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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Review

A novel and compact review on the role of oxidative stress in female reproduction

Authors: Jiayin Lu, Zixu Wang, Jing Cao, Yaoxing Chen, Yulan Dong

Published in: Reproductive Biology and Endocrinology | Issue 1/2018

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Abstract

In recent years, the study of oxidative stress (OS) has become increasingly popular. In particular, the role of OS on female fertility is very important and has been focused on closely. The occurrence of OS is due to the excessive production of reactive oxygen species (ROS). ROS are a double-edged sword; they not only play an important role as secondary messengers in many intracellular signaling cascades, but they also exert indispensable effects on pathological processes involving the female genital tract. ROS and antioxidants join in the regulation of reproductive processes in both animals and humans. Imbalances between pro-oxidants and antioxidants could lead to a number of female reproductive diseases. This review focuses on the mechanism of OS and a series of female reproductive processes, explaining the role of OS in female reproduction and female reproductive diseases caused by OS, including polycystic ovary syndrome (PCOS), endometriosis, preeclampsia and so on. Many signaling pathways involved in female reproduction, including the Keap1-Nrf2, NF-κB, FOXO and MAPK pathways, which are affected by OS, are described, providing new ideas for the mechanism of reproductive diseases.
Literature
1.
Burton GJ, Jauniaux E. Oxidative stress. Best Practice & Research Clinical Obstetrics & Gynaecology. 2011;25:287–99.CrossRef
2.
Cindrova-Davies T, Yung HW, Johns J, Spasic-Boskovic O, Korolchuk S, Jauniaux E, Burton GJ, Charnock-Jones DS. Oxidative stress, gene expression, and protein changes induced in the human placenta during labor. Am J Pathol. 2007;171:1168–79.PubMedPubMedCentralCrossRef
3.
Ruder EH, Hartman TJ, Goldman MB. Impact of oxidative stress on female fertility. Current Opinion in Obstetrics & Gynecology. 2009;21:219–22.CrossRef
4.
Attaran M, Pasqualotto E, Falcone T, Goldberg JM, Miller KF, Agarwal A, Sharma RK. The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. International Journal of Fertility and Womens Medicine. 2000;45:314–20.
5.
Szczepanska M, Kozlik J, Skrzypczak J, Mikolajczyk M. Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril. 2003;79:1288–93.PubMedCrossRef
6.
Van Langendonckt A, Casanas-Roux F, Donnez J. Oxidative stress and peritoneal endometriosis. Fertil Steril. 2002;77:861–70.PubMedCrossRef
7.
Pierce JD, Cackler AB, Arnett MG. Why should you care about free radicals? Rn. 2004;67:38–42.PubMed
8.
9.
Agarwal A, Allamaneni SSR. Role of free radicals in female reproductive diseases and assisted reproduction. Reprod BioMed Online. 2004;9:338–47.PubMedCrossRef
10.
Gupta S, Agarwal A, Banerjee J, Alvarez JG. The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: a systematic review. Obstetrical & Gynecological Survey. 2007;62:335–47.CrossRef
11.
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;10:1375–403.PubMedCrossRef
12.
Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84.PubMedCrossRef
13.
Banks WJ. Applied veterinary histology. 2nd ed. Baltimore, MD: William and Wilkins; 1981.
14.
Al-Gubory KH, Fowler PA, Garrel C. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol. 2010;42:1634–50.PubMedCrossRef
15.
Fujii J, Iuchi Y, Okada F: Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reproductive Biology and Endocrinology 2005, 3:10%18 Sep %19 review %! Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system.
16.
17.
Dhaunsi GS, Gulati S, Singh AK, Orak JK, Asayama K, Singh I. Demonstration of cu-ZN superoxide-dismutase in rat-liver peroxisomes - biochemical and immunochemical evidence. J Biol Chem. 1992;267:6870–3.PubMed
18.
Oberley LW. Mechanism of the tumor suppressive effect of MnSOD overexpression. Biomed Pharmacother. 2005;59:143–8.PubMedCrossRef
19.
20.
Spallholz JE, Roveri A, Yan L, Boylan LM, Kang CR, Ursini F. Glutathione-peroxidase and phospholipid HYDROPEROXIDE glutathione-peroxidase in tissues of BALB/c mice. FASEB J. 1991;5:A714.
