Exposure to the environmental endocrine disruptor TCDD and human reproductive dysfunction: Translating lessons from murine models

Reproductive Toxicology

Volumn 68, Issue , 2017, Pages 59-71

  Bruner Tran, Kaylon L ^a   Gnecco, Juan ^a   Ding, Tianbing ^a   Glore, Dana R ^a   Pensabene, Virginia ^a   Osteen, Kevin G ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Adenomyosis; Endometriosis; Epigenetics; Preterm birth; TCDD; Transgenerational

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; PROGESTERONE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA2; ENDOCRINE DISRUPTOR; POLYCHLORINATED DIBENZODIOXIN;

ADENOMYOSIS; ARTICLE; COMORBIDITY; ENDOMETRIOSIS; ENDOMETRIUM CELL; EPIGENETICS; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; HYSTERECTOMY; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PREGNANCY; PREMATURE LABOR; PROSPECTIVE STUDY; PUBERTY; QUALITY OF LIFE; REPRODUCTIVE HEALTH; REPRODUCTIVE TOXICITY; RISK ASSESSMENT; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; FEMALE; GENETIC EPIGENESIS; GENETICS; MALE; MOUSE; REPRODUCTION;

ANIMALS; ENDOCRINE DISRUPTORS; ENDOMETRIOSIS; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; FEMALE; HUMANS; MALE; MICE; POLYCHLORINATED DIBENZODIOXINS; REPRODUCTION;

EID: 84997447882     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2016.07.007     Document Type: Article

References (157)

1. [1] Bulun, S.E., Endometriosis. N. Engl. J. Med. 360:3 (2009), 268–279.
2. [2] Practice Committee of the American Society for Reproductive, M. Endometriosis and infertility: a committee opinion. Fertil. Steril. 98:3 (2012), 591–598.
3. [3] Brosens, I., et al. Risks of adverse pregnancy outcome in endometriosis. Fertil. Steril. 98:1 (2012), 30–35.
4. [4] Sinaii, N., et al. High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum. Reprod. 17:10 (2002), 2715–2724.
5. [5] Struble, J., Reid, S., Bedaiwy, M.A., Adenomyosis: a clinical review of a challenging gynecologic condition. J. Minim. Invasive Gynecol. 23:2 (2016), 164–185.
6. [6] Tirlapur, S.A., et al. The ‘evil twin syndrome' in chronic pelvic pain: a systematic review of prevalence studies of bladder pain syndrome and endometriosis. Int. J. Surg. 11:3 (2013), 233–237.
7. [7] Bruner-Tran, K.L., et al. Medical management of endometriosis: emerging evidence linking inflammation to disease pathophysiology. Minerva Ginecol. 65:2 (2013), 199–213.
8. [8] Kiyomizu, M., et al. Association of two polymorphisms in the peroxisome proliferator-activated receptor-gamma gene with adenomyosis, endometriosis, and leiomyomata in Japanese women. J. Soc. Gynecol. Investig. 13:5 (2006), 372–377.
9. [9] Guo, S.W., The association of endometriosis risk and genetic polymorphisms involving dioxin detoxification enzymes: a systematic review. Eur. J. Obstet. Gynecol. Reprod. Biol. 124:2 (2006), 134–143.
10. [10] Rier, S.E., et al. Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam. Appl. Toxicol. 21:4 (1993), 433–441.
11. [11] Bruner-Tran, K.L., Osteen, K.G., Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod. Toxicol. 31:3 (2011), 344–350.
12. [12] Bruner-Tran, K.L., et al. The potential role of environmental toxins in the pathophysiology of endometriosis. Gynecol. Obstet. Invest. 48:Suppl. 1 (1999), 45–56.
13. [13] Cummings, A.M., Metcalf, J.L., Birnbaum, L., Promotion of endometriosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin in rats and mice: time-dose dependence and species comparison. Toxicol. Appl. Pharmacol. 138:1 (1996), 131–139.
