Lifelong Exposure to Bisphenol A Alters Cardiac Structure/Function, Protein Expression, and DNA Methylation in Adult Mice
Abstract
Bisphenol A (BPA) is an estrogenizing endocrine disruptor compound of concern. Our objective was to test whether lifelong BPA would impact cardiac structure/function, calcium homeostasis protein expression, and the DNA methylation of cardiac genes. We delivered 0.5 and 5.0 µg/kg/day BPA lifelong from gestation day 11 or 200 µg/kg/day from gestation day 11 to postnatal day 21 via the drinking water to C57bl/6n mice. BPA 5.0 males and females had increased body weight, body mass index, body surface area, and adiposity. Echocardiography identified concentric remodeling in all BPA-treated males. Systolic and diastolic cardiac functions were essentially similar, but lifelong BPA enhanced male and reduced female sex-specific differences in velocity of circumferential shortening and ascending aorta velocity time integral. Diastolic blood pressure was increased in all BPA females. The calcium homeostasis proteins sarcoendoplasmic reticulum ATPase 2a (SERCA2a), sodium calcium exchanger-1, phospholamban (PLB), phospho-PLB, and calsequestrin 2 are important for contraction and relaxation. Changes in their expression suggest increased calcium mobility in males and reduced calcium mobility in females supporting the cardiac function changes. DNA methyltransferase 3a expression was increased in all BPA males and BPA 0.5 females and reduced in BPA 200 females. Global DNA methylation was increased in BPA 0.5 males and reduced in BPA 0.5 females. BPA induced sex-specific altered DNA methylation in specific CpG pairs in the calsequestrin 2 CpG island. These results suggest that continual exposure to BPA impacts cardiac structure/function, protein expression, and epigenetic DNA methylation marks in males and females.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Epigenetic alterations have been implicated in BPA-associated changes in pathology and function in several hormone-responsive tissues including the brain.
“Epigenetic alterations have been implicated in BPA-associated changes in pathology and function in several hormone-responsive tissues including the brain [ 49 , 130 , 138–141 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [140]
Cites
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) · Journal of the American Society of Echocardiography · doi:10.1016/j.echo.2005.10.005 · Cited by 11,318 · see citing works
Functions of DNA methylation: islands, start sites, gene bodies and beyond
Jones, P. A. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3230 · Cited by 6,061 · see citing works
Nagueh, S. F., Middleton, K. J., Kopelen, H. A., Zoghbi, W. A., & Quiñones, M. A. (1997) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(97)00344-6 · Cited by 3,024 · see citing works
Building the mammalian heart from two sources of myocardial cells
BUCKINGHAM, M. E., Meilhac, S. M., & Zaffran, S. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1710 · Cited by 1,196 · see citing works
In vivo effects of bisphenol A in laboratory rodent studies
Richter, C. A., Birnbaum, L. S., Farabollini, F., Newbold, R. R., Rubin, B. S., Talsness, C. E., Vandenbergh, J. G., Walser-Kuntz, D. R., & vom Saal, F. S. (2007) · Reproductive Toxicology · doi:10.1016/j.reprotox.2007.06.004 · Cited by 1,147 · see citing works
A review of dietary and non-dietary exposure to bisphenol-A
Geens, T., Aerts, D., Berthot, C., Bourguignon, J.-P., Goeyens, L., Lecomte, P., Maghuin‐Rogister, G., Pironnet, A.-M., Pussemier, L., Scippo, M., et al. (2012) · Food and Chemical Toxicology · doi:10.1016/j.fct.2012.07.059 · Cited by 976 · see citing works
Environmental chemicals in pregnant women in the United States: NHANES 2003–2004
Woodruff, T. J., Zota, A. R., & Schwartz, J. M. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1002727 · Cited by 930 · see citing works
The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity
Saal, F. S. V., Nagel, S. C., Coe, B., Angle, B. M., & Taylor, J. A. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.01.001 · Cited by 449 · see citing works
Clarke, M. E., Knight, S., & Prozesky, D. R. (2003) · Cited by 440 · see citing works
