Targeting oxidative stress to treat endometriosis

Expert Opinion on Therapeutic Targets

Volumn 19, Issue 11, 2015, Pages 1447-1464

  Harlev, Avi ^a,b   Gupta, Sajal ^a   Agarwal, Ashok ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

anti angiogenesis treatment; anti inflammatory; anti oxidants; endometriosis pathophysiology; endometriosis treatment; oxidative stress; reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; EPIGALLOCATECHIN GALLATE; IRON; MELATONIN; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; RESVERATROL; XANTHOHUMOL;

ANTIOXIDANT ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; DISEASE ASSOCIATION; DRUG TARGETING; ENDOMETRIOSIS; FEMALE; HUMAN; MULTIFACTORIAL INHERITANCE; NONHUMAN; OXIDATIVE STRESS; REVIEW; ANIMAL; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOPHYSIOLOGY;

ANIMALS; ANTIOXIDANTS; ENDOMETRIOSIS; FEMALE; HUMANS; MOLECULAR TARGETED THERAPY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84947039250     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2015.1077226     Document Type: Review

References (143)

1. Kennedy S, Bergqvist A, Chapron C, et al. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 2005;20:2698-704
2. Houston DE. Evidence for the risk of pelvic endometriosis by age, race and socioeconomic status. Epidemiol Rev 1984;6:167-91
3. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005;3:28
4. Wang Y, Sharma RK, Falcone T, et al. Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil Steril 1997;68:826-30
5. Gupta S, Ghulmiyyah J, Sharma R, et al. Power of proteomics in linking oxidative stress and female infertility. Biomed Res Int 2014;2014:916212
6. Mehedintu C, Plotogea M, Ionescu S, et al. Endometriosis still a challenge. J Med Life 2014;7:349-57
7. Abbas S, Ihle P, Koster I, et al. Prevalence and incidence of diagnosed endometriosis and risk of endometriosis in patients with endometriosis-related symptoms: findings from a statutory health insurance-based cohort in Germany. Eur J Obstet Gynecol Reprod Biol 2012;160:79-83
8. Practice bulletin no. 114: management of endometriosis. Obstet Gynecol 2010;116:223-36
9. Falcone T, Lebovic DI. Clinical management of endometriosis. Obstet Gynecol 2011;118:691-705
10. Cramer DW, Wilson E, Stillman RJ, et al. The relation of endometriosis to menstrual characteristics, smoking, and exercise. Jama 1986;255:1904-8
11. Arumugam K, Lim JM. Menstrual characteristics associated with endometriosis. Br J Obstet Gynaecol 1997;104:948-50
12. Candiani GB, Danesino V, Gastaldi A, et al. Reproductive and menstrual factors and risk of peritoneal and ovarian endometriosis. Fertil Steril 1991;56:230-4
13. Peterson CM, Johnstone EB, Hammoud AO, et al. Risk factors associated with endometriosis: importance of study population for characterizing disease in the ENDO Study. Am J Obstet Gynecol 2013;208:451.e1-11
14. Lafay Pillet MC, Schneider A, Borghese B, et al. Deep infiltrating endometriosis is associated with markedly lower body mass index: A 476 casecontrol study. Hum Reprod 2012;27:265-72
15. Matalliotakis IM, Cakmak H, Fragouli YG, et al. Epidemiological characteristics in women with and without endometriosis in the Yale series. Arch Gynecol Obstet 2008;277:389-93
16. Cramer DW, Missmer SA. The epidemiology of endometriosis. Ann N Y Acad Sci 2002;955:11-22
17. Hansen KA, Eyster KM. Genetics and genomics of endometriosis. Clin Obstet Gynecol 2010;53:403-12
18. Bellelis P, Podgaec S, Abrao MS. Environmental factors and endometriosis. Rev Assoc Med Bras 2011;57:448-52
19. Nishida M, Nasu K, Fukuda J, et al. Down-regulation of interleukin-1 receptor type 1 expression causes the dysregulated expression of CXC chemokines in endometriotic stromal cells: A possible mechanism for the altered immunological functions in endometriosis. J Clin Endocrinol Metab 2004;89:5094-100
20. Bukulmez O, Hardy DB, Carr BR, et al. Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology 2008;149:1190-204
