A review of the carcinogenic potential of bisphenol A

Reproductive Toxicology

Volumn 59, Issue , 2016, Pages 167-182

  Seachrist, Darcie D ^a   Bonk, Kristen W ^a   Ho, Shuk Mei ^b   Prins, Gail S ^c   Soto, Ana M ^d   Keri, Ruth A ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d TUFTS UNIVERSITY   (United States)

Author keywords

Bisphenol A; Cancer; Estrogen receptor; Mammary; Ovary; Prostate; Testes; Uterus

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; DRINKING WATER; ENDOCRINE DISRUPTOR; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE; POLLUTANT;

BREAST CANCER; BREAST DEVELOPMENT; CANCER INCIDENCE; CANCER RISK; CANCER SUSCEPTIBILITY; CARCINOGENICITY; CHEMICAL CARCINOGENESIS; EPIGENETICS; ESTROGEN ACTIVITY; FOOD CONTAMINATION; HEALTH HAZARD; HUMAN; LIVER CANCER; MOUSE MODEL; NONHUMAN; OVARY CANCER; PRENATAL EXPOSURE; PROSTATE CANCER; RAT MODEL; REVIEW; TESTIS CANCER; UTERUS CANCER; WATER SUPPLY; ANIMAL; BREAST NEOPLASMS; CELL TRANSFORMATION; CHEMICALLY INDUCED; FEMALE; GENITAL NEOPLASMS, FEMALE; GENITAL NEOPLASMS, MALE; MALE; POLLUTANT; RISK ASSESSMENT; RISK FACTOR; TOXICITY;

ANIMALS; BENZHYDRYL COMPOUNDS; BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; ENDOCRINE DISRUPTORS; ENVIRONMENTAL POLLUTANTS; FEMALE; GENITAL NEOPLASMS, FEMALE; GENITAL NEOPLASMS, MALE; HUMANS; MALE; PHENOLS; RISK ASSESSMENT; RISK FACTORS;

EID: 84959476306     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2015.09.006     Document Type: Review

References (145)

1. De Coster S., van Larebeke N. Endocrine-disrupting chemicals: associated disorders and mechanisms of action. J. Environ. Public Health 2012, 2012:713696.
2. N. Howlander, A.M. Noone, M. Krapcho, J. Garshell, D. Miller, S.F. Altekruse, et al, SEER Cancer Statistics Review, 1975-2012, National Cancer Institute. p. based on November 2014 SEER data submission.
3. Maffini M.V., Rubin B.S., Sonnenschein C., Soto A.M. Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol. Cell. Endocrinol. 2006, 254-255:179-186.
4. Brody J.G., Rudel R.A. Environmental pollutants and breast cancer. Environ. Health Perspect. 2003, 111:1007-1019.
5. Burridge E. Bisphenol A product profile. Eur. Chem. News 2003, 17:4-20.
6. Kuroda N., Kinoshita Y., Sun Y., Wada M., Kishikawa N., Nakashima K., et al. Measurement of bisphenol A levels in human blood serum and ascitic fluid by HPLC using a fluorescent labeling reagent. J. Pharm. Biomed. Anal. 2003, 30:1743-1749.
7. Lee Y.J., Ryu H.Y., Kim H.K., Min C.S., Lee J.H., Kim E., et al. Maternal and fetal exposure to bisphenol A in Korea. Reprod. Toxicol. 2008, 25:413-419.
8. Calafat A.M., Weuve J., Ye X., Jia L.T., Hu H., Ringer S., et al. Exposure to bisphenol A and other phenols in neonatal intensive care unit premature infants. Environ. Health Perspect. 2009, 117:639-644.
9. Edginton A.N., Ritter L. Predicting plasma concentrations of bisphenol A in children younger than 2 years of age after typical feeding schedules, using a physiologically based toxicokinetic model. Environ. Health Perspect. 2009, 117:645-652.
10. Nepomnaschy P.A., Baird D.D., Weinberg C.R., Hoppin J.A., Longnecker M.P., Wilcox A.J. Within-person variability in urinary bisphenol A concentrations: measurements from specimens after long-term frozen storage. Environ. Res. 2009, 109:734-737.
11. Calafat A.M., Kuklenyik Z., Reidy J.A., Caudill S.P., Ekong J., Needham L.L. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ. Health Perspect. 2005, 113:391-395.
