Exposure to phthalates affects calcium handling and intercellular connectivity of human stem cell-derived cardiomyocytes

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Posnack, Nikki Gillum ^a   Idrees, Rabia ^a   Ding, Hao ^a   Jaimes Iii, Rafael ^b   Stybayeva, Gulnaz ^c   Karabekian, Zaruhi ^a   Laflamme, Michael A ^d   Sarvazyan, Narine ^a  

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

^b The George Washington University   (United States)

^c University of California Davis   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CONNEXIN 43; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; PIRINIXIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PYRIMIDINE DERIVATIVE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHRONOTROPISM; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE POTENTIAL; HEART PACING; HUMAN; HUMAN CELL; INOTROPISM; PROTEIN EXPRESSION; AGONISTS; CARDIAC MUSCLE CELL; CYTOLOGY; DRUG EFFECTS; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; HEART CONTRACTION; HEART RATE; INTRACELLULAR SPACE; METABOLISM; SARCOPLASMIC RETICULUM; STEM CELL;

CALCIUM; CONNEXIN 43; DIETHYLHEXYL PHTHALATE; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; HEART RATE; HUMANS; INTRACELLULAR SPACE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PYRIMIDINES; SARCOPLASMIC RETICULUM; STEM CELLS;

EID: 84925799085     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121927     Document Type: Article

References (76)

1. FDA (2002) Safety Assessment of Di(2-ethylhexyl)phthalate (DEHP) Released from PVC Medical Devices. Available: http://www.fda.gov/downloads/MedicalDevices/./UCM080457.pdf.
2. Wittassek M, Koch HM, Angerer J, Brüning T (2011) Assessing exposure to phthalates-the human biomonitoring approach. Mol Nutr Food Res 55: 7-31. doi: 10.1002/mnfr.201000121 PMID: 20564479
3. Wittassek M, Wiesmuller GA, Koch HM, Eckard R, Dobler L, et al. (2007) Internal phthalate exposure over the last two decades-a retrospective human biomonitoring study. Int J Hyg Environ Health 210: 319-333. PMID: 17400024
4. Saravanabhavan G, Guay M, Langlois É, Giroux S, Murray J, et al. (2013) Biomonitoring of phthalate metabolites in the Canadian population through the Canadian Health Measures Survey (2007-2009). Int J Hyg Environ Health 216: 652-661. doi: 10.1016/j.ijheh.2012.12.009 PMID: 23419587
5. Berman T, Hochner-Celnikier D, Calafat AM, Needham LL, Amitai Y, et al. (2009) Phthalate exposure among pregnant women in Jerusalem, Israel: results of a pilot study. Environ Int 35: 353-357. doi: 10.1016/j.envint.2008.08.010 PMID: 18824263
6. Posnack NG (2014) The Adverse Cardiac Effects of Di(2-ethylhexyl)phthalate and Bisphenol A. Cardiovasc Toxicol. 14: 339-57. doi: 10.1007/s12012-014-9258-y PMID: 24811950
7. Gillum N, Karabekian Z, Swift LM, Brown RP, Kay MW, et al. (2009) Clinically relevant concentrations of di (2-ethylhexyl) phthalate (DEHP) uncouple cardiac syncytium. Toxicol Appl Pharmacol 236: 25-38. doi: 10.1016/j.taap.2008.12.027 PMID: 19344669
8. Posnack NG, Lee NH, Brown R, Sarvazyan N (2011) Gene expression profiling of DEHP-treated cardiomyocytes reveals potential causes of phthalate arrhythmogenicity. Toxicology 279: 54-64. doi: 10. 1016/j.tox.2010.09.007 PMID: 20920545
9. Rudy Y, Ackerman MJ, Bers DM, Clancy CE, Houser SR, et al. (2008) Systems approach to understanding electromechanical activity in the human heart: a national heart, lung, and blood institute workshop summary. Circulation 118: 1202-1211. doi: 10.1161/CIRCULATIONAHA.108.772715 PMID: 18779456
10. Loiselle DS, Gibbs CL (1979) Species differences in cardiac energetics. Am J Physiol 237: H90-8. PMID: 464076