21. Kobayashi H, Imanaka S, Nakamura H, et al. Understanding the role of epigenomic, genomic and genetic alterations in the development of endometriosis (review). Mol Med Rep 2014;9:1483-505
22. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am 1997;24:235-58
23. Giudice LC, Kao LC. Endometriosis. Lancet 2004;364:1789-99
24. JA S. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927;14:422-69
25. Halme J, Hammond MG, Hulka JF, et al. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 1984;64:151-4
26. Nunley WC Jr, Kitchin JD III. Congenital atresia of the uterine cervix with pelvic endometriosis. Arch Surg 1980;115:757-8
27. Dallaudiere B, Salut C, Hummel V, et al. MRI atlas of ectopic endometriosis. Diagn Interv Imaging 2013;94:263-80
28. El-Mahgoub S, Yaseen S. A positive proof for the theory of coelomic metaplasia. Am J Obstet Gynecol 1980;137:137-40
29. Signorile PG, Baldi A. Endometriosis: new concepts in the pathogenesis. Int J Biochem Cell Biol 2010;42:778-80
30. Signorile PG, Baldi F, Bussani R, et al. Embryologic origin of endometriosis: analysis of 101 human female fetuses. J Cell Physiol 2012;227:1653-6
31. Leyendecker G, Wildt L, Mall G. The pathophysiology of endometriosis and adenomyosis: tissue injury and repair. Arch Gynecol Obstet 2009;280:529-38
32. Quinn MJ. Endometriosis: The consequence of uterine denervation-reinnervation. Arch Gynecol Obstet 2011;284:1423-9
33. Maruyama T, Yoshimura Y. Stem cell theory for the pathogenesis of endometriosis. Front Biosci (Elite Ed) 2012;4:2854-63
34. Gargett CE, Schwab KE, Brosens JJ, et al. Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis. Mol Hum Reprod 2014;20:591-8
35. Swiersz LM. Role of endometriosis in cancer and tumor development. Ann N Y Acad Sci 2002;955:281-92
36. Laurent A, Nicco C, Chereau C, et al. Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer Res 2005;65:948-56
37. Ishikawa K, Takenaga K, Akimoto M, et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 2008;320:661-4
38. Ngo C, Chereau C, Nicco C, et al. Reactive oxygen species controls endometriosis progression. Am J Pathol 2009;175:225-34
39. Knebel A, Rahmsdorf HJ, Ullrich A, et al. Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. Embo J 1996;15:5314-25
40. Kim BY, Han MJ, Chung AS. Effects of reactive oxygen species on proliferation of Chinese hamster lung fibroblast (V79) cells. Free Radic Biol Med 2001;30:686-98
41. Haas M, Askari A, Xie Z. Involvement of Src and epidermal growth factor receptor in the signal-transducing function of Na+/K+-ATPase. J Biol Chem 2000;275:27832-7
42. Leconte M, Nicco C, Ngo C, et al. Antiproliferative effects of cannabinoid agonists on deep infiltrating endometriosis. Am J Pathol 2010;177:2963-70
43. Leconte M, Nicco C, Ngo C, et al. The mTOR/AKT inhibitor temsirolimus prevents deep infiltrating endometriosis in mice. Am J Pathol 2011;179:880-9
44. Somigliana E, Vigano P, Parazzini F, et al. Association between endometriosis and cancer: A comprehensive review and a critical analysis of clinical and epidemiological evidence. Gynecol Oncol 2006;101:331-41
45. Yagyu T, Tsuji Y, Haruta S, et al. Activation of mammalian target of rapamycin in postmenopausal ovarian endometriosis. Int J Gynecol Cancer 2006;16:1545-51
46. Clerkin JS, Naughton R, Quiney C, et al. Mechanisms of ROS modulated cell survival during carcinogenesis. Cancer Lett 2008;266:30-6
47. Capobianco A, Rovere-Querini P. Endometriosis, a disease of the macrophage. Front Immunol 2013;4:9
48. Podgaec S, Abrao MS, Dias JA Jr, et al. Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 2007;22:1373-9
49. Santulli P, Borghese B, Chouzenoux S, et al. Serum and peritoneal interleukin-33 levels are elevated in deeply infiltrating endometriosis. Hum Reprod 2012;27:2001-9
50. Oyinloye BE, Adenowo AF, Kappo AP. Reactive oxygen species, apoptosis, antimicrobial peptides and human inflammatory diseases. Pharmaceuticals (Basel) 2015;8:151-75
51. Bulun SE. Endometriosis. N Engl J Med 2009;360:268-79