Timms, B. G., Howdeshell, K. L., Barton, L., Bradley, S., Richter, C. A., & vom Saal, F. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502544102 · Cited by 394 · see citing works
Wolstenholme, J. T., Edwards, M., Shetty, S. R. J., Gatewood, J. D., Taylor, J. A., Rissman, E. F., & Connelly, J. J. (2012) · Endocrinology · doi:10.1210/en.2012-1195 · Cited by 319 · see citing works
Melzer, D. R., Osborne, N. J., Henley, W., Cipelli, R., Young, A., Money, C., McCormack, P., Luben, R., Khaw, K., Wareham, N. J., et al. (2012) · Circulation · doi:10.1161/circulationaha.111.069153 · Cited by 303 · see citing works
Bromer, J. G., Zhou, Y., Taylor, M. B., Doherty, L. F., & Taylor, H. S. (2010) · The FASEB Journal · doi:10.1096/fj.09-140533 · Cited by 303 · see citing works
Bisphenol A: Perinatal exposure and body weight
Rubin, B. S., & Soto, A. M. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.02.023 · Cited by 272 · see citing works
Yaoi, T., Itoh, K., Nakamura, K., Ogi, H., Fujiwara, Y., & Fushiki, S. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.09.028 · Cited by 229 · see citing works
Lind, P., & Lind, L. (2011) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2011.05.001 · Cited by 218 · see citing works
Sex is a potent modifier of the cardiovascular system
Leinwand, L. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci19429 · Cited by 190 · see citing works
Bisphenol A and Peripheral Arterial Disease: Results from the NHANES
Shankar, A., Teppala, S., & Sabanayagam, C. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104114 · Cited by 190 · see citing works
Noninvasive Assessment of Murine Pulmonary Arterial Pressure
Thibault, H., Kurtz, B., Raher, M. J., Shaik, R. S., Waxman, A. B., Dérumeaux, G., Halpern, E. F., Bloch, K. D., & Scherrer‐Crosbie, M. (2009) · Circulation Cardiovascular Imaging · doi:10.1161/circimaging.109.887109 · Cited by 182 · see citing works
Associations of Bisphenol A Exposure With Heart Rate Variability and Blood Pressure
Bae, S., Kim, J. H., Lim, Y., Park, H. Y., & Hong, Y. (2012) · Hypertension · doi:10.1161/hypertensionaha.112.197715 · Cited by 177 · see citing works
Histology Atlas of the Developing Mouse Heart with Emphasis on E11.5 to E18.5
Savolainen, S. M., Foley, J. F., & Elmore, S. A. (2009) · Toxicologic Pathology · doi:10.1177/0192623309335060 · Cited by 175 · see citing works
Transgenerational neuroendocrine disruption of reproduction
Walker, D. M., & Gore, A. C. (2011) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2010.215 · Cited by 167 · see citing works
Tang, W.-Y., Morey, L. M., Cheung, Y. Y., Birch, L., Prins, G. S., & Ho, S.-M. (2012) · Endocrinology · doi:10.1210/en.2011-1308 · Cited by 164 · see citing works
Sex is a potent modifier of the cardiovascular system
Leinwand, L. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319429 · Cited by 161 · see citing works
Yan, S., Chen, Y., Dong, M., Song, W., Belcher, S. M., & Wang, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025455 · Cited by 157 · see citing works
Formation of the Building Plan of the Human Heart
Sizarov, A., Ya, J., de Boer, B. A., Lamers, W. H., Christoffels, V. M., & Moorman, A. F. M. (2011) · Circulation · doi:10.1161/circulationaha.110.980607 · Cited by 154 · see citing works
Luczak, E. D., & Leinwand, L. A. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163156 · Cited by 143 · see citing works
Xiao, S., Diao, H., Smith, M. A., Song, X., & Ye, X. (2011) · Reproductive Toxicology · doi:10.1016/j.reprotox.2011.08.010 · Cited by 126 · see citing works
Use of NHANES Data to Link Chemical Exposures to Chronic Diseases: A Cautionary Tale
LaKind, J. S., Goodman, M. G., & Naiman, D. Q. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051086 · Cited by 116 · see citing works
Maternal and Social Origins of Hypertension
Barker, D. J. P., Osmond, C., Forsén, T., Kajantie, E., & Eriksson, J. G. (2007) · Hypertension · doi:10.1161/hypertensionaha.107.091512 · Cited by 112 · see citing works
Body Surface Area Prediction in Normal, Hypermuscular, and Obese Mice
Cheung, M. C., Spalding, P. B., Gutierrez, J. C., Balkan, W., Namias, N., Koniaris, L. G., & Zimmers, T. A. (2008) · Journal of Surgical Research · doi:10.1016/j.jss.2008.05.002 · Cited by 107 · see citing works
