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Correlation between dioxin and endometriosis: an epigenetic route to unravel the pathogenesis of the disease

Archives of Gynecology and Obstetrics volume 292, pages 973–986 (2015)Cite this article

Abstract

Introduction

Environmental toxicants can act as endocrine disrupters on the female reproductive system. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) is resistant to degradation and due to its lipophilic nature, accumulates in the fat tissue and in the food chain. Human and animal exposure to TCDD affects levels of the steroid receptors and steroid-responsive gene expression and has an impact on metabolism and serum transport of steroids. Gene expression is commonly altered in endometriosis and in the eutopic endometrium of women with the disease. Aberrantly expressed genes include those associated with the regulation of transcription, proliferation, sex steroid metabolism, apoptosis, cell cycle, the immune response and cell adhesion.

Methods

In this paper, we review the evidence about TCDD’s effect on eutopic and ectopic endometrium, in order to unravel the machinery behind the dysregulation of immune and hormonal homeostasis caused by this environmental toxicant.

Conclusion

The evidence collected in this review suggests that TCDD could modulate transcription at multiple levels, including the epigenetic level, and via microRNAs, thus disturbing the physiologic processes mediated through the aryl hydrocarbon receptor pathways. Exposure to TCDD also modulates the immune response by influencing the production and action of endometrial cytokines and chemokines, destroying mucosal immunity of the reproductive tract and re-directing the tissue distribution and behavior of leukocytes. Despite this large body of evidence, current human-based epidemiological studies on the association between TCDD and endometriosis remain controversial.

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References

  1. Laganà AS, Sturlese E, Retto G et al (2013) Interplay between misplaced Müllerian-derived stem cells and peritoneal immune dysregulation in the pathogenesis of endometriosis. Obstet Gynecol Int 2013:527041. doi:10.1155/2013/527041

    PubMed Central  PubMed  Google Scholar 

  2. Dunselman GAJ, Vermeulen N, Becker C et al (2014) ESHRE guideline: management of women with endometriosis. Hum Reprod 29:400–412. doi:10.1093/humrep/det457

    CAS  PubMed  Article  Google Scholar 

  3. Triolo O, Laganà AS, Sturlese E (2013) Chronic pelvic pain in endometriosis: an overview. J Clin Med Res 5:153–163

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Culley L, Law C, Hudson N et al (2013) The social and psychological impact of endometriosis on women’s lives: a critical narrative review. Hum Reprod Update 19:625–639. doi:10.1093/humupd/dmt027

    PubMed  Article  Google Scholar 

  5. Rock JA (1995) The revised American Fertility Society classification of endometriosis: reproducibility of scoring. ZOLADEX Endometriosis Study Group. Fertil Steril 63:1108–1110

    CAS  PubMed  Google Scholar 

  6. Haas D, Chvatal R, Habelsberger A et al (2011) Comparison of revised American Fertility Society and ENZIAN staging: a critical evaluation of classifications of endometriosis on the basis of our patient population. Fertil Steril 95:1574–1578. doi:10.1016/j.fertnstert.2011.01.135

    PubMed  Article  Google Scholar 

  7. Adamson GD, Pasta DJ (2010) Endometriosis fertility index: the new, validated endometriosis staging system. Fertil Steril 94:1609–1615. doi:10.1016/j.fertnstert.2009.09.035

    PubMed  Article  Google Scholar 

  8. Pizzo A, Salmeri FM, Ardita FV et al (2002) Behaviour of cytokine levels in serum and peritoneal fluid of women with endometriosis. Gynecol Obs Invest 54:82–87. doi:10.1159/000067717

    CAS  Article  Google Scholar 

  9. Sturlese E, Salmeri FM, Retto G et al (2011) Dysregulation of the Fas/FasL system in mononuclear cells recovered from peritoneal fluid of women with endometriosis. J Reprod Immunol 92:74–81

    CAS  PubMed  Article  Google Scholar 

  10. Hombach-Klonisch S, Pocar P, Kietz S, Klonisch T (2005) Molecular actions of polyhalogenated arylhydrocarbons (PAHs) in female reproduction. Curr Med Chem 12:599–616

    CAS  PubMed  Google Scholar 

  11. Thomas Zoeller R, Brown TR, Doan LL et al (2012) Endocrine-disrupting chemicals and public health protection: a statement of principles from the endocrine society. Endocrinology 153:4097–4110. doi:10.1210/en.2012-1422

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  12. Vaiserman AM (2012) Epigenetics in human disease. Epigenetics Hum Dis. doi:10.1016/B978-0-12-388415-2.00027-5

    Google Scholar 

  13. Hotchkiss AK, Rider CV, Blystone CR et al (2008) Fifteen years after “wingspread”—environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol Sci 105:235–259. doi:10.1093/toxsci/kfn030

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  14. Birnbaum LS, Tuomisto J (2000) Non-carcinogenic effects of TCDD in animals. Food Addit Contam 17:275–288. doi:10.1080/026520300283351

    CAS  PubMed  Article  Google Scholar 

  15. Anger DL, Foster WG (2008) The link between environmental toxicant exposure and endometriosis. Front Biosci 13:1578–1593. doi:10.2741/2782

    CAS  PubMed  Article  Google Scholar 

  16. Rier S, Foster WG (2003) Environmental dioxins and endometriosis. Semin Reprod Med 21:145–153. doi:10.1055/s-2003-41321

    CAS  PubMed  Article  Google Scholar 

  17. Bruner-Tran KL, Yeaman GR, Crispens MA et al (2008) Dioxin may promote inflammation-related development of endometriosis. Fertil Steril 89:1287–1298. doi:10.1016/j.fertnstert.2008.02.102

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  18. Fernández-González R, Yebra-Pimentel I, Martínez-Carballo E, Simal-Gándara J (2013) A critical review about the human exposure to polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs) and polychlorinated biphenyls (PCBs) through foods. Crit Rev Food Sci Nutr. doi:10.1080/10408398.2012.710279

    Google Scholar 

  19. Warner M, Eskenazi B, Mocarelli P et al (2002) Serum dioxin concentrations and breast cancer risk in the Seveso Women’s Health Study. Environ Health Perspect 110:625–628. doi:10.1289/ehp.02110625

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  20. Schiavon M, Ragazzi M, Rada EC (2013) A proposal for a diet-based local PCDD/F deposition limit. Chemosphere 93:1639–1645. doi:10.1016/j.chemosphere.2013.08.041

    CAS  PubMed  Article  Google Scholar 

  21. Schecter A, Wallace D, Pavuk M et al (2002) Dioxins in commercial United States baby food. J Toxicol Environ Health A 65:1937–1943. doi:10.1080/00984100290071450

