Environmental epigenetics and phytoestrogen/phytochemical exposures

Journal of Steroid Biochemistry and Molecular Biology

Volumn 139, Issue , 2014, Pages 270-276

  Guerrero Bosagna, Carlos M ^a   Skinner, Michael K ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Environmental exposures; Epigenetics; Phytochemicals; Phytoestrogens; Review; Transgenerational

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; AGLYCONE; BUTYL PARABEN; COUMESTROL; DAIDZEIN; DIETHYLSTILBESTROL; DIOXIN; FLAVONOID; FOLLITROPIN; GENISTEIN; ISOFLAVONE; LIGNAN; LUTEINIZING HORMONE; PHTHALIC ACID; PHYTOESTROGEN; PLANT MEDICINAL PRODUCT; QUERCETIN; RESVERATROL; STEROIDOGENIC FACTOR 1; VINCLOZOLIN;

APOPTOSIS; BLOOD PLACENTA BARRIER; BREAST MILK; CALORIC RESTRICTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA METHYLATION; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; HYPOSPADIAS; INHERITANCE; LIPID DIET; METABOLIC DISORDER; MOLECULAR INTERACTION; NONHUMAN; OBESITY; OVARY FOLLICLE; PHENOTYPE; PHYTOCHEMISTRY; PRECOCIOUS PUBERTY; PRENATAL EXPOSURE; REVIEW; SEXUAL AROUSAL; SEXUAL MATURATION; SEXUAL SELECTION; SPERMATOCYTE; TUMOR SUPPRESSOR GENE; UTERUS MALFORMATION; UTERUS MYOMA;

ENVIRONMENTAL EXPOSURES; EPIGENETICS; PHYTOCHEMICALS; PHYTOESTROGENS; REVIEW; TRANSGENERATIONAL;

ANIMALS; DIET; ENDOCRINE DISRUPTORS; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; EPIGENOMICS; EVOLUTION, MOLECULAR; GENE-ENVIRONMENT INTERACTION; HUMANS; PHYTOESTROGENS;

EID: 84889877875     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2012.12.011     Document Type: Review

References (111)

1. T.T. Schug, A. Janesick, B. Blumberg, and J.J. Heindel Endocrine disrupting chemicals and disease susceptibility Journal of Steroid Biochemistry and Molecular Biology 127 3-5 2011 204 215
2. D. Balabanic, M. Rupnik, and A.K. Klemencic Negative impact of endocrine-disrupting compounds on human reproductive health Reproduction, Fertility, and Development 23 3 2011 403 416
3. D. Caserta, A. Mantovani, R. Marci, A. Fazi, F. Ciardo, C. La Rocca, F. Maranghi, and M. Moscarini Environment and women's reproductive health Human Reproduction Update 17 3 2011 418 433
4. P.A. Fowler, M. Bellingham, K.D. Sinclair, N.P. Evans, P. Pocar, B. Fischer, K. Schaedlich, J.S. Schmidt, M.R. Amezaga, S. Bhattacharya, S.M. Rhind, and P.J. O'Shaughnessy Impact of endocrine-disrupting compounds (EDCs) on female reproductive health Molecular and Cellular Endocrinology 355 2 2012 231 239
5. C.R. Cederroth, C. Zimmermann, and S. Nef Soy, phytoestrogens and their impact on reproductive health Molecular and Cellular Endocrinology 355 2 2012 192 200
6. R. Croteau, T. Kutchan, and N. Lewis Natural products (secondary metabolites) W.G.B. Buchanan, R. Jones, Biochemistry and Molecular Biology of the Plants 2000 Courier Companies, Inc Somerset, NJ 1250 1318
7. O. Yu, W. Jung, J. Shi, R.A. Croes, G.M. Fader, B. McGonigle, and J.T. Odell Production of the isoflavones genistein and daidzein in non-legume dicot and monocot tissues Plant Physiology 124 2 2000 781 794
8. J. Liggins, L.J. Bluck, S. Runswick, C. Atkinson, W.A. Coward, and S.A. Bingham Daidzein and genistein content of fruits and nuts Journal of Nutritional Biochemistry 11 6 2000 326 331
