosis (op) mutation. Biol Reprod. 1996;54(2):478–84.

    Article  CAS  Google Scholar 

  • Aroor AR, DeMarco VG. Oxidative stress and obesity: the chicken or the egg? Diabetes. 2014;63(7):2216–8.

    Article  Google Scholar 

  • Behrman HR, Kodaman PH, Preston SL, Gao S. Oxidative stress and the ovary. J Soc Gynecol Investig. 2001;8(1_suppl):S40–2.

    Article  CAS  Google Scholar 

  • Behrman HR, Preston SL, Aten RF, Rinaudo P, Zreik TG. Hormone induction of ascorbic acid transport in immature granulosa cells. Endocrinology. 1996;137(10):4316–21.

    Article  CAS  Google Scholar 

  • Biri A, Bozkurt N, Turp A, Kavutcu M, Himmetoglu Ö, Durak I. Role of oxidative stress in intrauterine growth restriction. Gynecol Obstet Investig. 2007;64(4):187–92.

    Article  CAS  Google Scholar 

  • Bivalacqua TJ, et al. BASIC SCIENCE: superoxide anion production in the rat penis impairs erectile function in diabetes: influence of in vivo extracellular superoxide dismutase gene therapy. J Sex Med. 2005;2(2):187–98.

    Article  CAS  Google Scholar 

  • Blagden SP. Harnessing pandemonium: the clinical implications of tumor heterogeneity in ovarian cancer. Front Oncol. 2015;5:149.

    Article  Google Scholar 

  • Brannstrom M. Potential role of cytokines in ovarian physiology: the case for interleukin-1. The Ovary; 2004.

    Google Scholar 

  • Brännström M, Bonello N, Norman RJ, Robertson SA. Reduction of ovulation rate in the rat by administration of a neutrophil-depleting monoclonal antibody. J Reprod Immunol. 1995;29(3):265–70.

    Article  Google Scholar 

  • Brown MD, Sacks DB. Protein scaffolds in MAP kinase signalling. Cell Signal. 2009;21(4):462–9.

    Article  CAS  Google Scholar 

  • Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414(6865):813–20.

    Article  CAS  Google Scholar 

  • Buchanan TA, Denno KM, Sipos GF, Sadler TW. Diabetic teratogenesis: in vitro evidence for a multifactorial etiology with little contribution from glucose per se. Diabetes. 1994;43(5):656–60.

    Article  CAS  Google Scholar 

  • Burton G, Yung H-W, Cindrova-Davies T, Charnock-Jones D. Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta. 2009;30:43–8.

    Article  Google Scholar 

  • Burton GJ, Jauniaux E. Oxidative stress. Best Pract Res Clin Obstet Gynaecol. 2011;25(3):287–99.

    Article  Google Scholar 

  • Cai J, Jones DP. Superoxide in apoptosis: mitochondrial generation triggered by cytochromec loss. J Biol Chem. 1998;273(19):11401–4.

    Article  CAS  Google Scholar 

  • Carambula SF, et al. Caspase-3 is a pivotal mediator of apoptosis during regression of the ovarian corpus luteum. Endocrinology. 2002;143(4):1495–501.

    Article  CAS  Google Scholar 

  • Carlson JC, Sawada M, Boone DL, Stauffer JM. Stimulation of progesterone secretion in dispersed cells of rat corpora lutea by antioxidants. Steroids. 1995;60(3):272–6.

    Article  CAS  Google Scholar 

  • Chao HT, Lee SY, Lee HM, Liao TL, Wei YH, Kao SH. Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries. Ann N Y Acad Sci. 2005;1042(1):148–56.

    Article  CAS  Google Scholar 

  • Chaube S, Prasad P, Thakur S, Shrivastav T. Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro. Apoptosis. 2005;10(4):863–74.

    Article  CAS  Google Scholar 

  • Chaube SK, et al. Clomiphene citrate induces ROS-mediated apoptosis in mammalian oocytes. Open J Apoptosis. 2014;3:52–8.

    Article  Google Scholar 

  • Chauhan SP, Gupta LM, Hendrix NW, Berghella V. Intrauterine growth restriction: comparison of American College of Obstetricians and Gynecologists practice bulletin with other national guidelines. Am J Obstet Gynecol. 2009;200(4):409.e1–6.

    Article  Google Scholar 

  • Chen EY, Fujinaga M, Giaccia AJ. Hypoxic microenvironment within an embryo induces apoptosis and is essential for proper morphological development. Teratology. 1999;60(4):215–25.