Belcher, S. M., Chen, Y., Yan, S., & Wang, H. (2011) · Endocrinology · doi:10.1210/en.2011-1772 · Cited by 102 · see citing works
Quantitative Assessment of Regional Myocardial Function in Mice by Tissue Doppler Imaging
Sebag, I. A., Handschumacher, M. D., Ichinose, F., Morgan, J. G., Hataishi, R., Rodrigues, A. C. T., Guerrero, J. L., Steudel, W., Raher, M. J., Halpern, E. F., et al. (2005) · Circulation · doi:10.1161/circulationaha.104.474411 · Cited by 98 · see citing works
Self-citationDoppler echocardiographic estimation of left ventricular end-diastolic pressure after MI in rats
Prunier, F., Gaertner, R., Louedec, L., Michel, J., Mercadier, J.-J., & Escoubet, B. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01050.2001 · Cited by 91 · see citing works
Bisphenol A Binds to the Local Anesthetic Receptor Site to Block the Human Cardiac Sodium Channel
O’Reilly, A. O., Eberhardt, E., Weidner, C., Alzheimer, C., Wallace, B. A., & Lampert, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041667 · Cited by 69 · see citing works
Unraveling the secrets of a double life: Contractile versus signaling Ca2+ in a cardiac myocyte
Goonasekera, S. A., & Molkentin, J. D. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.05.001 · Cited by 67 · see citing works
Sebag, I. A., Gillis, M., Calderone, A., Kasneci, A., Meilleur, M., Haddad, R., Noiles, W., Patel, B. B., & Chalifour, L. E. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00088.2011 · Cited by 54 · see citing works
Self-citationExposure to bisphenol A in Canada: invoking the precautionary principle
Vandenberg, L. N. (2011) · Canadian Medical Association Journal · doi:10.1503/cmaj.101408 · Cited by 50 · see citing works
Perspectives on endocrine disruptor effects on metabolic sensors
Migliarini, B., Piccinetti, C. C., Martella, A., Maradonna, F., Gioacchini, G., & Carnevali, O. (2010) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2010.11.025 · Cited by 48 · see citing works
Factors controlling the activity of the SERCA2a pump in the normal and failing heart
Vandecaetsbeek, I., Raeymaekers, L., Wuytack, F., & Vangheluwe, P. (2009) · BioFactors · doi:10.1002/biof.63 · Cited by 47 · see citing works
Zarain‐Herzberg, Á., Estrada‐Avilés, R., & Fragoso-Medina, J. A. (2012) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y2012-057 · Cited by 34 · see citing works
Obesity and the developmental origins of health and disease
Kemp, M. W., Kallapur, S. G., Jobe, A. H., & Newnham, J. P. (2011) · Journal of Paediatrics and Child Health · doi:10.1111/j.1440-1754.2010.01940.x · Cited by 31 · see citing works
Egr-1 negatively regulates calsequestrin expression and calcium dynamics in ventricular cells
Kasneci, A., Kemeny-Suss, N. M., Komarova, S. V., & Chalifour, L. E. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn357 · Cited by 29 · see citing works
Self-citationHaddad, R., Kasneci, A., Mepham, K., Sebag, I. A., & Chalifour, L. E. (2012) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2012.10.018 · Cited by 21 · see citing works
Self-citationDevelopmental exposure to bisphenol A leads to cardiometabolic dysfunction in adult mouse offspring
Cagampang, F. R. A., Torrens, C., Anthony, F. W., & Hanson, M. A. (2012) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174412000153 · Cited by 19 · see citing works
Modulation of SR C a 2 +release by the triadin-to-calsequestrin ratio in ventricular myocytes
Kučerová, D., Baba, H. A., Boknı́k, P., Fabritz, L., Heinick, A., Máťuš, M., Müller, F. U., Neumann, J., Schmitz, W. L., & Kirchhefer, U. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00457.2011 · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
EFSA Panel on Food Contact Materials, E. A. P. A. (., Lambré, C., Baviera, J. M. B., Bolognesi, C., Chesson, A., Cocconcelli, P. S., Crebelli, R., Gott, D. M., Grob, K., Lampi, E., et al. (2023) · EFSA Journal · doi:10.2903/j.efsa.2023.6857 · Cited by 431 · see citing works
Low dose effects of bisphenol A
Vandenberg, L. N., Ehrlich, S., Belcher, S. M., Ben‐Jonathan, N., Dolinoy, D. C., Hugo, E. R., Hunt, P. A., Newbold, R. R., Rubin, B. S., Saili, K. S., et al. (2013) · Endocrine Disruptors · doi:10.4161/endo.26490 · Cited by 238 · see citing works