9. E.K. Shanle, and W. Xu Endocrine disrupting chemicals targeting estrogen receptor signaling: identification and mechanisms of action Chemical Research in Toxicology 24 1 2011 6 19
10. J.A. McLachlan Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals Endocrine Reviews 22 3 2001 319 341 (Pubitemid 32554362)
11. O. Kutuk, D. Telci, and H. Basaga Lipid peroxidation, gene expression and resveratol: implications in atherosclerosis M. Meskin, W. Bidlack, K. Randolph, Phytochemicals: Nutrient-Gene Interactions 2006 Taylor and Francis group Boca Raton, FL
12. J.W. Erdman Jr., T.M. Badger, J.W. Lampe, K.D. Setchell, and M. Messina Not all soy products are created equal: caution needed in interpretation of research results Journal of Nutrition 134 5 2004 1229S 1233S (Pubitemid 38619969)
13. N.R. Adams A changed responsiveness to oestrogen in ewes with clover disease Journal of Reproduction and Fertility Supplement 30 1981 223 230 (Pubitemid 12190812)
14. N.R. Adams Permanent infertility in ewes exposed to plant oestrogens Australian Veterinary Journal 67 6 1990 197 201
15. N.R. Adams Detection of the effects of phytoestrogens on sheep and cattle Journal of Animal Science 73 5 1995 1509 1515
16. K.D. Setchell, S.J. Gosselin, M.B. Welsh, J.O. Johnston, W.F. Balistreri, L.W. Kramer, B.L. Dresser, and M.J. Tarr Dietary estrogens - a probable cause of infertility and liver disease in captive cheetahs Gastroenterology 93 2 1987 225 233 (Pubitemid 17097584)
17. W.N. Jefferson, H.B. Patisaul, and C.J. Williams Reproductive consequences of developmental phytoestrogen exposure Reproduction 143 3 2012 247 260
18. D. Gallo, F. Cantelmo, M. Distefano, C. Ferlini, G.F. Zannoni, A. Riva, P. Morazzoni, E. Bombardelli, S. Mancuso, and G. Scambia Reproductive effects of dietary soy in female Wistar rats Food and Chemical Toxicology 37 5 1999 493 502 (Pubitemid 29306914)
19. C.M. Guerrero-Bosagna, P. Sabat, F.S. Valdovinos, L.E. Valladares, and S.J. Clark Epigenetic and phenotypic changes result from a continuous pre and post natal dietary exposure to phytoestrogens in an experimental population of mice BMC Physiology 8 2008 17
20. R.C. Santell, Y.C. Chang, M.G. Nair, and W.G. Helferich Dietary genistein exerts estrogenic effects upon the uterus, mammary gland and the hypothalamic/pituitary axis in rats Journal of Nutrition 127 2 1997 263 269 (Pubitemid 27079955)
21. F.J. Moller, P. Diel, O. Zierau, T. Hertrampf, J. Maass, and G. Vollmer Long-term dietary isoflavone exposure enhances estrogen sensitivity of rat uterine responsiveness mediated through estrogen receptor alpha Toxicology Letters 196 3 2010 142 153
22. F.J. Moller, O. Zierau, T. Hertrampf, A. Bliedtner, P. Diel, and G. Vollmer Long-term effects of dietary isoflavones on uterine gene expression profiles Journal of Steroid Biochemistry and Molecular Biology 113 3-5 2009 296 303
23. K. Takashima-Sasaki, M. Komiyama, T. Adachi, K. Sakurai, H. Kato, T. Iguchi, and C. Mori Effect of exposure to high isoflavone-containing diets on prenatal and postnatal offspring mice Bioscience, Biotechnology, and Biochemistry 70 12 2006 2874 2882 (Pubitemid 46021544)
24. W.N. Jefferson, and C.J. Williams Circulating levels of genistein in the neonate, apart from dose and route, predict future adverse female reproductive outcomes Reproductive Toxicology 31 3 2011 272 279
