Integrated bioinformatics, environmental epidemiologic and genomic approaches to identify environmental and molecular links between endometriosis and breast cancer

International Journal of Molecular Sciences

Volumn 16, Issue 10, 2015, Pages 25285-25322

  Roy, Deodutta ^a   Morgan, Marisa ^a   Yoo, Changwon ^a   Deoraj, Alok ^a   Roy, Sandhya ^b   Yadav, Vijay Kumar ^c   Garoub, Mohannad ^a   Assaggaf, Hamza ^a   Doke, Mayur ^a  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^b BMSNF Inc   (United States)

^c Department of Physics   (India)

Author keywords

Bioinformatics; Bisphenol A; Breast cancer; Endocrine disruptors; Endometriosis; Genomics; PCBs; Phthalates

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; B LYMPHOCYTE RECEPTOR; ENDOCRINE DISRUPTOR; GONADORELIN; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P53; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR; VASCULOTROPIN; AIR POLLUTANT; ESTROGEN;

ARTICLE; BIOINFORMATICS; BREAST CANCER; CANCER RISK; CANCER STAGING; DISEASE ASSOCIATION; ENDOMETRIOSIS; GENE INTERACTION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HUMAN; LAPAROSCOPY; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; AIR POLLUTANT; BREAST NEOPLASMS; FEMALE; GENETICS; HUMAN GENOME; META ANALYSIS; TOXICITY;

AIR POLLUTANTS; BREAST NEOPLASMS; ENDOCRINE DISRUPTORS; ENDOMETRIOSIS; ESTROGENS; FEMALE; GENOME, HUMAN; HUMANS;

EID: 84945268911     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161025285     Document Type: Article

References (73)

