Physiological response of cardiac tissue to bisphenol a: Alterations in ventricular pressure and contractility

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 2, 2015, Pages H267-H275

  Posnack, Nikki Gillum ^a   Brooks, Daina ^b   Chandra, Akhil ^b   Jaimes, Rafael ^b   Sarvazyan, Narine ^a   Kay, Matthew ^b  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b The George Washington University   (United States)

Author keywords

Calcium handling; Cardiac; Contraction; Endocrine disrupting chemical; Heart

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CALCIUM ION; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; FEMALE; HEART LEFT VENTRICLE PRESSURE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART PACING; HEART PERFORMANCE; HEART VENTRICLE PRESSURE; INOTROPISM; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SINUS RHYTHM; ANIMAL; CALCIUM SIGNALING; CELL CULTURE; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; HEART CONTRACTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CONDUCTION SYSTEM; HEART RATE; HEART VENTRICLE; IN VITRO STUDY; METABOLISM; NEWBORN; PATHOPHYSIOLOGY; SEX DIFFERENCE; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; ANIMALS, NEWBORN; BENZHYDRYL COMPOUNDS; CALCIUM SIGNALING; CARDIAC PACING, ARTIFICIAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HEART CONDUCTION SYSTEM; HEART RATE; HEART VENTRICLES; IN VITRO TECHNIQUES; MALE; MYOCARDIAL CONTRACTION; PHENOLS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; TIME FACTORS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR PRESSURE;

EID: 84937431769     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00272.2015     Document Type: Article

References (60)