25. T. Hertrampf, C. Ledwig, S. Kulling, A. Molzberger, F.J. Moller, O. Zierau, G. Vollmer, S. Moors, G.H. Degen, and P. Diel Responses of estrogen sensitive tissues in female Wistar rats to pre- and postnatal isoflavone exposure Toxicology Letters 191 2-3 2009 181 188
26. M.G. Wade, A. Lee, A. McMahon, G. Cooke, and I. Curran The influence of dietary isoflavone on the uterotrophic response in juvenile rats Food and Chemical Toxicology 41 11 2003 1517 1525 (Pubitemid 37088107)
27. H. Boettger-Tong, L. Murthy, C. Chiappetta, J.L. Kirkland, B. Goodwin, H. Adlercreutz, G.M. Stancel, and S. Makela A case of a laboratory animal feed with high estrogenic activity and its impact on in vivo responses to exogenously administered estrogens Environmental Health Perspectives 106 7 1998 369 373 (Pubitemid 28524101)
28. M.N. Jensen, and M. Ritskes-Hoitinga How isoflavone levels in common rodent diets can interfere with the value of animal models and with experimental results Laboratory Animals 41 1 2007 1 18 (Pubitemid 46174423)
29. J.E. Thigpen, K.D. Setchell, E. Padilla-Banks, J.K. Haseman, H.E. Saunders, G.F. Caviness, G.E. Kissling, M.G. Grant, and D.B. Forsythe Variations in phytoestrogen content between different mill dates of the same diet produces significant differences in the time of vaginal opening in CD-1 mice and F344 rats but not in CD Sprague-Dawley rats Environmental Health Perspectives 115 12 2007 1717 1726
30. H. Wang, S. Tranguch, H. Xie, G. Hanley, S.K. Das, and S.K. Dey Variation in commercial rodent diets induces disparate molecular and physiological changes in the mouse uterus Proceedings of the National Academy of Sciences of the United States of America 102 28 2005 9960 9965 (Pubitemid 40993675)
31. M.H. Traka, and R.F. Mithen Plant science and human nutrition: challenges in assessing health-promoting properties of phytochemicals Plant Cell 23 7 2011 2483 2497
32. G. McCarver, J. Bhatia, C. Chambers, R. Clarke, R. Etzel, W. Foster, P. Hoyer, J.S. Leeder, J.M. Peters, E. Rissman, M. Rybak, C. Sherman, J. Toppari, and K. Turner NTP-CERHR expert panel report on the developmental toxicity of soy infant formula Birth Defects Research. Part B, Developmental and Reproductive Toxicology 92 5 2011 421 468
33. M.S. Kurzer, and X. Xu Dietary phytoestrogens Annual Review of Nutrition 17 1997 353 381 (Pubitemid 27328805)
34. A.A. Mulligan, A.A. Welch, A.A. McTaggart, A. Bhaniani, and S.A. Bingham Intakes and sources of soya foods and isoflavones in a UK population cohort study (EPIC-Norfolk) European Journal of Clinical Nutrition 61 2 2007 248 254
35. M.S. Morton, O. Arisaka, N. Miyake, L.D. Morgan, and B.A. Evans Phytoestrogen concentrations in serum from Japanese men and women over forty years of age Journal of Nutrition 132 10 2002 3168 3171
36. M.A. van Erp-Baart, H.A. Brants, M. Kiely, A. Mulligan, A. Turrini, C. Sermoneta, A. Kilkkinen, and L.M. Valsta Isoflavone intake in four different European countries: the VENUS approach British Journal of Nutrition 89 Suppl 1 2003 S25 S30