    Article  CAS  Google Scholar 

  • Chéreau DA. Mémoires pour servir à l'étude des maladies des ovaires. Premier mémoire contenant: 1° les considérations anatomiques et physiologiques; 2° l'agénésie et les vices de conformation des ovaires; 3° l'inflammation aiguë des ovaires, ovarite aiguë, par Achille Chéreau. Fortin, Masson; 1844.

    Google Scholar 

  • Cooke MS, Evans MD, Dizdaroglu M, Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 2003;17(10):1195–214.

    Article  CAS  Google Scholar 

  • Covarrubias AE, et al. AP39, a modulator of mitochondrial bioenergetics, reduces antiangiogenic response and oxidative stress in hypoxia-exposed trophoblasts: relevance for preeclampsia pathogenesis. Am J Pathol. 2019;189(1):104–14.

    Article  CAS  Google Scholar 

  • Critchley HO, et al. Hypoxia-inducible factor-1α expression in human endometrium and its regulation by prostaglandin E-series prostanoid receptor 2 (EP2). Endocrinology. 2006;147(2):744–53.

    Article  CAS  Google Scholar 

  • de Lamirande E, O’Flaherty C. Sperm activation: role of reactive oxygen species and kinases. Biochim Biophys Acta Proteins Proteom. 2008;1784(1):106–15.

    Article  Google Scholar 

  • de Lamirande E, Tsai C, Harakat A, Gagnon C. Involvement of reactive oxygen species in human sperm arcosome reaction induced by A23187, lysophosphatidylcholine, and biological fluid ultrafiltrates. J Androl. 1998;19(5):585–94.

    Google Scholar 

  • Dennery PA. Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today. 2007;81(3):155–62.

    Article  CAS  Google Scholar 

  • Dharmarajan A, Hisheh S, Singh B, Parkinson S, Tilly KI, Tilly JL. Antioxidants mimic the ability of chorionic gonadotropin to suppress apoptosis in the rabbit corpus luteum in vitro: a novel role for superoxide dismutase in regulating bax expression. Endocrinology. 1999;140(6):2555–61.

    Article  CAS  Google Scholar 

  • Dincer Y, Akcay T, Erdem T, Ilker Saygili E, Gundogdu S. DNA damage, DNA susceptibility to oxidation and glutathione level in women with polycystic ovary syndrome. Scand J Clin Lab Invest. 2005;65(8):721–8.

    Article  CAS  Google Scholar 

  • Diamanti-Kandarakis E, Dunaif A. Insulin resistance and the polycystic ovary syndrome revisited: an update on mechanisms and implications. Endocr Rev. 2012;33(6):981–1030.

    Article  CAS  Google Scholar 

  • Du L, He F, Kuang L, Tang W, Li Y, Chen D. eNOS/iNOS and endoplasmic reticulum stress-induced apoptosis in the placentas of patients with preeclampsia. J Hum Hypertens. 2017;31(1):49–55.

    Article  CAS  Google Scholar 

  • Dumollard R, Ward Z, Carroll J, Duchen MR. Regulation of redox metabolism in the mouse oocyte and embryo. Development. 2007;134(3):455–65.

    Article  CAS  Google Scholar 

  • El-Far M, El-Sayed IH, El-Motwally AE-G, Hashem IA, Bakry N. Tumor necrosis factor-α and oxidant status are essential participating factors in unexplained recurrent spontaneous abortions. Clin Chem Lab Med. 2007;45(7):879–83.

    Article  CAS  Google Scholar 

  • Eriksson U, Borg L. Protection by free oxygen radical scavenging enzymes against glucose-induced embryonic malformations in vitro. Diabetologia. 1991;34(5):325–31.

    Article  CAS  Google Scholar 

  • Eriksson UJ, Borg LH. Diabetes and embryonic malformations: role of substrate-induced free-oxygen radical production for dysmorphogenesis in cultured rat embryos. Diabetes. 1993;42(3):411–9.

    Article  CAS  Google Scholar 

  • ESHRE TR, Group A-SPCW. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril. 2004;81(1):19–25.

    Article  Google Scholar 

  • Espey LL. Ovulation as an inflammatory reaction—a hypothesis. Biol Reprod. 1980;22(1):73–106.

    Article  CAS  Google Scholar 

  • Freeman BA, Crapo JD. Biology of disease: free radicals and tissue injury. Lab Invest. 1982;47(5):412–26.

    CAS  Google Scholar 

  • Fu J, Zhao L, Wang L, Zhu X. Expression of markers of endoplasmic reticulum stress-induced apoptosis in the placenta of women with early and late onset severe pre-eclampsia. Taiwanese J Obstet Gynecol. 2015;54(1):19–23.