1. Evans, J.M. An Integrative Approach to Fibroids, Endometriosis, and Breast Cancer Prevention. Integr. Med. 2008, 7, 28–31.
2. Lin, B.C.; Suzawa, M.; Blind, R.D.; Tobias, S.C.; Bulun, S.E.; Scanlan, T.S.; Ingraham, H.A. Stimulating the GPR30 estrogen receptor with a novel tamoxifen analogue activates SF-1 and promotes endometrial cell proliferation. Cancer Res. 2009, 69, 5415–5423.
3. Bertelsen, L.; Mellemkjær, L.; Frederiksen, K.; Kjær, S.K.; Brinton, L.A.; Sakoda, L.C.; van Valkengoed, I.; Olsen, J.H. Risk for breast cancer among women with endometriosis. Int. J. Cancer 2007, 120, 1372–1375.
4. Roy, D.; Palangat, M.; Chen, C.; Thomas, R.D.; Colerangle, J.; Atkinson, A.; Yan, Z. Biochemical and molecular changes at the cellular level in response to exposure to environmental estrogen-like chemicals. J. Toxicol. Environ. Health Part A 1997, 50, 1–30.
5. Roy, J.R.; Chakraborty, S.; Chakraborty, T.R. Estrogen-like endocrine disrupting chemicals affecting puberty in humans—A review. Med. Sci. Monit. 2009, 15, RA137–RA145.
6. UNEP/WHO. In State of the science of endocrine disrupting chemicals—2012. Bergman, A., Heindel, J.J., Jobling, S., Kidd, K.A., Zoeller, R.T., Eds.; WHO Press: Geneva, Switzerland, 2013, pp. 1–272. Available online: http://unep.org/pdf/9789241505031_eng.pdf (accessed on 22 October 2015).
7. Munn, S.; Goumenou, M. Report of the Endocrine Disrupters—Expert Advisory Group (ED EAG): Key scientific issues relevant to the identification and characterization of endocrine disrupting substances. Palgrave: London, UK, 2013; pp. 1–34. Available online: https://ec.europa.eu/jrc/sites/default/files/lbna25919enn.pdf (accessed on 22 October 2015).
8. Buranatrevedh, S.; Roy, D. Occupational exposure to endocrine-disrupting pesticides and the potential for developing hormonal cancers. J. Environ. Health 2001, 64, 17–29.
9. Liehr, J.G.; Somasunderan, A.; Roy, D. Natural and anthropogenic environmental estrogens: The scientific basis for risk assessment: Metabolism and fate of xeno-oestrogens in man. Pure Appl. Chem. 1998, 70, 1747–1758.
10. Calafat, A.M.; Wise, L.A.; Weuve, J.L.; Hauser, R.B.; Missmer, S.A. Association of exposure to phthalates with endometriosis and uterine leiomyomata: Findings from NHANES, 1999–2004. Environ. Health Perspect. 2010, 118, 825–832
11. Silva, M.J.; Barr, D.B.; Reidy, J.A.; Malek, N.A.; Hodge, C.C.; Caudill, S.P.; Brock, J.W.; Needham, L.L.; Calafat, A.M. Urinary levels of seven phthalate metabolites in the U.S. population from the National Health and Nutrition Examination Survey (NHANES) 1999–2000. Environ. Health Perspect. 2004, 112, 331–338.
12. Woodruff, T.J.; Zota, A.R.; Schwartz, J.M. Environmental Chemicals in Pregnant Women in the United States: NHANES 2003–2004. Environ. Health Perspect. 2011, 119, 878–885.
13. Fielden, M.R.; Halgren, R.G.; Tashiro, C.H.; Yeo, B.R.; Chittim, B.; Chou, K.; Zacharewski, T.R. Effects of gestational and lactational exposure to Aroclor 1242 on sperm quality and in vitro fertility in early adult and middle-aged mice. Reprod. Toxicol. 2001, 15, 281–292.
14. Ma, R.; Sassoon, D.A. PCBs exert an estrogenic effect through repression of the Wnt7a signaling pathway in the female reproductive tract. Environ. Health Perspect. 2006, 114, 898–904.
15. Rier, S.E.; Turner, W.E.; Martin, D.C.; Morris, R.; Lucier, G.W.; Clark, G.C. 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. 2001, 59, 147–159.
16. Moral, R.; Wang, R.; Russo, I.H.; Lamartiniere, C.A.; Pereira, J.; Russo, J. Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. J. Endocrinol. 2008, 196, 101–112.
17. Atkinson, A.; Roy, D. In vivo DNA adduct formation by bisphenol A. Environ. Mol. Mutagen. 1995, 26, 60–66.
18. Cabaton, N.J.; Wadia, P.R.; Rubin, B.S.; Zalko, D.; Schaeberle, C.M.; Askenase, M.H.; Gadbois, J.L.; Tharp, A.P.; Whitt, G.S.; Sonnenschein, C. Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ. Health Perspect. 2011, 119, 547–552.