    CAS  PubMed  Article  Google Scholar 

  22. Harrad S, Wang Y, Sandaradura S, Leeds A (2003) Human dietary intake and excretion of dioxin-like compounds. J Environ Monit 5:224–228. doi:10.1039/b211406b

    CAS  PubMed  Article  Google Scholar 

  23. Hamm JT, Chen CY, Birnbaum LS (2003) A mixture of dioxins, furans, and non-ortho PCBs based upon consensus toxic equivalency factors produces dioxin-like reproductive effects. Toxicol Sci 74:182–191. doi:10.1093/toxsci/kfg107

    CAS  PubMed  Article  Google Scholar 

  24. Igarashi T, Osuga U, Tsutsumi O et al (1999) Expression of Ah receptor and dioxin-related genes in human uterine endometrium in women with or without endometriosis. Endocr J 46:765–772. doi:10.1507/endocrj.46.765

    CAS  PubMed  Article  Google Scholar 

  25. Heilier JF, Nackers F, Verougstraete V et al (2005) Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometriotic (adenomyotic) nodules. Fertil Steril 84:305–312. doi:10.1016/j.fertnstert.2005.04.001

    CAS  PubMed  Article  Google Scholar 

  26. Porpora MG, Ingelido AM, di Domenico A et al (2006) Increased levels of polychlorobiphenyls in Italian women with endometriosis. Chemosphere 63:1361–1367. doi:10.1016/j.chemosphere.2005.09.022

    CAS  PubMed  Article  Google Scholar 

  27. Rier SE, Martin DC, Bowman RE et al (1993) Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol 21:433–441. doi:10.1006/faat.1993.1119

    CAS  PubMed  Article  Google Scholar 

  28. Rier SE, Turner WE, Martin DC et al (2001) Serum levels of TCDD and dioxin-like chemicals in rhesus monkeys chronically exposed to dioxin: correlation of increased serum PCB levels with endometriosis. Toxicol Sci 59:147–159. doi:10.1093/toxsci/59.1.147

    CAS  PubMed  Article  Google Scholar 

  29. Rier SE (2002) The potential role of exposure to environmental toxicants in the pathophysiology of endometriosis. Ann N Y Acad Sci 955:201–212 (discussion 230–232, 396–406)

    CAS  PubMed  Article  Google Scholar 

  30. Cummings AM, Metcalf JL, Birnbaum L (1996) Promotion of endometriosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin in rats and mice: time-dose dependence and species comparison. Toxicol Appl Pharmacol 138:131–139. doi:10.1006/taap.1996.0106

    CAS  PubMed  Article  Google Scholar 

  31. Johnson KL, Cummings AM, Birnbaum LS (1997) Promotion of endometriosis in mice by polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls. Environ Health Perspect 105:750–755. doi:10.1289/ehp.97105750

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  32. Mayani A, Barel S, Soback S, Almagor M (1997) Dioxin concentrations in women with endometriosis. Hum Reprod 12:373–375. doi:10.1093/humrep/12.2.373

    CAS  PubMed  Article  Google Scholar 

  33. Pauwels A, Schepens PJ, D’Hooghe T et al (2001) The risk of endometriosis and exposure to dioxins and polychlorinated biphenyls: a case-control study of infertile women. Hum Reprod 16:2050–2055. doi:10.1093/humrep/16.10.2050

    CAS  PubMed  Article  Google Scholar 

  34. Fierens S, Mairesse H, Heilier J-F et al (2007) Impact of iron and steel industry and waste incinerators on human exposure to dioxins, PCBs, and heavy metals: results of a cross-sectional study in Belgium. J Toxicol Environ Health A 70:222–226. doi:10.1080/15287390600884628

    CAS  PubMed  Article  Google Scholar 

  35. Foster WG (2008) Endocrine toxicants including 2,3,7,8-terachlorodibenzo-p-dioxin (TCDD) and dioxin-like chemicals and endometriosis: is there a link? J Toxicol Environ Health B Crit Rev 11:177–187. doi:10.1080/10937400701873456

    CAS  PubMed  Article  Google Scholar 

  36. Tsukino H, Hanaoka T, Sasaki H et al (2005) Associations between serum levels of selected organochlorine compounds and endometriosis in infertile Japanese women. Environ Res 99:118–125. doi:10.1016/j.envres.2005.04.003

    CAS  PubMed  Article  Google Scholar 

  37. Niskar AS, Needham LL, Rubin C et al (2009) Serum dioxins, polychlorinated biphenyls, and endometriosis: a case-control study in Atlanta. Chemosphere 74:944–949. doi:10.1016/j.chemosphere.2008.10.005

    CAS  PubMed  Article  Google Scholar 

  38. Tsutsumi O, Uechi H, Sone H et al (1998) Presence of dioxins in human follicular fluid: their possible stage-specific action on the development of preimplantation mouse embryos. Biochem Biophys Res Commun 250:498–501. doi:10.1006/bbrc.1998.9340

    CAS  PubMed  Article  Google Scholar 

  39. LaKind JS (2007) Recent global trends and physiologic origins of dioxins and furans in human milk. J Expo Sci Environ Epidemiol 17:510–524. doi:10.1038/sj.jes.7500543

    CAS  PubMed  Article  Google Scholar 

  40. Cai LY, Izumi S, Suzuki T et al (2011) Dioxins in ascites and serum of women with endometriosis: a pilot study. Hum Reprod 26:117–126. doi:10.1093/humrep/deq312

    CAS  PubMed  Article  Google Scholar 

  41. Eskenazi B, Mocarelli P, Warner M et al (2002) Serum dioxin concentrations and endometriosis: a cohort study in Seveso, Italy. Environ Health Perspect 110:629–634. doi:10.1289/ehp.02110629

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  42. Safe S (2004) Endocrine disruptors and human health: is there a problem. Toxicology 205:3–10. doi:10.1016/j.tox.2004.06.032

    CAS  PubMed  Article  Google Scholar 

  43. Case K, Clever LH, Colaianni LA et al (1997) Uniform requirements for manuscripts submitted to biomedical journals. Ann Intern Med 126:36–47. doi:10.1093/rheumatology/22.1.1-a

    Article  Google Scholar 

  44. Guo SW (2006) The association of endometriosis risk and genetic polymorphisms involving dioxin detoxification enzymes: a systematic review. Eur J Obstet Gynecol Reprod Biol 124:134–143. doi:10.1016/j.ejogrb.2005.10.002