14. [14] Yang, J.Z., Agarwal, S.K., Foster, W.G., Subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin modulates the pathophysiology of endometriosis in the cynomolgus monkey. Toxicol. Sci. 56:2 (2000), 374–381.
15. [15] Yang, J.Z., Continuous exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin inhibits the growth of surgically induced endometriosis in the ovariectomized mouse treated with high dose estradiol. Toxicol. Ind. Health 13:1 (1997), 15–25.
16. [16] Igarashi, T.M., et al. 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. 84:1 (2005), 67–74.
17. [17] Resuehr, D., et al. Progesterone-dependent regulation of endometrial cannabinoid receptor type 1 (CB1-R) expression is disrupted in women with endometriosis and in isolated stromal cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Fertil. Steril. 98:4 (2012), 948–956 e1.
18. [18] Bruner-Tran, K.L., Osteen, K.G., Dioxin-like PCBs and endometriosis. Syst. Biol. Reprod. Med. 56:2 (2010), 132–146.
19. [19] Porpora, M.G., et al. Role of environmental organochlorinated pollutants in the development of endometriosis. Clin. Exp. Obstet. Gynecol. 40:4 (2013), 565–567.
20. [20] Bruner-Tran, K.L., et al. Dioxin may promote inflammation-related development of endometriosis. Fertil. Steril. 89:5 Suppl (2008), 1287–1298.
21. [21] Heindel, J.J., Role of exposure to environmental chemicals in the developmental basis of reproductive disease and dysfunction. Semin. Reprod. Med. 24:3 (2006), 168–177.
22. [22] Chen, C.Y., et al. Disposition of polychlorinated dibenzo-p-dioxins: dibenzofurans, and non-ortho polychlorinated biphenyls in pregnant long evans rats and the transfer to offspring. Toxicol. Appl. Pharmacol. 173:2 (2001), 65–88.
23. [23] Nayyar, T., et al. Developmental exposure of mice to TCDD elicits a similar uterine phenotype in adult animals as observed in women with endometriosis. Reprod. Toxicol. 23:3 (2007), 326–336.
24. [24] Anway, M.D., et al. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:5727 (2005), 1466–1469.
25. [25] Manikkam, M., et al. Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLoS One, 7(2), 2012, e31901.
26. [26] Newbold, R.R., Developmental exposure to endocrine-disrupting chemicals programs for reproductive tract alterations and obesity later in life. Am. J. Clin. Nutr. 94:6 Suppl (2011), 1939S–1942S.
27. [27] Taylor, H.S., Endocrine disruptors affect developmental programming of HOX gene expression. Fertil. Steril. 89:2 Suppl (2008), e57–8.
28. [28] Anway, M.D., Skinner, M.K., Epigenetic programming of the germ line: effects of endocrine disruptors on the development of transgenerational disease. Reprod. Biomed. Online 16:1 (2008), 23–25.
29. [29] Eichenlaub-Ritter, U., Pacchierotti, F., Bisphenol A effects on mammalian oogenesis and epigenetic integrity of oocytes: a case study exploring risks of endocrine disrupting chemicals. Biomed Res Int, 2015, 2015 698795.
30. [30] Xin, F., Susiarjo, M., Bartolomei, M.S., Multigenerational and transgenerational effects of endocrine disrupting chemicals: a role for altered epigenetic regulation?. Semin. Cell Dev. Biol. 43 (2015), 66–75.
31. [31] Melnick, R., et al. Summary of the National Toxicology Program's report of the endocrine disruptors low-dose peer review. Environ. Health Perspect. 110:4 (2002), 427–431.
32. [32] Diamanti-Kandarakis, E., et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr. Rev. 30:4 (2009), 293–342.
33. [33] Gluckman, P.D., et al. Losing the war against obesity: the need for a developmental perspective. Sci. Transl. Med., 3(93), 2011, 93cm19.