21.
Proctor PH, Reynolds ES. Free-radicals and disease in man. Physiol Chem Phys Med NMR. 1984;16:175–95.PubMed
22.
Davies KJA, Wiese AG, Sevanian A, Kim EH: REPAIR SYSTEMS IN OXIDATIVE STRESS. Finch, C E and T E Johnson (Ed) Ucla (University of California-Los Angeles) Symposia on Molecular and Cellular Biology New Series, Vol 123 Molecular Biology of Aging; Colloquium, Sante Fe, New Mexico, USA, March 4-10, 1989 Xvii+430p Wiley-Liss: New York, New York, USA Illus 1990:123–142.
23.
Ketterer B, Meyer DJ. Glutathione TRANSFERASE - a possible role in the DETOXICATION and repair of DNA and lipid HYDROPEROXIDES. Mutat Res. 1989;214:33–40.PubMedCrossRef
24.
Kurlak LO, Green A, Loughna P, Pipkin FB. Oxidative stress markers in hypertensive states of pregnancy: preterm and term disease. Front Physiol. 2014;5:310.PubMedPubMedCentralCrossRef
25.
26.
Ishikawa M. Oxygen radicals-superoxide dismutase system and reproduction medicine. Nihon Sanka Fujinka Gakkai zasshi. 1993;45:842–8.PubMed
27.
Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N. Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci U S A. 2011;108:1462–7.PubMedPubMedCentralCrossRef
28.
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;72:720–6.PubMedCrossRef
29.
Tamate K, Sengoku K, Ishikawa M. The role of superoxide dismutase in the human ovary and fallopian tube. J Obstet Gynaecol (Tokyo 1995). 1995;21:401–9.CrossRef
30.
Geva E, Jaffe RB. Role of angiopoietins in reproductive tract angiogenesis. Obstetrical & Gynecological Survey. 2000;55:511–9.CrossRef
31.
Gordon JD, Mesiano S, Zaloudek CJ, Jaffe RB. Vascular endothelial growth factor localization in human ovary and fallopian tubes: possible role in reproductive function and ovarian cyst formation. J Clin Endocrinol Metab. 1996;81:353–9.PubMed
32.
Albrecht ED, Babischkin JS, Lidor Y, Anderson LD, Udoff LC, Pepe GJ. Effect of estrogen on angiogenesis in co-cultures of human endometrial cells and microvascular endothelial cells. Hum Reprod. 2003;18:2039–47.PubMedCrossRef
33.
Ushio-Fukai M, Alexander RW. Reactive oxygen species as mediators of angiogenesis signaling - role of NAD(P)H oxidase. Mol Cell Biochem. 2004;264:85–97.PubMedCrossRef
34.
Miyazaki T, Sueoka K, Dharmarajan AM, Atlas SJ, Bulkley GB, Wallach EE. Effect of inhibition of oxygen free-radical on ovulation and progesterone production by the INVITRO perfused rabbit ovary. J Reprod Fertil. 1991;91:207–12.PubMedCrossRef
35.
Behrman HR, Kodaman PH, Preston SL, Gao SP. Oxidative stress and the ovary. J Soc Gynecol Investig. 2001;8:S40–2.PubMed
36.
37.
Du BT, Takahashi K, Ishida GM, Nakahara K, Saito H, Kurachi H. Usefulness of intralovarian artery pulsatility and resistance indices measurement on the day of follicle aspiration for the assessment of oocyte quality. Fertil Steril. 2006;85:366–70.PubMedCrossRef
38.
Sugino N. Roles of reactive oxygen species in the corpus luteum. Anim Sci J. 2006;77:556–65.CrossRef
39.
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;10:31.CrossRef
40.
Ahmed A, Cudmore MJ. Can the biology of VEGF and haem oxygenases help solve pre-eclampsia? Biochem Soc Trans. 2009;37:1237–42.PubMedCrossRef
41.
Szpera-Gozdziewicz A, Breborowicz GH. Endothelial dysfunction in the pathogenesis of pre-eclampsia. Frontiers in Bioscience-Landmark. 2014;19:734–46.CrossRef
42.
Morohashi K, Iida H, Nomura M, Hatano O, Honda S, Tsukiyama T, Niwa O, Hara T, Takakusu A, Shibata Y, Omura T. Functional difference between AD4BP and ELP, and their distributions in STEROIDOGENIC tissues. Mol Endocrinol. 1994;8:643–53.PubMed
43.