37. A. Cassidy, J.E. Brown, A. Hawdon, M.S. Faughnan, L.J. King, J. Millward, L. Zimmer-Nechemias, B. Wolfe, and K.D. Setchell Factors affecting the bioavailability of soy isoflavones in humans after ingestion of physiologically relevant levels from different soy foods Journal of Nutrition 136 1 2006 45 51 (Pubitemid 43156483)
38. G.G. Kuiper, J.G. Lemmen, B. Carlsson, J.C. Corton, S.H. Safe, P.T. van der Saag, B. van der Burg, and J.A. Gustafsson Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta Endocrinology 139 10 1998 4252 4263 (Pubitemid 28513713)
39. T. Oseni, R. Patel, J. Pyle, and V.C. Jordan Selective estrogen receptor modulators and phytoestrogens Planta Medica 74 13 2008 1656 1665
40. M. Du, X. Yang, J.A. Hartman, P.S. Cooke, D.R. Doerge, Y.H. Ju, and W.G. Helferich Low-dose dietary genistein negates the therapeutic effect of tamoxifen in athymic nude mice Carcinogenesis 33 4 2012 895 901
41. A. Kortenkamp Ten years of mixing cocktails: a review of combination effects of endocrine-disrupting chemicals Environmental Health Perspectives 115 Suppl 1 2007 98 105
42. E. Silva, N. Rajapakse, and A. Kortenkamp Something from "nothing" - eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects Environmental Science and Technology 36 8 2002 1751 1756 (Pubitemid 34310943)
43. R.C. Habito, J. Montalto, E. Leslie, and M.J. Ball Effects of replacing meat with soyabean in the diet on sex hormone concentrations in healthy adult males British Journal of Nutrition 84 4 2000 557 563
44. C. Nagata, N. Takatsuka, H. Shimizu, H. Hayashi, T. Akamatsu, and K. Murase Effect of soymilk consumption on serum estrogen and androgen concentrations in Japanese men Cancer Epidemiology, Biomarkers and Prevention 10 3 2001 179 184 (Pubitemid 34288527)
45. K. Wada, K. Nakamura, T. Masue, Y. Sahashi, K. Ando, and C. Nagata Soy intake and urinary sex hormone levels in preschool Japanese children American Journal of Epidemiology 173 9 2011 998 1003
46. L. Hooper, J.J. Ryder, M.S. Kurzer, J.W. Lampe, M.J. Messina, W.R. Phipps, and A. Cassidy Effects of soy protein and isoflavones on circulating hormone concentrations in pre- and post-menopausal women: a systematic review and meta-analysis Human Reproduction Update 15 4 2009 423 440
47. A.M. Pino, L.E. Valladares, M.A. Palma, A.M. Mancilla, M. Yanez, and AlbalaF C. Dietary isoflavones affect sex hormone-binding globulin levels in postmenopausal women Journal of Clinical Endocrinology and Metabolism 85 8 2000 2797 2800 (Pubitemid 32269154)
48. J. Kim, S. Kim, K. Huh, Y. Kim, H. Joung, and M. Park High serum isoflavone concentrations are associated with the risk of precocious puberty in Korean girls Clinical Endocrinology 75 6 2011 831 835
49. A. Amsterdam, N. Abu-Rustum, J. Carter, and M. Krychman Persistent sexual arousal syndrome associated with increased soy intake Journal of Sexual Medicine 2 3 2005 338 340 (Pubitemid 40744373)
50. A.A. D'Aloisio, D.D. Baird, L.A. DeRoo, and D.P. Sandler Association of intrauterine and early-life exposures with diagnosis of uterine leiomyomata by 35 years of age in the Sister Study Environmental Health Perspectives 118 3 2010 375 381
51. A. Chandrareddy, O. Muneyyirci-Delale, S.I. McFarlane, and O.M. Murad Adverse effects of phytoestrogens on reproductive health: a report of three cases Complementary Therapies in Medicine 14 2 2008 132 135