52. Zhao Y, Gong P, Chen Y, et al. Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis. Sci Transl Med 2015;7:271ra9
53. Thubert T, Santulli P, Marcellin L, et al. Measurement of hs-CRP is irrelevant to diagnose and stage endometriosis: prospective study of 834 patients. Am J Obstet Gynecol 2014;210:533.e1-533.e10
54. Rakhila H, Girard K, Leboeuf M, et al. Macrophage migration inhibitory factor is involved in ectopic endometrial tissue growth and peritoneal-endometrial tissue interaction in vivo: A plausible link to endometriosis development. PLoS One 2014;9:e110434
55. Kim SH, Ihm HJ, Oh YS, et al. Increased nuclear expression of nuclear factor kappa-B p65 subunit in the eutopic endometrium and ovarian endometrioma of women with advanced stage endometriosis. Am J Reprod Immunol 2013;70:497-508
56. Tandrasasmita OM, Sutanto AM, Arifin PF, et al. Anti-inflammatory, antiangiogenic, and apoptosis-inducing activity of DLBS1442, a bioactive fraction of Phaleria macrocarpa, in a RL95-2 cell line as a molecular model of endometriosis. Int J Womens Health 2015;7:161-9
57. Gonzalez-Ramos R, Donnez J, Defrere S, et al. Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis. Mol Hum Reprod 2007;13:503-9
58. Viatour P, Merville MP, Bours V, et al. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 2005;30:43-52
59. Lousse JC, Van Langendonckt A, Gonzalez-Ramos R, et al. Increased activation of nuclear factor-kappa B (NFkappaB) in isolated peritoneal macrophages of patients with endometriosis. Fertil Steril 2008;90:217-20
60. Vigano P, Gaffuri B, Somigliana E, et al. Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture. Mol Hum Reprod 1998;4:1150-6
61. Gonzalez-Ramos R, Van Langendonckt A, Defrere S, et al. Agents blocking the nuclear factorkappaB pathway are effective inhibitors of endometriosis in an in vivo experimental model. Gynecol Obstet Invest 2008;65:174-86
62. Koks CA, Demir Weusten AY, Groothuis PG, et al. Menstruum induces changes in mesothelial cell morphology. Gynecol Obstet Invest 2000;50:13-18
63. Pitsos M, Kanakas N. The role of matrix metalloproteinases in the pathogenesis of endometriosis. Reprod Sci 2009;16:717-26
64. Paul S, Sharma AV, Mahapatra PD, et al. Role of melatonin in regulating matrix metalloproteinase-9 via tissue inhibitors of metalloproteinase-1 during protection against endometriosis. J Pineal Res 2008;44:439-49
65. Song WW, Lu H, Hou WJ, et al. Expression of vascular endothelial growth factor C and anti-angiogenesis therapy in endometriosis. Int J Clin Exp Pathol 2014;7:7752-9
66. Taylor RN, Yu J, Torres PB, et al. Mechanistic and therapeutic implications of angiogenesis in endometriosis. Reprod Sci 2009;16:140-6
67. Alpay Z, Saed GM, Diamond MP. Female infertility and free radicals: potential role in adhesions and endometriosis. J Soc Gynecol Investig 2006;13:390-8
68. Rosa e Silva JC, do Amara VF, Mendonca JL, et al. Serum markers of oxidative stress and endometriosis. Clin Exp Obstet Gynecol 2014;41:371-4
69. Santulli P, Chouzenoux S, Fiorese M, et al. Protein oxidative stress markers in peritoneal fluids of women with deep infiltrating endometriosis are increased. Hum Reprod 2015;30:49-60
70. Szczepanska M, Kozlik J, Skrzypczak J, et al. Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 2003;79:1288-93
71. Mier-Cabrera J, Aburto-Soto T, Burrola-Mendez S, et al. Women with endometriosis improved their peripheral antioxidant markers after the application of a high antioxidant diet. Reprod Biol Endocrinol 2009;7:54
72. Yallampalli C, Dong YL, Gangula PR, et al. Role and regulation of nitric oxide in the uterus during pregnancy and parturition. J Soc Gynecol Investig 1998;5:58-67
73. Osborn BH, Haney AF, Misukonis MA, et al. Inducible nitric oxide synthase expression by peritoneal macrophages in endometriosis-associated infertility. Fertil Steril 2002;77:46-51
74. Corradin SB, Fasel N, Buchmuller-Rouiller Y, et al. Induction of macrophage nitric oxide production by interferon-gamma and tumor necrosis factor-alpha is enhanced by interleukin-10. Eur J Immunol 1993;23:2045-8