11. Bers DM (2000) Calcium fluxes involved in control of cardiacmyocyte contraction. Circ Res 87: 275-281. PMID: 10948060
12. Feige JN, Gerber A, Casals-Casas C, Yang Q, Winkler C, et al. (2010) The pollutant diethylhexyl phthalate regulates hepatic energy metabolism via species-specific PPARalpha-dependent mechanisms. Environ Health Perspect 118: 234-241. doi: 10.1289/ehp.0901217 PMID: 20123618
13. Isenberg JS, Kamendulis LM, Smith JH, Ackley DC, Pugh G Jr, et al. (2000) Effects of Di-2-ethylhexyl phthalate (DEHP) on gap-junctional intercellular communication (GJIC), DNA synthesis, and peroxisomal beta oxidation (PBOX) in rat, mouse, and hamster liver. Toxicol Sci 56: 73-85. PMID: 10869455
14. Rosa A, Spagnoli FM, Brivanlou AH (2009) The miR-430/427/302 family controls mesendodermal fate specification via species-specific target selection. Dev Cell 16: 517-527. doi: 10.1016/j.devcel.2009. 02.007 PMID: 19386261
15. James D, Noggle SA, Swigut T, Brivanlou AH (2006) Contribution of human embryonic stem cells to mouse blastocysts. Dev Biol 295: 90-102. PMID: 16769046
16. Chong JJH, Yang X, Don CW, Minami E, Liu Y-W, et al. (2014) Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature. 510: 273-7. doi: 10.1038/nature13233 PMID: 24776797
17. Shiba Y, Fernandes S, Zhu W-Z, Filice D, Muskheli V, et al. (2012) Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 489: 322-325. doi: 10.1038/nature11317 PMID: 22864415
18. Laflamme MA, Chen KY, Naumova A V, Muskheli V, Fugate JA, et al. (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25: 1015-1024. PMID: 17721512
19. Chung CS, Campbell KS (2013) Temperature and transmural region influence functional measurements in unloaded left ventricular cardiomyocytes. Physiol Rep 1: e00158. doi: 10.1002/phy2.158 PMID: 24400159
20. Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, et al. (2009) Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104: e30-41. doi: 10.1161/CIRCRESAHA.108. 192237 PMID: 19213953
21. Ma J, Guo L, Fiene SJ, Anson BD, Thomson JA, et al. (2011) High purity human-induced pluripotent stem cell-derived cardiomyocytes: electrophysiological properties of action potentials and ionic currents. Am J Physiol Heart Circ Physiol 301: H2006-17. doi: 10.1152/ajpheart.00694.2011 PMID: 21890694
22. Xu C, Police S, Hassanipour M, Li Y, Chen Y, et al. (2011) Efficient generation and cryopreservation of cardiomyocytes derived from human embryonic stem cells. Regen Med 6: 53-66. doi: 10.2217/rme.10.91 PMID: 21175287
23. Van den Heuvel NHL, van Veen TAB, Lim B, Jonsson MKB (2014) Lessons from the heart: mirroring electrophysiological characteristics during cardiac development to in vitro differentiation of stem cell derived cardiomyocytes. J Mol Cell Cardiol 67: 12-25. doi: 10.1016/j.yjmcc.2013.12.011 PMID: 24370890
24. Sartiani L, Bettiol E, Stillitano F, Mugelli A, Cerbai E, et al. (2007) Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach. Stem Cells 25: 1136-1144. PMID: 17255522
25. Zhu W-ZZ, Santana LF, Laflamme MA (2009) Local control of excitation-contraction coupling in human embryonic stem cell-derived cardiomyocytes. PLoS One 4: e5407. doi: 10.1371/journal.pone.0005407 PMID: 19404384
26. Sirenko O, Cromwell EF, Crittenden C, Wignall JA, Wright FA, et al. (2013) Assessment of beating parameters in human induced pluripotent stem cells enables quantitative in vitro screening for cardiotoxicity. Toxicol Appl Pharmacol 273: 500-507. doi: 10.1016/j.taap.2013.09.017 PMID: 24095675
27. Braam SR, Mummery CL (2010) Human stem cell models for predictive cardiac safety pharmacology. Stem Cell Res 4: 155-156. doi: 10.1016/j.scr.2010.04.008 PMID: 20493455
