Please wait a minute...
J Zhejiang Univ (Med Sci)  2018, Vol. 47 Issue (4): 419-425    DOI: 10.3785/j.issn.1008-9292.2018.08.15
    
Research progress on oxidative stress in pathogenesis of endometriosis
HE Jiayi(),ZHANG Xinmei*()
Women's Hospital, Zhejiang University School of Medicine, Hangzhou 310006, China
Download: HTML( 6 )   PDF(945KB)
Export: BibTeX | EndNote (RIS)      

Abstract  

A large number of studies have shown that the oxidative imbalance is common in patients with endometriosis. Abnormal respiratory chain of mitochondrial, estrogen metabolism imbalance, iron overload, and ectopic foci may increase active oxygen, reduction of antioxidant enzyme and non-enzymatic substances may result in decreased antioxidant level, and the exposure to environmental hazards may further aggravate oxidative imbalance in patients with endometriosis. This article analyzes the oxidative imbalance and its role in the pathogenesis of endometriosis from the aspects of excessive oxide production and decreased antioxidant capacity.



Key wordsEndometriosis      Oxidative stress      Reactive oxygen species      Estrogens      Mitochondria      Electron transport      Review     
Received: 22 January 2018      Published: 04 December 2018
CLC:  R711.71  
  R363  
Corresponding Authors: ZHANG Xinmei     E-mail: 21718425@zju.edu.cn;zhangxinm@zju.edu.cn
Cite this article:

HE Jiayi,ZHANG Xinmei. Research progress on oxidative stress in pathogenesis of endometriosis. J Zhejiang Univ (Med Sci), 2018, 47(4): 419-425.

URL:

http://www.zjujournals.com/med/10.3785/j.issn.1008-9292.2018.08.15     OR     http://www.zjujournals.com/med/Y2018/V47/I4/419


氧化应激在子宫内膜异位症发病机制中的研究进展

近年来大量研究表明,子宫内膜异位症患者体内普遍存在氧化应激现象。线粒体呼吸链异常、雌激素代谢失衡、内环境铁过载和子宫内膜异位病灶可导致活性氧增多,抗氧化酶和非酶类物质减少导致患者体内抗氧化水平减弱,而环境因素则会加剧子宫内膜异位症患者的氧化抗氧化失衡。本文从氧化物过度产生和抗氧化能力下降两方面分析氧化应激及其在子宫内膜异位症发病中的作用,旨在为发现子宫内膜异位症新的治疗方案提供思路。