34. [34] Hanson, M.A., Low, F.M., Gluckman, P.D., Epigenetic epidemiology: the rebirth of soft inheritance. Ann. Nutr. Metab. 58:Suppl. 2 (2011), 8–15.
35. [35] Sweeney, M.F., et al. Environmental endocrine disruptors: effects on the human male reproductive system. Rev. Endocr. Metab. Disord., 2016, 347–357.
36. [36] Bofinger, D.P., et al. Effect of TCDD exposure on CYP1A1 and CYP1B1 expression in explant cultures of human endometrium. Toxicol. Sci. 62:2 (2001), 299–314.
37. [37] Nayyar, T., Bruner-Tran, K.L., Osteen, K., Developmental dioxin and endometriosis. Gupta, R., (eds.) Reproductive and Developmental Toxicology, 2011, Academic Press/Elsevier, USA.
38. [38] Peters, J.M., et al. Amelioration of TCDD-induced teratogenesis in aryl hydrocarbon receptor (AhR)-null mice. Toxicol. Sci. 47:1 (1999), 86–92.
39. [39] Nguyen, L.P., Bradfield, C.A., The search for endogenous activators of the aryl hydrocarbon receptor. Chem. Res. Toxicol. 21:1 (2008), 102–116.
40. [40] Adachi, J., et al. Indirubin and indigo are potent aryl hydrocarbon receptor ligands present in human urine. J. Biol. Chem. 276:34 (2001), 31475–31478.
41. [41] Denison, M.S., Nagy, S.R., Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 43 (2003), 309–334.
42. [42] Seidel, S.D., et al. Activation of the Ah receptor signaling pathway by prostaglandins. J. Biochem. Mol. Toxicol. 15:4 (2001), 187–196.
43. [43] Sinal, C.J., Bend, J.R., Aryl hydrocarbon receptor-dependent induction of cyp1a1 by bilirubin in mouse hepatoma hepa 1c1c7 cells. Mol. Pharmacol. 52:4 (1997), 590–609.
44. [44] Andrieux, L., et al. Aryl hydrocarbon receptor activation and cytochrome P450 1A induction by the mitogen-activated protein kinase inhibitor U0126 in hepatocytes. Mol. Pharmacol. 65:4 (2004), 934–943.
45. [45] Revel, A., et al. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm from DNA damage and apoptosis caused by benzo(a)pyrene. Reprod. Toxicol. 15:5 (2001), 479–486.
46. [46] Takamura, T., et al. Activation of the aryl hydrocarbon receptor pathway may ameliorate dextran sodium sulfate-induced colitis in mice. Immunol. Cell Biol. 88:6 (2010), 685–689.
47. [47] Birnbaum, L.S., Evidence for the role of the Ah receptor in response to dioxin. Prog. Clin. Biol. Res. 387 (1994), 139–154.
48. [48] Buck Louis, G.M., Persistent environmental pollutants and couple fecundity: an overview. Reproduction 147:4 (2014), R97–R104.
49. [49] Ramesh, A., et al. Bioavailability and risk assessment of orally ingested polycyclic aromatic hydrocarbons. Int. J. Toxicol. 23:5 (2004), 301–333.
50. [50] Lee, J., et al. Male and female mice show significant differences in hepatic transcriptomic response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. BMC Genomics, 16, 2015, 625.
51. [51] Myllymaki, S.A., et al. In utero and lactational exposure to TCDD; steroidogenic outcomes differ in male and female rat pups. Toxicol. Sci. 88:2 (2005), 534–544.
52. [52] Naville, D., et al. Low-dose food contaminants trigger sex-specific, hepatic metabolic changes in the progeny of obese mice. FASEB J. 27:9 (2013), 3860–3870.
53. [53] Sobolewski, M., et al. Sex-specific enhanced behavioral toxicity induced by maternal exposure to a mixture of low dose endocrine-disrupting chemicals. Neurotoxicology 45 (2014), 121–130.
54. [54] Heimler, I., et al. Dioxin perturbs, in a dose- and time-dependent fashion, steroid secretion, and induces apoptosis of human luteinized granulosa cells. Endocrinology 139:10 (1998), 4373–4379.