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
Gao, X., & Wang, H. (2014) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph110808399 · Cited by 168 · see citing works
Transgenerational inheritance of heart disorders caused by paternal bisphenol A exposure
Lombó, M., Fernández-Díez, C., González-Rojo, S., Navarro, C., Robles, V., & Herráez, M. P. (2015) · Environmental Pollution · doi:10.1016/j.envpol.2015.08.016 · Cited by 150 · see citing works
Cardiovascular toxicity and mechanism of bisphenol A and emerging risk of bisphenol S
Zhang, Y., Shan, C., Wang, Y., Qian, L.-L., Jia, D., Zhang, Y., Hao, X., & Xu, H. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.137952 · Cited by 143 · see citing works
Moon, S., Yu, S. H., Lee, C. B., Park, Y. J., Yoo, H. J., & Kim, D. S. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.142941 · Cited by 133 · see citing works
Ezz, H. S. A., Khadrawy, Y. A., & Mourad, I. M. (2013) · Cytotechnology · doi:10.1007/s10616-013-9672-1 · Cited by 126 · see citing works
Bao, W., Liu, B., Rong, S., Dai, S. Y., Trasande, L., & Lehmler, H. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.11620 · Cited by 128 · see citing works
The Adverse Cardiac Effects of Di(2-ethylhexyl)phthalate and Bisphenol A
Posnack, N. G. (2014) · Cardiovascular Toxicology · doi:10.1007/s12012-014-9258-y · Cited by 116 · see citing works
Faulk, C. D., Barks, A. K., Liu, K., Goodrich, J. M., & Dolinoy, D. C. (2013) · Epigenomics · doi:10.2217/epi.13.49 · Cited by 114 · see citing works
Prins, G. S., Patisaul, H. B., Belcher, S. M., & Vandenberg, L. N. (2018) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13125 · Cited by 107 · see citing works
Xia, W., Jiang, Y., Li, Y., Wan, Y., Liu, J., Ma, Y., Mao, Z., Chang, H., Li, G., Xu, B., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090443 · Cited by 102 · see citing works
Ramadan, M., Cooper, B. L., & Posnack, N. G. (2020) · Birth Defects Research · doi:10.1002/bdr2.1752 · Cited by 98 · see citing works
Endocrine-Disrupting Effects of Bisphenol A on the Cardiovascular System: A Review
Fonseca, M. I., Lorigo, M., & Cairrão, E. (2022) · Journal of Xenobiotics · doi:10.3390/jox12030015 · Cited by 99 · see citing works
Neurochemical and behavioral analysis by acute exposure to bisphenol A in zebrafish larvae model
Kim, S. S., Hwang, K.-S., Yang, J. Y., Chae, J. S., Kim, G. R., Kan, H., Jung, M. H., Lee, H.-Y., Song, J. S., Ahn, S., et al. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.124751 · Cited by 83 · see citing works
Chung, F. F., & Herceg, Z. (2020) · Environmental Health Perspectives · doi:10.1289/ehp6104 · Cited by 86 · see citing works
Marked for Life: Epigenetic Effects of Endocrine Disrupting Chemicals
Jacobs, M. N., Marczylo, E. L., Guerrero‐Bosagna, C., & Rüegg, J. (2017) · Annual Review of Environment and Resources · doi:10.1146/annurev-environ-102016-061111 · Cited by 81 · see citing works
Cai, S., Rao, X., Ye, J., Ling, Y., Mi, S., Chen, H., Fan, C., & Li, Y. (2020) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2020.110300 · Cited by 77 · see citing works
Şenyıldız, M., Karaman, E. F., Bas, S. S., Arda-Pirincci, P., & Özden, S. (2017) · Toxicology in Vitro · doi:10.1016/j.tiv.2017.07.028 · Cited by 76 · see citing works
Lejonklou, M. H., Dunder, L., Bladin, E., Pettersson, V., Rönn, M., Lind, L., Waldén, T. B., & Lind, P. (2017) · Environmental Health Perspectives · doi:10.1289/ehp505 · Cited by 76 · see citing works
Belcher, S. M., Gear, R. B., & Kendig, E. L. (2015) · Endocrinology · doi:10.1210/en.2014-1847 · Cited by 74 · see citing works
Perinatal Bisphenol A Exposure Increases Atherosclerosis in Adult Male PXR-Humanized Mice
Sui, Y., Park, S., Wang, F., & Zhou, C. (2018) · Endocrinology · doi:10.1210/en.2017-03250 · Cited by 70 · see citing works
Fang, C., Ning, B., Waqar, A. B., Niimi, M., Shen, L., Satoh, K., Shiomi, M., Ye, T., Dong, S., & Fan, J. (2015) · Journal of Applied Toxicology · doi:10.1002/jat.3103 · Cited by 66 · see citing works