关键词: 子宫内膜异位症,  氧化性应激,  活性氧,  雌激素类,  线粒体,  电子转运,  综述 
[1]   GREENE A D , LANG S A , KENDZIORSKI J A et al. Endometriosis:where are we and where are we going?[J]. Reproduction, 2016, 152 (3): R63- R78
doi: 10.1530/REP-16-0052
[2]   WINTERBOURN C C . Reconciling the chemistry and biology of reactive oxygen species[J]. Nat Chem Biol, 2008, 4 (5): 278- 286
doi: 10.1038/nchembio.85
[3]   CARVALHO L F , SAMADDER A N , AGARWAL A et al. Oxidative stress biomarkers in patients with endometriosis:systematic review[J]. Arch Gynecol Obstet, 2012, 286 (4): 1033- 1040
doi: 10.1007/s00404-012-2439-7
[4]   NU?EZ-CALONGE R , CORTéS S , GUTIERREZG L M et al. Oxidative stress in follicular fluid of young women with low response compared with fertile oocyte donors[J]. Reprod Biomed Online, 2016, 32 (4): 446- 456
doi: 10.1016/j.rbmo.2015.12.010
[5]   SANTULLI P , CHOUZENOUX S , FIORESE M et al. Protein oxidative stress markers in peritoneal fluids of women with deep infiltrating endometriosis are increased[J]. Hum Reprod, 2015, 30 (1): 49- 60
doi: 10.1093/humrep/deu290
[6]   JANA S K , DUTTA M , JOSHI M et al. 1H NMR based targeted metabolite profiling for understanding the complex relationship connecting oxidative stress with endometriosis[J]. Biomed Res Int, 2013, 2013 329058
[7]   TURKYILMAZ E , YILDIRIM M , CENDEK B D et al. Evaluation of oxidative stress markers and intra-extracellular antioxidant activities in patients with endometriosis[J]. Eur J Obstet Gynecol Reprod Biol, 2016, 199 164- 168
doi: 10.1016/j.ejogrb.2016.02.027
[8]   TURGUT A , ?ZLER A , G?RüK N Y et al. Copper, ceruloplasmin and oxidative stress in patients with advanced-stage endometriosis[J]. Eur Rev Med Pharmacol Sci, 2013, 17 (11): 1472- 1478
[9]   ROSA E S J C , DO A V F , MENDON?A J L et al. Serum markers of oxidative stress and endometriosis[J]. Clin Exp Obstet Gynecol, 2014, 41 (4): 371- 374
[10]   HARLEV A , GUPTA S , AGARWAL A . Targeting oxidative stress to treat endometriosis[J]. Expert Opin Ther Targets, 2015, 19 (11): 1447- 1464
doi: 10.1517/14728222.2015.1077226
[11]   ANDRISANI A , DONà G , BRUNATI A M et al. Increased oxidation-related glutathionylation and carbonic anhydrase activity in endometriosis[J]. Reprod Biomed Online, 2014, 28 (6): 773- 779
doi: 10.1016/j.rbmo.2014.01.016
[12]   NAGATA M . Inflammatory cells and oxygen radicals[J]. Curr Drug Targets Inflamm Allergy, 2005, 4 (4): 503- 504
doi: 10.2174/1568010054526322
[13]   DONNEZ J , BINDA M M , DONNEZ O et al. Oxidative stress in the pelvic cavity and its role in the pathogenesis of endometriosis[J]. Fertil Steril, 2016, 106 (5): 1011- 1017
doi: 10.1016/j.fertnstert.2016.07.1075
[14]   MCKINNON B D , KOCBEK V , NIRGIANAKIS K et al. Kinase signalling pathways in endometriosis:potential targets for non-hormonal therapeutics[J]. Hum Reprod Update, 2016, 22 (3): 382- 403
doi: 10.1093/humupd/dmv060
[15]   YUN B H, CHON S J, CHOI Y S, et al. Pathophysiology of endometriosis: role of high mobility group box-1 and Toll-like receptor 4 developing inflammation in endometrium[J/OL]. PLoS One, 2016, 11(2): e0148165.
[16]   徐建兴 . 呼吸链的电子漏路径和线粒体的超氧自由基代谢及其生物学意义[J]. 基础医学与临床, 2001, 21 (5): 389- 394
XU Jianxing . Electron leaks of respiratory chain and metabolism of superoxide anion in mitochondria and their biological significance[J]. Basic Medical Sciences and Clinics, 2001, 21 (5): 389- 394
doi: 10.3969/j.issn.1001-6325.2001.05.002
[17]   CHISTIAKOV D A , SHKURAT T P , MELNICHENKO A A et al. The role of mitochondrial dysfunction in cardiovascular disease:a brief review[J]. Ann Med, 2018, 50 (2): 121- 127
doi: 10.1080/07853890.2017.1417631
[18]   BOVERIS A , CADENAS E , STOPPANI A O . Role of ubiquinone in the mitochondrial generation of hydrogen peroxide[J]. Biochem J, 1976, 156 (2): 435- 444