Vega M, Carrasco I, Castillo T, Troncoso JL, Videla LA, Devoto L. Functional LUTEOLYSIS in response to hydrogen-peroxide in human luteal cells. J Endocrinol. 1995;147:177–82.PubMedCrossRef
44.
Tamura H, Takasaki A, Miwa I, Tanoguchi K, Maekawa R, Asada H, Taketani T, Matsuoka A, Yamagata Y, Shimamura K, et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res. 2008;44:280–7.PubMedCrossRef
45.
Fauser B, Chang J, Azziz R, Legro R, Dewailly D, Franks S, Tarlatzis BC, Fauser B, Balen A, Bouchard P, et al. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004(19):41–7.
46.
Costello MF, Shrestha B, Eden J, Johnson NP, Sjoblom P. Metformin versus oral contraceptive pill in polycystic ovary syndrome: a Cochrane review. Hum Reprod. 2007;22:1200–9.PubMedCrossRef
47.
Hilali N, Vural M, Camuzcuoglu H, Camuzcuoglu A, Aksoy N. Increased prolidase activity and oxidative stress in PCOS. Clin Endocrinol. 2013;79:105–10.CrossRef
48.
Cimino I, Casoni F, Liu X, Messina A, Parkash J, Jamin SP, Catteau-Jonard S, Collier F, Baroncini M, Dewailly D, et al. Novel role for anti-Mullerian hormone in the regulation of GnRH neuron excitability and hormone secretion. Nat Commun. 2016;7:10055.PubMedPubMedCentralCrossRef
49.
Franks S, Mc Carthy M, Hardy K. Development of polycystic ovary syndrome: involvement of genetic and environmental factors. Int J Androl. 2006;29:278–85.PubMedCrossRef
50.
Escobar-Morreale HF, Luque-Ramírez M, San Millán JL. The molecular-genetic basis of functional hyperandrogenism and the polycystic ovary syndrome. Endocr Rev. 2005;26:251–82.PubMedCrossRef
51.
Bremer AA, Miller WL. The serine phosphorylation hypothesis of polycystic ovary syndrome: a unifying mechanism of hyperandrogenemia and insulin resistance. Fertil Steril. 2008;89:1039–48.PubMedCrossRef
52.
53.
Wisdom SJ, Wilson R, McKillop JH, Walker JJ. Antioxidant systems in normal-pregnancy and in pregnancy-induced hypertension. Am J Obstet Gynecol. 1991;165:1701–4.PubMedCrossRef
54.
Wang Y, Walsh SW. Placental mitochondria as a source of oxidative stress in pre-eclampsia. Placenta. 1998;19:581–6.PubMedCrossRef
55.
Jauniaux E, Gulbis B, Burton GJ. The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus--a review. Placenta. 2003;24(Suppl A):S86–93.PubMedCrossRef
56.
Lim KH, Zhou Y, Janatpour M, McMaster M, Bass K, Chun SH, Fisher SJ. Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am J Pathol. 1997;151:1809–18.PubMedPubMedCentral
57.
Jaffe R, Jauniaux E, Hustin J. Maternal circulation in the first-trimester human placenta - myth or reality? Am J Obstet Gynecol. 1997;176:695–705.PubMedCrossRef
58.
Jauniaux E, Watson AL, Hempstock J, Bao YP, 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;157:2111–22.PubMedPubMedCentralCrossRef
59.
Sultana Z, Maiti K, Aitken J, Morris J, Dedman L, Smith R. Oxidative stress, placental ageing-related pathologies and adverse pregnancy outcomes. Am J Reprod Immunol. 2017;77: e12653.
60.
Witorsch RJ. Effects of elevated glucocorticoids on reproduction and development: relevance to endocrine disruptor screening. Crit Rev Toxicol. 2016;46:420–36.PubMedCrossRef
61.
Preutthipan S, Chen SH, Tilly JL, Kugu K, Lareu RR, Dharmarajan AM. Inhibition of nitric oxide synthesis potentiates apoptosis in the rabbit corpus luteum. Reprod BioMed Online. 2004;9:264–70.PubMedCrossRef
62.