19. Colerangle, J.B.; Roy, D. Profound effects of the weak environmental estrogen-like chemical bisphenol A on the growth of the mammary gland of Noble rats. J. Steroid Biochem. Mol. Biol. 1997, 60, 153–160.
20. Muñoz-de-Toro, M.; Markey, C.M.; Wadia, P.R.; Luque, E.H.; Rubin, B.S.; Sonnenschein, C.; Soto, A.M. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 2005, 146, 4138–4147.
21. Murray, T.J.; Maffini, M.V.; Ucci, A.A.; Sonnenschein, C.; Soto, A.M. Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reprod. Toxicol. 2007, 23, 383–390.
22. Newbold, R.R.; Jefferson, W.N.; Padilla-Banks, E. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod. Toxicol. 2007, 24, 253–258.
23. Signorile, P.G.; Spugnini, E.P.; Mita, L.; Mellone, P.; D’Avino, A.; Bianco, M.; Diano, N.; Caputo, L.; Rea, F.; Viceconte, R. Pre-natal exposure of mice to bisphenol A elicits an endometriosis-like phenotype in female offspring. Gen. Comp. Endocrinol. 2010, 168, 318–325.
24. Charlier, C.J.; Albert, A.I.; Zhang, L.; Dubois, N.G.; Plomteux, G.J. Polychlorinated biphenyls contamination in women with breast cancer. Clin. Chim. Acta 2004, 347, 177–181.
25. Cohn, B.A.; Terry, M.B.; Plumb, M.; Cirillo, P.M. Exposure to polychlorinated biphenyl (PCB) congeners measured shortly after giving birth and subsequent risk of maternal breast cancer before age 50. Breast Cancer Res. Treat. 2012, 136, 267–275.
26. Demers, A.; Ayotte, P.; Brisson, J.; Dodin, S.; Robert, J.; Dewailly, E. Plasma concentrations of polychlorinated biphenyls and the risk of breast cancer: A congener-specific analysis. Am. J. Epidemiol. 2002, 155, 629–635.
27. Gammon, M.D.; Wolff, M.S.; Neugut, A.I.; Eng, S.M.; Teitelbaum, S.L.; Britton, J.A.; Terry, M.B.; Levin, B.; Stellman, S.D.; Kabat, G.C. et al. Environmental toxins and breast cancer on Long Island. II. Organochlorine compound levels in blood. Cancer Epidemiol. Biomark. Prev. 2002, 11, 686–697.
28. Gatto, N.M.; Longnecker, M.P.; Press, M.F.; Sullivan-Halley, J.; McKean-Cowdin, R.; Bernstein, L. Serum organochlorines and breast cancer: A case–control study among African-American women. Cancer Causes Control 2007, 18, 29–39.
29. Itoh, H.; Iwasaki, M.; Hanaoka, T.; Kasuga, Y.; Yokoyama, S.; Onuma, H.; Nishimura, H.; Kusama, R.; Tsugane, S. Serum organochlorines and breast cancer risk in Japanese women: A case–control study. Cancer Causes Control 2009, 20, 567–580.
30. López-Carrillo, L.; Hernández-Ramírez, R.U.; Calafat, A.M.; Torres-Sánchez, L.; Galván-Portillo, M.; Needham, L.L.; Ruiz-Ramos, R.; Cebrián, M.E. Exposure to phthalates and breast cancer risk in northern Mexico. Environ. Health Perspect. 2010, 118, 539–544.
31. Pavuk, M.; Cerhan, J.R.; Lynch, C.F.; Kocan, A.; Petrik, J.; Chovancova, J. Case–control study of PCBs, other organochlorines and breast cancer in Eastern Slovakia. J. Exp. Sci. Environ. Epidemiol. 2003, 13, 267–275.
32. Recio-Vega, R.; Velazco-Rodriguez, V.; Ocampo-Gómez, G.; Hernandez-Gonzalez, S.; Ruiz-Flores, P.; Lopez-Marquez, F. Serum levels of polychlorinated biphenyls in Mexican women and breast cancer risk. J. Appl. Toxicol. 2011, 31, 270–278.
33. Wolff, M.S.; Zeleniuch-Jacquotte, A.; Dubin, N.; Toniolo, P. Risk of breast cancer and organochlorine exposure. Cancer Epidemiol. Biomark. Prev. 2000, 9, 271–277.
34. Yang, M.; Ryu, J.; Jeon, R.; Kang, D.; Yoo, K. Effects of bisphenol A on breast cancer and its risk factors. Arch. Toxicol. 2009, 83, 281–285.
35. Millikan, R.; DeVoto, E.; Duell, E.J.; Tse, C.K.; Savitz, D.A.; Beach, J.; Edmiston, S.; Jackson, S.; Newman, B. Dichlorodiphenyldichloroethene, polychlorinated biphenyls, and breast cancer among African-American and white women in North Carolina. Cancer Epidemiol. Biomark. Prev. 2000, 9, 1233–1240.
36. Louis, G.M.; Weiner, J.M.; Whitcomb, B.W.; Sperrazza, R.; Schisterman, E.F.; Lobdell, D.T.; Crickard, K.; Greizerstein, H.; Kostyniak, P.J. Environmental PCB exposure and risk of endometriosis. Hum. Reprod. 2005, 20, 279–285.
37. Reddy, B.S.; Rozati, R.; Reddy, S.; Kodampur, S.; Reddy, P.; Reddy, R. High plasma concentrations of polychlorinated biphenyls and phthalate esters in women with endometriosis: A prospective case control study. Fertil. Steril. 2006, 85, 775–779.