    Article  Google Scholar 

  • Fujii J, Ito J-i, Zhang X, Kurahashi T. Unveiling the roles of the glutathione redox system in vivo by analyzing genetically modified mice. J Clin Biochem Nutr. 2011;49(2):70–8.

    Article  CAS  Google Scholar 

  • Fujimura M, Morita-Fujimura Y, Noshita N, Sugawara T, Kawase M, Chan PH. The cytosolic antioxidant copper/zinc-superoxide dismutase prevents the early release of mitochondrial cytochrome c in ischemic brain after transient focal cerebral ischemia in mice. J Neurosci. 2000;20(8):2817–24.

    Article  CAS  Google Scholar 

  • Ghosh G, et al. Racial/ethnic differences in pregnancy-related hypertensive disease in nulliparous women. Ethn Dis. 2014;24(3):283.

    Google Scholar 

  • Gong S, Gabriel MCS, Zini A, Chan P, O'Flaherty C. Low amounts and high thiol oxidation of peroxiredoxins in spermatozoa from infertile men. J Androl. 2012;33(6):1342–51.

    Article  CAS  Google Scholar 

  • González F, Rote NS, Minium J, Kirwan JP. Reactive oxygen species-induced oxidative stress in the development of insulin resistance and hyperandrogenism in polycystic ovary syndrome. J Clin Endocrinol Metabol. 2006;91(1):336–40.

    Article  Google Scholar 

  • Greenlund LJ, Deckwerth TL, Johnson EM Jr. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron. 1995;14(2):303–15.

    Article  CAS  Google Scholar 

  • Gualtieri R, Mollo V, Duma G, Talevi R. Redox control of surface protein sulphhydryls in bovine spermatozoa reversibly modulates sperm adhesion to the oviductal epithelium and capacitation. Reproduction. 2009;138(1):33.

    Article  CAS  Google Scholar 

  • Guerin P, El Mouatassim S, Menezo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update. 2001;7(2):175–89.

    Article  CAS  Google Scholar 

  • Gupta S, Agarwal A, Banerjee J, Alvarez JG. The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: a systematic review. Obstet Gynecol Surv. 2007;62(5):335–47.

    Article  Google Scholar 

  • Heazell A, Lacey H, Jones C, Huppertz B, Baker P, Crocker I. Effects of oxygen on cell turnover and expression of regulators of apoptosis in human placental trophoblast. Placenta. 2008;29(2):175–86.

    Article  CAS  Google Scholar 

  • Hromadnikova I. Extracellular nucleic acids in maternal circulation as potential biomarkers for placental insufficiency. DNA Cell Biol. 2012;31(7):1221–32.

    Article  CAS  Google Scholar 

  • Huang Q, et al. Advanced oxidation protein products enhances soluble Fms-like tyrosine kinase 1 expression in trophoblasts: a possible link between oxidative stress and preeclampsia. Placenta. 2013;34(10):949–52.

    Article  CAS  Google Scholar 

  • Incalza MA, D'Oria R, Natalicchio A, Perrini S, Laviola L, Giorgino F. Oxidative stress and reactive oxygen species in endothelial dysfunction associated with cardiovascular and metabolic diseases. Vasc Pharmacol. 2018;100:1–19.

    Article  CAS  Google Scholar 

  • Irvine DS. Glutathione as a treatment for male infertility. Rev Reprod. 1996;1(1):6–12.

    Article  CAS  Google Scholar 

  • Ishii T, et al. Accelerated impairment of spermatogenic cells in SOD1-knockout mice under heat stress. Free Radic Res. 2005;39(7):697–705.

    Article  CAS  Google Scholar 

  • Ishii T, et al. Genetically induced oxidative stress in mice causes thrombocytosis, splenomegaly and placental angiodysplasia that leads to recurrent abortion. Redox Biol. 2014;2:679–85.

    Article  CAS  Google Scholar 

  • Iuchi Y, et al. Peroxiredoxin 4 knockout results in elevated spermatogenic cell death via oxidative stress. Biochem J. 2009;419(1):149–58.

    Article  CAS  Google Scholar 

  • Iwata K, et al. Analysis of compaction initiation in human embryos by using time-lapse cinematography. J Assist Reprod Genet. 2014;31(4):421–6.

    Article  Google Scholar 

  • Jauniaux E, Gulbis B, Burton GJ. Physiological implications of the materno–fetal oxygen gradient in human early pregnancy. Reprod Biomed Online. 2003;7(2):250–3.