Ghafourifar P, Richter C. Nitric oxide synthase activity in mitochondria. FEBS Lett. 1997;418:291–6.PubMedCrossRef
63.
Wang YP, Walsh SW, Guo JD, Zhang JY. Maternal levels of prostacyclin, thromboxane, vitamin-E, and lipid peroxides throughout normal-pregnancy. Am J Obstet Gynecol. 1991;165:1690–4.PubMedCrossRef
64.
Menon R, Fortunato SJ, Yu J, Milne GL, Sanchez S, Drobek CO, Lappas M, Taylor RN. Cigarette smoke induces oxidative stress and apoptosis in normal term fetal membranes. Placenta. 2011;32:317–22.PubMedCrossRef
65.
Sbrana E, Suter MA, Abramovici AR, Hawkins HK, Moss JE, Patterson L, Shope C, Aagaard-Tillery K. Maternal tobacco use is associated with increased markers of oxidative stress in the placenta. Am J Obstet Gynecol. 2011;205:7.CrossRef
66.
Smith R, Maiti K, Aitken RJ. Unexplained antepartum stillbirth: a consequence of placental aging? Placenta. 2013;34:310–3.PubMedCrossRef
67.
Oner-Iyidogan Y, Kocak H, Gurdol F, Korkmaz D, Buyru F. Indices of oxidative stress in eutopic and ectopic endometria of women with endometriosis. Gynecol Obstet Investig. 2004;57:214–7.CrossRef
68.
Ota H, Igarashi S, Tanaka T. Xanthine oxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis. Fertil Steril. 2001;75:785–90.PubMedCrossRef
69.
Agarwal A, Gupta S, Sikka S. The role of free radicals and antioxidants in reproduction. Current Opinion in Obstetrics & Gynecology. 2006;18:325–32.CrossRef
70.
Bedaiwy MA, Falcone T, Sharma RK, Goldberg JM, Attaran M, Nelson DR, Agarwal A. Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial. Hum Reprod. 2002;17:426–31.PubMedCrossRef
71.
Mier-Cabrera J, Jimenez-Zamudio L, Garcia-Latorre E, Cruz-Orozco O, Hernandez-Guerrero C. Quantitative and qualitative peritoneal immune profiles, T-cell apoptosis and oxidative stress-associated characteristics in women with minimal and mild endometriosis. BJOG. 2011;118:6–16.PubMedCrossRef
72.
Kajihara H, Yamada Y, Kanayama S, Furukawa N, Noguchi T, Haruta S, Yoshida S, Sado T, Oi H, Kobayashi H. New insights into the pathophysiology of endometriosis: from chronic inflammation to danger signal. Gynecol Endocrinol. 2011;27:73–9.PubMedCrossRef
73.
Li YQ, Zhang ZX, Xu YJ, Ni W, Chen SX, Yang Z, Ma D. N-acetyl-L-cysteine and pyrrolidine dithiocarbamate inhibited nuclear factor-kappa B activation in alveolar macrophages by different mechanisms. Acta Pharmacol Sin. 2006;27:339–46.PubMedCrossRef
74.
75.
McCubrey JA, LaHair MM, Franklin RA. Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal. 2006;8:1775–89.PubMedCrossRef
76.
Madazli R, Benian A, Aydin S, Uzun H, Tolun N. The plasma and placental levels of malondialdehyde, glutathione and superoxide dismutase in pre-eclampsia. J Obstet Gynaecol. 2002;22:477–80.PubMedCrossRef
77.
Matsubara K, Higaki T, Matsubara Y, Nawa A. Nitric oxide and reactive oxygen species in the pathogenesis of preeclampsia. Int J Mol Sci. 2015;16:4600–14.PubMedPubMedCentralCrossRef
78.
Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK. Preeclampsia - an endothelial-cell disorder. Am J Obstet Gynecol. 1989;161:1200–4.PubMedCrossRef
79.
Hubel CA, Roberts JM, Taylor RN, Musci TJ, Rogers GM, McLaughlin MK. Lipid-peroxidation in pregnancy - new perspectives on preeclampsia. Am J Obstet Gynecol. 1989;161:1025–34.PubMedCrossRef
80.
Uzun H, Benian A, Madazli R, Topcuoglu MA, Aydin S, Albayrak M. Circulating oxidized low-density lipoprotein and paraoxonase activity in preeclampsia. Gynecol Obstet Investig. 2005;60:195–200.CrossRef
81.