Zhang, X., Zhang, T., Han, Z., Liu, J., Liu, Y., Ma, J., Li, L., & Shen, W. (2014) · Reproduction Fertility and Development · doi:10.1071/rd14113 · Cited by 63 · see citing works
Hu, Y., Zhang, L., Wu, X., Hou, L., Li, Z., Ju, J., Li, Q., Qin, W., Li, J., Zhang, Q., et al. (2016) · Toxicology Letters · doi:10.1016/j.toxlet.2016.03.008 · Cited by 62 · see citing works
Estrogen and Bisphenol A in Hypertension
Wehbe, Z., Nasser, S. A., EL‐Yazbi, A. F., Nasreddine, S., & Eid, A. H. (2020) · Current Hypertension Reports · doi:10.1007/s11906-020-1022-z · Cited by 61 · see citing works
Bisphenol A Exposure Enhances Atherosclerosis in WHHL Rabbits
Fang, C., Ning, B., Waqar, A. B., Niimi, M., Shen, L., Satoh, K., Shiomi, M., Ye, T., Dong, S., & Fan, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110977 · Cited by 61 · see citing works
Machuki, J. O., Zhang, H., Harding, S. E., & Sun, H. (2017) · Acta Physiologica · doi:10.1111/apha.12978 · Cited by 61 · see citing works
Data integration, analysis, and interpretation of eight academic CLARITY-BPA studies
Heindel, J. J., Belcher, S. M., Flaws, J. A., Prins, G. S., Ho, S., Mao, J., Patisaul, H. B., Ricke, W. A., Rosenfeld, C. S., Soto, A. M., et al. (2020) · Reproductive Toxicology · doi:10.1016/j.reprotox.2020.05.014 · Cited by 61 · see citing works
Jiang, Y., Xia, W., Yang, J., Zhu, Y., Chang, H., Liu, J., Huo, W., Xu, B., Chen, X., Li, Y., et al. (2015) · Toxicology · doi:10.1016/j.tox.2015.01.001 · Cited by 60 · see citing works
Bae, S., Lim, Y.-H., Lee, Y. A., Shin, C. H., Oh, S., & Hong, Y. (2016) · Hypertension · doi:10.1161/hypertensionaha.116.08281 · Cited by 60 · see citing works
Gear, R. B., Kendziorski, J. A., & Belcher, S. M. (2017) · Toxicology Letters · doi:10.1016/j.toxlet.2017.05.011 · Cited by 59 · see citing works
Lombó, M., González-Rojo, S., Fernández-Díez, C., & Herráez, M. P. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.01.004 · Cited by 57 · see citing works
Kumar, D., & Thakur, M. K. (2017) · The Journal of Toxicological Sciences · doi:10.2131/jts.42.281 · Cited by 54 · see citing works
Posnack, N. G., Brooks, D. M., Chandra, A. A., Jaimes, R., Sarvazyan, N. A., & Kay, M. W. (2015) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00272.2015 · Cited by 53 · see citing works
Byun, H., Bénachour, N., Zalko, D., Frisardi, M. C., Colicino, E., Takser, L., & Baccarelli, A. (2014) · Toxicology · doi:10.1016/j.tox.2014.12.019 · Cited by 52 · see citing works
High-Throughput Screening to Identify Chemical Cardiotoxic Potential
Krishna, S., Berridge, B., & Kleinstreuer, N. (2021) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.0c00382 · Cited by 52 · see citing works
Natural Products in Mitigation of Bisphenol A Toxicity: Future Therapeutic Use
Sirasanagandla, S. R., Al‐Huseini, I., Sakr, H. F., Moqadass, M., Das, S., Juliana, N., & Abu, I. F. (2022) · Molecules · doi:10.3390/molecules27175384 · Cited by 50 · see citing works
Moreman, J., Takesono, A., Trznadel, M., Winter, M. J., Perry, A., Wood, M. E., Rogers, N. J., Kudoh, T., & Tyler, C. R. (2018) · Environmental Science & Technology · doi:10.1021/acs.est.8b01095 · Cited by 49 · see citing works
Back to the future: transgenerational transmission of xenobiotic-induced epigenetic remodeling
Jiménez‐Chillarón, J. C., Nijland, M. J., Ascensão, A. A. M. R., Sardão, V. A., Magalhães, J., Hitchler, M. J., Domann, F. E., & Oliveira, P. J. (2015) · Epigenetics · doi:10.1080/15592294.2015.1020267 · Cited by 45 · see citing works
Valokola, M. G., Karimi, G., Razavi, B. M., Kianfar, M., Jafarian, A. H., Jaafari, M. R., & Imenshahidi, M. (2018) · Environmental Toxicology · doi:10.1002/tox.22687 · Cited by 45 · see citing works
Ferguson, M., Lorenzen‐Schmidt, I., & Pyle, W. G. (2019) · Scientific Reports · doi:10.1038/s41598-019-52350-y · Cited by 45 · see citing works
Patel, B. B., Kasneci, A., Bolt, A. M., Lalla, V. D., Iorio, M. R. D., Raad, M., Mann, K. K., & Chalifour, L. E. (2015) · Toxicological Sciences · doi:10.1093/toxsci/kfv073 · Cited by 43 · see citing works
Self-citationNeff, A. M., Blanco, S. C., Flaws, J. A., Bagchi, I. C., & Bagchi, M. K. (2019) · Endocrinology · doi:10.1210/en.2018-00872 · Cited by 41 · see citing works