38. Heilier, J.; Nackers, F.; Verougstraete, V.; Tonglet, R.; Lison, D.; Donnez, J. Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometriotic (adenomyotic) nodules. Fertil. Steril. 2005, 84, 305–312.
39. Kim, S.H.; Chun, S.; Jang, J.Y.; Chae, H.D.; Kim, C.; Kang, B.M. Increased plasma levels of phthalate esters in women with advanced-stage endometriosis: A prospective case-control study. Fertil. Steril. 2011, 95, 357–359.
40. Niskar, A.S.; Needham, L.L.; Rubin, C.; Turner, W.E.; Martin, C.A.; Patterson, D.G.; Hasty, L.; Wong, L.; Marcus, M. Serum dioxins, polychlorinated biphenyls, and endometriosis: A case-control study in Atlanta. Chemosphere 2009, 74, 944–949.
41. Pauwels, A.; Schepens, P.J.; D’Hooghe, T.; Delbeke, L.; Dhont, M.; Brouwer, A.; Weyler, J. The risk of endometriosis and exposure to dioxins and polychlorinated biphenyls: A case-control study of infertile women. Hum. Reprod. 2001, 16, 2050–2055.
42. Porpora, M.G.; Medda, E.; Abballe, A.; Bolli, S.; de Angelis, I.; di Domenico, A.; Ferro, A.; Ingelido, A.M.; Maggi, A.; Panici, P.B. Endometriosis and organochlorinated environmental pollutants: A case-control study on Italian women of reproductive age. Environ. Health Perspect. 2009, 117, 1070–1075.
43. Trabert, B.; de Roos, A.J.; Schwartz, S.M.; Peters, U.; Scholes, D.; Barr, D.B.; Holt, V.L. Non-dioxin-like polychlorinated biphenyls and risk of endometriosis. Environ. Health Perspect. 2010, 118, 1280–1285.
44. Tsukino, H.; Hanaoka, T.; Sasaki, H.; Motoyama, H.; Hiroshima, M.; Tanaka, T.; Kabuto, M.; Niskar, A.S.; Rubin, C.; Patterson, D.G. Associations between serum levels of selected organochlorine compounds and endometriosis in infertile Japanese women. Environ. Res. 2005, 99, 118–125.
45. Upson, K.; Sathyanarayana, S.; de Roos, A.J.; Thompson, M.L.; Scholes, D.; Dills, R.; Holt, V.L. Phthalates and risk of endometriosis. Environ. Res. 2013, 126, 91–97.
46. Louis, G.M.B.; Peterson, C.M.; Chen, Z.; Croughan, M.; Sundaram, R.; Stanford, J.; Varner, M.W.; Kennedy, A.; Giudice, L.; Fujimoto, V.Y. Bisphenol a and phthalates and endometriosis: The endometriosis: Natural history, diagnosis and outcomes study. Fertil. Steril. 2013, 100, 162–169. e2.
47. Cobellis, L.; Latini, G.; de Felice, C.; Razzi, S.; Paris, I.; Ruggieri, F.; Mazzeo, P.; Petraglia, F. High plasma concentrations of di-(2-ethylhexyl)-phthalate in women with endometriosis. Hum. Reprod. 2003, 18, 1512–1515.
48. Huang, P.C.; Tsai, E.M.; Li, W.F.; Liao, P.C.; Chung, M.C.; Wang, Y.H.; Wang, S.L. Association between phthalate exposure and glutathione S-transferase M1 polymorphism in adenomyosis, leiomyoma and endometriosis. Hum. Reprod. 2010, 25, 986–994.
49. Itoh, H.; Iwasaki, M.; Nakajima, Y.; Endo, Y.; Hanaoka, T.; Sasaki, H.; Tanaka, T.; Yang, B.; Tsugane, S. A case-control study of the association between urinary cadmium concentration and endometriosis in infertile Japanese women. Sci. Total Environ. 2008, 402, 171–175.
50. Reddy, B.; Rozati, R.; Reddy, B.; Raman, N. Association of phthalate esters with endometriosis in Indian women. Int. J. Obstet. Gynaecol. 2006, 113, 515–520.
51. Itoh, H.; Iwasaki, M.; Hanaoka, T.; Sasaki, H.; Tanaka, T.; Tsugane, S. Urinary bisphenol-A concentration in infertile Japanese women and its association with endometriosis: A cross-sectional study. Environ. Health Prev. Med. 2007, 12, 258–264.
52. De, S.; Ghosh, S.; Chatterjee, R.; Chen, Y.; Moses, L.; Kesari, A.; Hoffman, E.P.; Dutta, S.K. PCB congener specific oxidative stress response by microarray analysis using human liver cell line. Environ. Int. 2010, 36, 907–917.
53. Burney, R.O.; Talbi, S.; Hamilton, A.E.; Vo, K.C.; Nyegaard, M.; Nezhat, C.R.; Lessey, B.A.; Giudice, L.C. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 2007, 148, 3814–3826.
54. Hever, A.; Roth, R.B.; Hevezi, P.; Marin, M.E.; Acosta, J.A.; Acosta, H.; Rojas, J.; Herrera, R.; Grigoriadis, D.; White, E. et al. Human endometriosis is associated with plasma cells and overexpression of B lymphocyte stimulator. Proc. Natl. Acad. Sci. USA 2007, 104, 12451–12456.