Wallukat G, Homuth V, Fischer T, Lindschau C, Horstkamp B, Jupner A, Baur E, Nissen E, Vetter K, Neichel D, et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT(1) receptor. J Clin Investig. 1999;103:945–52.PubMedCrossRef
82.
Griendling KK, Sorescu D, Lassegue B, Ushio-Fukai M. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol. 2000;20:2175–83.PubMedCrossRef
83.
Raijmakers MTM, Peters WHM, Steegers EAP, Poston L. NAD(P)H oxidase associated superoxide production in human placenta from normotensive and pre-eclamptic women. Placenta. 2004;25:S85–9.PubMedCrossRef
84.
Walsh SW. Eicosanoids in preeclampsia. Prostaglandins Leukotrienes and Essential Fatty Acids. 2004;70:223–32.CrossRef
85.
Klemmensen AK, Tabor A, Osterdal ML, Knudsen VK, Halldorsson TI, Mikkelsen TB, Olsen SF. Intake of vitamin C and E in pregnancy and risk of pre-eclampsia: prospective study among 57 346 women. BJOG. 2009;116:964–74.PubMedCrossRef
86.
Liu GH, Dong YL, Wang ZX, Cao J, Chen YX. Restraint stress delays endometrial adaptive remodeling during mouse embryo implantation. Stress-the International Journal on the Biology of Stress. 2015;18:699–709.CrossRef
87.
Liu GH, Dong YL, Wang ZX, Cao J, Chen YX. Restraint stress alters immune parameters and induces oxidative stress in the mouse uterus during embryo implantation. Stress-the International Journal on the Biology of Stress. 2014;17:494–503.CrossRef
88.
Perucci LO, Correa MD, Dusse LM, Gomes KB, Sousa LP. Resolution of inflammation pathways in preeclampsia-a narrative review. Immunol Res. 2017;65:774–89.PubMedCrossRef
89.
90.
Wojsiat J, Korczynski J, Borowiecka M, Zbikowska HM. The role of oxidative stress in female infertility and in vitro fertilization. Postepy Hig Med Dosw (Online). 2017;71:359–66.CrossRef
91.
Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236:313–22.PubMedCrossRef
92.
Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999;13:76–86.PubMedPubMedCentralCrossRef
93.
Cho HY, Reddy SP, Debiase A, Yamamoto M, Kleeberger SR. Gene expression profiling of NRF2-mediated protection against oxidative injury. Free Radic Biol Med. 2005;38:325–43.PubMedCrossRef
94.
Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem. 2000;275:16023–9.PubMedCrossRef
95.
Cheng XH, Chapple SJ, Patel B, Puszyk W, Sugden D, Yin XK, Mayr M, Siow RCM, Mann GE. Gestational diabetes mellitus impairs Nrf2-mediated adaptive antioxidant defenses and redox signaling in fetal endothelial cells in utero. Diabetes. 2013;62:4088–97.PubMedPubMedCentralCrossRef
96.
Lim R, Barker G, Lappas M. The transcription factor Nrf2 is decreased after spontaneous term labour in human fetal membranes where it exerts anti-inflammatory properties. Placenta. 2015;36:7–17.PubMedCrossRef
97.
Kansanen E, Kuosmanen SM, Leinonen H, Levonen AL. The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox Biol. 2013;1:45–9.PubMedPubMedCentralCrossRef
98.
Guan L, Zhang L, Gong ZC, Hou XN, Xu YX, Feng XH, Wang HY, You H. FoxO3 inactivation promotes human Cholangiocarcinoma tumorigenesis and Chemoresistance through Keap1-Nrf2 signaling. Hepatology. 2016;63:1914–27.PubMedCrossRef
99.
Gilmore TD. Introduction to NF-kappaB: players, pathways, perspectives. Oncogene. 2006;25:6680–4.PubMedCrossRef
100.
101.
Haddad JJ. Oxygen-sensing mechanisms and the regulation of redox-responsive transcription factors in development and pathophysiology. Respir Res. 2002;3:27.CrossRef
102.
Scheidereit C. IkappaB kinase complexes: gateways to NF-kappaB activation and transcription. Oncogene. 2006;25:6685–705.PubMedCrossRef
103.