52. K. North, and J. Golding A maternal vegetarian diet in pregnancy is associated with hypospadias. The ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood BJU International 85 1 2000 107 113
53. J.E. Chavarro, T.L. Toth, S.M. Sadio, and R. Hauser Soy food and isoflavone intake in relation to semen quality parameters among men from an infertility clinic Human Reproduction 23 11 2008 2584 2590
54. M. Cotterchio, B.A. Boucher, M. Manno, S. Gallinger, A. Okey, and P. Harper Dietary phytoestrogen intake is associated with reduced colorectal cancer risk Journal of Nutrition 136 12 2006 3046 3053 (Pubitemid 44878571)
55. J. Thanos, M. Cotterchio, B.A. Boucher, N. Kreiger, and L.U. Thompson Adolescent dietary phytoestrogen intake and breast cancer risk (Canada) Cancer Causes and Control 17 10 2006 1253 1261 (Pubitemid 44772825)
56. S.A. Lee, X.O. Shu, H. Li, G. Yang, H. Cai, W. Wen, B.T. Ji, J. Gao, Y.T. Gao, and W. Zheng Adolescent and adult soy food intake and breast cancer risk: results from the Shanghai Women's Health Study American Journal of Clinical Nutrition 89 6 2009 1920 1926
57. A. Warri, N.M. Saarinen, S. Makela, and L. Hilakivi-Clarke The role of early life genistein exposures in modifying breast cancer risk British Journal of Cancer 98 9 2008 1485 1493 (Pubitemid 351652325)
58. T.G. McEvoy, J.J. Robinson, C.J. Ashworth, J.A. Rooke, and K.D. Sinclair Feed and forage toxicants affecting embryo survival and fetal development Theriogenology 55 1 2001 113 129 (Pubitemid 32060567)
59. M. Clark, and B. Galef Perinatal influences on the reproductive behavior of adult rodents T.A. Mousseau, C.W. Fox, Maternal Effects as Adaptations 1998 Oxford University Press New York, NY 261 271
60. D.R. Doerge Bioavailability of soy isoflavones through placental/lactational transfer and soy food Toxicology and Applied Pharmacology 254 2 2011 145 147
61. D.R. Doerge, M.I. Churchwell, H.C. Chang, R.R. Newbold, and K.B. Delclos Placental transfer of the soy isoflavone genistein following dietary and gavage administration to Sprague-Dawley rats Reproductive Toxicology 15 2 2001 105 110 (Pubitemid 32377801)
62. P. Diel, T. Hertrampf, J. Seibel, U. Laudenbach-Leschowsky, S. Kolba, and G. Vollmer Combinatorial effects of the phytoestrogen genistein and of estradiol in uterus and liver of female Wistar rats Journal of Steroid Biochemistry and Molecular Biology 102 1-5 2006 60 70 (Pubitemid 44781188)
63. C.L. Hughes, G. Liu, S. Beall, W.G. Foster, and V. Davis Effects of genistein or soy milk during late gestation and lactation on adult uterine organization in the rat Experimental Biology and Medicine (Maywood) 229 1 2004 108 117 (Pubitemid 38101685)
64. W.N. Jefferson, E. Padilla-Banks, E.H. Goulding, S.P. Lao, R.R. Newbold, and C.J. Williams Neonatal exposure to genistein disrupts ability of female mouse reproductive tract to support preimplantation embryo development and implantation Biology of Reproduction 80 3 2009 425 431
65. A.A. Franke, B.M. Halm, L.J. Custer, Y. Tatsumura, and S. Hebshi Isoflavones in breastfed infants after mothers consume soy American Journal of Clinical Nutrition 84 2 2006 406 413 (Pubitemid 44699153)