    CAS  PubMed  Article  Google Scholar 

  45. Guo SW (2004) The link between exposure to dioxin and endometriosis: a critical reappraisal of primate data. Gynecol Obstet Invest 57:157–173. doi:10.1159/000076374

    CAS  PubMed  Article  Google Scholar 

  46. Lim Y, Yang J, Kim Y et al (2004) Assessment of human health risk of dioxin in Korea. Env Monit Assess 92:211–228

    CAS  Article  Google Scholar 

  47. De Felip E, Porpora MG, Di Domenico A et al (2004) Dioxin-like compounds and endometriosis: a study on Italian and Belgian women of reproductive age. Toxicol Lett 150:203–209. doi:10.1016/j.toxlet.2004.01.008

    PubMed  Article  CAS  Google Scholar 

  48. Guo SW (2005) Glutathione S-transferases M1/T1 gene polymorphisms and endometriosis: a meta-analysis of genetic association studies. Mol Hum Reprod 11:729–743. doi:10.1093/molehr/gah206

    CAS  PubMed  Article  Google Scholar 

  49. Newbold RR (2004) Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol Appl Pharmacol 199:142–150. doi:10.1016/j.taap.2003.11.033

    CAS  PubMed  Article  Google Scholar 

  50. Moore RW, Parsons JA, Bookstaff RC, Peterson RE (1989) Plasma concentrations of pituitary hormones in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated male rats. J Biochem Toxicol 4:165–172

    CAS  PubMed  Article  Google Scholar 

  51. Li X, Johnson DC, Rozman KK (1995) Reproductive effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in female rats: ovulation, hormonal regulation, and possible mechanism(s). Toxicol Appl Pharmacol 133:321–327. doi:10.1006/taap.1995.1157

    CAS  PubMed  Article  Google Scholar 

  52. Safe S, Wang F, Porter W et al (1998) Ah receptor agonists as endocrine disruptors: antiestrogenic activity and mechanisms. Toxicol Lett 102:343–347

    PubMed  Article  Google Scholar 

  53. Klinge CM, Bowers JL, Kulakosky PC et al (1999) The aryl hydrocarbon receptor (AHR)/AHR nuclear translocator (ARNT) heterodimer interacts with naturally occurring estrogen response elements. Mol Cell Endocrinol 157:105–119. doi:10.1016/S0303-7207(99)00165-3

    CAS  PubMed  Article  Google Scholar 

  54. Ohtake F, Takeyama K, Matsumoto T et al (2003) Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 423:545–550. doi:10.1038/nature01606

    CAS  PubMed  Article  Google Scholar 

  55. Poland A, Glover E, Kende AS (1976) Stereospecific, high affinity binding of 2,3,7,8 tetrachlorodibenzo p dioxin by hepatic cytosol. Evidence that the binding species is receptor for induction of aryl hydrocarbon hydroxylase. J Biol Chem 251:4936–4946

    CAS  PubMed  Google Scholar 

  56. Fernandez-Salguero PM, Hilbert DM, Rudikoff S et al (1996) Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol Appl Pharmacol 140:173–179. doi:10.1006/taap.1996.0210

    CAS  PubMed  Article  Google Scholar 

  57. Denis M, Cuthill S, Wikström AC et al (1988) Association of the dioxin receptor with the Mr 90,000 heat shock protein: a structural kinship with the glucocorticoid receptor. Biochem Biophys Res Commun 155:801–807. doi:10.1016/S0006-291X(88)80566-7

    CAS  PubMed  Article  Google Scholar 

  58. Perdew GH (1988) Association of the Ah receptor with the 90-kDa heat shock protein. J Biol Chem 263:13802–13805. doi:10.1073/pnas.1302856110

    CAS  PubMed  Google Scholar 

  59. Carver LA, Bradfield CA (1997) Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J Biol Chem 272:11452–11456. doi:10.1074/jbc.272.17.11452

    CAS  PubMed  Article  Google Scholar 

  60. Ma Q, Whitlock JP (1997) A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Chem 272:8878–8884. doi:10.1074/jbc.272.14.8878

    CAS  PubMed  Article  Google Scholar 

  61. Meyer BK, Pray-Grant MG, Vanden Heuvel JP, Perdew GH (1998) Hepatitis B virus X-associated protein 2 is a subunit of the unliganded aryl hydrocarbon receptor core complex and exhibits transcriptional enhancer activity. Mol Cell Biol 18:978–988

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  62. Pollenz RS, Sattler CA, Poland A (1994) The aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator protein show distinct subcellular localizations in Hepa 1c1c7 cells by immunofluorescence microscopy. Mol Pharmacol 45:428–438

    CAS  PubMed  Google Scholar 

  63. Reyes H, Reisz-Porszasz S, Hankinson O (1992) Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science 256:1193–1195. doi:10.1126/science.256.5060.1193

    CAS  PubMed  Article  Google Scholar 

  64. Denison MS, Fisher JM, Whitlock JP (1988) The DNA recognition site for the dioxin-Ah receptor complex. Nucleotide sequence and functional analysis. J Biol Chem 263:17221–17224

    CAS  PubMed  Google Scholar 

  65. Bock KW (1994) Aryl hydrocarbon or dioxin receptor: biologic and toxic responses. Rev Physiol Biochem Pharmacol 125:1–42

    CAS  PubMed  Google Scholar 

  66. Carlson DB, Perdew GH (2002) A dynamic role for the Ah receptor in cell signaling? Insights from a diverse group of Ah receptor interacting proteins. J Biochem Mol Toxicol 16:317–325. doi:10.1002/jbt.10051

    CAS  PubMed  Article  Google Scholar 

  67. Gu YZ, Hogenesch JB, Bradfield CA (2000) The PAS superfamily: sensors of environmental and developmental signals. Annu Rev Pharmacol Toxicol 40:519–561. doi:10.1146/annurev.pharmtox.40.1.519

    CAS  PubMed  Article  Google Scholar 

  68. Bock KW, Köhle C (2006) Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem Pharmacol 72:393–404. doi:10.1016/j.bcp.2006.01.017

    CAS  PubMed  Article  Google Scholar 

  69. Marlowe JL, Knudsen ES, Schwemberger S, Puga A (2004) The aryl hydrocarbon receptor displaces p300 from E2F-dependent promoters and represses S phase-specific gene expression. J Biol Chem 279:29013–29022. doi:10.1074/jbc.M404315200

    CAS  PubMed  Article  Google Scholar 

  70. Huang G, Elferink CJ (2005) Multiple mechanisms are involved in Ah receptor-mediated cell cycle arrest. Mol Pharmacol 67:88–96. doi:10.1124/mol.104.002410