12. Dodds E.C. The pharmacological action and clinical use of drugs with a camphor- and coramine-like action: (section of therapeutics and pharmacology). Proc. R. Soc. Med. 1936, 29:655-657.
13. Thomas P., Dong J. Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J. Steroid Biochem. Mol. Biol. 2006, 102:175-179.
14. NTP Carcinogenesis bioassay of bisphenol A (CAS No. 80-05-7) in F344 rats and B6C3F1 mice (feed study). Natl. Toxicol. Program Tech. Rep. Ser. 1982, 215:1-116.
15. Huff J. Does exposure to bisphenol A represent a human health risk?. Regul. Toxicol. Pharmacol. 2003, 37:407-408.
16. Welshons W.V., Thayer K.A., Judy B.M., Taylor J.A., Curran E.M., vom Saal F.S. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ. Health Perspect. 2003, 111:994-1006.
17. vom Saal F.S., Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ. Health Perspect. 2005, 113:926-933.
18. Vandenberg L.N., Colborn T., Hayes T.B., Heindel J.J., Jacobs D.R.J., Lee D.H., et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. 2012, 33:378-455.
19. Vandenberg L.N., Ehrlich S., Belcher S.M., Ben-Jonathan N., Dolinoy D.C., Hugo E.R., et al. Low dose effects of bisphenol A: an integrated review of in vitro, laboratory animal, and epidemiology studies. Endocr. Disrupt. 2013, 1:0-1.
20. Schonfelder G., Wittfoht W., Hopp H., Talsness C.E., Paul M., Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ. Health Perspect. 2002, 110:A703-7.
21. Ikezuki Y., Tsutsumi O., Takai Y., Kamei Y., Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum. Reprod. 2002, 17:2839-2841.
22. Taylor J.A., Vom Saal F.S., Welshons W.V., Drury B., Rottinghaus G., Hunt P.A., et al. Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: relevance for human exposure. Environ. Health Perspect. 2011, 119:422-430.
23. Taylor J.A., Welshons W.V., vom Saal F.S. No effect of route of exposure (oral; subcutaneous injection) on plasma bisphenol A throughout 24h after administration in neonatal female mice. Reprod. Toxicol. 2008, 25:169-176.
24. Tyl R.W., Myers C.B., Marr M.C., Thomas B.F., Keimowitz A.R., Brine D.R., et al. Three-generation reproductive toxicity study of dietary bisphenol A in CD Sprague-Dawley rats. Toxicol. Sci. 2002, 68:121-146.
25. Welshons W.V., Nagel S.C., vom Saal F.S. Large effects from small exposures: III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 2006, 147:S56-69.
26. Tyl R.W., Myers C.B., Marr M.C., Sloan C.S., Castillo N.P., Veselica M.M., et al. Two-generation reproductive toxicity study of dietary bisphenol A in CD-1 (Swiss) mice. Toxicol. Sci. 2008, 104:362-384.
27. Spearow J.L., Doemeny P., Sera R., Leffler R., Barkley M. Genetic variation in susceptibility to endocrine disruption by estrogen in mice. Science 1999, 285:1259-1261.
28. Keri R.A., Ho S.M., Hunt P.A., Knudsen K.E., Soto A.M., Prins G.S. An evaluation of evidence for the carcinogenic activity of bisphenol A. Reprod. Toxicol. 2007, 24:240-252.
29. Goodman J.E., Witorsch R.J., McConnell E.E., Sipes I.G., Slayton T.M., Yu C.J., et al. Weight-of-evidence evaluation of reproductive and developmental effects of low doses of bisphenol A. Crit. Rev. Toxicol. 2009, 39:1-75.
30. Melnick R., Lucier G., Wolfe M., Hall R., Stancel G., Prins G., et al. Summary of the National Toxicology Program's report of the endocrine disruptors low-dose peer review. Environ. Health Perspect. 2002, 110:427-431.
31. Vandenberg L.N., Chahoud I., Padmanabhan V., Paumgartten F.J., Schoenfelder G. Biomonitoring studies should be used by regulatory agencies to assess human exposure levels and safety of bisphenol A. Environ. Health Perspect. 2010, 118:1051-1054.