66. D.R. Doerge, N.C. Twaddle, M.I. Churchwell, R.R. Newbold, and K.B. Delclos Lactational transfer of the soy isoflavone, genistein, in Sprague-Dawley rats consuming dietary genistein Reproductive Toxicology 21 3 2006 307 312 (Pubitemid 43294561)
67. J.R. Levy, K.A. Faber, L. Ayyash, and C.L. Hughes Jr. The effect of prenatal exposure to the phytoestrogen genistein on sexual differentiation in rats Proceedings of the Society for Experimental Biology and Medicine 208 1 1995 60 66
68. M.K. Skinner, M. Manikkam, and C. Guerrero-Bosagna Epigenetic transgenerational actions of endocrine disruptors Reproductive Toxicology 31 3 2011 337 343
69. W.Y. Tang, L.M. Morey, Y.Y. Cheung, L. Birch, G.S. Prins, and S.M. Ho Neonatal exposure to estradiol/bisphenol A alters promoter methylation and expression of Nsbp1 and Hpcal1 genes and transcriptional programs of Dnmt3a/b and Mbd2/4 in the rat prostate gland throughout life Endocrinology 153 1 2012 42 55
70. T. Yaoi, K. Itoh, K. Nakamura, H. Ogi, Y. Fujiwara, and S. Fushiki Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A Biochemical and Biophysical Research Communications 376 3 2008 563 567
71. W.Y. Tang, R. Newbold, K. Mardilovich, W. Jefferson, R.Y. Cheng, M. Medvedovic, and S.M. Ho Persistent hypomethylation in the promoter of nucleosomal binding protein 1 (Nsbp1) correlates with overexpression of Nsbp1 in mouse uteri neonatally exposed to diethylstilbestrol or genistein Endocrinology 149 12 2008 5922 5931
72. C.J. Park, W.H. Nah, J.E. Lee, Y.S. Oh, and M.C. Gye Butyl paraben-induced changes in DNA methylation in rat epididymal spermatozoa Andrologia 44 Suppl 1 2012 187 193
73. F. Perera, W.Y. Tang, J. Herbstman, D. Tang, L. Levin, R. Miller, and S.M. Ho Relation of DNA methylation of 5'-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma PLoS One 4 2 2009 e4488
74. C. Stouder, and A. Paoloni-Giacobino Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm Reproduction 139 2 2010 373 379
75. M.K. Skinner, M. Manikkam, and C. Guerrero-Bosagna Epigenetic transgenerational actions of environmental factors in disease etiology Trends in Endocrinology and Metabolism 21 4 2010 214 222
76. R. Feil, and M.F. Fraga Epigenetics and the environment: emerging patterns and implications Nature Reviews Genetics 13 2 2012 97 109
77. J.A. Hackett, J.J. Zylicz, and M.A. Surani Parallel mechanisms of epigenetic reprogramming in the germline Trends in Genetics 28 4 2012 164 174
78. C. Alabert, and A. Groth Chromatin replication and epigenome maintenance Nature Reviews Molecular Cell Biology 13 3 2012 153 167
79. C. Guerrero-Bosagna, and M.K. Skinner Environmentally induced epigenetic transgenerational inheritance of phenotype and disease Molecular and Cellular Endocrinology 354 1-2 2012 3 8
80. B.D. Lyn-Cook, E. Blann, P.W. Payne, J. Bo, D. Sheehan, and K. Medlock Methylation profile and amplification of proto-oncogenes in rat pancreas induced with phytoestrogens Proceedings of the Society for Experimental Biology and Medicine 208 1 1995 116 119
81. J.K. Day, A.M. Bauer, C. DesBordes, Y. Zhuang, B.E. Kim, L.G. Newton, V. Nehra, K.M. Forsee, R.S. MacDonald, C. Besch-Williford, T.H. Huang, and D.B. Lubahn Genistein alters methylation patterns in mice Journal of Nutrition 132 8 Suppl 2002 2419S 2423S (Pubitemid 34848119)