Hu MCT, Lee DF, Xia WY, Golfman LS, Fu OY, Yang JY, Zou YY, Bao SL, Hanada N, Saso H, et al. I kappa B kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell. 2004;117:225–37.PubMedCrossRef
104.
Li Z, Zhang H, Chen Y, Fan L, Fang J. Forkhead transcription factor FOXO3a protein activates nuclear factor kappaB through B-cell lymphoma/leukemia 10 (BCL10) protein and promotes tumor cell survival in serum deprivation. J Biol Chem. 2012;287:17737–45.PubMedPubMedCentralCrossRef
105.
Sakamoto Y, Harada T, Horie S, Iba Y, Taniguchi F, Yoshida S, Iwabe T, Terakawa N. Tumor necrosis factor-alpha-induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kappa P activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab. 2003;88:730–5.PubMedCrossRef
106.
Lousse JC, Van Langendonckt A, Gonzalez-Ramos R, Defrere S, Renkin E, Donnez J. Increased activation of nuclear factor-kappa B (NF-kappa B) in isolated peritoneal macrophages of patients with, endometriosis. Fertil Steril. 2008;90:217–20.PubMedCrossRef
107.
Veillat V, Lavoie CH, Metz CN, Roger T, Labelle Y, Akoum A. Involvement of nuclear factor-kappa B in macrophage migration inhibitory factor gene transcription up-regulation induced by interleukin-1 beta in ectopic endometrial cells. Fertil Steril. 2009;91:2148–56.PubMedCrossRef
108.
Cao WG, Morin M, Sengers V, Metz C, Roger T, Maheux R, Akoum A. Tumour necrosis factor-alpha up-regulates macrophage migration inhibitory factor expression in endometrial stromal cells via the nuclear transcription factor NF-kappa B. Hum Reprod. 2006;21:421–8.PubMedCrossRef
109.
Grund EM, Kagan D, Tran CA, Zeitvogel A, Starzinski-Powitz A, Nataraja S, Palmer SS. Tumor necrosis factor-alpha regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor kappa B in human endometriotic epithelial cells. Mol Pharmacol. 2008;73:1394–404.PubMedCrossRef
110.
Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999;96:857–68.PubMedCrossRef
111.
Van Der Vos KE, Coffer PJ. The extending network of FOXO transcriptional target genes. Antioxid Redox Signal. 2011;14:579–92.PubMedCrossRef
112.
Goto T, Takano M, Albergaria A, Briese J, Pomeranz KM, Cloke B, Fusi L, Feroze-Zaidi F, Maywald N, Sajin M, et al. Mechanism and functional consequences of loss of FOXO1 expression in endometrioid endometrial cancer cells. Oncogene. 2008;27:9–19.PubMedCrossRef
113.
Kajihara T, Brosens JJ, Ishihara O. The role of FOXO1 in the decidual transformation of the endometrium and early pregnancy. Med Mol Morphol. 2013;46:61–8.PubMedCrossRef
114.
Kajihara T, Jones M, Fusi L, Takano M, Feroze-Zaidi F, Pirianov G, Mehmet H, Ishihara O, Higham JM, Lam EW, Brosens JJ. Differential expression of FOXO1 and FOXO3a confers resistance to oxidative cell death upon endometrial decidualization. Mol Endocrinol. 2006;20:2444–55.PubMedCrossRef
115.
Kyo S, Sakaguchi J, Kiyono T, Shimizu Y, Maida Y, Mizumoto Y, Mori N, Nakamura M, Takakura M, Miyake K, et al. Forkhead transcription factor FOXO1 is a direct target of progestin to inhibit endometrial epithelial cell growth. Clin Cancer Res. 2011;17:525–37.PubMedCrossRef
116.
Gellersen B, Brosens J. Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol. 2003;178:357–72.PubMedCrossRef
117.
Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol. 2000;10:1201–4.PubMedCrossRef
118.
Eijkelenboom A, Burgering BM. FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol. 2013;14:83–97.PubMedCrossRef
119.
Leitao B, Jones MC, Fusi L, Higham J, Lee Y, Takano M, Goto T, Christian M, Lam EWF, Brosens JJ. Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signals. Faseb Journal. 2010;24:1541–51. %1548 May %1549 Article %! Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signalsPubMedPubMedCentralCrossRef
120.
