Lifelong exposure to bisphenol a alters cardiac structure/function, protein expression, and DNA methylation in adult mice

Toxicological Sciences

Volumn 133, Issue 1, 2013, Pages 174-185

  Patel, Bhavini B ^a   Raad, Mohamad ^a   Sebag, Igal A ^b   Chalifour, Lorraine E ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Cardiac function; DNA methylation; Endocrine disruptors; Endocrine toxicology; Protein expression

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CALSEQUESTRIN; CALSEQUESTRIN 2; DNA METHYLTRANSFERASE 3A; DRINKING WATER; PHOSPHOLAMBAN; PHOSPHOPHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM CALCIUM EXCHANGE PROTEIN 1; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; BODY SURFACE; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CARDIOVASCULAR PARAMETERS; CONTROLLED STUDY; CPG ISLAND; DIASTOLIC BLOOD PRESSURE; DNA METHYLATION; ECHOCARDIOGRAPHY; EPIGENETICS; FEMALE; FETUS; HEART FUNCTION; LIFELONG EXPOSURE; LONG TERM EXPOSURE; MALE; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PRENATAL EXPOSURE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEX DIFFERENCE; SYSTOLIC BLOOD PRESSURE; TISSUE STRUCTURE; WEIGHT GAIN;

ANIMALS; BENZHYDRYL COMPOUNDS; BLOOD PRESSURE; BODY WEIGHT; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ECHOCARDIOGRAPHY; ENDOCRINE DISRUPTORS; FEMALE; GESTATIONAL AGE; HEART; HEART FUNCTION TESTS; MALE; MICE; ORGAN SIZE; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SEX FACTORS; SODIUM-CALCIUM EXCHANGER; TIME FACTORS;

MUS;

EID: 84876815733     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft026     Document Type: Article

References (44)