32. vom Saal F.S., Welshons W.V. Evidence that bisphenol A (BPA) can be accurately measured without contamination in human serum and urine, and that BPA causes numerous hazards from multiple routes of exposure. Mol. Cell. Endocrinol. 2014, 398:101-113.
33. Dave N., Chow L.M.L., Gudelsky G.A., LaSance K., Qi X., Desai P.B. Preclinical pharmacological evaluation of letrozole as a novel treatment for gliomas. Mol. Cancer Ther. 2015, 14:857-864.
34. Siegfried J.M., Hershberger P.A., Stabile L.P. Estrogen receptor signaling in lung cancer. Semin. Oncol. 2009, 36:524.
35. Caiazza F., Ryan E.J., Doherty G., Winter D.C., Sheahan K. Estrogen receptors and their implications in colorectal carcinogenesis. Front. Oncol. 2015, 5:1-9.
36. Lang I.A., Galloway T.S., Scarlett A., Henley W.E., Depledge M., Wallace R.B., et al. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 2008, 300:1303-1310.
37. Tsai W.T. Human health risk on environmental exposure to bisphenol-A: a review. J. Environ. Sci. Health C. Environ. Carcinog Ecotoxicol. Rev. 2006, 24:225-255.
38. Yang M., Ryu J.H., Jeon R., Kang D., Yoo K.Y. Effects of bisphenol A on breast cancer and its risk factors. Arch. Toxicol. 2009, 83:281-285.
39. Trabert B., Falk R., Figueroa J., Graubard B., Garcia-Closas M., Lissowska J., et al. Urinary bisphenol A-glucuronide and postmenopausal breast cancer in Poland. Cancer Causes Control 2014, 25:1587-1593.
40. Garcia-Closas M., Brinton L.A., Lissowska J., Chatterjee N., Peplonska B., Anderson W.F., et al. Established breast cancer risk factors by clinically important tumour characteristics. Br. J. Cancer 2006, 95:123-129.
41. Neville M.C., McFadden T.B., Forsyth I. Hormonal regulation of mammary differentiation and milk secretion. J. Mammary Gland Biol. Neoplasia 2002, 7:49-66.
42. Russo I.H., Russo J. Mammary gland neoplasia in long-term rodent studies. Environ. Health Perspect. 1996, 104:938-967.
43. Munoz-de-Toro M., Markey C.M., Wadia P.R., Luque E.H., Rubin B.S., Sonnenschein C., et al. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 2005, 146:4138-4147.
44. Reed C.E., Fenton S.E. Exposure to diethylstilbestrol during sensitive life stages: a legacy of heritable health effects. Birth Defects Res. C Embryo Today 2013, 99:134-146.
45. Agius L.M. Theory in the Pathophysiology of Carcinogenesis 2011, Bentham Science Publishers.
46. 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.
47. Acevedo N., Davis B., Schaeberle C.M., Sonnenschein C., Soto A.M. Perinatally administered bisphenol a as a potential mammary gland carcinogen in rats. Environ. Health Perspect. 2013, 121:1040-1046.
48. 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.
49. Gullino P.M., Pettigrew H.M., Grantham F.H. N-Nitrosomethylurea as mammary-gland carcinogen in rats. J. Natl. Cancer Inst. 1975, 54:401-414.
50. Russo J., Wilgus G., Russo I.H. Susceptibility of the mammary gland to carcinogenesis: I differentiation of the mammary gland as determinant of tumor incidence and type of lesion. Am. J .Pathol. 1979, 96:721-736.
51. Maffini M.V., Soto A.M., Calabro J.M., Ucci A.A., Sonnenschein C. The stroma as a crucial target in rat mammary gland carcinogenesis. J. Cell Sci. 2004, 117:1495-1502.
52. Barcellos-Hoff M.H., Ravani S.A. Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells. Cancer Res. 2000, 60:1254-1260.
53. Durando M., Kass L., Piva J., Sonnenschein C., Soto A.M., Luque E.H., et al. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ. Health Perspect. 2007, 115:80-86.
54. Jenkins S., Raghuraman N., Eltoum I., Carpenter M., Russo J., Lamartiniere C.A. Oral exposure to bisphenol a increases dimethylbenzanthracene-induced mammary cancer in rats. Environ. Health Perspect. 2009, 117:910-915.
55. Betancourt A.M., Eltoum I.A., Desmond R.A., Russo J., Lamartiniere C.A. In utero exposure to bisphenol A shifts the window of susceptibility for mammary carcinogenesis in the rat. Environ. Health Perspect. 2010, 118:1614-1619.