55. Sha, G.; Wu, D.; Zhang, L.; Chen, X.; Lei, M.; Sun, H.; Lin, S.; Lang, J. Differentially expressed genes in human endometrial endothelial cells derived from eutopic endometrium of patients with endometriosis compared with those from patients without endometriosis. Hum. Reprod. 2007, 22, 3159–3169.
56. Spirtes, P.; Glymour, C.N.; Scheines, R. Causation, Prediction, and Search. Adaptive Computation and Machine Learning; MIT Press: Cambridge, MA, USA, 2000.
57. Melin, A.; Sparen, P.; Bergqvist, A. The risk of cancer and the role of parity among women with endometriosis. Hum. Reprod. 2007, 22, 3021–3026.
58. Irahara, N.; Miyoshi, Y.; Taguchi, T.; Tamaki, Y.; Noguchi, S. Quantitative analysis of aromatase mRNA expression derived from various promoters (I. 4, I. 3, PII and I. 7) and its association with expression of TNF-α, IL-6 and COX-2 mRNAs in human breast cancer. Int. J. Cancer 2006, 118, 1915–1921.
59. Roy, D.; Colerangle, J.B.; Singh, K.P. Is exposure to environmental or industrial endocrine disrupting estrogen-like chemicals able to cause genomic instability? Front. Biosci. 1998, 3, d913–d928.
60. Roy, D.; Cai, Q.; Felty, Q.; Narayan, S. Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers. J. Toxicol. Environ. Health Part B 2007, 10, 235–257.
61. Fernández, M.F.; Santa-Marina, L.; Olea-Serrano, M.F.; Rivas, A.M.; Aurrekoetxea, J.J.; Expósito, J.; Lorenzo, M.; Torné, P.; Villalobos, M.; Pedraza, V. Breast cancer risk and the combined effect of environmental estrogens. Cancer Causes Control 2004, 15, 591–600.
62. Palmer, J.R.; Wise, L.A.; Hatch, E.E.; Troisi, R.; Titus-Ernstoff, L.; Strohsnitter, W.; Kaufman, R.; Herbst, A.L.; Noller, K.L.; Hyer, M. et al. Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol. Biomark. Prev. 2006, 15, 1509–1514.
63. Treeck, O.; Elemenler, E.; Kriener, C.; Horn, F.; Springwald, A.; Hartmann, A.; Ortmann, O. Polymorphisms in the promoter region of ESR2 gene and breast cancer susceptibility. J. Steroid Biochem. Mol. Biol. 2009, 114, 207–211.
64. Xue, Q.; Lin, Z.; Cheng, Y.H.; Huang, C.C.; Marsh, E.; Yin, P.; Milad, M.P.; Confino, E.; Reierstad, S.; Innes, J. et al. Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol. Reprod. 2007, 77, 681–687.
65. Bulun, S.E. Endometriosis. N. Engl. J. Med. 2009, 360, 268–279.
66. Al-Zahrani, A.; Sandhu, M.S.; Luben, R.N.; Thompson, D.; Baynes, C.; Pooley, K.A.; Luccarini, C.; Munday, H.; Perkins, B.; Smith, P. et al. IGF1 and IGFBP3 tagging polymorphisms are associated with circulating levels of IGF1, IGFBP3 and risk of breast cancer. Hum. Mol. Genet. 2006, 15, 1–10.
67. Raulic, S.; Ramos-Valdes, Y.; DiMattia, G.E. Stanniocalcin 2 expression is regulated by hormone signalling and negatively affects breast cancer cell viability in vitro. J. Endocrinol. 2008, 197, 517–529.
68. Wood, C.E.; Kaplan, J.R.; Fontenot, M.B.; Williams, J.K.; Cline, J.M. Endometrial profile of tamoxifen and low-dose estradiol combination therapy. Clin. Cancer Res. 2010, 16, 946–956.
69. Gruvberger, S.; Ringner, M.; Chen, Y.; Panavally, S.; Saal, L.H.; Borg, A.; Ferno, M.; Peterson, C.; Meltzer, P.S. Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res. 2001, 61, 5979–5984.
70. Modugno, F.; Ness, R.B.; Chen, C.; Weiss, N.S. Inflammation and endometrial cancer: A hypothesis. Cancer Epidemiol. Biomark. Prev. 2005, 14, 2840–2847.
71. Kunkle, B.; Bae, S.; Singh, K.P.; Roy, D. Increased risk of childhood brain tumors among children whose parents had farm related pesticide exposures during pregnancy. JP J. Biostat. 2014, 11, 89–101.
72. Kunkle, B.; Yoo, C.; Roy, D. Discovering gene–environment interactions in Glioblastoma through a comprehensive data integration bioinformatics method. Neurotoxicology 2013, 35, 1–14.
73. Kunkle, B.; Yoo, C.; Roy, D. Reverse engineering of modified genes by bayesian network analysis defines molecular determinants critical to the development of glioblastoma. PLoS ONE 2013, 8, e64140.