Dose-dependent incidence of hepatic tumors in adult mice following perinatal exposure to bisphenol A

Environmental Health Perspectives

Volumn 122, Issue 5, 2014, Pages 485-491

  Weinhouse, Caren ^a   Anderson, Olivia S ^a   Bergin, Ingrid L ^a   Vandenbergh, David J ^b   Gyekis, Joseph P ^b   Dingman, Marc A ^b   Yang, Jingyun ^b   Dolinoy, Dana C ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4, 4' ISOPROPYLIDENEDIPHENOL; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; 4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; CANCER INCIDENCE; CARCINOGENICITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HELICOBACTER HEPATICUS; HISTOPATHOLOGY; INFLAMMATION; LIMIT OF QUANTITATION; LIVER CELL CARCINOMA; LIVER TUMOR; MALE; MOUSE; NONHUMAN; PERINATAL DRUG EXPOSURE; POLYMERASE CHAIN REACTION; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; STEATOSIS; VIRUS INFECTION; ANIMAL; CHEMICALLY INDUCED; DIAGNOSIS; GENETICS; LIVER NEOPLASMS; TOXICITY;

ANIMALS; BENZHYDRYL COMPOUNDS; FEMALE; LIVER NEOPLASMS; MALE; MICE; PHENOLS; POLYMORPHISM, SINGLE NUCLEOTIDE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84899761237     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1307449     Document Type: Article

References (38)