1. Aekplakorn W, Chailurkit LO, Ongphiphadhanakul B. Association of serum bisphenol a with hypertension in thai population. Int J Hypertens 2015: 594189, 2015.
2. Aris A. Estimation of bisphenol A (BPA) concentrations in pregnant women, fetuses and nonpregnant women in Eastern Townships of Canada. Reprod Toxicol 45C: 8-13, 2013.
3. Arutunyan A, Webster DR, Swift LM, Sarvazyan N. Localized injury in cardiomyocyte network: a new experimental model of ischemia-reperfusion arrhythmias. Am J Physiol Heart Circ Physiol 280: H1905-H1915, 2001.
4. Azar T, Sharp J, Lawson D. Heart rates of male and female Sprague- Dawley and spontaneously hypertensive rats housed singly or in groups. J Am Assoc Lab Anim Sci 50: 175-184, 2011.
5. Bae S, Hong YC. Exposure to bisphenol A from drinking canned beverages increases blood pressure: randomized crossover trial. Hypertension 65: 313-319, 2015.
6. Bae S, Kim JH, Lim YH, Park HY, Hong YC. Associations of bisphenol A exposure with heart rate variability and blood pressure. Hypertension 60: 786-793, 2012.
7. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP, Kobeissi ZA, Hobai IA, Lemmon CA, Burnett AL, O’Rourke B, Rodriguez ER, Huang PL, Lima JAC, Berkowitz DE, Hare JM. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416: 337-339, 2002.
8. Becker K, Göen T, Seiwert M, Conrad A, Pick-Fuss H, Müller J, Wittassek M, Schulz C, Kolossa-Gehring M. GerES IV: phthalate metabolites and bisphenol A in urine of German children. Int J Hyg Environ Health 212: 685-692, 2009.
9. Bers DM, Grandi E. Calcium/calmodulin-dependent kinase II regulation of cardiac ion channels. J Cardiovasc Pharmacol 54: 180-187, 2009.
10. Bers DM, Guo T. Calcium signaling in cardiac ventricular myocytes. Ann NY Acad Sci 1047: 86-98, 2005.
11. Bers DM. Excitation-Contraction Coupling and Cardiac Contractile Force (2nd ed.). The Netherlands: Springer, 2001.
12. Bers DM. Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 70: 23-49, 2008.
13. Bokkers BG, Slob W. A comparison of ratio distributions based on the NOAEL and the benchmark approach for subchronic-to-chronic extrapolation. Toxicol Sci 85: 1033-1040, 2005.
14. Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113: 391-395, 2005.
15. Calafat AM, Weuve J, Ye X, Jia LT, Hu H, Ringer S, Huttner K, Hauser R. Exposure to bisphenol A and other phenols in neonatal intensive care unit premature infants. Environ Health Perspect 117: 639-644, 2009.
16. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect 116: 39-44, 2008.
17. Deutschmann A, Hans M, Meyer R, Häberlein H, Swandulla D. Bisphenol A inhibits voltage-activated Ca2_ channels in vitro: mechanisms and structural requirements. Mol Pharmacol 83: 501-511, 2013.
18. Duty SM, Mendonca K, Hauser R, Calafat AM, Ye X, Meeker JD, Ackerman R, Cullinane J, Faller J, Ringer S. Potential sources of bisphenol A in the neonatal intensive care unit. Pediatrics 131: 483-489, 2013.
19. Endoh M. Force-frequency relationship in intact mammalian ventricular myocardium: physiological and pathophysiological relevance. Eur J Pharmacol 500: 73-86, 2004.
20. Gao X, Liang Q, Chen Y, Wang HS. Molecular mechanisms underlying the rapid arrhythmogenic action of bisphenol A in female rat hearts. Endocrinology 154: 4607-4617, 2013.
21. Geens T, Aerts D, Berthot C, Bourguignon JP, Goeyens L, Lecomte P, Maghuin-Rogister G, Pironnet AM, Pussemier L, Scippo ML, Van Loco J, Covaci A. A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol 50: 3725-3740, 2012.
22. Geens T, Goeyens L, Covaci A. Are potential sources for human exposure to bisphenol-A overlooked? Int J Hyg Environ Health 214: 339-347, 2011.
23. Gillis AM, Kulisz E, Mathison HJ. Cardiac electrophysiological variables in blood-perfused and buffer-perfused, isolated, working rabbit heart. Am J Physiol Heart Circ Physiol 271: H784-H789, 1996.
24. Hormann AM, Vom Saal FS, Nagel SC, Stahlhut RW, Moyer CL, Ellersieck MR, Welshons WV, Toutain PL, Taylor JA. Holding thermal receipt paper and eating food after using hand sanitizer results in high serum bioactive and urine total levels of bisphenol A (BPA). PLos One 9: e110509, 2014.
25. Jalife J, Zipes DP. Cardiac Electrophysiology (5th ed.). Philadelphia, PA: Saunders/Elsevier, 2009, p.1155.
26. Janssen PML, Periasamy M. Determinants of frequency-dependent contraction and relaxation of mammalian myocardium. J Mol Cell Cardiol 43: 523-531, 2007.
27. Kaddar N, Bendridi N, Harthe C, de Ravel MR, Bienvenu AL, Cuilleron CY, Mappus E, Pugeat M, Dechaud H. Development of a radioimmunoassay for the measurement of bisphenol A in biological samples. Anal Chim Acta 645: 1-4, 2009.
28. Katz AM, Lorell BH. Regulation of cardiac contraction and relaxation. Circulation 102: IV-69-IV-74, 2000.
29. Khan SA, Skaf MW, Harrison RW, Lee K, Minhas KM, Kumar A, Fradley M, Shoukas AA, Berkowitz DE, Hare JM. Nitric oxide regulation of myocardial contractility and calcium cycling: independent impact of neuronal and endothelial nitric oxide synthases. Circ Res 92: 1322-1329, 2003.
30. Klabunde R. Cardiovascular Physiology Concepts (2nd. ed.). Baltimore, MD: Lippincott, Williams & Wilkins, 2011.
31. Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, Wallace RB, Melzer D. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300: 1303-1310, 2008.