55. [55] Heimler, I., et al. Modulation of ovarian follicle maturation and effects on apoptotic cell death in Holtzman rats exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in utero and lactationally. Reprod. Toxicol. 12:1 (1998), 69–73.
56. [56] Okino, S.T., Whitlock, J.P. Jr., The aromatic hydrocarbon receptor, transcription, and endocrine aspects of dioxin action. Vitam. Horm. 59 (2000), 241–264.
57. [57] Hankinson, O., The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 35 (1995), 307–340.
58. [58] Olsen, H., Enan, E., Matsumura, F., Regulation of glucose transport in the NIH 3T3 L1 preadipocyte cell line by TCDD. Environ. Health Perspect. 102:5 (1994), 454–458.
59. [59] Sorg, O., et al. 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) poisoning in Victor Yushchenko: identification and measurement of TCDD metabolites. Lancet 374:9696 (2009), 1179–1185.
60. [60] Harrad, S., et al. Human dietary intake and excretion of dioxin-like compounds. J. Environ. Monit. 5:2 (2003), 224–228.
61. [61] Malisch, R., Kotz, A., Dioxins and PCBs in feed and food—review from European perspective. Sci. Total Environ. 491–492 (2014), 2–10.
62. [62] Pompa, G., Caloni, F., Fracchiolla, M.L., Dioxin and PCB contamination of fish and shellfish: assessment of human exposure. Review of the international situation. Vet. Res. Commun. 27:Suppl. 1 (2003), 159–167.
63. [63] Schecter, A., et al. Characterization of dioxin exposure in firefighters: residents, and chemical workers in the Irkutsk Region of Russian Siberia. Chemosphere 47:2 (2002), 147–156.
64. [64] Birnbaum, L.S., Endocrine effects of prenatal exposure to PCBs, dioxins, and other xenobiotics: implications for policy and future research. Environ. Health Perspect. 102:8 (1994), 676–679.
65. [65] Aylward, L.L., Hays, S.M., Temporal trends in human TCDD body burden: decreases over three decades and implications for exposure levels. J. Expo. Anal. Environ. Epidemiol. 12:5 (2002), 319–328.
66. [66] Archibong, A.E., et al. Endocrine disruptive actions of inhaled benzo(a)pyrene on ovarian function and fetal survival in fisher F-344 adult rats. Reprod. Toxicol. 34:4 (2012), 635–643.
67. [67] Vanker, A., et al. Home environment and indoor air pollution exposure in an African birth cohort study. Sci. Total Environ. 536 (2015), 362–367.
68. [68] Ramos, Y., et al. Spatio-temporal models to estimate daily concentrations of fine particulate matter in Montreal: Kriging with external drift and inverse distance-weighted approaches. J. Expo. Sci. Environ. Epidemiol. 26 (2016), 405–414.
69. [69] Vandenberg, L.N., et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. 33:3 (2012), 378–455.
70. [70] Homberger, E., et al. The Seveso accident: its nature, extent and consequences. Ann. Occup. Hyg. 22:4 (1979), 327–367.
71. [71] Wesselink, A., et al. Maternal dioxin exposure and pregnancy outcomes over 30 years of follow-up in Seveso. Environ. Int. 63 (2014), 143–148.
72. [72] Warner, M., et al. Serum dioxin concentrations and quality of ovarian function in women of Seveso. Environ. Health Perspect. 115:3 (2007), 336–340.
73. [73] Eskenazi, B., et al. Maternal serum dioxin levels and birth outcomes in women of Seveso, Italy. Environ. Health Perspect. 111:7 (2003), 947–953.
74. [74] Eskenazi, B., et al. Serum dioxin concentrations and endometriosis: a cohort study in Seveso, Italy. Environ. Health Perspect. 110:7 (2002), 629–634.