Labied S, Kajihara T, Madureira PA, Fusi L, Jones MC, Higham JM, Varshochi R, Francis JM, Zoumpoulidou G, Essafi A, et al. Progestins regulate the expression and activity of the forkhead transcription factor FOXO1 in differentiating human endometrium. Mol Endocrinol. 2006;20:35–44.PubMedCrossRef
121.
Dhillon AS, Hagan S, Rath O, Kolch W. MAP kinase signalling pathways in cancer. Oncogene. 2007;26:3279–90.PubMedCrossRef
122.
Lee CH, Ying TH, Chiou HL, Hsieh SC, Wen SH, Chou RH, Hsieh YH. Alpha-mangostin induces apoptosis through activation of reactive oxygen species and ASK1/p38 signaling pathway in cervical cancer cells. Oncotarget. 2017;8:47425–39.PubMedPubMedCentral
123.
Bredeson S, Papaconstantinou J, Deford JH, Kechichian T, Syed TA, Saade GR, Menon R. HMGB1 promotes a p38MAPK associated non-infectious inflammatory response pathway in human fetal membranes. PLoS One. 2014;9:18.CrossRef
124.
Menon R, Papaconstantinou J. p38 mitogen activated protein kinase (MAPK): a new therapeutic target for reducing the risk of adverse pregnancy outcomes. Expert Opin Ther Targets. 2016;20:1397–412.PubMedPubMedCentralCrossRef
125.
Matsuzaki S, Darcha C. Co-operation between the AKT and ERK signaling pathways may support growth of deep endometriosis in a fibrotic microenvironment in vitro. Hum Reprod. 2015;30:1606–16.PubMedCrossRef
126.
Yotova IY, Quan P, Leditznig N, Beer U, Wenzl R, Tschugguel W. Abnormal activation of Ras/Raf/MAPK and RhoA/ROCKII signalling pathways in eutopic endometrial stromal cells of patients with endometriosis. Hum Reprod. 2011;26:885–97.PubMedCrossRef
127.
Velarde MC, Aghajanova L, Nezhat CR, Giudice LC. Increased mitogen-activated protein kinase kinase/extracellularly regulated kinase activity in human endometrial stromal fibroblasts of women with endometriosis reduces 3′,5′-cyclic adenosine 5′-monophosphate inhibition of cyclin D1. Endocrinology. 2009;150:4701–12.PubMedPubMedCentralCrossRef
128.
Yoshino O, Osuga Y, Hirota Y, Koga K, Hirata T, Harada M, Morimoto C, Yano T, Nishii O, Tsutsumi O, Taketani Y. Possible pathophysiological roles of mitogen-activated protein kinases (MAPKs) in endometriosis. Am J Reprod Immunol. 2004;52:306–11.PubMedCrossRef
129.
Huang F, Cao J, Liu Q, Zou Y, Li H, Yin T. MAPK/ERK signal pathway involved expression of COX-2 and VEGF by IL-1beta induced in human endometriosis stromal cells in vitro. Int J Clin Exp Pathol. 2013;6:2129–36.PubMedPubMedCentral
130.
Andrade SS, Azevedo Ade C, Monasterio IC, Paredes-Gamero EJ, Goncalves GA, Bonetti TC, Albertoni G, Schor E, Barreto JA, Luiza Oliva M, et al. 17beta-estradiol and steady-state concentrations of H2O2: antiapoptotic effect in endometrial cells from patients with endometriosis. Free Radic Biol Med. 2013;60:63–72.PubMedCrossRef
131.
Rahman MM, Sykiotis GP, Nishimura M, Bodmer R, Bohmann D. Declining signal dependence of Nrf2-MafS-regulated gene expression correlates with aging phenotypes. Aging Cell. 2013;12:554–62.PubMedPubMedCentralCrossRef
132.
133.
Sheu SS, Nauduri D, Anders MW. Targeting antioxidants to mitochondria: a new therapeutic direction. Biochimica Et Biophysica Acta-Molecular Basis of Disease. 2006;1762:256–65.CrossRef
Metadata
Title
A novel and compact review on the role of oxidative stress in female reproduction
Authors
Jiayin Lu
Zixu Wang
Jing Cao
Yaoxing Chen
Yulan Dong
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2018
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0391-5

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