Kasneci, A., Lee, J. S., Yun, T. J., Shang, J., Lampen, S. I. R., Gomolin, T., Cheong, C., & Chalifour, L. E. (2017) · Toxicological Sciences · doi:10.1093/toxsci/kfx133 · Cited by 39 · see citing works
Self-citationAwada, Z., Nasr, R., Akika, R., Cahais, V., Cuenin, C., Zhivagui, M., Herceg, Z., Ghantous, A., & Zgheib, N. K. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0725-y · Cited by 41 · see citing works
Hyun, S., Lee, C. Y., Ko, M. Y., Chon, S., Kim, Y., Seo, J., Kim, K. K., & Ka, M. (2021) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2021.115696 · Cited by 37 · see citing works
The State of Research and Weight of Evidence on the Epigenetic Effects of Bisphenol A
Nia, A. B. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24097951 · Cited by 36 · see citing works
Disruption of neonatal cardiomyocyte physiology following exposure to bisphenol-a
Ramadan, M., Sherman, M. G., Jaimes, R., Chaluvadi, A., Swift, L., & Posnack, N. G. (2018) · Scientific Reports · doi:10.1038/s41598-018-25719-8 · Cited by 36 · see citing works
Bisphenol A and its effects on the systemic organs of children
Zulkifli, S., Rahman, A. A., Kadir, S. H. S. A., & Nor, N. S. M. (2021) · European Journal of Pediatrics · doi:10.1007/s00431-021-04085-0 · Cited by 37 · see citing works
Zarain‐Herzberg, Á., Estrada‐Avilés, R., & Fragoso-Medina, J. A. (2012) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y2012-057 · Cited by 34 · see citing works
Khan, D., & Ahmed, S. A. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00091 · Cited by 34 · see citing works
Tiny trouble: microplastics, nanoplastics, and their heartfelt impact on cardiovascular health
Zhang, T., Liao, Y., Ling, J., Zhang, J., Zhang, D., Yin, X., Yu, P., & Liu, X. (2025) · Cardiovascular Research · doi:10.1093/cvr/cvaf068 · Cited by 32 · see citing works
MicroRNA expression in response to bisphenol A is associated with high blood pressure
Kim, J. H., Cho, Y. H., & Hong, Y. (2020) · Environment International · doi:10.1016/j.envint.2020.105791 · Cited by 31 · see citing works
Mohsenzadeh, M. S., Razavi, B. M., Imenshahidi, M., Mohajeri, S. A., Rameshrad, M., & Hosseinzadeh, H. (2020) · Phytotherapy Research · doi:10.1002/ptr.6861 · Cited by 31 · see citing works
Elevated Serum Bisphenol A Level in Patients with Dilated Cardiomyopathy
Xiong, Q., Liu, X., Shen, Y., Yu, P., Chen, S., Hu, J., Yu, J., Li, J., Wang, H., Cheng, X., et al. (2015) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph120505329 · Cited by 32 · see citing works
Rameshrad, M., Imenshahidi, M., Razavi, B. M., Iranshahi, M., & Hosseinzadeh, H. (2018) · Phytotherapy Research · doi:10.1002/ptr.6175 · Cited by 29 · see citing works
Effects of bisphenol A exposure during cardiac cell differentiation
Escarda‐Castro, E., Herráez, M. P., & Lombó, M. (2021) · Environmental Pollution · doi:10.1016/j.envpol.2021.117567 · Cited by 29 · see citing works
Singh, R. D., Koshta, K., Tiwari, R., Khan, H., Sharma, V., & Srivastava, V. K. (2021) · Frontiers in Toxicology · doi:10.3389/ftox.2021.663372 · Cited by 30 · see citing works
Patel, B. B., Raad, M., Sebag, I. A., & Chalifour, L. E. (2015) · Toxicology Reports · doi:10.1016/j.toxrep.2015.09.008 · Cited by 27 · see citing works
Self-citationKlint, H., Lejonklou, M. H., Karimullina, E. M., Rönn, M., Lind, L., Lind, P., & Brittebo, E. B. (2016) · Upsala Journal of Medical Sciences · doi:10.1080/03009734.2016.1225870 · Cited by 27 · see citing works
Effects of Environment and Lifestyle Factors on Premature Ovarian Failure
Yang, Y., Huang, W., & Yuan, L. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-981-33-4187-6_4 · Cited by 26 · see citing works
Camacho, L., Basavarajappa, M. S., Chang, C., Han, T., Kobets, T., Koturbash, I., Surratt, G., Lewis, S. M., Vanlandingham, M. M., Fuscoe, J. C., et al. (2015) · Food and Chemical Toxicology · doi:10.1016/j.fct.2015.04.009 · Cited by 25 · see citing works
Altered heart proteome in fructose-fed Fisher 344 rats exposed to bisphenol A
Ljunggren, S., Iggland, M., Rönn, M., Lind, L., Lind, P., & Karlsson, H. (2016) · Toxicology · doi:10.1016/j.tox.2016.02.007 · Cited by 23 · see citing works