75. [75] Bois, F.Y., Eskenazi, B., Possible risk of endometriosis for Seveso, Italy, residents: an assessment of exposure to dioxin. Environ. Health Perspect. 102:5 (1994), 476–477.
76. [76] DeFranco, E., et al. Air pollution and stillbirth risk: exposure to airborne particulate matter during pregnancy is associated with fetal death. PLoS One, 10(3), 2015, e0120594.
77. [77] DeFranco, E., et al. Exposure to airborne particulate matter during pregnancy is associated with preterm birth: a population-based cohort study. Environ. Health, 15(1), 2016, 6.
78. [78] Stillerman, K.P., et al. Environmental exposures and adverse pregnancy outcomes: a review of the science. Reprod. Sci. 15:7 (2008), 631–650.
79. [79] Candela, S., et al. Air pollution from incinerators and reproductive outcomes: a multisite study. Epidemiology 24:6 (2013), 863–870.
80. [80] Wilson, C.L., et al. Assessment of dioxin and dioxin-like compounds in mainstream smoke from selected US cigarette brands and reference cigarettes. Food Chem. Toxicol. 46:5 (2008), 1721–1733.
81. [81] Camlin, N.J., McLaughlin, E.A., Holt, J.E., Through the smoke: use of in vivo and in vitro cigarette smoking models to elucidate its effect on female fertility. Toxicol. Appl. Pharmacol. 281:3 (2014), 266–275.
82. [82] Levy, D., et al. Smoking and adverse maternal and child health outcomes in Brazil. Nicotine Tob. Res. 15:11 (2013), 1797–1804.
83. [83] Stone, W.L., Bailey, B., Khraisha, N., The pathophysiology of smoking during pregnancy: a systems biology approach. Front. Biosci. (Elite Ed.) 6 (2014), 318–328.
84. [84] Mocarelli, P., et al. Perinatal exposure to low doses of dioxin can permanently impair human semen quality. Environ. Health Perspect. 119:5 (2011), 713–718.
85. [85] Rolland, M., et al. Decline in semen concentration and morphology in a sample of 26,609 men close to general population between 1989 and 2005 in France. Hum. Reprod. 28:2 (2013), 462–470.
86. [86] T.J. Woodruff et al., Proceedings of the Summit on Environmental Challenges to Reproductive Health and Fertility: executive summary. Fertil. Steril. 89 (2 Suppl.) (2008) e1–e20.
87. [87] Lewis, J., Smokey bear in vietnam. Environ. Hist. 11:3 (2006), 598–603.
88. [88] Anh, N.T., et al. Maternal risk factors associated with increased dioxin concentrations in breast milk in a hot spot of dioxin contamination in Vietnam. J. Expo. Sci. Environ. Epidemiol. 24:5 (2014), 489–496.
89. [89] Nghi, T.N., et al. Dioxins and nonortho PCBs in breast milk of Vietnamese mothers living in the largest hot spot of dioxin contamination. Environ. Sci. Technol. 49:9 (2015), 5732–5742.
90. [90] Schecter, A., et al. A follow-up: high level of dioxin contamination in Vietnamese from agent orange, three decades after the end of spraying. J. Occup. Environ. Med. 44:3 (2002), 218–220.
91. [91] Tai, P.T., et al. Dioxin exposure in breast milk and infant neurodevelopment in Vietnam. Occup. Environ. Med. 70:9 (2013), 656–662.
92. [92] Herbicides., I.o.M.U.C.t.R.t.H.E.i.V.V.o.E.t., Veterans and agent orange: health effects of herbicides used in Vietnam. 1994, Washington DC: National Academic Press.
93. [93] Stanley, J., Blain, J.D., (eds.) Challenges in Military Health Care: Perspectives on Health Status and the Provision of Care, 1993, Transaction Publishers.
94. [94] Mari, M., Domingo, J.L., Toxic emissions from crematories: a review. Environ. Int. 36:1 (2010), 131–137.