75. Wang H, Zhou L, Gupta A, et al. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am J Physiol Endocrinol Metab 2006;290:E798-807
76. Kitawaki J, Kusuki I, Koshiba H, et al. Detection of aromatase cytochrome P-450 in endometrial biopsy specimens as a diagnostic test for endometriosis. Fertil Steril 1999;72:1100-6
77. Wang J, Ohara N, Wang Z, et al. A novel selective progesterone receptor modulator asoprisnil (J867) downregulates the expression of EGF, IGF-I, TGFbeta3 and their receptors in cultured uterine leiomyoma cells. Hum Reprod 2006;21:1869-77
78. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327:524-6
79. Verma S, Wang CH, Li SH, et al. A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis. Circulation 2002;106:913-19
80. Kinugasa S, Shinohara K, Wakatsuki A. Increased asymmetric dimethylarginine and enhanced inflammation are associated with impaired vascular reactivity in women with endometriosis. Atherosclerosis 2011;219:784-8
81. Defrere S, Van Langendonckt A, Vaesen S, et al. Iron overload enhances epithelial cell proliferation in endometriotic lesions induced in a murine model. Hum Reprod 2006;21:2810-16
82. Kruitwagen RF, Poels LG, Willemsen WN, et al. Immunocytochemical markerprofile of endometriotic epithelial, endometrial epithelial, and mesothelial cells: A comparative study. Eur J Obstet Gynecol Reprod Biol 1991;41:215-23
83. Maines MD. The heme oxygenase system: A regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997;37:517-54
84. Kristiansen M, Graversen JH, Jacobsen C, et al. Identification of the haemoglobin scavenger receptor. Nature 2001;409:198-201
85. Lousse JC, Defrere S, Van Langendonckt A, et al. Iron storage is significantly increased in peritoneal macrophages of endometriosis patients and correlates with iron overload in peritoneal fluid. Fertil Steril 2009;91:1668-75
86. Van Langendonckt A, Casanas-Roux F, Donnez J. Iron overload in the peritoneal cavity of women with pelvic endometriosis. Fertil Steril 2002;78:712-18
87. D'Hooghe TM, Debrock S. Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons. Hum Reprod Update 2002;8:84-8
88. Balla G, Jacob HS, Balla J, et al. Ferritin: A cytoprotective antioxidant strategem of endothelium. J Biol Chem 1992;267:18148-53
89. Van Langendonckt A, Casanas-Roux F, Dolmans MM, et al. Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 2002;77:561-70
90. Allavena G, Carrarelli P, Del Bello B, et al. Autophagy is upregulated in ovarian endometriosis: A possible interplay with p53 and heme oxygenase-1. Fertil Steril 2015;103(5):1244-51.e1
91. Sauberlich HE. Pharmacology of vitamin C. Annu Rev Nutr 1994;14:371-91
92. Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med 2011;51:1000-13
93. Durak Y, Kokcu A, Kefeli M, et al. Effect of vitamin C on the growth of experimentally induced endometriotic cysts. J Obstet Gynaecol Res 2013;39:1253-8
94. Darling AM, Chavarro JE, Malspeis S, et al. A prospective cohort study of Vitamins B, C, E, and multivitamin intake and endometriosis. J Endometr 2013;5:17-26
95. Mier-Cabrera J, Genera-Garcia M, De la Jara-Diaz J, et al. Effect of vitamins C and E supplementation on peripheral oxidative stress markers and pregnancy rate in women with endometriosis. Int J Gynaecol Obstet 2008;100:252-6
96. Santanam N, Kavtaradze N, Murphy A, et al. Antioxidant supplementation reduces endometriosis-related pelvic pain in humans. Transl Res 2013;161:189-95
97. Amaya SC, Savaris RF, Filipovic CJ, et al. Resveratrol and endometrium: A closer look at an active ingredient of red wine using in vivo and in vitro models. Reprod Sci 2014;21:1362-9
98. Csaki C, Mobasheri A, Shakibaei M. Synergistic chondroprotective effects of curcumin and resveratrol in human articular chondrocytes: inhibition of IL-1beta-induced NF-kappaB-mediated inflammation and apoptosis. Arthritis Res Ther 2009;11:R165