28. Jonsson MKB, Wang Q-DD, Becker B (2011) Impedance-based detection of beating rhythm and proarrhythmic effects of compounds on stem cell-derived cardiomyocytes. Assay Drug Dev Technol 9: 589-599. doi: 10.1089/adt.2011.0396 PMID: 22085047
29. Li L-X, Chen L, Meng X-Z, Chen B-H, Chen S-Q, et al. (2013) Exposure levels of environmental endocrine disruptors in mother-newborn pairs in China and their placental transfer characteristics. PLoS One 8: e62526. doi: 10.1371/journal.pone.0062526 PMID: 23667484
30. Liu J, Fu JD, Siu CW, Li RA (2007) Functional sarcoplasmic reticulum for calcium handling of human embryonic stem cell-derived cardiomyocytes: insights for driven maturation. Stem Cells 25: 3038-3044. PMID: 17872499
31. Lee Y-K, Ng K-M, Lai W-H, Chan Y-C, Lau Y-M, et al. (2011) Calcium homeostasis in human induced pluripotent stem cell-derived cardiomyocytes. Stem Cell Rev 7: 976-986. doi: 10.1007/s12015-011- 9273-3 PMID: 21614516
32. Bers DM (2002) Calcium and cardiac rhythms: physiological and pathophysiological. Circ Res 90: 14-17. PMID: 11786512
33. Bers DM (2008) Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 70: 23-49. PMID: 17988210
34. Pogwizd SM, Schlotthauer K, Li L, Yuan W, Bers DM (2001) Arrhythmogenesis and Contractile Dysfunction in Heart Failure: Roles of Sodium-Calcium Exchange, Inward Rectifier Potassium Current, and Residual Beta Adrenergic Responsiveness. Circ Res 88: 1159-1167. PMID: 11397782
35. Louch WE, Stokke MK, Sjaastad I, Christensen G, Sejersted OM (2012) No rest for the weary: diastolic calcium homeostasis in the normal and failing myocardium. Physiology (Bethesda) 27: 308-323. doi: 10.1152/physiol.00021.2012 PMID: 23026754
36. Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415: 198-205. PMID: 11805843
37. Klaunig JE, Babich MA, Baetcke KP, Cook JC, Corton JC, et al. (2003) PPARalpha agonist-induced rodent tumors: modes of action and human relevance. Crit Rev Toxicol 33: 655-780. PMID: 14727734
38. HuberWW, Grasl-Kraupp B, Schulte-Hermann R (1996) Hepatocarcinogenic potential of di(2-ethylhexyl) phthalate in rodents and its implications on human risk. Crit Rev Toxicol 26: 365-481. PMID: 8817083
39. Gonzalez FJ, Shah YM (2008) PPARalpha: mechanism of species differences and hepatocarcinogenesis of peroxisome proliferators. Toxicology 246: 2-8. PMID: 18006136
40. Lapinskas PJ, Brown S, Leesnitzer LM, Blanchard S, Swanson C, et al. (2005) Role of PPARalpha in mediating the effects of phthalates and metabolites in the liver. Toxicology 207: 149-163. PMID: 15590130
41. Posnack NG, Swift LM, Kay MW, Lee NH, Sarvazyan N (2012) Phthalate Exposure Changes the Metabolic Profile of Cardiac Muscle Cells. Environ Health Perspect 120: 1243-1251. doi: 10.1289/ehp.1205056 PMID: 22672789
42. Domeier TL, Blatter LA, Zima A V (2009) Alteration of sarcoplasmic reticulum Ca2+ release termination by ryanodine receptor sensitization and in heart failure. J Physiol 587: 5197-5209. doi: 10.1113/jphysiol.2009.177576 PMID: 19736296
43. Jaeger RJ, Rubin RJ (1973) Extraction, localization, and metabolism of di-2-ethylhexyl phthalate from PVC plastic medical devices. Environ Health Perspect 3: 95-102. PMID: 4735799
44. Inoue K, Kawaguchi M, Yamanaka R, Higuchi T, Ito R, et al. (2005) Evaluation and analysis of exposure levels of di(2-ethylhexyl) phthalate from blood bags. Clin Chim Acta 358: 159-166. PMID: 15893743
45. Latini G, De Felice C, Presta G, Del Vecchio A, Paris I, et al. (2003) Exposure to Di(2-ethylhexyl)phthalate in humans during pregnancy. A preliminary report. Biol Neonate 83: 22-24. PMID: 12566679