[19]   CHO S , LEE Y M , CHOI Y S et al. Mitochondria DNA polymorphisms are associated with susceptibility to endometriosis[J]. DNA Cell Biol, 2012, 31 (3): 317- 322
doi: 10.1089/dna.2011.1279
[20]   GOVATATI S , DEENADAYAL M , SHIVAJI S et al. Mitochondrial displacement loop alterations are associated with endometriosis[J]. Fertil Steril, 2013, 99 (7): 1980- 6
doi: 10.1016/j.fertnstert.2013.02.021
[21]   GOVATATI S, TIPIRISETTI N R, PERUGU S, et al. Mitochondrial genome variations in advanced stage endometriosis: a study in South Indian population[J/OL]. PLoS One, 2012, 7(7): e40668.
[22]   GOVATATI S , DEENADAYAL M , SHIVAJI S et al. Mitochondrial NADH:ubiquinone oxidoreductase alterations are associated with endometriosis[J]. Mitochondrion, 2013, 13 (6): 782- 790
doi: 10.1016/j.mito.2013.05.003
[23]   CHAN D C . Mitochondria:dynamic organelles in disease, aging, and development[J]. Cell, 2006, 125 (7): 1241- 1252
doi: 10.1016/j.cell.2006.06.010
[24]   CHATTERJEE A , MAMBO E , SIDRANSKY D . Mitochondrial DNA mutations in human cancer[J]. Oncogene, 2006, 25 (34): 4663- 4674
doi: 10.1038/sj.onc.1209604
[25]   ZOROV D B , JUHASZOVA M , SOLLOTT S J . Mitochondrial ROS-induced ROS release:an update and review[J]. Biochim Biophys Acta, 2006, 1757 (5-6): 509- 517
doi: 10.1016/j.bbabio.2006.04.029
[26]   冯阳, 刘建军, 黄钢 . 线粒体膜通透性转换孔结构与功能研究进展[J]. 上海交通大学学报(医学版), 2012, 32 (3): 356- 360
FENG Yang , LIU Jianjun , HUANG Gang . Research progress of structure and function of mitochondrial permeability transition pore[J]. Journal of Shanghai Jiaotong University(Medical Science), 2012, 32 (3): 356- 360
doi: 10.3969/j.issn.1674-8115.2012.03.026
[27]   ZHANG Y , LI X R , ZHAO L et al. DJ-1 preserving mitochondrial complex I activity plays a critical role in resveratrol-mediated cardioprotection against hypoxia/reoxygenation-induced oxidative stress[J]. Biomed Pharmacother, 2018, 98 545- 552
doi: 10.1016/j.biopha.2017.12.094
[28]   HEVIR N , RIBI?-PUCELJ M , LANI?NIK R T . Disturbed balance between phase Ⅰ and Ⅱ metabolizing enzymes in ovarian endometriosis:a source of excessive hydroxy-estrogens and ROS?[J]. Mol Cell Endocrinol, 2013, 367 (1-2): 74- 84
doi: 10.1016/j.mce.2012.12.019
[29]   AL-GUBORY K H , FOWLER P A , GARREL C . The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes[J]. Int J Biochem Cell Biol, 2010, 42 (10): 1634- 1650
doi: 10.1016/j.biocel.2010.06.001
[30]   GONZáLEZ-RAMOS R , DEFRōRE S , DEVOTO L . Nuclear factor-kappaB:a main regulator of inflammation and cell survival in endometriosis pathophysiology[J]. Fertil Steril, 2012, 98 (3): 520- 528
doi: 10.1016/j.fertnstert.2012.06.021
[31]   ALVARADO-DíAZ C P , Nú?EZ M T , DEVOTO L et al. Endometrial expression and in vitro modulation of the iron transporter divalent metal transporter-1:implications for endometriosis[J]. Fertil Steril, 2016, 106 (2): 393- 401
doi: 10.1016/j.fertnstert.2016.04.002
[32]   IWABUCHI T , YOSHIMOTO C , SHIGETOMI H et al. Oxidative stress and antioxidant defense in endometriosis and its malignant transformation[J]. Oxid Med Cell Longev, 2015, 2015 848595
[33]   ALIZADEH M , MAHJOUB S , ESMAELZADEH S et al. Evaluation of oxidative stress in endometriosis:A case-control study[J]. Caspian J Intern Med, 2015, 6 (1): 25- 29
[34]   DI E G , D'ALFONSO A , LEOCATA P et al. Increased levels of oxidative and carbonyl stress markers in normal ovarian cortex surrounding endometriotic cysts[J]. Gynecol Endocrinol, 2014, 30 (11): 808- 812
doi: 10.3109/09513590.2014.938625
[35]   KAO S H , HUANG H C , HSIEH R H et al. Oxidative damage and mitochondrial DNA mutations with endometriosis[J]. Ann N Y Acad Sci, 2005, 1042 186- 194