van Esterik, J. C. J., Vitins, A. P., Hodemaekers, H. M., Kamstra, J. H., Legler, J., Pennings, J. L. A., Steegenga, W. T., Lute, C., Jelı́nek, J., Issa, J. J., et al. (2014) · Toxicology Letters · doi:10.1016/j.toxlet.2014.10.021 · Cited by 22 · see citing works
Salamanca‐Fernández, E., Rodríguez‐Barranco, M., Petrova, D., Larrañaga, N., Guevara, M., Moreno‐Iribas, C., Chirlaque, M. D., Colorado-Yohar, S. M., Arrebola, J. P., Vela-Soria, F., et al. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.127697 · Cited by 22 · see citing works
Shen, Y., Li, X., Wang, H., Wang, Y., Tao, L., Wang, P., & Zhang, H. (2023) · Toxicology · doi:10.1016/j.tox.2023.153678 · Cited by 22 · see citing works
Shang, J., Corriveau, J., Champoux-Jenane, A., Gagnon, J., Moss, E., Dumas, P., Gaudreau, É., Chevrier, J., & Chalifour, L. E. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy276 · Cited by 21 · see citing works
Self-citationMa, J., Ross, L. E., Grube, C., & Wang, H. (2024) · Chemosphere · doi:10.1016/j.chemosphere.2024.141567 · Cited by 21 · see citing works
Cheng, M.-D., Li, C., Pei, X.-Y., Zhang, Y., Jia, D., Zuo, Y.-B., Cai, S., Li, P., Xin, H., & Zhang, Y. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.115391 · Cited by 20 · see citing works
Ma, J., Hong, K., & Wang, H. (2017) · Endocrinology · doi:10.1210/en.2016-1702 · Cited by 20 · see citing works
The effects of bisphenols on the cardiovascular system ex vivo and in vivo
Tvrdý, V., Dias, P., Najmanová, I., Carazo, A., Jirkovský, E., Pourová, J., Fadraersada, J., Moravcová, M., Mašič, L. P., Dolenc, M. S., et al. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.137565 · Cited by 19 · see citing works
Filice, M., Leo, S., Mazza, R., Amelio, D., Garofalo, F., Imbrogno, S., Cerra, M. C., & Gattuso, A. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.116177 · Cited by 17 · see citing works
Liu, J., Chen, T., Wang, S., Wu, H., & Xu, S. (2022) · Toxicology · doi:10.1016/j.tox.2022.153190 · Cited by 17 · see citing works
Sex-specific effects of bisphenol A on the signaling pathway of ESRRG in the human placenta
Zou, Z., Harris, L. K., Forbes, K. A., & Heazell, A. E. P. (2022) · Biology of Reproduction · doi:10.1093/biolre/ioac044 · Cited by 16 · see citing works
Evaluation of the bisphenol A-induced vascular toxicity on human umbilical artery
Fonseca, M. I., Lorigo, M., & Cairrão, E. (2023) · Environmental Research · doi:10.1016/j.envres.2023.115628 · Cited by 16 · see citing works
Haddad, R., Kasneci, A., Sebag, I. A., & Chalifour, L. E. (2013) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2013-0014 · Cited by 16 · see citing works
Self-citationKoneva, L. A., Vyas, A. K., McEachin, R. C., Puttabyatappa, M., Wang, H. ‐., Sartor, M. A., & Padmanabhan, V. (2017) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22071 · Cited by 16 · see citing works
Alexandre‐Santos, B., Reis, G. D. S., Medeiros, G. R., Stockler‐Pinto, M. B., Oliveira, N. D. S. D. A., Miranda‐Alves, L., da Nóbrega, A. C. L., Magliano, D. C., & Frantz, E. D. C. (2024) · Environmental Research · doi:10.1016/j.envres.2024.119781 · Cited by 15 · see citing works
Endocrine Disruption and Reproductive Pathology
Belcher, S. M., Cline, J. M., Conley, J. M., Groeters, S., Jefferson, W. N., Law, M., Mackey, E. E., Suen, A. A., Williams, C. J., Dixon, D., et al. (2019) · Toxicologic Pathology · doi:10.1177/0192623319879903 · Cited by 15 · see citing works
Bayav, İ., Darendelioğlu, E., & Çağlayan, C. (2024) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.23655 · Cited by 14 · see citing works
Ryu, D., Rahman, M. S., & Pang, M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18091909 · Cited by 13 · see citing works
Gan, P., Baicu, C. F., Watanabe, H., Wang, K., Tao, G., Judge, D. P., Zile, M. R., Makita, T., Mukherjee, R. D., & Sucov, H. M. (2020) · Human Molecular Genetics · doi:10.1093/hmg/ddaa234 · Cited by 12 · see citing works
Application of the Key Characteristics of Carcinogens to Bisphenol A
Ricker, K., Cheng, V., Hsieh, C., Tsai, F. C., Osborne, G., Li, K., Yilmazer-Musa, M., Sandy, M. S., Cogliano, V. J., Schmitz, R., et al. (2024) · International Journal of Toxicology · doi:10.1177/10915818231225161 · Cited by 11 · see citing works
The effect of endocrine disruptors on the cardiovascular system: does sex matter?