95. [95] Aurell, J., Gullett, B.K., Yamamoto, D., Emissions from open burning of simulated military waste from forward operating bases. Environ. Sci. Technol. 46:20 (2012), 11004–11012.
96. [96] Doucet, I., Desert Storm syndrome: sick soldiers and dead children?. Med. War 10:3 (1994), 183–194.
97. [97] Emmerova, M., Jirava, F., Is Gulf war syndrome really a mystery?. Med. Confl. Surviv. 20:3 (2004), 209–217.
98. [98] Woodall, B.D., et al. Emissions from small-scale burns of simulated deployed U.S. military waste. Environ. Sci. Technol. 46:20 (2012), 10997–11003.
99. [99] Ding, T., et al. Developmental dioxin exposure of either parent is associated with an increased risk of preterm birth in adult mice. Reprod. Toxicol. 31:3 (2011), 351–358.
100. [100] Vercellini, P., et al. Adenomyosis: epidemiological factors. Best Pract. Res. Clin. Obstet. Gynaecol. 20:4 (2006), 465–477.
101. [101] Cockerham, A.Z., Adenomyosis: a challenge in clinical gynecology. J. Midwifery Womens Health 57:3 (2012), 212–220.
102. [102] Bruner-Tran, K.L., et al. Developmental toxicant exposure is associated with transgenerational adenomyosis in a murine model. Biol. Reprod., 2016 (pending).
103. [103] Bruner-Tran, K.L., et al. The role of endocrine disruptors in the epigenetics of reproductive disease and dysfunction: potential relevance to humans. Curr. Obstet. Gynecol. Rep. 1:3 (2012), 116–123.
104. [104] Jichan, N., Xishi, L., Guo, S.W., Promoter hypermethylation of progesterone receptor isoform B (PR-B) in adenomyosis and its rectification by a histone deacetylase inhibitor and a demethylation agent. Reprod. Sci. 17:11 (2010), 995–1005.
105. [105] Li, Y., et al. Accumulation of nerve growth factor and its receptors in the uterus and dorsal root ganglia in a mouse model of adenomyosis. Reprod. Biol. Endocrinol., 9, 2011, 30.
106. [106] Valentini, A.L., et al. Adenomyosis: from the sign to the diagnosis Imaging, diagnostic pitfalls and differential diagnosis: a pictorial review. Radiol. Med. 116:8 (2011), 1267–1287.
107. [107] D.R. Glore et al., Developmental dioxin exposure promotes a hyper-inflammatory peritoneal microenvironment which may contribute to the endometriosis-like phenotype in American Society for Reproductive Medicine. San Diego, CA, 2012.
108. [108] Williams, R., White, H., The greater omentum: its applicability to cancer surgery and cancer therapy. Curr. Probl. Surg. 23:11 (1986), 789–865.
109. [109] Krist, L.F., et al. Novel isolation and purification method permitting functional cytotoxicity studies of macrophages from milky spots in the greater omentum. J. Immunol. Methods 184:2 (1995), 253–261.
110. [110] Krist, L.F., et al. Cellular composition of milky spots in the human greater omentum: an immunochemical and ultrastructural study. Anat. Rec. 241:2 (1995), 163–174.
111. [111] Westcott, E., et al. Fatty acid compositions of lipids in mesenteric adipose tissue and lymphoid cells in patients with and without Crohn's disease and their therapeutic implications. Inflamm. Bowel Dis. 11:9 (2005), 820–827.
112. [112] Pond, C.M., Adipose tissue and the immune system. Prostaglandins Leukot. Essent. Fatty Acids 73:1 (2005), 17–30.
113. [113] Williams, K.E., et al. Urine, peritoneal fluid and omental fat proteomes of reproductive age women: endometriosis-related changes and associations with endocrine disrupting chemicals. J. Proteom. 113 (2015), 194–205.
114. [114] Pande, K., Moran, S.M., Bradfield, C.A., Aspects of dioxin toxicity are mediated by interleukin 1-like cytokines. Mol. Pharmacol. 67:5 (2005), 1393–1398.