    CAS  PubMed  Article  Google Scholar 

  71. Tian Y, Ke S, Denison MS et al (1999) Ah receptor and NF-kappaB interactions, a potential mechanism for dioxin toxicity. J Biol Chem 274:510–515

    CAS  PubMed  Article  Google Scholar 

  72. Pollenz RS (2002) The mechanism of AH receptor protein down-regulation (degradation) and its impact on AH receptor-mediated gene regulation. Chem Biol Interact 141:41–61. doi:10.1016/S0009-2797(02)00065-0

    CAS  PubMed  Article  Google Scholar 

  73. Hankinson O (2005) Role of coactivators in transcriptional activation by the aryl hydrocarbon receptor. Arch Biochem Biophys 433:379–386

    CAS  PubMed  Article  Google Scholar 

  74. Schrenk D (1998) Impact of dioxin-type induction of drug-metabolizing enzymes on the metabolism of endo- and xenobiotics. Biochem Pharmacol 55:1155–1162. doi:10.1016/S0006-2952(97)00591-1

    CAS  PubMed  Article  Google Scholar 

  75. Nguyen LP, Bradfield CA (2008) The search for endogenous activators of the aryl hydrocarbon receptor. Chem Res Toxicol 21:102–116. doi:10.1021/tx7001965

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  76. Endler A, Chen L, Shibasaki F (2014) Coactivator recruitment of AhR/ARNT1. Int J Mol Sci 15:11100–11110. doi:10.3390/ijms150611100

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  77. Teske S, Bohn AA, Regal JF et al (2005) Activation of the aryl hydrocarbon receptor increases pulmonary neutrophilia and diminishes host resistance to influenza A virus. Am J Physiol Lung Cell Mol Physiol 289:L111–L124. doi:10.1152/ajplung.00318.2004

    CAS  PubMed  Article  Google Scholar 

  78. Tibbetts TA, Conneely OM, O’Malley BW (1999) Progesterone via its receptor antagonizes the pro-inflammatory activity of estrogen in the mouse uterus. Biol Reprod 60:1158–1165. doi:10.1095/biolreprod60.5.1158

    CAS  PubMed  Article  Google Scholar 

  79. Majewski AC, Hansen PJ (2002) Progesterone inhibits rejection of xenogeneic transplants in the sheep uterus. Horm Res 58:128–135. doi:10.1159/000063578

    CAS  PubMed  Article  Google Scholar 

  80. Mendelson CR, Hardy DB (2006) Role of the progesterone receptor (PR) in the regulation of inflammatory response pathways and aromatase in the breast. J Steroid Biochem Mol Biol 102:241–249. doi:10.1016/j.jsbmb.2006.09.029

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  81. Gleicher N, el-Roeiy A, Confino E, Friberg J (1987) Is endometriosis an autoimmune disease? Obstet Gynecol 70:115–122. doi:10.1016/0020-7292(88)90292-5

    CAS  PubMed  Google Scholar 

  82. Rier SE, Yeaman GR (1997) Immune aspects of endometriosis: relevance of the uterine mucosal immune system. Semin Reprod Endocrinol 15:209–220. doi:10.1055/s-2008-1068750

    CAS  PubMed  Article  Google Scholar 

  83. Braun DP, Dmowski WP (1998) Endometriosis: abnormal endometrium and dysfunctional immune response. Curr Opin Obstet Gynecol 10:365–369. doi:10.1097/00001703-199810000-00003

    CAS  PubMed  Article  Google Scholar 

  84. Iborra A, Palacio JR, Ulcova-Gallova Z, Martínez P (2000) Autoimmune response in women with endometriosis. Am J Reprod Immunol 44:236–241

    CAS  PubMed  Article  Google Scholar 

  85. Bruner-Tran KL, Eisenberg E, Yeaman GR et al (2002) Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab 87:4782–4791. doi:10.1210/jc.2002-020418

    CAS  PubMed  Article  Google Scholar 

  86. Maeda N, Izumiya C, Oguri H et al (2002) Aberrant expression of intercellular adhesion molecule-1 and killer inhibitory receptors induces immune tolerance in women with pelvic endometriosis. Fertil Steril 77:679–683. doi:10.1016/S0015-0282(01)03249-6

    PubMed  Article  Google Scholar 

  87. Sidell N, Han SW, Parthasarathy S (2002) Regulation and modulation of abnormal immune responses in endometriosis. Ann N Y Acad Sci 955:159–173 (discussion 199–200, 396–406)

    CAS  PubMed  Article  Google Scholar 

  88. Yeaman GR, Collins JE, Lang GA (2002) Autoantibody responses to carbohydrate epitopes in endometriosis. Ann N Y Acad Sci 955:174–182 (discussion 199–200, 396–406)

    CAS  PubMed  Article  Google Scholar 

  89. Matarese G, De Placido G, Nikas Y, Alviggi C (2003) Pathogenesis of endometriosis: natural immunity dysfunction or autoimmune disease? Trends Mol Med 9:223–228. doi:10.1016/S1471-4914(03)00051-0

    CAS  PubMed  Article  Google Scholar 

  90. Takemoto K, Nakajima M, Fujiki Y et al (2004) Role of the aryl hydrocarbon receptor and Cyp1b1 in the antiestrogenic activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Arch Toxicol 78:309–315. doi:10.1007/s00204-004-0550-7

    CAS  PubMed  Article  Google Scholar 

  91. Safe S, Krishnan V (1995) Chlorinated hydrocarbons: estrogens and antiestrogens. Toxicol Lett 82:731–736

    PubMed  Article  Google Scholar 

  92. Astroff B, Rowlands C, Dickerson R, Safe S (1990) 2,3,7,8-Tetrachlorodibenzo-p-dioxin inhibition of 17 beta-estradiol-induced increases in rat uterine epidermal growth factor receptor binding activity and gene expression. Mol Cell Endocrinol 72:247–252

    CAS  PubMed  Article  Google Scholar 

  93. Boverhof DR, Burgoon LD, Williams KJ, Zacharewski TR (2008) Inhibition of estrogen-mediated uterine gene expression responses by dioxin. Mol Pharmacol 73:82–93. doi:10.1124/mol.107.040451

    CAS  PubMed  Article  Google Scholar 

  94. Brauze D, Crow JS, Malejka-Giganti D (1997) Modulation by beta-naphthoflavone of ovarian hormone dependent responses in rat uterus and liver in vivo. Can J Physiol Pharmacol 75:1022–1029

    CAS  PubMed  Article  Google Scholar 

  95. Boverhof DR, Kwekel JC, Humes DG et al (2006) Dioxin induces an estrogen-like, estrogen receptor-dependent gene expression response in the murine uterus. Mol Pharmacol 69:1599–1606. doi:10.1124/mol.105.019638