1. Bae, S., Kim, J. H., Lim, Y. H., Park, H. Y., and Hong, Y. C. (2012). Associations of bisphenol A exposure with heart rate variability and blood pressure. Hypertension 60, 786-793.
2. Barker, D. J., Osmond, C., Forsen, T. J., Kajantie, E., and Eriksson, J. G. (2007). Maternal and social origins of hypertension. Hypertension 50, 565-571.
3. Belcher, S. M., Chen, Y., Yan, S., and Wang, H. S. (2012). Rapid estrogen receptor-mediated mechanisms determine the sexually dimorphic sensitivity of ventricular myocytes to 17β-estradiol and the environmental endocrine disruptor bisphenol A. Endocrinology 153, 712-720.
4. Bromer, J. G., Zhou, Y., Taylor, M. B., Doherty, L., and Taylor, H. S. (2010). Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J. 24, 2273-2280.
5. Buckingham, M., Meilhac, S., and Zaffran, S. (2005). Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6, 826-835.
6. Cagampang, F. R., Torrens, C., Anthony, F. W., and Hanson, M. A. (2012). Developmental exposure to bisphenol A leads to cardiometabolic dysfunction in adult mouse offspring. J. Dev. Orig. Health Dis. 3, 287-292.
7. Cheung, M. C., Spalding, P. B., Gutierrez, J. C., Balkan, W., Namias, N., Koniaris, L. G., and Zimmers, T. A. (2009). Body surface area prediction in normal, hypermuscular, and obese mice. J. Surg. Res. 153, 326-331.
8. Geens, T., Aerts, D., Berthot, C., Bourguignon, J. P., Goeyens, L., Lecomte, P., Maghuin-Rogister, G., Pironnet, A. M., Pussemier, L., Scippo, M. L., et al. (2012). A review of dietary and non-dietary exposure to bisphenol-A. Food Chem. Toxicol. 50, 3725-3740.
9. Goonasekera, S. A., and Molkentin, J. D. (2012). Unraveling the secrets of a double life: Contractile versus signaling Ca2+ in a cardiac myocyte. J. Mol. Cell. Cardiol. 52, 317-322.
10. Haddad, R., Kasneci, A., Mepham, K., Sebag, I. A., and Chalifour, L. E. (2013). Gestational exposure to diethylstilbestrol alters cardiac structure/ function, protein expression and DNA methylation in adult male mice progeny. Toxicol. Appl. Pharmacol. 266, 27-37.
11. Jones, P. A. (2012). Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13, 484-492.
12. Kasneci, A., Kemeny-Suss, N. M., Komarova, S. V., and Chalifour, L. E. (2009). Early growth factor response 1 (Egr-1) negatively regulates expression of calsequestrin in cardiomyocytes in vitro. Cardiovasc. Res. 81, 695-702.
13. Kemp, M. W., Kallapur, S. G., Jobe, A. H., and Newnham, J. P. (2012). Obesity and the developmental origins of health and disease. J. Paediatr. Child Health 48, 86-90.
14. Kučerova, D., Baba, H. A., Boknik, P., Fabritz, L., Heinick, A., Mat'uš, M., Muller, F. U., Neumann, J., Schmitz, W., and Kirchhefer, U. (2012). Modulation of SR Ca2+ release by the triadin-to-calsequestrin ratio in ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 302, H2008-H2017.
15. LaKind, J. S., Goodman, M., and Naiman, D. Q. (2012). Use of NHANES data to link chemical exposures to chronic diseases: A cautionary tale. PLoS ONE 7, e51086.
16. Lang, R. M., Bierig, M., Devereux, R. B., Flachskampf, F. A., Foster, E., Pellikka, P. A., Picard, M. H., Roman, M. J., Seward, J., Shanewise, J. S., et al. (2005). Recommendations for chamber quantification: A report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J. Am. Soc. Echocardiogr. 18, 1440-1463.
17. Leinwand, L. A. (2003). Sex is a potent modifier of the cardiovascular system. J. Clin. Invest. 112, 302-307.
18. Lind, P. M., and Lind, L. (2011). Circulating levels of bisphenol A and phthalates are related to carotid atherosclerosis in the elderly. Atherosclerosis 218, 207-213.
19. Luczak, E. D., and Leinwand, L. A. (2009). Sex-based cardiac physiology. Annu. Rev. Physiol. 71, 1-18.
20. Melzer, D., Osborne, N. J., Henley, W. E., Cipelli, R., Young, A., Money, C., McCormack, P., Luben, R., Khaw, K. T., Wareham, N. J., et al. (2012). Urinary bisphenol A concentration and risk of future coronary artery disease in apparently healthy men and women. Circulation 125, 1482-1490.
21. Migliarini, B., Piccinetti, C. C., Martella, A., Maradonna, F., Gioacchini, G., and Carnevali, O. (2011). Perspectives on endocrine disruptor effects on metabolic sensors. Gen. Comp. Endocrinol. 170, 416-423.
22. Nagueh, S. F., Middleton, K. J., Kopelen, H. A., Zoghbi, W. A., and Quinones, M. A. (1997). Doppler tissue imaging: A noninvasive technique for evaluation of left ventricular relaxation and estimation of filling pressures. J. Am. Coll. Cardiol. 30, 1527-1533.