82. N. Kikuno, H. Shiina, S. Urakami, K. Kawamoto, H. Hirata, Y. Tanaka, S. Majid, M. Igawa, and R. Dahiya Genistein mediated histone acetylation and demethylation activates tumor suppressor genes in prostate cancer cells International Journal of Cancer 123 3 2008 552 560 (Pubitemid 351898412)
83. S. Majid, N. Kikuno, J. Nelles, E. Noonan, Y. Tanaka, K. Kawamoto, H. Hirata, L.C. Li, H. Zhao, S.T. Okino, R.F. Place, D. Pookot, and R. Dahiya Genistein induces the p21WAF1/CIP1 and p16INK4a tumor suppressor genes in prostate cancer cells by epigenetic mechanisms involving active chromatin modification Cancer Research 68 8 2008 2736 2744 (Pubitemid 351556271)
84. S. Majid, A.A. Dar, A.E. Ahmad, H. Hirata, K. Kawakami, V. Shahryari, S. Saini, Y. Tanaka, A.V. Dahiya, G. Khatri, and R. Dahiya BTG3 tumor suppressor gene promoter demethylation, histone modification and cell cycle arrest by genistein in renal cancer Carcinogenesis 30 4 2009 662 670
85. Y. Li, L. Liu, L.G. Andrews, and T.O. Tollefsbol Genistein depletes telomerase activity through cross-talk between genetic and epigenetic mechanisms International Journal of Cancer 125 2 2009 286 296
86. A. Vardi, R. Bosviel, N. Rabiau, M. Adjakly, S. Satih, P. Dechelotte, J.P. Boiteux, L. Fontana, Y.J. Bignon, L. Guy, and D.J. Bernard-Gallon Soy phytoestrogens modify DNA methylation of GSTP1, RASSF1A, EPH2 and BRCA1 promoter in prostate cancer cells In Vivo 24 4 2010 393 400
87. N. Sato, N. Yamakawa, M. Masuda, K. Sudo, I. Hatada, and M. Muramatsu Genome-wide DNA methylation analysis reveals phytoestrogen modification of promoter methylation patterns during embryonic stem cell differentiation PLoS One 6 4 2011 e19278
88. H. Matsukura, K. Aisaki, K. Igarashi, Y. Matsushima, J. Kanno, M. Muramatsu, K. Sudo, and N. Sato Genistein promotes DNA demethylation of the steroidogenic factor 1 (SF-1) promoter in endometrial stromal cells Biochemical and Biophysical Research Communications 412 2 2011 366 372
89. K. Vanhees, S. Coort, E.J. Ruijters, R.W. Godschalk, F.J. van Schooten, and S. Barjesteh van Waalwijk van Doorn-Khosrovani Epigenetics: prenatal exposure to genistein leaves a permanent signature on the hematopoietic lineage FASEB Journal 25 2 2011 797 807
90. C. Guerrero-Bosagna, P. Sabat, and L. Valladares Environmental signaling and evolutionary change: can exposure of pregnant mammals to environmental estrogens lead to epigenetically induced evolutionary changes in embryos? Evolution and Development 7 4 2005 341 350 (Pubitemid 40995915)
91. D.C. Dolinoy, D. Huang, and R.L. Jirtle Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development Proceedings of the National Academy of Sciences of the United States of America 104 2007 13056 13061 (Pubitemid 351737592)
92. M.D. Anway, A.S. Cupp, M. Uzumcu, and M.K. Skinner Epigenetic transgenerational actions of endocrine disruptors and male fertility Science 308 5727 2005 1466 1469 (Pubitemid 40791300)
93. M. Uzumcu, H. Suzuki, and M.K. Skinner Effect of the anti-androgenic endocrine disruptor vinclozolin on embryonic testis cord formation and postnatal testis development and function Reproductive Toxicology 18 6 2004 765 774 (Pubitemid 38987963)
94. M.D. Anway, C. Leathers, and M.K. Skinner Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease Endocrinology 147 12 2006 5515 5523 (Pubitemid 44833467)