    Article  Google Scholar 

  • Jauniaux E, Watson AL, Hempstock J, Bao Y-P, Skepper JN, Burton GJ. Onset of maternal arterial blood flow and placental oxidative stress: a possible factor in human early pregnancy failure. Am J Pathol. 2000;157(6):2111–22.

    Article  CAS  Google Scholar 

  • Jiang Z, et al. DNA damage regulates ARID1A stability via SCF ubiquitin ligase in gastric cancer cells. Eur Rev Med Pharmacol Sci. 2015;19(17):3194–200.

    Google Scholar 

  • Joham AE, Teede HJ, Ranasinha S, Zoungas S, Boyle J. Prevalence of infertility and use of fertility treatment in women with polycystic ovary syndrome: data from a large community-based cohort study. J Women's Health. 2015;24(4):299–307.

    Article  Google Scholar 

  • Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol. 2006;70(5):1469–80.

    Article  CAS  Google Scholar 

  • Kodaman PH, Behrman HR. Endocrine-regulated and protein kinase C-dependent generation of superoxide by rat preovulatory follicles. Endocrinology. 2001;142(2):687–93.

    Article  CAS  Google Scholar 

  • Krishna U, Bhalerao S. Placental insufficiency and fetal growth restriction. J Obstet Gynecol India. 2011;61(5):505–11.

    Article  Google Scholar 

  • Kumar TR, Wiseman AL, Kala G, Kala SV, Matzuk MM, Lieberman MW. Reproductive defects in γ-glutamyl transpeptidase-deficient mice. Endocrinology. 2000;141(11):4270–7.

    Article  CAS  Google Scholar 

  • Kwan S-Y, et al. Loss of ARID1A expression leads to sensitivity to ROS-inducing agent elesclomol in gynecologic cancer cells. Oncotarget. 2016;7(35):56933.

    Article  Google Scholar 

  • Levine AJ, Puzio-Kuter AM. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science. 2010;330(6009):1340–4.

    Article  CAS  Google Scholar 

  • Levy R, Smith SD, Chandler K, Sadovsky Y, Nelson DM. Apoptosis in human cultured trophoblasts is enhanced by hypoxia and diminished by epidermal growth factor. Am J Phys Cell Phys. 2000;278(5):C982–8.

    CAS  Google Scholar 

  • Levy R, et al. Trophoblast apoptosis from pregnancies complicated by fetal growth restriction is associated with enhanced p53 expression. Am J Obstet Gynecol. 2002;186(5):1056–61.

    Article  CAS  Google Scholar 

  • Li Y, et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet. 1995;11(4):376–81.

    Article  CAS  Google Scholar 

  • Lian I, et al. Increased endoplasmic reticulum stress in decidual tissue from pregnancies complicated by fetal growth restriction with and without pre-eclampsia. Placenta. 2011;32(11):823–9.

    Article  CAS  Google Scholar 

  • Manandhar G, et al. Peroxiredoxin 2 and peroxidase enzymatic activity of mammalian spermatozoa. Biol Reprod. 2009;80(6):1168–77.

    Article  CAS  Google Scholar 

  • Manes C, Lai N. Nonmitochondrial oxygen utilization by rabbit blastocysts and surface production of superoxide radicals. Reproduction. 1995;104(1):69–75.

    Article  CAS  Google Scholar 

  • Many A, Hubel CA, Fisher SJ, Roberts JM, Zhou Y. Invasive cytotrophoblasts manifest evidence of oxidative stress in preeclampsia. Am J Pathol. 2000;156(1):321–31.

    Article  CAS  Google Scholar 

  • Men H, Monson RL, Parrish JJ, Rutledge JJ. Degeneration of cryopreserved bovine oocytes via apoptosis during subsequent culture. Cryobiology. 2003;47(1):73–81.

    Article  CAS  Google Scholar 

  • Miesel R, Drzejczak PJĘ, Kurpisz M. Oxidative stress during the interaction of gametes. Biol Reprod. 1993;49(5):918–23.

    Article  CAS  Google Scholar 

  • Mifsud W, Sebire NJ. Placental pathology in early-onset and late-onset fetal growth restriction. Fetal Diagn Ther. 2014;36(2):117–28.

    Article  Google Scholar 

  • Migdal C, Serres M. Espèces réactives de l’oxygène et stress oxydant. médecine/sciences. 2011;27(4):405–12.

    Article  Google Scholar 

  • Miller H, Wilson R, Jenkins C, MacLean MA, Roberts J, Walker JJ. Glutathione levels and miscarriage. Fertil Steril. 2000;74(6):1257–8.