56. Lamartiniere C.A., Jenkins S., Betancourt A.M., Wang J., Russo J. Exposure to the endocrine disruptor bisphenol A alters susceptibility for mammary cancer. Horm. Mol. Biol. Clin. Investig. 2011, 5:45-52.
57. Tokunaga M., Land C.E., Yamamoto T., Asano M., Tokuoka S., Ezaki H., et al. Incidence of female breast cancer among atomic bomb survivors, Hiroshima and Nagasaki, 1950-1980. Radiat. Res. 1987, 112:243-272.
58. Betancourt A.M., Wang J., Jenkins S., Mobley J., Russo J., Lamartiniere C.A. Altered carcinogenesis and proteome in mammary glands of rats after prepubertal exposures to the hormonally active chemicals bisphenol a and genistein. J. Nutr. 2012, 142:1382S-1388S.
59. Vandenberg L.N., Maffini M.V., Schaeberle C.M., Ucci A.A., Sonnenschein C., Rubin B.S., et al. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod. Toxicol. 2008, 26:210-219.
60. Vandenberg L.N., Maffini M.V., Wadia P.R., Sonnenschein C., Rubin B.S., Soto A.M. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 2007, 148:116-127.
61. Wadia P.R., Cabaton N.J., Borrero M.D., Rubin B.S., Sonnenschein C., Shioda T., et al. Low-dose BPA exposure alters the mesenchymal and epithelial transcriptomes of the mouse fetal mammary gland. PLoS One 2013, 8:e63902.
62. Wadia P.R., Vandenberg L.N., Schaeberle C.M., Rubin B.S., Sonnenschein C., Soto A.M. Perinatal bisphenol A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environ. Health Perspect. 2007, 115:592-598.
63. Ayyanan A., Laribi O., Schuepbach-Mallepell S., Schrick C., Gutierrez M., Tanos T., et al. Perinatal exposure to bisphenol A increases adult mammary gland progesterone response and cell number. Mol. Endocrinol. 2011, 25:1915-1923.
64. Weber Lozada K., Keri R.A. Bisphenol A increases mammary cancer risk in two distinct mouse models of breast cancer. Biol. Reprod. 2011, 85:490-497.
65. Soto A., Brisken C., Schaeberle C., Sonnenschein C. Does cancer start in the womb? Altered mammary gland development and predisposition to breast cancer due to in utero exposure to endocrine disruptors. J. Mammary Gland Biol. Neoplasia 2013, 18:199-208.
66. Wang D., Gao H., Bandyopadhyay A., Wu A., Yeh I.-T., Chen Y., et al. Pubertal bisphenol A exposure alters murine mammary stem cell function leading to early neoplasia in regenerated glands. Cancer Prev. Res. (Phila.) 2014, 7:445-455.
67. Tiede B., Kang Y. From milk to malignancy: the role of mammary stem cells in development, pregnancy and breast cancer. Cell Res. 2011, 21:245-257.
68. Jenkins S., Wang J., Eltoum I., Desmond R., Lamartiniere C.A. Chronic oral exposure to bisphenol A results in a nonmonotonic dose response in mammary carcinogenesis and metastasis in MMTV-erbB2 mice. Environ. Health Perspect. 2011, 119:1604-1609.
69. Dhimolea E., Wadia P.R., Murray T.J., Settles M.L., Treitman J.D., Sonnenschein C., et al. Prenatal exposure to BPA alters the epigenome of the rat mammary gland and increases the propensity to neoplastic development. PLoS One 2014, 9:e99800.
70. Tharp A.P., Maffini M.V., Hunt P.A., VandeVoort C.A., Sonnenschein C., Soto A.M. Bisphenol A alters the development of the rhesus monkey mammary gland. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:8190-8195.
71. Susiarjo M., Hassold T.J., Freeman E., Hunt P.A. Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genet. 2007, 3:e5.
72. Hunt P.A., Koehler K.E., Susiarjo M., Hodges C.A., Ilagan A., Voigt R.C., et al. Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr. Biol. 2003, 13:546-553.
73. Hunt P.A., Lawson C., Gieske M., Murdoch B., Smith H., Marre A., et al. Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:17525-17530.