    CAS  PubMed  Article  Google Scholar 

  96. Hernandez-Ochoa I, Barnett-Ringgold KR, Dehlinger SL et al (2010) The ability of the aryl hydrocarbon receptor to regulate ovarian follicle growth and estradiol biosynthesis in mice depends on stage of sexual maturity. Biol Reprod 83:698–706. doi:10.1095/biolreprod.110.087015

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  97. Lin TM, Rasmussen NT, Moore RW et al (2003) Region-specific inhibition of prostatic epithelial bud formation in the urogenital sinus of C57BL/6 mice exposed in utero to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 76:171–181. doi:10.1093/toxsci/kfg218

    CAS  PubMed  Article  Google Scholar 

  98. Ohtake F, Fujii-Kuriyama Y, Kawajiri K, Kato S (2011) Cross-talk of dioxin and estrogen receptor signals through the ubiquitin system. J Steroid Biochem Mol Biol 127:102–107. doi:10.1016/j.jsbmb.2011.03.007

    CAS  PubMed  Article  Google Scholar 

  99. Lee AJ, Cai MX, Thomas PE et al (2003) Characterization of the oxidative metabolites of 17β-estradiol and estrone formed by 15 selectively expressed human cytochrome P450 isoforms. Endocrinology 144:3382–3398. doi:10.1210/en.2003-0192

    CAS  PubMed  Article  Google Scholar 

  100. Swedenborg E, Pongratz I (2010) AhR and ARNT modulate ER signaling. Toxicology 268:132–138. doi:10.1016/j.tox.2009.09.007

    CAS  PubMed  Article  Google Scholar 

  101. Ohtake F, Baba A, Takada I et al (2007) Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446:562–566. doi:10.1038/nature05683

    CAS  PubMed  Article  Google Scholar 

  102. Meyer ME, Gronemeyer H, Turcotte B et al (1989) Steroid hormone receptors compete for factors that mediate their enhancer function. Cell 57:433–442. doi:10.1016/0092-8674(89)90918-5

    CAS  PubMed  Article  Google Scholar 

  103. Buchanan DL, Setiawan T, Lubahn DB et al (1999) Tissue compartment-specific estrogen receptor-α participation in the mouse uterine epithelial secretory response. Endocrinology 140:484–491. doi:10.1210/en.140.1.484

    CAS  PubMed  Google Scholar 

  104. Bulun SE (2000) Aromatase deficiency and estrogen resistance: from molecular genetics to clinic. Semin Reprod Med 18:31–39. doi:10.1055/s-2000-13481

    CAS  PubMed  Article  Google Scholar 

  105. Fazleabas AT, Brudney A, Chai D et al (2003) Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril 80:820–827. doi:10.1016/S0015-0282(03)00982-8

    PubMed  Article  Google Scholar 

  106. Bulun SE (2009) Endometriosis. N Engl J Med 360:268–279. doi:10.1056/NEJMra0804690

    CAS  PubMed  Article  Google Scholar 

  107. Agarwal VR, Bulun SE, Leitch M et al (1996) Use of alternative promoters to express the aromatase cytochrome P450 (CYP19) gene in breast adipose tissues of cancer-free and breast cancer patients. J Clin Endocrinol Metab 81:3843–3849. doi:10.1210/jc.81.11.3843

    CAS  PubMed  Google Scholar 

  108. Agarwal VR, Ashanullah CI, Simpson ER, Bulun SE (1997) Alternatively spliced transcripts of the aromatase cytochrome P450 (CYP19) gene in adipose tissue of women. J Clin Endocrinol Metab 82:70–74. doi:10.1210/jc.82.1.70

    CAS  PubMed  Google Scholar 

  109. Attar E, Bulun SE (2006) Aromatase and other steroidogenic genes in endometriosis: translational aspects. Hum Reprod Update 12:49–56. doi:10.1093/humupd/dmi034

    CAS  PubMed  Article  Google Scholar 

  110. Bulun SE, Mahendroo MS, Simpson ER (1994) Aromatase gene expression in adipose tissue: relationship to breast cancer. J Steroid Biochem Mol Biol 49:319–326. doi:10.1016/0960-0760(94)90274-7

    CAS  PubMed  Article  Google Scholar 

  111. Simpson ER, Zhao Y, Agarwal VR et al (1997) Aromatase expression in health and disease. Recent Prog Horm Res 52:185–213 (discussion 213–214)

    CAS  PubMed  Google Scholar 

  112. Fang Z, Yang S, Gurates B et al (2002) Genetic or enzymatic disruption of aromatase inhibits the growth of ectopic uterine tissue. J Clin Endocrinol Metab 87:3460–3466. doi:10.1210/jc.87.7.3460

    CAS  PubMed  Article  Google Scholar 

  113. Bulun SE, Imir G, Utsunomiya H et al (2005) Aromatase in endometriosis and uterine leiomyomata. J Steroid Biochem Mol Biol 95:57–62

    CAS  PubMed  Article  Google Scholar 

  114. Langoi D, Pavone ME, Gurates B et al (2013) Aromatase inhibitor treatment limits progression of peritoneal endometriosis in baboons. Fertil Steril. doi:10.1016/j.fertnstert.2012.11.021

    PubMed Central  PubMed  Google Scholar 

  115. Fischle W, Wang Y, Allis CD (2003) Histone and chromatin cross-talk. Curr Opin Cell Biol 15:172–183. doi:10.1016/S0955-0674(03)00013-9

    CAS  PubMed  Article  Google Scholar 

  116. Fujii-Kuriyama Y, Mimura J (2003) Transcriptional roles of AhR in expression of biological effects induced by endocrine disruptors. Pure Appl Chem 75:1819–1826. doi:10.1351/pac200375111819

    CAS  Article  Google Scholar 

  117. Baba T, Mimura J, Nakamura N et al (2005) Intrinsic function of the aryl hydrocarbon (dioxin) receptor as a key factor in female reproduction. Mol Cell Biol 25:10040–10051. doi:10.1128/MCB.25.22.10040-10051.2005

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  118. Matthews J, Wihlén B, Thomsen J, Gustafsson J-A (2005) Aryl hydrocarbon receptor-mediated transcription: ligand-dependent recruitment of estrogen receptor alpha to 2,3,7,8-tetrachlorodibenzo-p-dioxin-responsive promoters. Mol Cell Biol 25:5317–5328. doi:10.1128/MCB.25.13.5317-5328.2005