    Article  CAS  Google Scholar 

  • Miyazaki T, Sueoka K, Dharmarajan A, Atlas S, Bulkley G, Wallach E. Effect of inhibition of oxygen free radical on ovulation and progesterone production by the in-vitro perfused rabbit ovary. Reproduction. 1991;91(1):207–12.

    Article  CAS  Google Scholar 

  • Mizuuchi M, Cindrova-Davies T, Olovsson M, Charnock-Jones DS, Burton GJ, Yung HW. Placental endoplasmic reticulum stress negatively regulates transcription of placental growth factor via ATF4 and ATF6β: implications for the pathophysiology of human pregnancy complications. J Pathol. 2016;238(4):550–61.

    Article  CAS  Google Scholar 

  • Mohammadi M. Oxidative stress and polycystic ovary syndrome: a brief review. Int J Prevent Med. 2019;10:86.

    Article  Google Scholar 

  • Morgan PE, Dean RT, Davies MJ. Inhibition of glyceraldehyde-3-phosphate dehydrogenase by peptide and protein peroxides generated by singlet oxygen attack. Eur J Biochem. 2002;269(7):1916–25.

    Article  CAS  Google Scholar 

  • Morriss G. Growing embryos in vitro. Nature. 1979;278(5703):402.

    Article  CAS  Google Scholar 

  • Murdoch W. Inhibition by oestradiol of oxidative stress-induced apoptosis in pig ovarian tissues. Reproduction. 1998;114(1):127–30.

    Article  CAS  Google Scholar 

  • Nakamura BN, et al. Lack of maternal glutamate cysteine ligase modifier subunit (Gclm) decreases oocyte glutathione concentrations and disrupts preimplantation development in mice. Endocrinology. 2011;152(7):2806–15.

    Article  CAS  Google Scholar 

  • Nakamura T, Sakamoto K. Reactive oxygen species up-regulates cyclooxygenase-2, p53, and Bax mRNA expression in bovine luteal cells. Biochem Biophys Res Commun. 2001;284(1):203–10.

    Article  CAS  Google Scholar 

  • Nasr-Esfahani MH, Aitken JR, Johnson MH. Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development. 1990;109(2):501–7.

    Article  CAS  Google Scholar 

  • Nasr-Esfahani MM, Johnson MH. The origin of reactive oxygen species in mouse embryos cultured in vitro. Development. 1991;113(2):551–60.

    Article  CAS  Google Scholar 

  • New D, Coppola P. Effects of different oxygen concentrations on the development of rat embryos in culture. Reproduction. 1970;21(1):109–18.

    Article  CAS  Google Scholar 

  • Nishikawa T, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000;404(6779):787–90.

    Article  CAS  Google Scholar 

  • Nur Torun A, Vural M, Cece H, Camuzcuoglu H, Toy H, Aksoy N. Paraoxonase-1 is not affected in polycystic ovary syndrome without metabolic syndrome and insulin resistance, but oxidative stress is altered. Gynecol Endocrinol. 2011;27(12):988–92.

    Article  CAS  Google Scholar 

  • O'Flaherty C, Rico de Souza A. Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner. Biol Reprod. 2011;84(2):238–47.

    Article  CAS  Google Scholar 

  • Paria B, Dey S. Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc Natl Acad Sci. 1990;87(12):4756–60.

    Article  CAS  Google Scholar 

  • Pontes IE, Afra KF, Silva JR, Borges PS, Clough GF, Alves JG. Microvascular reactivity in women with gestational diabetes mellitus studied during pregnancy. Diabetol Metab Syndr. 2015;7(1):1–6.

    Article  Google Scholar 

  • Poston L, Briley A, Seed P, Kelly F, Shennan A, Consortium ViP-eT. Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial. Lancet. 2006;367(9517):1145–54.

    Article  CAS  Google Scholar 

  • Powe CE, Levine RJ, Karumanchi SA. Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation. 2011;123(24):2856–69.

    Article  Google Scholar 

  • Raineri I, et al. Strain-dependent high-level expression of a transgene for manganese superoxide dismutase is associated with growth retardation and decreased fertility. Free Radic Biol Med. 2001;31(8):1018–30.

    Article  CAS  Google Scholar 

  • Rapoport R, Sklan D, Wolfenson D, Shaham-Albalancy A, Hanukoglu I. Antioxidant capacity is correlated with steroidogenic status of the corpus luteum during the bovine estrous cycle. Biochim Biophys Acta. 1998;1380(1):133–40.