1. Acevedo N., Davis B, Schaeberle CM, Sonnenschein C, Soto AM. 2013. Perinatally administered bisphenol A as a potential mammary gland carcinogen in rats. Environ Health Perspect 121:1040-1046; http://dx.doi.org/10.1289/ehp.1306734.
2. Allen D. G, Pearse G, Haseman J K, Maronpot RR. 2004. Prediction of rodent carcinogenesis: an evaluation of prechronic liver lesions as forecasters of liver tumors in NTP carcinogenicity studies. Toxicol Pathol 32:393-401.
3. Anderson O. S, Nahar MS, Faulk C, Jones TR, Liao C, Kannan K, et al. 2012. Epigenetic responses following maternal dietary exposure to physiologically relevant levels of bisphenol A. Environ Mol Mutagen 53:334-342
4. Anderson O. S, Peterson KE, Sanchez BN, Zhang Z, Mancuso P, Dolinoy D.C. 2013. Perinatal bisphenol A exposure promotes hyperactivity, lean body composition, and hormonal responses across the murine life course. FASEB J 27:1784-1792.
5. Babu S., Uppu S, Claville MO, Uppu RM. 2013. Prooxidant actions of bisphenol A (BPA) phenoxyl radicals: implications to BPA-related oxidative stress and toxicity. Toxicol Mech Methods 23:273-280.
6. Bergeron R. M, Thompson TB, Leonard LS, Pluta L, Gaido KW. 1999. Estrogenicity of bisphenol A in a human endometrial carcinoma cell line. Mol Cell Endocrinol 150:179-187.
7. Betancourt A. M, Wang J, Jenkins S, Mobley J, Russo J, Lamartiniere C.A. 2012. Altered carcinogenesis and proteome in mammary glands of rats after prepubertal exposures to the hormonally active chemicals bisphenol A and genistein. J Nutr 142:1382S-1388S.
8. Bilger A., Bennett LM, Carabeo RA, Chiaverotti TA, Dvorak C, Liss K. M, et al. 2004. A potent modifier of liver cancer risk on distal mouse chromosome 1: linkage analysis and characterization of congenic lines. Genetics 167:859-866.
9. Calafat A. M, Ye X, Wong L-Y, Reidy JA, Needham LL. 2008. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 116:39-44; doi:10.1289/ehp.10753.
10. Cui J., Shen Y, Li R. 2013. Estrogen synthesis and signaling pathways during aging: from periphery to brain. Trends Mol Med 19:197-209.
11. Diamanti-Kandarakis E., Bourguignon JP, Giudice L., Hauser R, Prins G. S, Soto AM, et al. 2009. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30:293-342.
12. Drinkwater N.R. 1994. Genetic control of hepatocarcinogenesis in C3H mice. Drug Metab Rev 26:201-208.
13. Eaton K. A, Opp JS, Gray BM, Bergin IL, Young VB. 2011. Ulcerative typhlocolitis associated with Helicobacter mastomyrinus in telomerase-deficient mice. Vet Pathol 48:713-725.
14. Giannitrapani L., Soresi M, La Spada E, Cervello M, D'Alessandro N, Montalto G. 2006. Sex hormones and risk of liver tumor. Ann NY Acad Sci 1089:228-236.
15. Goodson W. H, Luciani MG, Sayeed SA, Jaffee IM, Moore DH, Dairkee S.H. 2011. Activation of the mTOR pathway by low levels of xenoestrogens in breast epithelial cells from high-risk women. Carcinogenesis 32:1724-1733.
16. Hassan Z. K, Elobeid MA, Virk P, Omer SA, ElAmin M, Daghestani M. H, et al. 2012. Bisphenol A induces hepatotoxicity through oxidative stress in rat model. Oxid Med Cell Longev 2012:194829; doi:10.1155/2012/194829
17. Hayashi S., Fujii E, Kato A, Kimura K, Mizoguchi K, Suzuki M, et al. 2008. Characterization of multinuclear hepatocytes induced in rats by mitemcinal (GM-611), an erythromycin derivative. Toxicol Pathol 36:858-865.
18. Hoenerhoff M. J, Pandiri AR, Lahousse SA, Hong HH, Ton TV, Masinde T., et al. 2011. Global gene profiling of spontaneous hepatocellular carcinoma in B6C3F1 mice: similarities in the molecular landscape with human liver cancer. Toxicol Pathol 39:678-699.
19. Hunt P. A, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt R. C, et al. 2003. Bisphenol A exposure causes meiotic aneuploidy in the female mouse. Curr Biol 13:546-553.
20. Institute of Laboratory Animal Resources. 1996. Guide for the Care and Use of Laboratory Animals. Washington, DC:National Academy Press. Available: http://www.nap. edu/catalog.php?record_id=5140 [accessed 24 February 2014].
21. Kops G. JPL, Weaver BAA, Cleveland DW. 2005. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer 5:773-785.
22. Lang I. A, Galloway TS, Scarlett A, Henley WE, Depledge M, Wallace R. B, et al. 2008. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300:1303-1310.
23. Maronpot R.R. 2009. Biological basis of differential susceptibility to hepatocarcinogenesis among mouse strains. J Toxicol Pathol 22:11-33.
24. Moon M. K, Kim MJ, Jung IK, Koo YD, Ann HY, Lee KJ, et al. 2012. Bisphenol A impairs mitochondrial function in the liver at doses below the no observed adverse effect level. J Korean Med Sci 27:644-652.
25. NTP (National Toxicology Program). 1982. Carcinogenesis Bioassay of Bisphenol A (CAS No. 80-05-7) in F344 Rats and B6C3F1 Mice (Feed Study). Technical Report 215. Research Triangle Park, NC:NTP. Available: http://ntp.niehs.nih.gov/ ntp/htdocs/LT_rpts/tr215.pdf [accessed 4 March 2014].
26. Prins G. S, Tang WY, Belmonte J, Ho SM. 2008. Perinatal exposure to oestradiol and bisphenol A alters the prostate epigenome and increases susceptibility to carcinogenesis. Basic Clin Pharmacol Toxicol 102:134-138.
27. Ramirez M. C, Bourguignon NS, Bonaventura MM, Lux-Lantos V, Libertun C., Becu-Villalobo, D. 2012. Neonatal xenoestrogen exposure alters growth hormone-dependent liver proteins and genes in adult female rats. Toxicol Lett 213:325-331.
28. Scampini G., Nava A, Newman AJ, Della Torre P, Mazué G. 1993. Multinucleated hepatocytes induced by rifabutin in rats. Toxicol Pathol 21:369-376.
29. Shaw J. J, Shah SA. 2011. Rising incidence and demographics of hepatocellular carcinoma in the USA: What does it mean? Expert Rev Gastroenterol Hepatol 5:365-370.
30. Sieli P. T, Jašarevic E, Warzak DA, Ma, J, Ellersieck MR, Liao C, et al. 2011. Comparison of serum bisphenol A concentrations in mice exposed to bisphenol A through the diet versus oral bolus exposure. Environ Health Perspect 119:1260-1265; doi:10.1289/ehp.1003385.
31. Thoolen B., Maronpot RR, Harada T, Nyska A, Rousseaux C, Nolte T. et al. 2010. Proliferative and nonproliferative lesions of the rat and mouse hepatobiliary system. Toxicol Pathol 38(7 suppl):5S-81S.
32. Vandenberg L. N, Ehrlich S, Belcher SM, Ben-Jonathan N, Dolinoy D. C, Hugo ER, et al. 2013. Low dose effects of Bisphenol A: an integrated review of in vitro, laboratory animal, and epidemiology studies. Endocr Disruptors 1(1):e25078; doi:10.4161/endo.26490.
33. Vandenberg L. N, Maffini MV, Wadia PR, Sonnenschein C, Rubin B. S, Soto AM. 2007. Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 148:116-127.
34. vom Saal FS, Akingbemi BT, Belcher SM, Birnbaum LS, Crain DA, Eriksen M. et al. 2007. Chapel Hill bisphenol A expert panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol 24:131-138.
35. Waterland R. A, Jirtle RL. 2003. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23:5293-5300.
36. Wu J. F, Tsai WY, Hsu HY, Ni YH, Chen HL, Tsuei DJ. 2010. Effect of puberty onset on spontaneous hepatitis B virus e antigen seroconversion in men. Gastroenterology 138:942-948. e1; doi: 10.1053/j.gastro.2009.11.051.
37. Wunderlich M. L, Dodge ME, Dhawan RK, Shek WR. 2011. Multiplexed fluorometric immunoassay testing methodology and troubleshooting. J Vis Exp 58:e3715, doi:10.3791/3715.
38. Zalko D., Soto AM, Dolo L, Dorio C, Rathahao E, Debrauwer L, et al. 2003. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ Health Perspect 111:309-319; doi:10.1289/ehp.5603.