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  119. Ahmed S, Valen E, Sandelin A, Matthews J (2009) Dioxin increases the interaction between aryl hydrocarbon receptor and estrogen receptor alpha at human promoters. Toxicol Sci 111:254–266. doi:10.1093/toxsci/kfp144

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  120. Beischlag TV, Perdew GH (2005) ER alpha-AHR-ARNT protein-protein interactions mediate estradiol-dependent transrepression of dioxin-inducible gene transcription. J Biol Chem 280:21607–21611. doi:10.1074/jbc.C500090200

    CAS  PubMed  Article  Google Scholar 

  121. Nayyar T, Bruner-Tran KL, Piestrzeniewicz-Ulanska D, Osteen KG (2007) Developmental exposure of mice to TCDD elicits a similar uterine phenotype in adult animals as observed in women with endometriosis. Reprod Toxicol 23:326–336. doi:10.1016/j.reprotox.2006.09.007

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  122. Igarashi TM, Bruner-Tran KL, Yeaman GR et al (2005) Reduced expression of progesterone receptor-B in the endometrium of women with endometriosis and in cocultures of endometrial cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fertil Steril 84:67–74. doi:10.1016/j.fertnstert.2005.01.113

    CAS  PubMed  Article  Google Scholar 

  123. Herington JL, Bruner-Tran KL, Lucas JA, Osteen KG (2011) Immune interactions in endometriosis. Expert Rev Clin Immunol 7:611–626. doi:10.1586/eci.11.53

    PubMed Central  PubMed  Article  Google Scholar 

  124. Poellinger L (2000) Mechanistic aspects—the dioxin (aryl hydrocarbon) receptor. Food Addit Contam 17:261–266. doi:10.1080/026520300283333

    CAS  PubMed  Article  Google Scholar 

  125. Laupeze B, Amiot L, Sparfel L et al (2002) Polycyclic aromatic hydrocarbons affect functional differentiation and maturation of human monocyte-derived dendritic cells. J Immunol 168:2652–2658

    CAS  PubMed  Article  Google Scholar 

  126. Van Grevenynghe J, Rion S, Le Ferrec E et al (2003) Polycyclic aromatic hydrocarbons inhibit differentiation of human monocytes into macrophages. J Immunol 170:2374–2381

    PubMed  Article  Google Scholar 

  127. Yang JH (1999) Expression of dioxin-responsive genes in human endometrial cells in culture. Biochem Biophys Res Commun 257:259–263. doi:10.1006/bbrc.1999.0451

    CAS  PubMed  Article  Google Scholar 

  128. González-Ramos R, Donnez J, Defrère S et al (2007) Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis. Mol Hum Reprod 13:503–509. doi:10.1093/molehr/gam033

    PubMed  Article  CAS  Google Scholar 

  129. Buck Louis GM, Weiner JM, Whitcomb BW et al (2005) Environmental PCB exposure and risk of endometriosis. Hum Reprod 20:279–285. doi:10.1093/humrep/deh575

    CAS  Article  Google Scholar 

  130. Abrahams VM, Collins JE, Wira CR et al (2003) Inhibition of human polymorphonuclear cell oxidative burst by 17-beta-estradiol and 2,3,7,8-tetrachlorodibenzo-p-dioxin. Am J Reprod Immunol 50:463–472

    PubMed  Article  Google Scholar 

  131. Cao W-G, Morin M, Metz C et al (2005) Stimulation of macrophage migration inhibitory factor expression in endometrial stromal cells by interleukin 1, beta involving the nuclear transcription factor NFkappaB. Biol Reprod 73:565–570. doi:10.1095/biolreprod.104.038331

    CAS  PubMed  Article  Google Scholar 

  132. Schweppe KW, Wynn RM (1981) Ultrastructural changes in endometriotic implants during the menstrual cycle. Obstet Gynecol 58:465–473

    CAS  PubMed  Google Scholar 

  133. Bruner-Tran KL, Rier SE, Eisenberg E, Osteen KG (1999) The potential role of environmental toxins in the pathophysiology of endometriosis. Gynecol Obstet Invest 48(Suppl 1):45–56. doi:10.1159/000052868

    CAS  PubMed  Article  Google Scholar 

  134. Ruby CE, Leid M, Kerkvliet NI (2002) 2,3,7,8-Tetrachlorodibenzo-p-dioxin suppresses tumor necrosis factor a and anti-CD40-induced activation of NF-kappaB/Rel in dendritic cells : p50 homodimer activation is not affected. Mol Pharmacol 62:722–728

    CAS  PubMed  Article  Google Scholar 

  135. Thatcher TH, Maggirwar SB, Baglole CJ et al (2007) Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the nuclear factor-kappaB component RelB. Am J Pathol 170:855–864. doi:10.2353/ajpath.2007.060391

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  136. Baldi L, Brown K, Franzoso G, Siebenlist U (1996) Critical role for lysines 21 and 22 in signal-induced, ubiquitin-mediated proteolysis of I kappa B-alpha. J Biol Chem 271:376–379. doi:10.1074/jbc.271.1.376

    CAS  PubMed  Article  Google Scholar 

  137. Roff M, Thompson J, Rodriguez MS et al (1996) Role of IkappaBalpha ubiquitination in signal-induced activation of NFkappaB in vivo. J Biol Chem 271:7844–7850. doi:10.1074/jbc.271.13.7844

    CAS  PubMed  Article  Google Scholar 

  138. Laird SM, Tuckerman EM, Dalton CF et al (1997) The production of leukaemia inhibitory factor by human endometrium: presence in uterine flushings and production by cells in culture. Hum Reprod 12:569–574

    CAS  PubMed  Article  Google Scholar 

  139. Laird SM, Tuckerman EM, Cork BA, Li TC (2000) Expression of nuclear factor kappa B in human endometrium; role in the control of interleukin 6 and leukaemia inhibitory factor production. Mol Hum Reprod 6:34–40

    CAS  PubMed  Article  Google Scholar 

  140. Camacho IA, Hassuneh MR, Nagarkatti M, Nagarkatti PS (2001) Enhanced activation-induced cell death as a mechanism of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced immunotoxicity in peripheral T cells. Toxicology 165:51–63. doi:10.1016/S0300-483X(01)00391-2

    CAS  PubMed  Article  Google Scholar 

  141. Guo SW (2007) Nuclear factor-kappaB (NF-kappaB): an unsuspected major culprit in the pathogenesis of endometriosis that is still at large? Gynecol Obstet Invest 63:71–97. doi:10.1159/000096047

    CAS  PubMed  Article  Google Scholar 

  142. Neumann M, Naumann M (2007) Beyond IkappaBs: alternative regulation of NF-kappaB activity. FASEB J 21:2642–2654. doi:10.1096/fj.06-7615rev