    Article  CAS  Google Scholar 

  • Rashidi B, Haghollahi F, Shariat M, Zayerii F. The effects of calcium-vitamin D and metformin on polycystic ovary syndrome: a pilot study. Taiwanese J Obstet Gynecol. 2009;48(2):142–7.

    Article  Google Scholar 

  • Retèl J, et al. Mutational specificity of oxidative DNA damage. Mutat Res. 1993;299(3–4):165–82.

    Article  Google Scholar 

  • Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med. 2010;49(11):1603–16.

    Article  CAS  Google Scholar 

  • Rhee SG. H2O2, a necessary evil for cell signaling. Science. 2006;312(5782):1882–3.

    Article  Google Scholar 

  • Rhee SG, Kang SW, Jeong W, Chang T-S, Yang K-S, Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol. 2005;17(2):183–9.

    Article  CAS  Google Scholar 

  • Rivera-Nieves J, Thompson WC, Levine RL, Moss J. Thiols mediate superoxide-dependent NADH modification of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem. 1999;274(28):19525–31.

    Article  CAS  Google Scholar 

  • Roberts VH, Smith J, McLea SA, Heizer AB, Richardson JL, Myatt L. Effect of increasing maternal body mass index on oxidative and nitrative stress in the human placenta. Placenta. 2009;30(2):169–75.

    Article  CAS  Google Scholar 

  • Rojas V, Hirshfield KM, Ganesan S, Rodriguez-Rodriguez L. Molecular characterization of epithelial ovarian cancer: implications for diagnosis and treatment. Int J Mol Sci. 2016;17(12):2113.

    Article  Google Scholar 

  • Roos WP, Thomas AD, Kaina B. DNA damage and the balance between survival and death in cancer biology. Nat Rev Cancer. 2016;16(1):20–33.

    Article  CAS  Google Scholar 

  • Rothstein JD, Bristol LA, Hosler B, Brown RH, Kuncl RW. Chronic inhibition of superoxide dismutase produces apoptotic death of spinal neurons. Proc Natl Acad Sci. 1994;91(10):4155–9.

    Article  CAS  Google Scholar 

  • Roughton SA, Lareu RR, Bittles AH, Dharmarajan AM. Fas and Fas ligand messenger ribonucleic acid and protein expression in the rat corpus luteum during apoptosis-mediated luteolysis. Biol Reprod. 1999;60(4):797–804.

    Article  CAS  Google Scholar 

  • Runchel C, Matsuzawa A, Ichijo H. Mitogen-activated protein kinases in mammalian oxidative stress responses. Antioxid Redox Signal. 2011;15(1):205–18.

    Article  CAS  Google Scholar 

  • Sadler T, Hunter E, Wynn R, Phillips L. Evidence for multifactorial origin of diabetes-induced embryopathies. Diabetes. 1989;38(1):70–4.

    Article  CAS  Google Scholar 

  • Saed GM, Diamond MP, Fletcher NM. Updates of the role of oxidative stress in the pathogenesis of ovarian cancer. Gynecol Oncol. 2017;145(3):595–602.

    Article  CAS  Google Scholar 

  • Sasagawa I, et al. Possible involvement of the membrane-bound form of peroxiredoxin 4 in acrosome formation during spermiogenesis of rats. Eur J Biochem. 2001;268(10):3053–61.

    Article  CAS  Google Scholar 

  • Sato EF, et al. Dynamic aspects of ovarian superoxide dismutase isozymes during the ovulatory process in the rat. FEBS Lett. 1992;303(2–3):121–5.

    CAS  Google Scholar 

  • Sawada M, Carlson J. Intracellular regulation of progesterone secretion by the superoxide radical in the rat corpus luteum. Endocrinology. 1996;137(5):1580–4.

    Article  CAS  Google Scholar 

  • Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med. 2001;30(11):1191–212.

    Article  CAS  Google Scholar 

  • Scifres CM, Nelson DM. Intrauterine growth restriction, human placental development and trophoblast cell death. J Physiol. 2009;587(14):3453–8.

    Article  CAS  Google Scholar 

  • Sharma R, Biedenharn KR, Fedor JM, Agarwal A. Lifestyle factors and reproductive health: taking control of your fertility. Reprod Biol Endocrinol. 2013;11(1):1–15.

    Article  Google Scholar 

  • Shigetomi H, Higashiura Y, Kajihara H, Kobayashi H. A potential link of oxidative stress and cell cycle regulation for development of endometriosis. Gynecol Endocrinol. 2012;28(11):897–902.

    Article  CAS  Google Scholar 

  • Shikone T, Yamoto M, Kokawa K, Yamashita K, Nishimori K, Nakano R. Apoptosis of human corpora lutea during cyclic luteal regression and early pregnancy. J Clin Endocrinol Metabol. 1996;81(6):2376–80.