46. Latini G, De Felice C, Presta G, Del Vecchio A, Paris I, et al. (2003) In utero exposure to di-(2-ethylhexyl) phthalate and duration of human pregnancy. Environ Health Perspect 111: 1783-1785. PMID: 14594632
47. Pakalin S, Aschberger K, Cosgrove O, Lund B, Paya-Perez A, et al. (2008) "Bis-(2-Ethylhexyl) Phthalate, DEHP), Summary Risk Assessment report. Available: http://publications.jrc.ec.europa.eu/repository/bitstream/111111111/1001/1/dehpsum042.pdf
48. Environmental Protection Agency (n.d.) Di(2-ethylhexyl)phthalate (DEHP): Reference Dose. Available: http://www.epa.gov/iris/subst/0014.htm
49. Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, et al. (2005) Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 113: 1056-1061. PMID: 16079079
50. Hauser R, Meeker JD, Duty S, Silva MJ, Calafat AM (2006) Altered semen quality in relation to urinary concentrations of phthalate monoester and oxidative metabolites. Epidemiology 17: 682-691. PMID: 17003688
51. Duty SM, Singh NP, Silva MJ, Barr DB, Brock JW, et al. (2003) The relationship between environmental exposures to phthalates and DNA damage in human sperm using the neutral comet assay. Environ Health Perspect 111: 1164-1169. PMID: 12842768
52. Joensen UN, Frederiksen H, Jensen MB, Lauritsen MP, Olesen IA, et al. (2012) Phthalate excretion pattern and testicular function: a study of 881 healthy Danish men. Environ Health Perspect 120: 1397-1403. doi: 10.1289/ehp.1205113 PMID: 22832070
53. Colon I, Caro D, Bourdony CJ, Rosario O (2000) Identification of phthalate esters in the serum of young Puerto Rican girls with premature breast development. Environ Health Perspect 108: 895-900. PMID: 11035999
54. Stahlhut RW, van Wijngaarden E, Dye TD, Cook S, Swan SH (2007) Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult U.S. males. Environ Health Perspect 115: 876-882. PMID: 17589594
55. Zhang Y, Lin L, Cao Y, Chen B, Zheng L, et al. (2009) Phthalate levels and low birth weight: a nested case-control study of Chinese newborns. J Pediatr 155: 500-504. doi: 10.1016/j.jpeds.2009.04.007 PMID: 19555962
56. Meeker JD, Hu H, Cantonwine DE, Lamadrid-Figueroa H, Calafat AM, et al. (2009) Urinary phthalate metabolites in relation to preterm birth in Mexico city. Environ Health Perspect 117: 1587-1592. doi: 10.1289/ehp.0800522 PMID: 20019910
57. Karle VA, Short BL, Martin GR, Bulas DI, Getson PR, et al. (1997) Extracorporeal membrane oxygenation exposes infants to the plasticizer, di(2-ethylhexyl)phthalate. Crit Care Med 25: 696-703. PMID: 9142038
58. Shneider B, Schena J, Truog R, Jacobson M, Kevy S (1989) Exposure to di(2-ethylhexyl)phthalate in infants receiving extracorporeal membrane oxygenation. N Engl J Med 320: 1563. PMID: 2725594
59. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, et al. (2001) Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ Res 88: 333-339. PMID: 11179202
60. Sobarzo CM, Lustig L, Ponzio R, Suescun MO, Denduchis B (2009) Effects of di(2-ethylhexyl) phthalate on gap and tight junction protein expression in the testis of prepubertal rats. Microsc Res Tech 72: 868-877. doi: 10.1002/jemt.20741 PMID: 19526522
61. Kang KS, Lee YS, Kim HS, Kim SH (2002) DI-(2-ethylhexyl) phthalate-induced cell proliferation is involved in the inhibition of gap junctional intercellular communication and blockage of apoptosis in mouse Sertoli cells. J Toxicol Environ Heal A 65: 447-459. PMID: 11936224
62. Kamendulis LM, Isenberg JS, Smith JH, G. P Jr, Lington AW, et al. (2002) Comparative effects of phthalate monoesters on gap junctional intercellular communication and peroxisome proliferation in rodent and primate hepatocytes. J Toxicol Env Heal A 65: 569-588.