    CAS  PubMed  Article  Google Scholar 

  143. Wieser F, Vigne JL, Ryan I et al (2005) Sulindac suppresses nuclear factor-κB activation and RANTES gene and protein expression in endometrial stromal cells from women with endometriosis. J Clin Endocrinol Metab 90:6441–6447. doi:10.1210/jc.2005-0972

    CAS  PubMed  Article  Google Scholar 

  144. Calicchio R, Doridot L, Miralles F et al (2014) DNA methylation, an epigenetic mode of gene expression regulation in reproductive science. Curr Pharm Des 20:1726–1750. doi:10.2174/13816128113199990517

    CAS  PubMed  Article  Google Scholar 

  145. Naqvi H, Ilagan Y, Krikun G, Taylor HS (2014) Altered genome-wide methylation in endometriosis. Reprod Sci. doi:10.1177/1933719114532841

    PubMed  Google Scholar 

  146. Wu Y, Halverson G, Basir Z et al (2005) Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am J Obstet Gynecol 193:371–380. doi:10.1016/j.ajog.2005.01.034

    CAS  PubMed  Article  Google Scholar 

  147. Holliday R (2006) Epigenetics: a historical overview. Epigenetics 1:76–80. doi:10.4161/epi.1.2.2762

    PubMed  Article  Google Scholar 

  148. Nasu K, Kawano Y, Tsukamoto Y et al (2011) Aberrant DNA methylation status of endometriosis: epigenetics as the pathogenesis, biomarker and therapeutic target. J Obstet Gynaecol Res 37:683–695. doi:10.1111/j.1447-0756.2011.01663.x

    CAS  PubMed  Article  Google Scholar 

  149. Czyz W, Morahan JM, Ebers GC, Ramagopalan SV (2012) Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences. BMC Med 10:93. doi:10.1186/1741-7015-10-93

    PubMed Central  PubMed  Article  Google Scholar 

  150. Cortessis VK, Thomas DC, Joan Levine A et al (2012) Environmental epigenetics: prospects for studying epigenetic mediation of exposure-response relationships. Hum Genet 131:1565–1589. doi:10.1007/s00439-012-1189-8

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  151. Guo SW (2009) Epigenetics of endometriosis. Mol Hum Reprod 15:587–607. doi:10.1093/molehr/gap064

    CAS  PubMed  Article  Google Scholar 

  152. Wu Y, Shi X, Guo SW (2008) The knockdown of progesterone receptor isoform B (PR-B) promotes proliferation in immortalized endometrial stromal cells. Fertil Steril 90:1320–1323. doi:10.1016/j.fertnstert.2007.10.049

    CAS  PubMed  Article  Google Scholar 

  153. Laird PW, Jaenisch R (1996) The role of DNA methylation in cancer genetic and epigenetics. Annu Rev Genet 30:441–464. doi:10.1146/annurev.genet.30.1.441

    CAS  PubMed  Article  Google Scholar 

  154. Lister R, Pelizzola M, Dowen RH et al (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322. doi:10.1038/nature08514

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  155. Huck-Hui N, Bird A (1999) DNA methylation and chromatin modification. Curr Opin Genet Dev 9:158–163. doi:10.1016/S0959-437X(99)80024-0

    Article  Google Scholar 

  156. Borghese B, Barbaux S, Mondon F et al (2010) Research resource: genome-wide profiling of methylated promoters in endometriosis reveals a subtelomeric location of hypermethylation. Mol Endocrinol 24:1872–1885. doi:10.1210/me.2010-0160

    CAS  PubMed  Article  Google Scholar 

  157. Izawa M, Taniguchi F, Terakawa N, Harada T (2013) Epigenetic aberration of gene expression in endometriosis. Front Biosci (Elite Ed) 5:900–910

    Article  Google Scholar 

  158. Fraga MF, Ballestar E, Paz MF et al (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102:10604–10609. doi:10.1073/pnas.0500398102

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  159. Taylor HS, Bagot C, Kardana A et al (1999) HOX gene expression is altered in the endometrium of women with endometriosis. Hum Reprod 14:1328–1331. doi:10.1093/humrep/14.5.1328

    CAS  PubMed  Article  Google Scholar 

  160. Meyer JL, Zimbardi D, Podgaec S et al (2014) DNA methylation patterns of steroid receptor genes ESR1, ESR2 and PGR in deep endometriosis compromising the rectum. Int J Mol Med 33:897–904. doi:10.3892/ijmm.2014.1637

    CAS  PubMed  Google Scholar 

  161. Guo SW (2012) The endometrial epigenome and its response to steroid hormones. Mol Cell Endocrinol 358:185–196. doi:10.1016/j.mce.2011.10.025

    CAS  PubMed  Article  Google Scholar 

  162. Ito T, Bulger M, Pazin MJ et al (1997) ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90:145–155. doi:10.1016/S0092-8674(00)80321-9

    CAS  PubMed  Article  Google Scholar 

  163. Takai N, Narahara H (2007) Human endometrial and ovarian cancer cells: histone deacetylase inhibitors exhibit antiproliferative activity, potently induce cell cycle arrest, and stimulate apoptosis. Curr Med Chem 14:2548–2553. doi:10.2174/092986707782023299

    CAS  PubMed  Article  Google Scholar 

  164. Nasu K, Kawano Y, Kai K et al (2014) Aberrant histone modification in endometriosis. Front Biosci Landmark Ed 19:1202–1214. doi:10.2741/4276

    PubMed  Article  Google Scholar 

  165. Kawano Y, Nasu K, Li H et al (2011) Application of the histone deacetylase inhibitors for the treatment of endometriosis: histone modifications as pathogenesis and novel therapeutic target. Hum Reprod 26:2486–2498. doi:10.1093/humrep/der203

    CAS  PubMed  Article  Google Scholar 

  166. Duenas-Gonzalez A, Candelaria M, Perez-Plascencia C et al (2008) Valproic acid as epigenetic cancer drug: preclinical, clinical and transcriptional effects on solid tumors. Cancer Treat Rev 34:206–222. doi:10.1016/j.ctrv.2007.11.003

    CAS  PubMed  Article  Google Scholar 

  167. Mann BS, Johnson JR, He K et al (2007) Vorinostat for treatment of cutaneous manifestations of advanced primary cutaneous T-cell lymphoma. Clin Cancer Res 13:2318–2322

    CAS  PubMed  Article  Google Scholar 

  168. Gerstner T, Bell N, König S (2008) Oral valproic acid for epilepsy—long-term experience in therapy and side effects. Expert Opin Pharmacother 9:285–292. doi:10.1517/14656566.9.2.285