74. Greathouse K.L., Bredfeldt T., Everitt J.I., Lin K., Berry T., Kannan K., et al. Environmental estrogens differentially engage the histone methyltransferase EZH2 to increase risk of uterine tumorigenesis. Mol. Cancer Res. 2012, 10:546-557.
75. Nikaido Y., Danbara N., Tsujita-Kyutoku M., Yuri T., Uehara N., Tsubura A. Effects of prepubertal exposure to xenoestrogen on development of estrogen target organs in female CD-1 mice. In Vivo 2005, 19:487-494.
76. 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.
77. Newbold R.R., Jefferson W.N., Padilla-Banks E. Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ. Health Perspect. 2009, 117:879-885.
78. Kato H., Ota T., Furuhashi T., Ohta Y., Iguchi T. Changes in reproductive organs of female rats treated with bisphenol A during the neonatal period. Reprod. Toxicol. 2003, 17:283-288.
79. Fernandez M., Bourguignon N., Lux-Lantos V., Libertun C. Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ. Health Perspect. 2010, 118:1217-1222.
80. Kandaraki E., Chatzigeorgiou A., Livadas S., Palioura E., Economou F., Koutsilieris M., et al. Endocrine disruptors and polycystic ovary syndrome (PCOS): elevated serum levels of bisphenol A in women with PCOS. J. Clin. Endocrinol. Metab. 2011, 96:E480-E484.
81. Bailey C.L., Ueland F.R., Land G.L., DePriest P.D., Gallion H.H., Kryscio R.J., et al. The malignant potential of small cystic ovarian tumors in women over 50 years of age. Gynecol. Oncol. 1998, 69:3-7.
82. Modesitt S.C., Pavlik E.J., Ueland F.R., DePriest P.D., Kryscio R.J., van Nagell J.R. Risk of malignancy in unilocular ovarian cystic tumors less than 10 centimeters in diameter. Obstet. Gynecol. 2003, 102:594-599.
83. Schildkraut J.M., Schwingl P.J., Bastos E., Evanoff A., Hughes C. Epithelial ovarian cancer risk among women with polycystic ovary syndrome. Obstet. Gynecol. 1996, 88:554-559.
84. Dumesic D.A., Lobo R.A. Cancer risk and PCOS. Steroids 2013, 78:782-785.
85. Newbold R.R., Bullock B.C., McLachlan J.A. Uterine adenocarcinoma in mice following developmental treatment with estrogens: a model for hormonal carcinogenesis. Cancer Res. 1990, 50:7677-7681.
86. Hiroi H., Tsutsumi O., Takeuchi T., Momoeda M., Ikezuki Y., Okamura A., et al. Differences in serum bisphenol a concentrations in premenopausal normal women and women with endometrial hyperplasia. Endocr. J. 2004, 51:595-600.
87. Fukata H., Miyagawa H., Yamazaki N., Mori C. Comparison of ELISA- and LC-MS-based methodologies for the exposure assessment of bisphenol A. Toxicol. Mech. Methods 2006, 16:427-430.
88. Dekant W., Volkel W. Human exposure to bisphenol A by biomonitoring: methods, results and assessment of environmental exposures. Toxicol. Appl. Pharmacol. 2008, 228:114-134.
89. Pollack A.Z., Buck Louis G.M., Chen Z., Sun L., Trabert B., Guo Y., et al. Bisphenol A benzophenone-type ultraviolet filters, and phthalates in relation to uterine leiomyoma. Environ. Res. 2015, 137:101-107.
90. Schonfelder G., Friedrich K., Paul M., Chahoud I. Developmental effects of prenatal exposure to bisphenol a on the uterus of rat offspring. Neoplasia 2004, 6:584-594.
91. Prejean J.D., Peckham J.C., Casey A.E., Griswold D.P., Weisburger E.K., Weisburger J.H. Spontaneous tumors in Sprague-Dawley rats and Swiss mice. Cancer Res. 1973, 33:2768-2773.
92. Kitamura T., Nishimura S., Sasahara K., Yoshida M., Ando J., Takahashi M., et al. Transplacental administration of diethylstilbestrol (DES) causes lesions in female reproductive organs of Donryu rats, including endometrial neoplasia. Cancer Lett. 1999, 141:219-228.