99. Bulun SE, Cheng YH, Pavone ME, et al. Estrogen receptor-beta, estrogen receptoralpha, and progesterone resistance in endometriosis. Semin Reprod Med 2010;28:36-43
100. Rossi T, Gallo C, Bassani B, et al. Drink your prevention: beverages with cancer preventive phytochemicals. Pol Arch Med Wewn 2014;124:713-22
101. Bruner-Tran KL, Osteen KG, Taylor HS, et al. Resveratrol inhibits development of experimental endometriosis in vivo and reduces endometrial stromal cell invasiveness in vitro. Biol Reprod 2011;84:106-12
102. Ergenoglu AM, Yeniel AO, Erbas O, et al. Regression of endometrial implants by resveratrol in an experimentally induced endometriosis model in rats. Reprod Sci 2013;20:1230-6
103. Ozcan Cenksoy P, Oktem M, Erdem O, et al. A potential novel treatment strategy: inhibition of angiogenesis and inflammation by resveratrol for regression of endometriosis in an experimental rat model. Gynecol Endocrinol 2014;1-6
104. Yavuz S, Aydin NE, Celik O, et al. Resveratrol successfully treats experimental endometriosis through modulation of oxidative stress and lipid peroxidation. J Cancer Res Ther 2014;10:324-9
105. Bayoglu Tekin Y, Guven S, Kirbas A, et al. Is resveratrol a potential substitute for leuprolide acetate in experimental endometriosis? Eur J Obstet Gynecol Reprod Biol 2015;184:1-6
106. Rudzitis-Auth J, Menger MD, Laschke MW. Resveratrol is a potent inhibitor of vascularization and cell proliferation in experimental endometriosis. Hum Reprod 2013;28:1339-47
107. Maia H Jr, Haddad C, Pinheiro N, et al. Advantages of the association of resveratrol with oral contraceptives for management of endometriosis-related pain. Int J Womens Health 2012;4:543-9
108. Hardeland R. Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification to radical avoidance. Endocrine 2005;27:119-30
109. Reiter RJ, Tan DX, Manchester LC, et al. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: A review of the evidence. Cell Biochem Biophys 2001;34:237-56
110. Cox KE, Piva M, Sharpe-Timms KL. Differential regulation of matrix metalloproteinase-3 gene expression in endometriotic lesions compared with endometrium. Biol Reprod 2001;65:1297-303
111. Collette T, Maheux R, Mailloux J, et al. Increased expression of matrix metalloproteinase-9 in the eutopic endometrial tissue of women with endometriosis. Hum Reprod 2006;21:3059-67
112. Paul S, Bhattacharya P, Das Mahapatra P, et al. Melatonin protects against endometriosis via regulation of matrix metalloproteinase-3 and an apoptotic pathway. J Pineal Res 2010;49:156-68
113. Cetinkaya N, Attar R, Yildirim G, et al. The effects of different doses of melatonin treatment on endometrial implants in an oophorectomized rat endometriosis model. Arch Gynecol Obstet 2014;291(3):591-8
114. Guney M, Oral B, Karahan N, et al. Regression of endometrial explants in a rat model of endometriosis treated with melatonin. Fertil Steril 2008;89:934-42
115. Schwertner A, Conceicao Dos Santos CC, Costa GD, et al. Efficacy of melatonin in the treatment of endometriosis: A phase II, randomized, double-blind, placebocontrolled trial. Pain 2013;154:874-81
116. Yao J, Zhang B, Ge C, et al. Xanthohumol, a Polyphenol Chalcone Present in Hops, Activating Nrf2 Enzymes To Confer Protection against Oxidative Damage in PC12 Cells. J Agric Food Chem 2015;63(5):1521-31
117. Dell'Eva R, Ambrosini C, Vannini N, et al. AKT/NF-kappaB inhibitor xanthohumol targets cell growth and angiogenesis in hematologic malignancies. Cancer 2007;110:2007-11
118. Zhao F, Nozawa H, Daikonnya A, et al. Inhibitors of nitric oxide production from hops (Humulus lupulus L.). Biol Pharm Bull 2003;26:61-5
119. Gerhauser C, Alt A, Heiss E, et al. Cancer chemopreventive activity of Xanthohumol, a natural product derived from hop. Mol Cancer Ther 2002;1:959-69
120. Rudzitis-Auth J, Korbel C, Scheuer C, et al. Xanthohumol inhibits growth and vascularization of developing endometriotic lesions. Hum Reprod 2012;27:1735-44
121. Nagle DG, Ferreira D, Zhou YD. Epigallocatechin-3-gallate (EGCG): chemical and biomedical perspectives. Phytochemistry 2006;67:1849-55