63. Olson EN (2004) A decade of discoveries in cardiac biology. Nat Med 10: 467-474. PMID: 15122248
64. Satin J, Itzhaki I, Rapoport S, Schroder EA, Izu L, et al. (2008) Calcium Handling in Human Embryonic Stem Cell Derived Cardiomyocytes. Stem Cells. 26: 1961-72. doi: 10.1634/stemcells.2007-0591 PMID: 18483424
65. Dolnikov K, Shilkrut M, Zeevi-Levin N, Gerecht-Nir S, Amit M, et al. (2006) Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction. Stem Cells 24: 236-245. PMID: 16322641
66. Gyorke S, Gyorke I, Terentyev D, Viatchenko-Karpinski S, Williams SC (2004) Modulation of sarcoplasmic reticulum calcium release by calsequestrin in cardiac myocytes. Biol Res 37: 603-607. PMID: 15709687
67. Terentyev D, Viatchenko-Karpinski S, Valdivia HH, Escobar AL, Gyorke S (2002) Luminal Ca2+ controls termination and refractory behavior of Ca2+-induced Ca2+ release in cardiac myocytes. Circ Res 91: 414-420. PMID: 12215490
68. Radwański PB, Belevych AE, Brunello L, Carnes CA, Györke S (2013) Store-dependent deactivation: cooling the chain-reaction of myocardial calcium signaling. J Mol Cell Cardiol 58: 77-83. doi: 10.1016/j.yjmcc.2012.10.008 PMID: 23108187
69. Kalyanasundaram A, Viatchenko-Karpinski S, Belevych AE, Lacombe VA, Hwang HS, et al. (2012) Functional consequences of stably expressing a mutant calsequestrin (CASQ2D307H) in the CASQ2 null background. Am J Physiol Heart Circ Physiol 302: H253-61. doi: 10.1152/ajpheart.00578.2011 PMID: 21984545
70. Glukhov A V, Kalyanasundaram A, Lou Q, Hage LT, Hansen BJ, et al. (2013) Calsequestrin 2 deletion causes sinoatrial node dysfunction and atrial arrhythmias associated with altered sarcoplasmic reticulum calcium cycling and degenerative fibrosis within the mouse atrial pacemaker complex. Eur Heart J. doi: 10.1093/eurheartj/eht452
71. Pieske B, Sütterlin M, Schmidt-Schweda S, Minami K, Meyer M, et al. (1996) Diminished post-rest potentiation of contractile force in human dilated cardiomyopathy. Functional evidence for alterations in intracellular Ca2+ handling. J Clin Invest 98: 764-776. PMID: 8698869
72. Eisner DA, Choi HS, Diaz ME, O'Neill SC, Trafford AW (2000) Integrative Analysis of Calcium Cycling in Cardiac Muscle. Circ Res 87: 1087-1094. PMID: 11110764
73. Li S, Chen G, Li RA (2013) Calcium signalling of human pluripotent stem cell-derived cardiomyocytes. J Physiol 591: 5279-5290. doi: 10.1113/jphysiol.2013.256495 PMID: 24018947
74. Baartscheer A, Schumacher CA, Belterman CNW, Coronel R, Fiolet JWT (2003) SR calcium handling and calcium after-transients in a rabbit model of heart failure. Cardiovasc Res 58: 99-108. PMID: 12667950
75. January CT, Fozzard HA (1988) Delayed afterdepolarizations in heart muscle: mechanisms and relevance. Pharmacol Rev 40: 219-227. PMID: 3065793
76. Lockyer P, Schisler JC, Patterson C, Willis MS (2010) Minireview: Won't get fooled again: the nonmetabolic roles of peroxisome proliferator-activated receptors (PPARs) in the heart. Mol Endocrinol 24: 1111-1119. doi: 10.1210/me.2009-0374 PMID: 20016041