93. Long X., Steinmetz R., Ben-Jonathan N., Caperell-Grant A., Young P.C., Nephew K.P., et al. Strain differences in vaginal responses to the xenoestrogen bisphenol A. Environ. Health Perspect. 2000, 108:243-247.
94. Rothschild T.C., Calhoon R.E., Boylan E.S. Genital tract abnormalities in female rats exposed to diethylstilbestrol in utero. Reprod. Toxicol. 1987, 1:193-202.
95. Okuda K., Takiguchi M., Yoshihara S. In vivo estrogenic potential of 4-methyl-2,4-bis(4-hydroxyphenyl) pent-1-ene, an active metabolite of bisphenol A, in uterus of ovariectomized rat. Toxicol. Lett. 2010, 197:7-11.
96. Greathouse K.L., Cook J.D., Lin K., Davis B.J., Berry T.D., Bredfeldt T.G., et al. Identification of uterine leiomyoma genes developmentally reprogrammed by neonatal exposure to diethylstilbestrol. Reprod. Sci. 2008, 15:765-778.
97. Newbold R.R., Moore A.B., Dixon D. Characterization of uterine leiomyomas in CD-1 mice following developmental exposure to diethylstilbestrol (DES). Toxicol. Pathol. 2002, 30:611-616.
98. Everitt J.I., Wolf D.C., Howe S.R., Goldsworthy T.L., Walker C. Rodent model of reproductive tract leiomyomata: clinical and pathological features. Am. J. Pathol. 1995, 146:1556-1567.
99. Walker C.L., Hunter D., Everitt J.I. Uterine leiomyoma in the Eker rat: a unique model for important diseases of women. Genes Chromosomes Cancer 2003, 38:349-356.
100. Maekawa A., Onodera H., Tanigawa H., Furuta K., Matsuoka C., Kanno J., et al. Spontaneous neoplastic and non-neoplastic lesions in aging Donryu rats. Jpn. J. Cancer Res. 1986, 77:882-890.
101. Yoshida M., Shimomoto T., Katashima S., Watanabe G., Taya K., Maekawa A. Maternal exposure to low doses of bisphenol A has no effects on development of female reproductive tract and uterine carcinogenesis in Donryu rats. J. Reprod. Dev. 2004, 50:349-360.
102. Schonfelder G., Flick B., Mayr E., Talsness C., Paul M., Chahoud I. In utero exposure to low doses of bisphenol A lead to long-term deleterious effects in the vagina. Neoplasia 2002, 4:98-102.
103. Tarapore P., Ying J., Ouyang B., Burke B., Bracken B., Ho S.M. Exposure to bisphenol A correlates with early-onset prostate cancer and promotes centrosome amplification and anchorage-independent growth in vitro. PLoS One 2014, 9:e90332.
104. Greene R.R., Burrill M.W., Ivy A.C. Experimental intersexuality. The effects of estrogens on the antenatal sexual development of the rat. Am. J. Anat. 1940, 67:305-345.
105. Allgeier S.H., Vezina C.M., Lin T.M., Moore R.W., Silverstone A.E., Mukai M., et al. Estrogen signaling is not required for prostatic bud patterning or for its disruption by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 2009, 239:80-86.
106. Leav I., Ho S.M., Ofner P., Merk F.B., Kwan P.W., Damassa D. Biochemical alterations in sex hormone-induced hyperplasia and dysplasia of the dorsolateral prostates of Noble rats. J. Natl. Cancer Inst. 1988, 80:1045-1053.
107. Modugno F., Weissfeld J.L., Trump D.L., Zmuda J.M., Shea P., Cauley J.A., et al. Allelic variants of aromatase and the androgen and estrogen receptors: toward a multigenic model of prostate cancer risk. Clin. Cancer Res. 2001, 7:3092-3096.
108. Hu W.-Y., Shi G.-B., Lam H.-M., Hu D.-P., Ho S.-M., Madueke I.C., et al. Estrogen-initiated transformation of prostate epithelium derived from normal human prostate stem-progenitor cells. Endocrinology 2011, 152:2150-2163.
109. Ichihara T., Yoshino H., Imai N., Tsutsumi T., Kawabe M., Tamano S., et al. Lack of carcinogenic risk in the prostate with transplacental and lactational exposure to bisphenol A in rats. J. Toxicol. Sci. 2003, 28:165-171.