    CAS  Google Scholar 

  • Shimamura K, Sugino N, Yoshida Y, Nakamura Y, Ogino K, Kato H. Changes in lipid peroxide and antioxidant enzyme activities in corpora lutea during pseudopregnancy in rats. Reproduction. 1995;105(2):253–7.

    Article  CAS  Google Scholar 

  • Shirai F, Kawaguchi M, Yutsudo M, Dohi Y. Human peripheral blood polymorphonuclear leukocytes at the ovulatory period are in an activated state. Mol Cell Endocrinol. 2002;196(1–2):21–8.

    Article  CAS  Google Scholar 

  • Silva F, Marques A, Chaveiro A. Reactive oxygen species: a double-edged sword in reproduction. Open Vet Sci J. 2010;4(1)

    Google Scholar 

  • Şimşek M, Naziroǧlu M, Şimşek 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(4):227–31.

    Article  Google Scholar 

  • Snezhkina AV, et al. ROS generation and antioxidant defense systems in normal and malignant cells. Oxid Med Cell Longev. 2019;2019:6175804.

    Article  Google Scholar 

  • Sprague AH, Khalil RA. Inflammatory cytokines in vascular dysfunction and vascular disease. Biochem Pharmacol. 2009;78(6):539–52.

    Article  CAS  Google Scholar 

  • Steegers EA, Von Dadelszen P, Duvekot JJ, Pijnenborg R. Pre-eclampsia. Lancet. 2010;376(9741):631–44.

    Article  Google Scholar 

  • Sugino N. Reactive oxygen species in ovarian physiology. Reprod Med Biol. 2005;4(1):31–44.

    CAS  Google Scholar 

  • Sugino N, Nakamura Y, Takeda O, Ishimatsu M, Kato H. Changes in activities of superoxide dismutase and lipid peroxide in corpus luteum during pregnancy in rats. Reproduction. 1993;97(2):347–51.

    Article  CAS  Google Scholar 

  • 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(1):19–25.

    Article  CAS  Google Scholar 

  • Sugino N, Telleria CM, Gibori G. Differential regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase in the rat corpus luteum: induction of manganese superoxide dismutase messenger ribonucleic acid by inflammatory cytokines. Biol Reprod. 1998;59(1):208–15.

    Article  CAS  Google Scholar 

  • Sun SY, et al. Maternal near miss according to World Health Organization classification among women with a hydatidiform mole: experience at the New England trophoblastic disease center, 1994–2013. J Reprod Med. 2016;61(5–6):210–4.

    Google Scholar 

  • Takeda T, et al. ARID1A gene mutation in ovarian and endometrial cancers. Oncol Rep. 2016;35(2):607–13.

    Article  CAS  Google Scholar 

  • Takiguchi S, et al. Differential regulation of apoptosis in the corpus luteum of pregnancy and newly formed corpus luteum after parturition in rats. Biol Reprod. 2004;70(2):313–8.

    Article  CAS  Google Scholar 

  • Tanaka M, et al. Participation of reactive oxygen species in PGF2alpha-induced apoptosis in rat luteal cells. J Reprod Fertil. 2000;120(2):239–45.

    Article  CAS  Google Scholar 

  • Tannetta D, Sargent I. Placental disease and the maternal syndrome of preeclampsia: missing links? Curr Hypertens Rep. 2013;15(6):590–9.

    Article  CAS  Google Scholar 

  • Tatone C, et al. Sirtuin functions in female fertility: possible role in oxidative stress and aging. Oxidative Med Cell Longev. 2015;2015:659687.

    Article  Google Scholar 

  • Tenório MB, Ferreira RC, Moura FA, Bueno NB, de Oliveira ACM, Goulart MOF. Cross-talk between oxidative stress and inflammation in preeclampsia. Oxid Med Cell Longev. 2019;2019:8238727.

    Article  Google Scholar 

  • Tiwari M, et al. Involvement of reactive oxygen species in meiotic cell cycle regulation and apoptosis in mammalian oocytes. React Oxygen Spec. 2016;1(2):110–6.

    Google Scholar 

  • Tokuhiro K, Ikawa M, Benham AM, Okabe M. Protein disulfide isomerase homolog PDILT is required for quality control of sperm membrane protein ADAM3 and male fertility. Proc Natl Acad Sci. 2012;109(10):3850–5.

    Article  CAS  Google Scholar 

  • Tordella L, et al. SWI/SNF regulates a transcriptional program that induces senescence to prevent liver cancer. Genes Dev. 2016;30(19):2187–98.