doi: 10.1196/annals.1338.021
[36]   MATSUZAKI S , SCHUBERT B . Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis[J]. Fertil Steril, 2010, 93 (7): 2431- 2432
doi: 10.1016/j.fertnstert.2009.08.068
[37]   POLAK G , WERTEL I , BARCZY?SKI B et al. Increased levels of oxidative stress markers in the peritoneal fluid of women with endometriosis[J]. Eur J Obstet Gynecol Reprod Biol, 2013, 168 (2): 187- 190
doi: 10.1016/j.ejogrb.2012.12.043
[38]   OYINLOYE B E , ADENOWO A F , KAPPO A P . Reactive oxygen species, apoptosis, antimicrobial peptides and human inflammatory diseases[J]. Pharmaceuticals(Basel), 2015, 8 (2): 151- 175
doi: 10.3390/ph8020151
[39]   GRANDE G , VINCENZONI F , MILARDI D et al. Cervical mucus proteome in endometriosis[J]. Clin Proteomics, 2017, 14 7
doi: 10.1186/s12014-017-9142-4
[40]   ANDRADE S S , AZEVEDO ADE C , MONASTERIO I C et al. 17β-estradiol and steady-state concentrations of H2O2:antiapoptotic effect in endometrial cells from patients with endometriosis[J]. Free Radic Biol Med, 2013, 60 63- 72
doi: 10.1016/j.freeradbiomed.2013.01.034
[41]   MESSALLI E M , SCHETTINO M T , MAININI G et al. The possible role of zinc in the etiopathogenesis of endometriosis[J]. Clin Exp Obstet Gynecol, 2014, 41 (5): 541- 546
[42]   SOYLU K O , PINAR N , ?ZGüR T et al. The protective role of dexpanthenol on the endometrial implants in an experimentally induced rat endometriosis model[J]. Reprod Sci, 2017, 24 (2): 285- 290
doi: 10.1177/1933719116653682
[43]   DARLING A M , CHAVARRO J E , MALSPEIS S et al. A prospective cohort study of vitamins B, C, E, and multivitamin intake and endometriosis[J]. J Endometr, 2013, 5 (1): 17- 26
doi: 10.5301/je.5000151
[44]   PARAZZINI F , CHIAFFARINO F , SURACE M et al. Selected food intake and risk of endometriosis[J]. Hum Reprod, 2004, 19 (8): 1755- 1759
doi: 10.1093/humrep/deh395
[45]   MIER-CABRERA J , ABURTO-SOTO T , BURROLA-MéNDEZ S et al. Women with endometriosis improved their peripheral antioxidant markers after the application of a high antioxidant diet[J]. Reprod Biol Endocrinol, 2009, 7 54
doi: 10.1186/1477-7827-7-54
[46]   SANTANAM N , KAVTARADZE N , MURPHY A et al. Antioxidant supplementation reduces endometriosis-related pelvic pain in humans[J]. Transl Res, 2013, 161 (3): 189- 195
[47]   TRABER M G , ATKINSON J . VITAMIN E, antioxidant and nothing more[J]. Free Radic Biol Med, 2007, 43 (1): 4- 15
[48]   LAMBRINOUDAKI I V , AUGOULEA A , CHRISTODOULAKOS G E et al. Measurable serum markers of oxidative stress response in women with endometriosis[J]. Fertil Steril, 2009, 91 (1): 46- 50
doi: 10.1016/j.fertnstert.2007.11.021
[49]   YAMAWAKI H , PAN S , LEE R T et al. Fluid shear stress inhibits vascular inflammation by decreasing thioredoxin-interacting protein in endothelial cells[J]. J Clin Invest, 2005, 115 (3): 733- 738
doi: 10.1172/JCI200523001
[50]   HJORTS? M D , ANDERSEN M H . The expression, function and targeting of haem oxygenase-1 in cancer[J]. Curr Cancer Drug Targets, 2014, 14 (4): 337- 347
doi: 10.2174/1568009614666140320111306
[51]   CHEN W , MAGHZAL G J , AYER A et al. Absence of the biliverdin reductase-a gene is associated with increased endogenous oxidative stress[J]. Free Radic Biol Med, 2018, 115 156- 165
doi: 10.1016/j.freeradbiomed.2017.11.020
[52]   ROCHETTE L , ZELLER M , COTTIN Y et al. Redox functions of heme oxygenase-1 and biliverdin reductase in diabetes[J]. Trends Endocrinol Metab, 2018, 29 (2): 74- 85
doi: 10.1016/j.tem.2017.11.005
[53]   SUN J , BRAND M , ZENKE Y et al. Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network[J]. Proc Natl Acad Sci U S A, 2004, 101 (6): 1461- 1466
doi: 10.1073/pnas.0308083100