32. Lee YJ, Ryu HY, Kim HK, Min CS, Lee JH, Kim E, Nam BH, Park JH, Jung JY, Jang DD, Park EY, Lee KH, Ma JY, Won HS, Im MW, Leem JH, Hong YC, Yoon HS. Maternal and fetal exposure to bisphenol A in Korea. Reprod Toxicol 25: 413-419, 2008.
33. Liang Q, Gao X, Chen Y, Hong K, Wang HS. Cellular mechanism of the nonmonotonic dose response of bisphenol A in rat cardiac myocytes. Environ Health Perspect 122: 601-608, 2014.
34. Lind PM, Lind L. Circulating levels of bisphenol A and phthalates are related to carotid atherosclerosis in the elderly. Atherosclerosis 218: 207-213, 2011.
35. Melzer D, Gates P, Osborne NJ, Osborn NJ, Henley WE, Cipelli R, Young A, Money C, McCormack P, Schofield P, Mosedale D, Grainger D, Galloway TS. Urinary bisphenol a concentration and angiography- defined coronary artery stenosis. PLos One 7: e43378, 2012.
36. Melzer D, Osborne NJ, Henley WE, Cipelli R, Young A, Money C, McCormack P, Luben R, Khaw KT, Wareham NJ, Galloway TS. Urinary bisphenol A concentration and risk of future coronary artery disease in apparently healthy men and women. Circulation 125: 1482-1490, 2012.
37. Melzer D, Rice NE, Lewis C, Henley WE, Galloway TS. Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLos One 5: e8673, 2010.
38. Mercader M, Swift LM, Sood S, Asfour H, Kay MW, Sarvazyan N. Use of endogenous NADH fluorescence for real-time in situ visualization of epicardial radiofrequency ablation lesions and gaps. Am J Physiol Heart Circ Physiol 302: H2131-H2138, 2012.
39. O’Reilly AO, Eberhardt E, Weidner C, Alzheimer C, Wallace BA, Lampert A. Bisphenol a binds to the local anesthetic receptor site to block the human cardiac sodium channel. PLos One 7: e41667, 2012.
40. Padmanabhan V, Siefert K, Ransom S, Johnson T, Pinkerton J, Anderson L, Tao L, Kannan K. Maternal bisphenol-A levels at delivery: a looming problem? J Perinatol 28: 258-263, 2008.
41. Palomeque J, Petroff MV, Sapia L, Gende OA, Mundiña-Weilenmann C, Mattiazzi A. Multiple alterations in Ca2+ handling determine the negative staircase in a cellular heart failure model. J Card Fail 13: 143-154, 2007.
42. Pant J, Ranjan P, Deshpande SB. Bisphenol A decreases atrial contractility involving NO-dependent G-cyclase signaling pathway. J Appl Toxicol 31: 698-702, 2011.
43. Patel BB, Raad M, Sebag IA, Chalifour LE. Lifelong exposure to bisphenol a alters cardiac structure/function, protein expression, and DNA methylation in adult mice. Toxicol Sci 133: 174-185, 2013.
44. Pieske B, Sütterlin M, Schmidt-Schweda S, Minami K, Meyer M, Olschewski M, Holubarsch C, Just H, Hasenfuss G. Diminished postrest potentiation of contractile force in human dilated cardiomyopathy. Functional evidence for alterations in intracellular Ca2+ handling. J Clin Invest 98: 764-776, 1996.
45. Posnack NG, Jaimes IIIR, Asfour H, Swift LM, Wengrowski AM, Sarvazyan N, Kay MW. Bisphenol A exposure and cardiac electrical conduction in excised rat hearts. Environ Health Perspect 122: 384-390, 2014.
46. Posnack NG, Lee NH, Brown R, Sarvazyan N. Gene expression profiling of DEHP-treated cardiomyocytes reveals potential causes of phthalate arrhythmogenicity. Toxicology 279: 54-64, 2011.
47. Posnack NG. The adverse cardiac effects of di(2-ethylhexyl)phthalate and bisphenol A. Cardiovasc Toxicol 14: 339-357, 2014.
48. Rossman E. Abnormal frequency-dependent responses represent the pathophysiologic signature of contractile failure in human myocardium. J Mol Cell Cardiol 36: 33-42, 2004.
49. Sathyanarayana S, Braun JM, Yolton K, Liddy S, Lanphear BP. Case report: high prenatal bisphenol a exposure and infant neonatal neurobehavior. Environ Health Perspect 119: 1170-1175, 2011.
50. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 110: A703-A707, 2002.
51. Shankar A, Teppala S, Sabanayagam C. Bisphenol A and peripheral arterial disease: results from the NHANES. Environ Health Perspect; doi:10.1289/ehp.1104114.
52. Shankar A, Teppala S. Urinary bisphenol A and hypertension in a multiethnic sample of US adults. J Environ Public Health 2012: 481641, 2012.
53. Tomaselli GF, Zipes DP. What causes sudden death in heart failure? Circ Res 95: 754-763, 2004.
54. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Cien Saude Colet 17: 407-434, 2012.
55. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol 24: 139-177, 2007.
56. Vandenberg LN, Hunt PA, Myers JP, Vom Saal FS. Human exposures to bisphenol A: mismatches between data and assumptions. Rev Environ Health 28: 37-58, 2013.
57. Wang F, Hua J, Chen M, Xia Y, Zhang Q, Zhao R, Zhou W, Zhang Z, Wang B. High urinary bisphenol A concentrations in workers and possible laboratory abnormalities. Occup Environ Med 69: 679-684, 2012.
58. Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, Sonnenschein C, Watson CS, Zoeller RT, Belcher SM. In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol 24: 178-198, 2007.
59. Yan S, Chen Y, Dong M, Song W, Belcher SM, Wang HS. Bisphenol A and 17-estradiol promote arrhythmia in the female heart via alteration of calcium handling. PLos One 6: e25455, 2011.
60. Zhang T, Sun H, Kannan K. Blood and urinary bisphenol A concentrations in children, adults, and pregnant women from china: partitioning between blood and urine and maternal and fetal cord blood. Environ Sci Technol 47: 4686-4694, 2013.