Molecular mechanisms underlying the rapid arrhythmogenic action of bisphenol A in female rat hearts

Endocrinology

Volumn 154, Issue 12, 2013, Pages 4607-4617

  Gao, Xiaoqian ^a   Liang, Qian ^a   Chen, Yamei ^a   Wang, Hong Sheng ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; ESTROGEN RECEPTOR BETA; INOSITOL TRISPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOLAMBAN; PHOSPHOLIPASE C; RYANODINE RECEPTOR; BENZHYDRYL DERIVATIVE; CALCIUM; CALCIUM CHANNEL L TYPE; CYCLIC AMP; MITOGEN ACTIVATED PROTEIN KINASE; PHENOL DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARRHYTHMOGENESIS; ARTICLE; CALCIUM TRANSPORT; CARDIOTOXICITY; CELL ISOLATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; HEART CELL CULTURE; HEART MUSCLE CELL; LOW DRUG DOSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEART ARRHYTHMIA; METABOLISM; TOXICITY;

ANIMALS; ARRHYTHMIAS, CARDIAC; BENZHYDRYL COMPOUNDS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOPLASMIC RETICULUM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MYOCYTES, CARDIAC; PHENOLS; RATS; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION;

EID: 84888235995     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1737     Document Type: Article

References (42)

1. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect. 2010;118:1055-1070.
2. 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. 2005;113: 391-395.
3. Ye X, Pierik FH, Mackenbach JP, et al. Urinary metabolite concentrations of organophosphorous pesticides, bisphenol A, and phthalates among pregnant women in Rotterdam, The Netherlands: the Generation R study. Environ Res. 2008;108:260-267.
4. Lakind JS, Naiman DQ. Daily intake of bisphenol A and potential sources of exposure: 2005-2006 National Health and Nutrition Examination Survey. J Expo Sci Environ Epidemiol. 2011;21:272- 279.
5. Hoekstra EJ, Simoneau C. Release of bisphenol A from polycarbonate: a review. Crit Rev Food Sci Nutr. 2013;53:386-402.
6. Wetherill YB, Akingbemi BT, Kanno J, et al. In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol. 2007;24:178- 198.
7. Welshons WV, Nagel SC, vom Saal FS. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology. 2006;147:S56-S69.
8. Zoeller RT, Brown TR, Doan LL, et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology. 2012;153:4097-4110.
9. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, et al. Endocrine- disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30:293-342.
10. Melzer D, Osborne NJ, Henley WE, et al. Urinary bisphenol a concentration and risk of future coronary artery disease in apparently healthy men and women. Circulation. 2012;125:1482-1490.
11. 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. 2010;5(1):e8673.
12. 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. 2008;300:1303-1310.
13. Shankar A, Teppala S, Sabanayagam C. Bisphenol A and peripheral arterial disease: results from the NHANES. Environ Health Perspect. 2012;120:1297-1300.
14. Yan S, Chen Y, Dong M, Song W, Belcher SM, Wang H-S. Bisphenol A and 17β-estradiol promote arrhythmia in the female heart via alteration of calcium handling. PLoS One. 2011;6:e25455.
15. Belcher SM, Chen Y, Yan S, Wang H-S. Rapid estrogen receptor-mediated mechanisms determine the sexually dimorphic sensitivity of ventricular myocytes to 17β-estradiol and the environmental endocrine disruptor bisphenol A. Endocrinology. 2012;153:712-720.
16. Yan S, Song W, Chen Y, Hong K, Rubinstein J, Wang H-S. Low-dose bisphenol A and estrogen increase ventricular arrhythmias following ischemia-reperfusion in female rat hearts. Food Chem Toxicol. 2013;56C:75-80.
17. 2+ cycling and signaling in cardiac myocytes. Annu Rev Physiol. 2008;70:23-49.
18. Betzenhauser MJ, Marks AR. Ryanodine receptor channelopathies. Pflugers Arch. 2010;460:467-480.
19. Van Petegem F. Ryanodine receptors: structure and function. J Biol Chem. 2012;287:31624-31632.
20. Kranias EG, Hajjar RJ. Modulation of cardiac contractility by the phopholamban/SERCA2a regulatome. Circ Res. 2012;110:1646- 1660.
21. Bouskine A, Nebout M, Mograbi B, Brucker-Davis F, Roger C, Fenichel P. Estrogens promote human testicular germ cell cancer through a membrane-mediated activation of extracellular regulated kinase and protein kinase A. Endocrinology. 2008;149:565-573.
22. Bouskine A, Nebout M, Brucker-Davis F, Benahmed M, Fenichel P. Low doses of bisphenol A promote human seminoma cell proliferation by activating PKA and PKG via a membrane G-protein-coupled estrogen receptor. Environ Health Perspect. 2009;117:1053- 1058.
23. Huang H, Tan WJ, Wang CC, Leung LK. Bisphenol A induces cor-ticotropin- releasing hormone expression in the placental cells JEG-3. Reprod Toxicol. 2012;34:317-322.
24. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002; 415:198-205.
25. 2+ release channel (ryanodine receptor): defective regulation in failing hearts. Cell. 2000;101:365-376.
26. 2+ signals in pancreatic α-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ Health Perspect. 2005;113: 969-977.
27. 2+ signaling induced by bisphenol A in cultured rat hippocampal neurons. Neuro Endocrinol Lett. 2006;27:97-104.
28. Lee S, Suk K, Kim IK, et al. Signaling pathways of bisphenol A-induced apoptosis in hippocampal neuronal cells: role of calciuminduced reactive oxygen species, mitogen-activated protein kinases, and nuclear factor-κB. J Neurosci Res. 2008;86:2932-2942.
29. 2+ fluxes and viability in Madin-Darby canine renal tubular cells. Drug Chem Toxicol. 2011;34:454-461.
30. Soriano S, Alonso-Magdalena P, Garcia-Arevalo M, et al. Rapid insulinotropic action of low doses of bisphenol-A on mouse and human islets of Langerhans: role of estrogen receptor β. PLoS One. 2012;7:e31109.
31. 2+ signalling. Springerplus. 2013;2:54.
32. 2+/calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc Res. 2007;73:631-640.
33. Swaminathan PD, Purohit A, Hund TJ, Anderson ME. Calmodulin-dependent protein kinase II: linking heart failure and arrhythmias. Circ Res. 2012;110:1661-1677.
34. 2+/calmodulin-dependent kinase II (CaMKII). Circulation. 2012;126:2125-2139.
35. Grimm M, Brown JH. β-Adrenergic receptor signaling in the heart: role of CaMKII. J Mol Cell Cardiol. 2010;48:322-330.
36. Levin ER. Rapid signaling by steroid receptors. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1425-R1430.
37. Kelly MJ, Ronnekleiv OK. Membrane-initiated actions of estradiol that regulate reproduction, energy balance and body temperature. Front Neuroendocrinol. 2012;33:376-387.
38. Qiu J, Bosch MA, Tobias SC, et al. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J Neurosci. 2003;23:9529- 9540.
39. McConnachie G, Langeberg LK, Scott JD. AKAP signaling complexes: getting to the heart of the matter. Trends Mol Med. 2006; 12:317-323.
40. Kapiloff MS, Jackson N, Airhart N. mAKAP and the ryanodine receptor are part of a multi-component signaling complex on the cardiomyocyte nuclear envelope. J Cell Sci. 2001;114:3167-3176.
41. Ptak A, Gregoraszczuk EL. Bisphenol A induces leptin receptor expression, creating more binding sites for leptin, and activates the JAK/Stat, MAPK/ERK and PI3K/Akt signalling pathways in human ovarian cancer cell. Toxicol Lett. 2012;210:332-337.
42. Belcher SM, Le HH, Spurling L, Wong JK. Rapid estrogenic regulation of extracellular signal-regulated kinase 1/2 signaling in cerebellar granule cells involves a G protein- and protein kinase A-dependent mechanism and intracellular activation of protein phosphatase 2A. Endocrinology. 2005;146:5397-5406.