    CAS  PubMed  Article  Google Scholar 

  169. Monteiro JB, Colón-Díaz M, García M et al (2014) Endometriosis is characterized by a distinct pattern of histone 3 and histone 4 lysine modifications. Reprod Sci 21:305–318. doi:10.1177/1933719113497267

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  170. Laudanski P, Charkiewicz R, Kuzmicki M et al (2013) MicroRNAs expression profiling of eutopic proliferative endometrium in women with ovarian endometriosis. Reprod Biol Endocrinol 11:78. doi:10.1186/1477-7827-11-78

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  171. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. doi:10.1016/S0092-8674(04)00045-5

    CAS  PubMed  Article  Google Scholar 

  172. Ibrahim SA, Hassan H, Götte M (2014) MicroRNA-dependent targeting of the extracellular matrix as a mechanism of regulating cell behavior. Biochim Biophys Acta 1840:2609–2620. doi:10.1016/j.bbagen.2014.01.022

    CAS  PubMed  Article  Google Scholar 

  173. Guida M, Marra ML, Marra M et al (2013) Association between exposure to dioxin-like polychlorinated biphenyls and miR-191 expression in human peripheral blood mononuclear cells. Mutat Res 753:36–41. doi:10.1016/j.mrgentox.2012.12.018

    CAS  PubMed  Article  Google Scholar 

  174. Singh NP, Singh UP, Guan H et al (2012) Prenatal exposure to TCDD triggers significant modulation of microrna expression profile in the thymus that affects consequent gene expression. PLoS One. doi:10.1371/journal.pone.0045054

    Google Scholar 

  175. Ohlsson Teague EMC, Van der Hoek KH, Van der Hoek MB et al (2009) MicroRNA-regulated pathways associated with endometriosis. Mol Endocrinol 23:265–275. doi:10.1210/me.2008-0387

    PubMed  Article  CAS  Google Scholar 

  176. Hawkins SM, Creighton CJ, Han DY et al (2011) Functional microRNA involved in endometriosis. Mol Endocrinol 25:821–832. doi:10.1210/me.2010-0371

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  177. Burney RO, Talbi S, Hamilton AE et al (2007) Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 148:3814–3826. doi:10.1210/en.2006-1692

    CAS  PubMed  Article  Google Scholar 

  178. Burney RO, Hamilton AE, Aghajanova L et al (2009) MicroRNA expression profiling of eutopic secretory endometrium in women with versus without endometriosis. Mol Hum Reprod 15:625–631. doi:10.1093/molehr/gap068

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  179. Adammek M, Greve B, Kässens N et al (2013) MicroRNA miR-145 inhibits proliferation, invasiveness, and stem cell phenotype of an in vitro endometriosis model by targeting multiple cytoskeletal elements and pluripotency factors. Fertil Steril. doi:10.1016/j.fertnstert.2012.11.055

    PubMed  Google Scholar 

  180. Shi XY, Gu L, Chen J et al (2014) Downregulation of miR-183 inhibits apoptosis and enhances the invasive potential of endometrial stromal cells in endometriosis. Int J Mol Med 33:59–67. doi:10.3892/ijmm.2013.1536

    CAS  PubMed Central  PubMed  Google Scholar 

  181. Baltimore D, Boldin MP, O’Connell RM et al (2008) MicroRNAs: new regulators of immune cell development and function. Nat Immunol 9:839–845. doi:10.1038/ni.f.209

    CAS  PubMed  Article  Google Scholar 

  182. Bi Y, Liu G, Yang R (2009) MicroRNAs: novel regulators during the immune response. J Cell Physiol 218:467–472. doi:10.1002/jcp.21639

    CAS  PubMed  Article  Google Scholar 

  183. Petracco RG, Kong A, Grechukhina O et al (2012) Global gene expression profiling of proliferative phase endometrium reveals distinct functional subdivisions. Reprod Sci 19:1138–1145. doi:10.1177/1933719112443877

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  184. Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP (2010) Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod 16:297–310. doi:10.1093/molehr/gaq010

    CAS  PubMed  Article  Google Scholar 

  185. Kobayashi H, Iwai K, Niiro E et al (2014) Fetal programming theory: implication for the understanding of endometriosis. Hum Immunol 75:208–217. doi:10.1016/j.humimm.2013.12.012

    CAS  PubMed  Article  Google Scholar 

  186. Wolf M, Klug J, Hackenberg R et al (1992) Human CC10, the homologue of rabbit uteroglobin: genomic cloning, chromosomal localization and expression in endometrial cell lines. Hum Mol Genet 1:371–378

    CAS  PubMed  Article  Google Scholar 

  187. Bruner-Tran KL, Ding T, Osteen KG (2010) Dioxin and endometrial progesterone resistance. Semin Reprod Med 28:59–68. doi:10.1055/s-0029-1242995

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  188. Giudice LC, Evers JLH, Healy DL (2012) Endometriosis: science and practice. Endometr Sci Pract. doi:10.1002/9781444398519

    Google Scholar 

  189. Osteen KG, Bruner-Tran KL, Eisenberg E (2005) Reduced progesterone action during endometrial maturation: a potential risk factor for the development of endometriosis. Fertil Steril 83:529–537. doi:10.1016/j.fertnstert.2004.11.026

    CAS  PubMed  Article  Google Scholar 

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Authors and Affiliations

  1. Department of Environmental Sciences, Safety, Territory, Food and Health, University of Messina, Via C. Valeria 1, 98125, Messina, Italy

    Vincenza Sofo, Francesca Maria Salmeri & Maria Alfa

  2. Department of Gynecology and Obstetrics, Münster University Hospital, 48149, Münster, Germany

    Martin Götte

  3. Department of Pediatric, Gynecological, Microbiological and Biomedical Sciences, University of Messina, Via C. Valeria 1, 98125, Messina, Italy

    Antonio Simone Laganà, Onofrio Triolo, Emanuele Sturlese, Giovanni Retto & Roberta Granese

  4. Department of Obstetrics and Gynecology, São Paulo University (USP), São Paulo, Brazil

    Mauricio Simões Abrão

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  1. Vincenza Sofo
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Sofo, V., Götte, M., Laganà, A.S. et al. Correlation between dioxin and endometriosis: an epigenetic route to unravel the pathogenesis of the disease. Arch Gynecol Obstet 292, 973–986 (2015). https://doi.org/10.1007/s00404-015-3739-5

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Keywords

  • 2,3,7,8-Tetrachlorodibenzo-p-dioxin
  • Aryl hydrocarbon receptor
  • Endometriosis
  • Sex hormone receptors
  • Epigenetics