115. [115] Vogel, C.F., et al. Modulation of the chemokines KC and MCP-1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice. Arch. Biochem. Biophys. 461:2 (2007), 169–175.
116. [116] Herington, J.L., et al. Immune interactions in endometriosis. Expert Rev. Clin. Immunol. 7:5 (2011), 611–626.
117. [117] Kobayashi, H., et al. Pathogenesis of endometriosis: the role of initial infection and subsequent sterile inflammation (Review). Mol. Med. Rep. 9:1 (2014), 9–15.
118. [118] Fortin, C.N., Saed, G.M., Diamond, M.P., Predisposing factors to post-operative adhesion development. Hum. Reprod. Update 21:4 (2015), 536–551.
119. [119] Herington, J.L., et al. Development and prevention of postsurgical adhesions in a chimeric mouse model of experimental endometriosis. Fertil. Steril. 95:4 (2011), 1295–1301 e1.
120. [120] Herington, J.L., et al. Dietary fish oil supplementation inhibits formation of endometriosis-associated adhesions in a chimeric mouse model. Fertil. Steril. 99:2 (2013), 543–550.
121. [121] Imudia, A.N., et al. Pathogenesis of Intra-abdominal and pelvic adhesion development. Semin. Reprod. Med. 26:4 (2008), 289–297.
122. [122] Zoghbi, H.Y., Beaudet, A.L., Epigenetics and human disease. Cold Spring Harb. Perspect. Biol., 8(2), 2016.
123. [123] Su, X., Wellen, K.E., Rabinowitz, J.D., Metabolic control of methylation and acetylation. Curr. Opin. Chem. Biol. 30 (2016), 52–60.
124. [124] Bai, H., et al. Genetic and epigenetic heterogeneity of epithelial ovarian cancer and the clinical implications for molecular targeted therapy. J. Cell. Mol. Med. 20 (2016), 581–593.
125. [125] Golabek, K., et al. Potential use of histone deacetylase inhibitors in cancer therapy. Contemp. Oncol. (Pozn.) 19:6 (2016), 436–440.
126. [126] Sinha, D., et al. Resveratrol for breast cancer prevention and therapy: preclinical evidence and molecular mechanisms. Semin. Cancer Biol., 2016 pii: S1044-579X(15)30001-8.
127. [127] Gabory, A., Attig, L., Junien, C., Epigenetic mechanisms involved in developmental nutritional programming. World J. Diabetes 2:10 (2011), 164–175.
128. [128] Morgan, H.D., et al. Epigenetic reprogramming in mammals. Hum. Mol. Genet. 14 (2005), R47–R58 Spec No. 1.
129. [129] Kim, J.J., et al. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol. Hum. Reprod. 13:5 (2007), 323–332.
130. [130] Naqvi, H., et al. Altered genome-wide methylation in endometriosis. Reprod. Sci. 21:10 (2014), 1237–1243.
131. [131] Wu, Y., et al. Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis. Fertil. Steril. 87:1 (2007), 24–32.
132. [132] Andersson, K.L., et al. DNA methylation of HOXA10 in eutopic and ectopic endometrium. Hum. Reprod. 29:9 (2014), 1906–1911.
133. [133] Xiaomeng, X., et al. Aberrant histone acetylation and methylation levels in woman with endometriosis. Arch. Gynecol. Obstet. 287:3 (2013), 487–494.
134. [134] Zidan, H.E., et al. COX-2 gene promoter DNA methylation status in eutopic and ectopic endometrium of Egyptian women with endometriosis. J. Reprod. Immunol. 112 (2015), 63–67.
135. [135] Dyson, M.T., et al. Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis. PLoS Genet., 10(3), 2014, e1004158.
136. [136] Kobayashi, H., et al. Understanding the role of epigenomic: genomic and genetic alterations in the development of endometriosis (review). Mol. Med. Rep. 9:5 (2014), 1483–1505.