Assenza, M. R., Gaggi, G., Credico, A. D., Ghinassi, B., & Barbagallo, F. (2025) · Environmental Research · doi:10.1016/j.envres.2025.121612 · Cited by 10 · see citing works
Linking bisphenol potential with deleterious effect on immune system: a review
Jain, R., Jain, A. K., Jain, S., Thakur, S. S., & Jain, S. K. (2022) · The Nucleus · doi:10.1007/s13237-022-00383-6 · Cited by 10 · see citing works
Rubinstein, J., Pinney, S. M., Xie, C., & Wang, H. (2024) · Environmental Health · doi:10.1186/s12940-024-01114-x · Cited by 9 · see citing works
Yoon, D.-S., Kim, J.-S., Hong, M.-S., Byeon, E., Sayed, A. E. H., Park, H. G., Lee, J., & Lee, M. (2024) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2024.116553 · Cited by 8 · see citing works
Ma, J., Niklewski, P., & Wang, H. (2022) · Food and Chemical Toxicology · doi:10.1016/j.fct.2022.113589 · Cited by 8 · see citing works
Feiteiro, J., Rocha, S. M., Mariana, M., Maia, C. J., & Cairrão, E. (2022) · Toxics · doi:10.3390/toxics10090529 · Cited by 7 · see citing works
Kamaludin, R., Rasdi, Z., Othman, M. H. D., & Kadir, S. H. S. A. (2024) · Sustainable Environment Research · doi:10.1186/s42834-024-00219-9 · Cited by 6 · see citing works
Visker, J. R., Dangott, L. J., Leszczynski, E. C., & Ferguson, D. P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249459 · Cited by 6 · see citing works
Olasunkanmi, O. I., Aremu, J., Wong, M., Licinio, J., & Zheng, P. (2024) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.10.028 · Cited by 6 · see citing works
Sirasanagandla, S. R., Mushaiqri, M. A., Ghafri, F. A., Al-Abri, N., & Al‐Huseini, I. (2023) · Applied Sciences · doi:10.3390/app132413163 · Cited by 4 · see citing works
Jenzri, M., Bouraoui, Z., Guerbèj, H., Jebali, J., & Gharred, T. (2025) · Ecotoxicology · doi:10.1007/s10646-025-02925-5 · Cited by 3 · see citing works
The EDCs as epigenetic disruptors: Implications for development and health
Herráez, M. P., Lombó, M., & González-Rojo, S. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-824464-7.00022-2 · Cited by 3 · see citing works
Miller, R. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803239-8.00007-7 · Cited by 3 · see citing works
Camacho, L., & Pogribny, I. P. (2017) · Springer eBooks · doi:10.1007/978-3-319-31143-2_32-1 · Cited by 2 · see citing works
Khan, N. M., Scott, V., Ghasemzadeh‐Hasankolaei, M., Padmanabhan, V., Vyas, A. K., Evans, N. P., & Bellingham, M. (2025) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2025.104669 · Cited by 2 · see citing works
- Authors
- Patel, B. B., Raad, M., Sebag, I. A., & Chalifour, L. E.
- Affiliations
- Jewish General Hospital (CA)
- Venue
- Toxicological Sciences
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-02-15
- Volume
- 133
- Issue
- 1
- Pages
- 174-185
- ISSN
- 1096-0929 (ISSN-L)
- 1096-6080
- OpenAlex
- W2163044427
- Cited by
- 114
- References
- 45
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 9 · 2023: 7 · 2022: 8 · 2021: 6 · 2020: 16 · 2019: 7 · 2018: 7 · 2017: 12 · 2016: 6 · 2015: 12 · 2014: 7 · 2013: 5 · 2012: 1
- FWCI
- 7.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Toxicological Sciences (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Canadian Institutes of Health Research (MOP -89788)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Keywords
- bisphenol A, endocrine disruptors, cardiac structure and function, calcium homeostasis, DNA methylation, sex differences, cardiac remodeling, SERCA2a, phospholamban, CASQ2, DNMT3A, global DNA methylation, CpG islands, diastolic blood pressure, adiposity, epigenetics
- MeSH terms
- DNA Methyltransferase 3A, Bisphenol A Compounds, Animals, Benzhydryl Compounds, Blood Pressure, Body Weight, Calcium-Binding Proteins, Carrier Proteins, Dose-Response Relationship, Drug, Echocardiography, Female, Gestational Age, Heart, Heart Function Tests, Male, Organ Size, Phenols, Pregnancy, Prenatal Exposure Delayed Effects, Sex Factors, Time Factors, DNA Methylation, Sodium-Calcium Exchanger, Mice, Endocrine Disruptors, Sarcoplasmic Reticulum Calcium-Transporting ATPases
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review