110. Prins G.S., Birch L., Couse J.F., Choi I., Katzenellenbogen B., Korach K.S. Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor alpha: studies with alpha-ERKO and beta-ERKO mice. Cancer Res. 2001, 61:6089-6097.
111. Wu J.H., Jiang X.R., Liu G.M., Liu X.Y., He G.L., Sun Z.Y. Oral exposure to low-dose bisphenol A aggravates testosterone-induced benign hyperplasia prostate in rats. Toxicol. Ind. Health 2011, 27:810-819.
112. Brandt J.Z., Silveira L.T.R., Grassi T.F., Anselmo-Franci J.A., Fávaro W.J., Felisbino S.L., et al. Indole-3-carbinol attenuates the deleterious gestational effects of bisphenol A exposure on the prostate gland of male F1 rats. Reprod. Toxicol. 2014, 43:56-66.
113. Ho S.-M., Tang W.-Y., Belmonte de Frausto J., Prins G.S. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res. 2006, 66:5624-5632.
114. Prins G.S., Ye S.-H., Birch L., Ho S.-M., Kannan K. Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reprod. Toxicol. 2011, 31:1-9.
115. Vandenberg L.N., Hauser R., Marcus M., Olea N., Welshons W.V. Human exposure to bisphenol A (BPA). Reprod. Toxicol. 2007, 24:139-177.
116. Wong R.L., Wang Q., Trevino L.S., Bosland M.C., Chen J., Medvedovic M., et al. Identification of secretaglobin Scgb2a1 as a target for developmental reprogramming by BPA in the rat prostate. Epigenetics 2015, 10:127-134.
117. Ittmann M., Huang J., Radaelli E., Martin P., Signoretti S., Sullivan R., et al. Animal models of human prostate cancer: the consensus report of the New York meeting of the Mouse Models of Human Cancers Consortium Prostate Pathology Committee. Cancer Res. 2013, 73:2718-2736.
118. Castro B., Sánchez P., Torres J.M., Preda O., del Moral R.G., Ortega E. Bisphenol A exposure during adulthood alters expression of aromatase and 5α-reductase isozymes in rat prostate. PLoS One 2013, 8:e55905.
119. Godoy A., Kawinski E., Li Y., Oka D., Alexiev B., Azzouni F., et al. 5alpha-reductase type 3 expression in human benign and malignant tissues: a comparative analysis during prostate cancer progression. Prostate 2011, 71:1033-1046.
120. Arase S., Ishii K., Igarashi K., Aisaki K., Yoshio Y., Matsushima A., et al. Endocrine disrupter bisphenol A increases in situ estrogen production in the mouse urogenital sinus. Biol. Reprod. 2011, 84:734-742.
121. Ho S.M., Johnson A., Tarapore P., Janakiram V., Zhang X., Leung Y.K. Environmental epigenetics and its implication on disease risk and health outcomes. ILAR J. 2012, 53:289-305.
122. Prins G.S., Tang W.-Y., Belmonte J., Ho S.-M. Perinatal exposure to oestradiol and bisphenol A alters the prostate epigenome and increases susceptibility to carcinogenesis. Basic Clin. Pharmacol. Toxicol. 2008, 102:134-138.
123. Tang W.-Y., Morey L.M., Cheung Y.Y., Birch L., Prins G.S., Ho S.-M. 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 2012, 153:42-55.
124. Chen T.C., Wadsten P., Su S., Rawlinson N., Hofman F.M., Hill C.K., et al. The type IV phosphodiesterase inhibitor rolipram induces expression of the cell cycle inhibitors p2(Cip1) and p27(Kip1), resulting in growth inhibition, increased differentiation, and subsequent apoptosis of malignant A-172 glioma cells. Cancer Biol. Ther. 2002, 1:268-276.
125. Narita M., Murata T., Shimizu K., Sugiyama T., Nakagawa T., Manganiello V.C., et al. Phosphodiesterase 4 in osteoblastic osteosarcoma cells as a potential target for growth inhibition. Anticancer Drugs 2003, 14:377-381.
126. Jiang N., Zhou L.Q., Zhang X.Y. Downregulation of the nucleosome-binding protein 1 (NSBP1) gene can inhibit the in vitro and in vivo proliferation of prostate cancer cells. Asian J. Androl. 2010, 12:709-717.