137. [137] Dyson, M.T., et al. Aberrant expression and localization of deoxyribonucleic acid methyltransferase 3B in endometriotic stromal cells. Fertil. Steril. 104:4 (2015), 953–963 e2.
138. [138] Wu, Y., et al. Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics 1:2 (2006), 106–111.
139. [139] Saare, M., et al. The influence of menstrual cycle and endometriosis on endometrial methylome. Clin. Epigenet., 8, 2016, p2.
140. [140] Guerrero-Bosagna, C., Skinner, M.K., Environmentally induced epigenetic transgenerational inheritance of phenotype and disease. Mol. Cell. Endocrinol. 354:1–2 (2012), 3–8.
141. [141] Malassine, A., Frendo, J.L., Evain-Brion, D., A comparison of placental development and endocrine functions between the human and mouse model. Hum. Reprod. Update 9:6 (2003), 531–539.
142. [142] Seok, J., et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. U. S. A. 110:9 (2013), 3507–3512.
143. [143] Takao, K., Miyakawa, T., Genomic responses in mouse models greatly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. U. S. A. 112:4 (2015), 1167–1172.
144. [144] Eddie, S.L., et al. Microphysiological modeling of the reproductive tract: a fertile endeavor. Exp. Biol. Med. (Maywood) 239:9 (2014), 1192–1202.
145. [145] Young, E.W., Beebe, D.J., Fundamentals of microfluidic cell culture in controlled microenvironments. Chem. Soc. Rev. 39:3 (2010), 1036–1048.
146. [146] Wikswo, J.P., et al. Scaling and systems biology for integrating multiple organs-on-a-chip. Lab Chip 13:18 (2013), 3496–3511.
147. [147] Bruner, K.L., et al. Transforming growth factor beta mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium. Proc. Natl. Acad. Sci. U. S. A. 92:16 (1995), 7362–7366.
148. [148] Cunha, G.R., Cooke, P.S., Kurita, T., Role of stromal-epithelial interactions in hormonal responses. Arch. Histol. Cytol. 67:5 (2004), 417–434.
149. [149] Buchanan, D.L., et al. Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin in mouse uterus: critical role of the aryl hydrocarbon receptor in stromal tissue. Toxicol. Sci. 57:2 (2000), 302–311.
150. [150] Hutson, M.S., et al. Organs-on-chips as bridges for predictive toxicology. Appl. In Vitro Toxicol. 2 (2016), 97–101.
151. [151] Esch, M.B., King, T.L., Shuler, M.L., The role of body-on-a-chip devices in drug and toxicity studies. Annu. Rev. Biomed. Eng. 13 (2011), 55–72.
152. [152] Lantada, A.D., Morgado, P.L., García, P.O., Micro-manufacturing technologies for biodevices: interacting at a cellular scale. Lantada, A.D., (eds.) Handbook on Advanced Design and Manufacturing Technologies for Biomedical Devices, 2013, Springer Science & Business Media, 225–245.
153. [153] Bale, S.S., et al. In vitro platforms for evaluating liver toxicity. Exp. Biol. Med. (Maywood) 239:9 (2014), 1180–1191.
154. [154] Smith, G.D., Takayama, S., Swain, J.E., Rethinking in vitro embryo culture: new developments in culture platforms and potential to improve assisted reproductive technologies. Biol. Reprod., 86(3), 2012, 62.
155. [155] Swain, J.E., et al. Thinking big by thinking small: application of microfluidic technology to improve ART. Lab Chip 13:7 (2013), 1213–1224.
156. [156] Vogel, C., et al. Effect of subchronic 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on immune system and target gene responses in mice: calculation of benchmark doses for CYP1A1 and CYP1A2 related enzyme activities. Arch. Toxicol. 71:6 (1997), 372–382.
157. [157] Bruner-Tran, K.L., et al. Developmental exposure of mice to dioxin promotes transgenerational testicular inflammation and an increased risk of preterm birth in unexposed mating partners. PLoS One, 9(8), 2014, e105084.