23. O'Reilly, A. O., Eberhardt, E., Weidner, C., Alzheimer, C., Wallace, B. A., and Lampert, A. (2012). Bisphenol A binds to the local anesthetic receptor site to block the human cardiac sodium channel. PLoS ONE 7, e41667.
24. Prunier, F., Gaertner, R., Louedec, L., Michel, J. B., Mercadier, J. J., and Escoubet, B. (2002). Doppler echocardiographic estimation of left ventricular end-diastolic pressure after MI in rats. Am. J. Physiol. Heart Circ. Physiol. 283, H346-H352.
25. Richter, C. A., Birnbaum, L. S., Farabollini, F., Newbold, R. R., Rubin, B. S., Talsness, C. E., Vandenbergh, J. G., Walser-Kuntz, D. R., and vom Saal, F. S. (2007). In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 24, 199-224.
26. Rubin, B. S., and Soto, A. M. (2009). Bisphenol A: Perinatal exposure and body weight. Mol. Cell. Endocrinol. 304, 55-62.
27. Savolainen, S. M., Foley, J. F., and Elmore, S. A. (2009). Histology atlas of the developing mouse heart with emphasis on E11.5 to E18.5. Toxicol. Pathol. 37, 395-414.
28. Sebag, I. A., Gillis, M. A., Calderone, A., Kasneci, A., Meilleur, M., Haddad, R., Noiles, W., Patel, B., and Chalifour, L. E. (2011). Sex hormone control of left ventricular structure/function: Mechanistic insights using echocardiography, expression, and DNA methylation analyses in adult mice. Am. J. Physiol. Heart Circ. Physiol. 301, H1706-H1715.
29. Sebag, I. A., Handschumacher, M. D., Ichinose, F., Morgan, J. G., Hataishi, R., Rodrigues, A. C., Guerrero, J. L., Steudel, W., Raher, M. J., Halpern, E. F., et al. (2005). Quantitative assessment of regional myocardial function in mice by tissue Doppler imaging: Comparison with hemodynamics and sonomicrometry. Circulation 111, 2611-2616.
30. Shankar, A., Teppala, S., and Sabanayagam, C. (2012). Bisphenol A and peripheral arterial disease: Results from the NHANES. Environ. Health Perspect. 120, 1297-1300.
31. Sizarov, A., Ya, J., de Boer, B. A., Lamers, W. H., Christoffels, V. M., and Moorman, A. F. (2011). Formation of the building plan of the human heart: Morphogenesis, growth, and differentiation. Circulation 123, 1125-1135.
32. Tang, W. Y., Morey, L. M., Cheung, Y. Y., Birch, L., Prins, G. S., and Ho, S. M. (2012). 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, 42-55.
33. Thibault, H. B., Kurtz, B., Raher, M. J., Shaik, R. S., Waxman, A., Derumeaux, G., Halpern, E. F., Bloch, K. D., and Scherrer-Crosbie, M. (2010). Noninvasive assessment of murine pulmonary arterial pressure: Validation and application to models of pulmonary hypertension. Circ. Cardiovasc. Imaging 3, 157-163.
34. Timms, B. G., Howdeshell, K. L., Barton, L., Bradley, S., Richter, C. A., and vom Saal, F. S. (2005). Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. Proc. Natl. Acad. Sci. U.S.A. 102, 7014-7019.
35. Vandecaetsbeek, I., Raeymaekers, L., Wuytack, F., and Vangheluwe, P. (2009). Factors controlling the activity of the SERCA2a pump in the normal and failing heart. Biofactors 35, 484-499.
36. Vandenberg, L. N. (2011). Exposure to bisphenol A in Canada: Invoking the precautionary principle. CMAJ 183, 1265-1270.
37. Vom Saal, F. S., Nagel, S. C., Coe, B. L., Angle, B. M., and Taylor, J. A. (2012). The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity. Mol. Cell. Endocrinol. 354, 74-84.
38. Walker, D. M., and Gore, A. C. (2011). Transgenerational neuroendocrine disruption of reproduction. Nat. Rev. Endocrinol. 7, 197-207.
39. Wolstenholme, J. T., Edwards, M., Shetty, S. R., Gatewood, J. D., Taylor, J. A., Rissman, E. F., and Connelly, J. J. (2012). Gestational exposure to bisphenol a produces transgenerational changes in behaviors and gene expression. Endocrinology 153, 3828-3838.
40. Woodruff, T. J., Zota, A. R., and Schwartz, J. M. (2011). Environmental chemicals in pregnant women in the United States: NHANES 2003-2004. Environ. Health Perspect. 119, 878-885.
41. Xiao, S., Diao, H., Smith, M. A., Song, X., and Ye, X. (2011). Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reprod. Toxicol. 32, 434-441.
42. Yan, S., Chen, Y., Dong, M., Song, W., Belcher, S. M., and Wang, H. S. (2011). Bisphenol A and 17β-estradiol promote arrhythmia in the female heart via alteration of calcium handling. PLoS ONE 6, e25455.
43. Yaoi, T., Itoh, K., Nakamura, K., Ogi, H., Fujiwara, Y., and Fushiki, S. (2008). Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem. Biophys. Res. Commun. 376, 563-567.
44. Zarain-Herzberg, A., Estrada-Aviles, R., and Fragoso-Medina, J. (2012). Regulation of sarco(endo)plasmic reticulum Ca2+-ATPase and calsequestrin gene expression in the heart. Can. J. Physiol. Pharmacol. 90, 1017-1028.