127. Song G., Zhou L.Q., Weng M., He Q., He Z.S., Hao J.R., et al. Expression of nucleosomal binding protein 1 in normal prostate benign prostate hyperplasia, and prostate cancer and significance thereof. Zhonghua Yi Xue Za Zhi 2006, 86:1962-1965.
128. Lacroix M. Significance detection and markers of disseminated breast cancer cells. Endocr. Relat. Cancer 2006, 13:1033-1067.
129. Munakata K., Uemura M., Takemasa I., Ozaki M., Konno M., Nishimura J., et al. SCGB2A1 is a novel prognostic marker for colorectal cancer associated with chemoresistance and radioresistance. Int. J. Oncol. 2014, 44:1521-1528.
130. Prins G.S., Hu W.Y., Shi G.B., Hu D.P., Majumdar S., Li G., et al. Bisphenol A promotes human prostate stem-progenitor cell self-renewal and increases in vivo carcinogenesis in human prostate epithelium. Endocrinology 2014, 155.
131. Ho S.M., Cheong A., Lam H.M., Hu W.Y., Shi G.B., Zhu X., et al. Exposure of human prostaspheres to bisphenol A epigenetically regulates SNORD family non-coding RNAs via histone modification. Endocrinology 2015, 156:3984-3995. en20151067.
132. Zhang W.Z., Yong L., Jia X.D., Li N., Fan Y.X. Combined subchronic toxicity of bisphenol A and dibutyl phthalate on male rats. Biomed. Environ. Sci. 2013, 26:63-69.
133. LaRocca J., Boyajian A., Brown C., Smith S.D., Hixon M. Effects of in utero exposure to bisphenol A or diethylstilbestrol on the adult male reproductive system. Birth Defects Res. B Dev. Reprod. Toxicol. 2011, 92:526-533.
134. Vrooman L.A., Oatley J.M., Griswold J.E., Hassold T.J., Hunt P.A. Estrogenic exposure alters the spermatogonial stem cells in the developing testis, permanently reducing crossover levels in the adult. PLoS Genet. 2015, 11:e1004949.
135. Nanjappa M.K., Simon L., Akingbemi B.T. The industrial chemical bisphenol A (BPA) interferes with proliferative activity and development of steroidogenic capacity in rat Leydig cells. Biol. Reprod. 2012, 86:135. 1-12.
136. Nahar M.S., Liao C., Kannan K., Dolinoy D.C. Fetal liver bisphenol A concentrations and biotransformation gene expression reveal variable exposure and altered capacity for metabolism in humans. J. Biochem. Mol. Toxicol. 2013, 27:116-123.
137. Nahar M.S., Kim J.H., Sartor M.A., Dolinoy D.C. Bisphenol A-associated alterations in the expression and epigenetic regulation of genes encoding xenobiotic metabolizing enzymes in human fetal liver. Environ. Mol. Mutagen. 2013, 55:184-195.
138. Weinhouse C., Anderson O.S., Bergin I.L., Vandenbergh D.J., Gyekis J.P., Dingman M.A., et al. Dose-dependent incidence of hepatic tumors in adult mice following perinatal exposure to bisphenol A. Environ. Health Perspect. 2014, 122:485-491.
139. Maronpot R.R. Biological basis of differential susceptibility to hepatocarcinogenesis among mouse strains. J. Toxicol. Pathol. 2009, 22:11-33.
140. IARC Cancer incidence in five continents. IARC Sci. Publ. 2002, VIII:1-781.
141. IARC, International Agency for Research on Cancer Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans, Lyons, France, 1982.
142. Dunning W.F., Curtis M.R., Maun M.E. The effect of dietary fat and carbohydrate on diethylstilbestrol-induced mammary cancer in rats. Cancer Res. 1949, 9:354-361.
143. Kirkman H., Bacon R.L. Estrogen-induced tumors of the kidney. I. Incidence of renal tumors in intact and gonadectomized male golden hamsters treated with diethylstilbestrol. J. Natl. Cancer Inst. 1952, 13:745-755.
144. Herbst A.L., Ulfelder H., Poskanzer D.C. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N. Engl. J. Med. 1971, 284:878-881.
145. Hoover R.N., Hyer M., Pfeiffer R.M., Adam E., Bond B., Cheville A.L., et al. Adverse health outcomes in women exposed in utero to diethylstilbestrol. N. Engl. J. Med. 2011, 365:1304-1314.