122. Beltz LA, Bayer DK, Moss AL, et al. Mechanisms of cancer prevention by green and black tea polyphenols. Anticancer Agents Med Chem 2006;6:389-406
123. Laschke MW, Schwender C, Scheuer C, et al. Epigallocatechin-3-gallate inhibits estrogen-induced activation of endometrial cells in vitro and causes regression of endometriotic lesions in vivo. Hum Reprod 2008;23:2308-18
124. Xu H, Becker CM, Lui WT, et al. Green tea epigallocatechin-3-gallate inhibits angiogenesis and suppresses vascular endothelial growth factor C/vascular endothelial growth factor receptor 2 expression and signaling in experimental endometriosis in vivo. Fertil Steril 2011;96:1021-8
125. Matsuzaki S, Darcha C. Antifibrotic properties of epigallocatechin-3-gallate in endometriosis. Hum Reprod 2014;29:1677-87
126. Chen Z, Zhu QY, Tsang D, et al. Degradation of green tea catechins in tea drinks. J Agric Food Chem 2001;49:477-82
127. Wang CC, Xu H, Man GC, et al. Prodrug of green tea epigallocatechin-3-gallate (Pro-EGCG) as a potent anti-angiogenesis agent for endometriosis in mice. Angiogenesis 2013;16:59-69
128. Delneste Y, Jeannin P, Potier L, et al. Nacetyl-L-cysteine exhibits antitumoral activity by increasing tumor necrosis factor alpha-dependent T-cell cytotoxicity. Blood 1997;90:1124-32
129. Biaglow JE, Varnes ME, Epp ER, et al. Cellular protection against damage by hydroperoxides: role of glutathione. Basic Life Sci 1988;49:567-73
130. Martinez E, Domingo P. N-acetylcysteine as chemoprotectant in cancer chemotherapy. Lancet 1991;338:249
131. Albini A, D'Agostini F, Giunciuglio D, et al. Inhibition of invasion, gelatinase activity, tumor take and metastasis of malignant cells by N-acetylcysteine. Int J Cancer 1995;61:121-9
132. Eylar E, Rivera-Quinones C, Molina C, et al. N-acetylcysteine enhances T cell functions and T cell growth in culture. Int Immunol 1993;5:97-101
133. Liang CM, Lee N, Cattell D, et al. Glutathione regulates interleukin-2 activity on cytotoxic T-cells. J Biol Chem 1989;264:13519-23
134. Liang SM, Liang CM, Hargrove ME, et al. Regulation by glutathione of the effect of lymphokines on differentiation of primary activated lymphocytes. Influence of glutathione on cytotoxic activity of CD3-AK. J Immunol 1991;146:1909-13
135. Foyouzi N, Berkkanoglu M, Arici A, et al. Effects of oxidants and antioxidants on proliferation of endometrial stromal cells. Fertil Steril 2004;82(Suppl 3):1019-22
136. Wu Y, Guo SW. Inhibition of proliferation of endometrial stromal cells by trichostatin A, RU486, CDB-2914, N-acetylcysteine, and ICI 182780. Gynecol Obstet Invest 2006;62:193-205
137. Pittaluga E, Costa G, Krasnowska E, et al. More than antioxidant: N-acetyl-Lcysteine in a murine model of endometriosis. Fertil Steril 2010;94:2905-8
138. Onalan G, Gulumser C, Mulayim B, et al. Effects of amifostine on endometriosis, comparison with N-acetyl cysteine, and leuprolide as a new treatment alternative: A randomized controlled trial. Arch Gynecol Obstet 2014;289:193-200
139. Ray K, Fahrmann J, Mitchell B, et al. Oxidation-sensitive nociception involved in endometriosis-associated pain. Pain 2015;156:528-39
140. Porpora MG, Brunelli R, Costa G, et al. A promise in the treatment of endometriosis: an observational cohort study on ovarian endometrioma reduction by N-acetylcysteine. Evid Based Complement Alternat Med 2013;2013:240702
141. Taguchi A, Wada-Hiraike O, Kawana K, et al. Resveratrol suppresses inflammatory responses in endometrial stromal cells derived from endometriosis: A possible role of the sirtuin 1 pathway. J Obstet Gynaecol Res 2014;40:770-8
142. Kocadal NC, Attar R, Yildirim G, et al. Melatonin treatment results in regression of endometriotic lesions in an ooferectomized rat endometriosis model. J Turk Ger Gynecol Assoc 2013;14:81-6
143. Koc O, Gunduz B, Topcuoglu A, et al. Effects of pinealectomy and melatonin supplementation on endometrial explants in a rat model. Eur J Obstet Gynecol Reprod Biol 2010;153:72-6