95. M.D. Anway, M.A. Memon, M. Uzumcu, and M.K. Skinner Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis Journal of Andrology 27 6 2006 868 879 (Pubitemid 44846027)
96. C. Guerrero-Bosagna, M. Settles, B. Lucker, and M.K. Skinner Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome PLoS One 5 9 2010
97. S. Salian, T. Doshi, and G. Vanage Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to Bisphenol A Life Sciences 85 1-2 2009 11 18
98. K.L. Bruner-Tran, and K.G. Osteen Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations Reproductive Toxicology 2010
99. M. Manikkam, C. Guerrero-Bosagna, R. Tracey, M.M. Haque, and M.K. Skinner Transgenerational Actions of Environmental Compounds on Reproductive Disease and Epigenetic Biomarkers of Ancestral Exposures PLoS One 7 2 2012 e31901
100. D. Vyssotski Transgenerational epigenetic compensation Evolocus 1 2011 1 6
101. L.L. Kujjo, E.A. Chang, R.J. Pereira, S. Dhar, B. Marrero-Rosado, S. Sengupta, H. Wang, J.B. Cibelli, and G.I. Perez Chemotherapy-induced late transgenerational effects in mice PLoS One 6 3 2011 e17877
102. G. Kaati, L.O. Bygren, M. Pembrey, and M. Sjostrom Transgenerational response to nutrition, early life circumstances and longevity European Journal of Human Genetics 15 7 2007 784 790 (Pubitemid 46965412)
103. R.A. Waterland, M. Travisano, K.G. Tahiliani, M.T. Rached, and S. Mirza Methyl donor supplementation prevents transgenerational amplification of obesity International Journal of Obesity (London) 2008
104. G.A. Dunn, and T.L. Bale Maternal high-fat diet effects on third-generation female body size via the paternal lineage Endocrinology 152 6 2011 2228 2236
105. T. Pentinat, M. Ramon-Krauel, J. Cebria, R. Diaz, and J.C. Jimenez-Chillaron Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition Endocrinology 151 12 2010 5617 5623
106. D. Crews, A.C. Gore, T.S. Hsu, N.L. Dangleben, M. Spinetta, T. Schallert, M.D. Anway, and M.K. Skinner Transgenerational epigenetic imprints on mate preference Proceedings of the National Academy of Sciences of the United States of America 104 14 2007 5942 5946 (Pubitemid 47175638)
107. S.H. Hakkinen, S.O. Karenlampi, I.M. Heinonen, H.M. Mykkanen, and A.R. Torronen Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries Journal of Agricultural and Food Chemistry 47 6 1999 2274 2279 (Pubitemid 29325110)
108. A. Amin, and M. Buratovich The anti-cancer charm of flavonoids: a cup-of-tea will do! Recent Patents on Anticancer Drug Discovery 2 2 2007 109 117 (Pubitemid 46957317)
109. A.I. Smeds, P.C. Eklund, R.E. Sjoholm, S.M. Willfor, S. Nishibe, T. Deyama, and B.R. Holmbom Quantification of a broad spectrum of lignans in cereals, oilseeds, and nuts Journal of Agricultural and Food Chemistry 55 4 2007 1337 1346
110. D.C. Dolinoy, J.R. Weidman, R.A. Waterland, and R.L. Jirtle Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome Environmental Health Perspectives 114 4 2006 567 572
111. S. Majid, A.A. Dar, V. Shahryari, H. Hirata, A. Ahmad, S. Saini, Y. Tanaka, A.V. Dahiya, and R. Dahiya Genistein reverses hypermethylation and induces active histone modifications in tumor suppressor gene B-Cell translocation gene 3 in prostate cancer Cancer 116 1 2010 66 76