    Article  CAS  Google Scholar 

  • Tripathi A, et al. Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radic Res. 2009;43(3):287–94.

    Article  CAS  Google Scholar 

  • Tripathi A, et al. Melatonin protects against clomiphene citrate-induced generation of hydrogen peroxide and morphological apoptotic changes in rat eggs. Eur J Pharmacol. 2011;667(1–3):419–24.

    Article  CAS  Google Scholar 

  • Tripathi A, Shrivastav TG, Chaube SK. An increase of granulosa cell apoptosis mediates aqueous neem (Azadirachta indica) leaf extract-induced oocyte apoptosis in rat. Int J Appl Basic Med Res. 2013;3(1):27.

    Article  Google Scholar 

  • Troy CM, Shelanski ML. Down-regulation of copper/zinc superoxide dismutase causes apoptotic death in PC12 neuronal cells. Proc Natl Acad Sci. 1994;91(14):6384–7.

    Article  CAS  Google Scholar 

  • Tsunoda S, Kawano N, Miyado K, Kimura N, Fujii J. Impaired fertilizing ability of superoxide dismutase 1-deficient mouse sperm during in vitro fertilization. Biol Reprod. 2012;87(5):121, 1–6.

    Article  Google Scholar 

  • Vaka VR, et al. Role of mitochondrial dysfunction and reactive oxygen species in mediating hypertension in the reduced uterine perfusion pressure rat model of preeclampsia. Hypertension. 2018;72(3):703–11.

    Article  CAS  Google Scholar 

  • Vaughan J, Walsh S. Oxidative stress reproduces placental abnormalities of preeclampsia. Hypertens Pregnancy. 2002;21(3):205–23.

    Article  CAS  Google Scholar 

  • Wang J, Yi J. Cancer cell killing via ROS: to increase or decrease, that is the question. Cancer Biol Ther. 2008;7(12):1875–84.

    Article  CAS  Google Scholar 

  • Wang X, Martindale JL, Liu Y, Holbrook NJ. The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem J. 1998;333(2):291–300.

    Article  CAS  Google Scholar 

  • Waris G, Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog. 2006;5:14.

    Article  Google Scholar 

  • Westermarck J, Kähäri VM. Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 1999;13(8):781–92.

    Article  CAS  Google Scholar 

  • Wu F, Tian F-J, Lin Y. Oxidative stress in placenta: health and diseases. Biomed Res Int. 2015, 2015:293271.

    Google Scholar 

  • Wu Y, Gu Y, Guo S, Dai Q, Zhang W. Expressing status and correlation of ARID1A and histone H2B on breast cancer. Biomed Res Int. 2016;2016:7593787.

    Google Scholar 

  • Xie H, Chen P, Huang H, Liu L, Zhao F. Reactive oxygen species downregulate ARID1A expression via its promoter methylation during the pathogenesis of endometriosis. Eur Rev Med Pharmacol Sci. 2017;21(20):4509–15.

    CAS  Google Scholar 

  • Yim SH, et al. Identification and characterization of alternatively transcribed form of peroxiredoxin IV gene that is specifically expressed in spermatids of postpubertal mouse testis. J Biol Chem. 2011;286(45):39002–12.

    Article  CAS  Google Scholar 

  • Yung H-w, et al. Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol. 2008;173(2):451–62.

    Article  CAS  Google Scholar 

  • Zabul P, et al. A proposed molecular mechanism of high-dose vitamin D3 supplementation in prevention and treatment of preeclampsia. Int J Mol Sci. 2015;16(6):13043–64.

    Article  CAS  Google Scholar 

  • Zhuang B, et al. Oxidative stress-induced C/EBPβ inhibits β-catenin signaling molecule involving in the pathology of preeclampsia. Placenta. 2015;36(8):839–46.

    Article  CAS  Google Scholar 

  • Zsengellér ZK, et al. Trophoblast mitochondrial function is impaired in preeclampsia and correlates negatively with the expression of soluble fms-like tyrosine kinase 1. Pregnancy Hypertens. 2016;6(4):313–9.

    Article  Google Scholar 

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Goutami, L., Jena, S.R., Swain, A., Samanta, L. (2022). Pathological Role of Reactive Oxygen Species on Female Reproduction. In: Roychoudhury, S., Kesari, K.K. (eds) Oxidative Stress and Toxicity in Reproductive Biology and Medicine. Advances in Experimental Medicine and Biology, vol 1391. Springer, Cham. https://doi.org/10.1007/978-3-031-12966-7_12

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