[54]   HEARD M E , MELNYK S B , SIMMEN F A et al. High-fat diet promotion of endometriosis in an immunocompetent mouse model is associated with altered peripheral and ectopic lesion redox and inflammatory status[J]. Endocrinology, 2016, 157 (7): 2870- 2882
doi: 10.1210/en.2016-1092
[55]   NAZ?RO?LU M , YüKSEL M , K?SE S A et al. Recent reports of Wi-Fi and mobile phone-induced radiation on oxidative stress and reproductive signaling pathways in females and males[J]. J Membr Biol, 2013, 246 (12): 869- 875
doi: 10.1007/s00232-013-9597-9
[56]   CHO Y J , PARK S B , HAN M . Di-(2-ethylhexyl)-phthalate induces oxidative stress in human endometrial stromal cells in vitro[J]. Mol Cell Endocrinol, 2015, 407 9- 17
doi: 10.1016/j.mce.2015.03.003
[57]   HE Y , SHI J Z , ZHANG R J et al. Effects of hydrogen gas inhalation on endometriosis in rats[J]. Reprod Sci, 2017, 24 (2): 324- 331
doi: 10.1177/1933719116655622
[1] SHI Ting, YE Xiujin. Roles of CCAAT enhancer binding protein α in acute myeloblastic leukemia[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 552-557.
[2] LI Gaopeng, HE Jia, WANG Qingqing. Progress on cancer associated fibroblasts in tumor immunoregulation[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 558-563.
[3] WANG Qingmei, SHU Min, XU Qianzi, XIE Yiyi, RUAN Shengzhe, WANG Jianda, ZENG Linghui. Effects of Honokiol on cognitive function in mice with kainic acid-induced epilepsy[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 450-456.
[4] YE Jianyu, SUN Ziyu, HU Weiwei. Roles of astrocytes in cerebral infarction and related therapeutic strategies[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 493-498.
[5] ZHU Feng, FAN Miao, XU Ziwei, CAI Yiting, CHEN Yizhen, YU Shuang, ZENG Linghui. Neuroprotective effect of rapamycin against Parkinson's disease in mice[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 465-472.
[6] ZHAO Yu, ZHANG Feng, ZHAO Xiaoping, YUAN Wei, ZHANG Jinhua, WANG Yi. Shenmai injection protects mitochondria from oxidative injury in myocardial cells and its mechanism[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 507-513.
[7] WANG Xiaoling, OUYANG Xumei, SUN Xiaoyi. Application of mesenchymal stem cells in antineoplastic drugs delivery for tumor-targeted therapy[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 525-533.
[8] HU Caiqin, ZHU Biao. Progress on pathogenesis of progressive multifocal leukoence-phalopathy[J]. J Zhejiang Univ (Med Sci), 2018, 47(5): 534-540.
[9] ZHANG Lifeng,ZHANG Xinmei. Research progress on roles of vitamin D in endometriosis[J]. J Zhejiang Univ (Med Sci), 2018, 47(4): 413-418.
[10] XU Zhili,CUI Yiyi,LI Yan,GUO Yong. Research progress on nonspecific immune microenvironment in breast cancer[J]. J Zhejiang Univ (Med Sci), 2018, 47(4): 426-434.
[11] WANG Xingxing,WANG Panpan,YANG Xuyan. Research progress on systemic lupus erythematosus overlapping organ-specific autoimmune diseases[J]. J Zhejiang Univ (Med Sci), 2018, 47(4): 435-440.
[12] WANG Wei,LIU Zhen,LIU Jun,ZHEN Ping,LI Xusheng,SONG Mingjia. Choice of total knee arthroplasty: posterior cruciate ligament preserved or not[J]. J Zhejiang Univ (Med Sci), 2018, 47(3): 313-319.
[13] QIAN Bo,ZHANG Yanling,MO Xuming. Research progress on transcription factors and signal pathways involved in congenital esophageal atresia[J]. J Zhejiang Univ (Med Sci), 2018, 47(3): 239-243.
[14] TIAN Guangfeng,GAO Hui,HU Shasha,SHU Qiang. Research progress on genetic and epigenetic mechanisms in congenital heart disease[J]. J Zhejiang Univ (Med Sci), 2018, 47(3): 227-238.
[15] CHEN Ting,ZHAO Zhengyan,JIANG Pingping,SHU Qiang. Research progress on phenotype and genotype of hyperphenylalaninemia[J]. J Zhejiang Univ (Med Sci), 2018, 47(3): 219-226.