Trichloroethylene disrupts cardiac gene expression and calcium homeostasis in rat myocytes

Toxicological Sciences

Volumn 104, Issue 1, 2008, Pages 135-143

  Caldwell, Patricia T ^a   Thorne, Patricia A ^a   Johnson, Paula D ^b   Boitano, Scott ^a,c   Runyan, Raymond B ^a   Selmin, Ornella ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Calcium flux; Cardiac development; Environmental toxicants; Trichloroethylene

Indexed keywords

PROTEIN SERCA2A; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRICHLOROETHYLENE; VASOPRESSIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARDIOTOXICITY; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; DIGITAL IMAGING; EMBRYO; GENE EXPRESSION; HEART DEVELOPMENT; HEART MUSCLE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CELL LINE; GENE EXPRESSION; HOMEOSTASIS; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; RNA, MESSENGER; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SIGNAL TRANSDUCTION; SOLVENTS; TRICHLOROETHYLENE;

RATTUS; RODENTIA;

EID: 45549094238     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn078     Document Type: Article

References (48)

1. Arai, M., Alpert, N. R., MacLennan, D. H., Barton, P., and Periasamy, M. (1993). Alterations in sarcoplasmic reticulum, gene expression in human heart failure. A possible mechanism for alterations in systolic and diastolic properties of the failing myocardium. Circ. Res. 72 463-469.
2. Armoundas, A. A., Rose, J., Aggarwal, R., Stuyvers, B. D., O'Rourke, B., Kass, D. A., Marban, E., Shorofsky, S. R., Tomaselli, G. F., and William Balke, C. (2007). Cellular and molecular determinants of altered Ca2+ handling in the failing rabbit heart: Primary defects in SR Ca2+ uptake and release mechanisms. Am. J. Physiol. Heart Circ. Physiol. 292, H1607-H1618.
3. Baker, D. L., Hashimoto, K., Grupp, I. L., Ji, Y., Reed, T., Loukianov, E., Grupp, G., Bhagwhat, A., Hoit, B., Walsh, R., et al. (1998). Targeted overexpression of the sarcoplasmic reticulum Ca2+-ATPase increases cardiac contractility in transgenic mouse hearts. Circ. Res. 83, 1205-1214.
4. Boyer, A. S., Finch, W. T., and Runyan, R. B. (2000). Trichloroethylene inhibits development of embryonic heart valve precursors in vitro. Toxicol. Sci. 53, 109-117.
5. Bove, F., Shim, Y., and Zeitz, P. (2002). Drinking water contaminants and adverse pregnancy outcomes: A review. Environ. Health Perspect. 110(Suppl. 1), 61-74. (Review).
6. Buck, E. D., Wilhelm, G. L., and Pessah, I. N. (1999). Mechanisms of δ-hexachlorocyclohexane toxicity: I. Relationship between altered ventricular myocyte contractility and ryanodine receptor function. J. Pharmacol. Exp. Ther. 289, 477-485.
7. CDC. (1998). Trends in infant mortality attributable to birth defects - United States, 1990-1995. Available at: http://www.cdc.gov/mmwr/preview/ mmwrhtml/00054921.htm Accessed 15 January 2008
8. Chandrashekhar, Y., Prahash A. J., Sen, S., Gupta, S., Roy, S., and Anand, I. S. (2003). The role of arginine vasopressin and its receptors in the normal and failing rat heart. J. Mol. Cell. Cardiol. 35 495-504.
9. Collier, J. M., Selmin, O., Johnson, P. D., and Runyan, R. B. (2003). Trichloroethylene effects on gene expression during cardiac development. Birth Defects Res. A Clin. Mol. Teratol. 67, 488-495.
10. Drake, V. J., Koprowski, S. L., Hu, N., Smith, S. M., and Lough, J. (2006a). Cardiogenic effects of trichloroethylene and trichloroacetic acid following exposure during heart specification of avian development. Toxicol. Sci. 94, 153-162.
11. Drake, V. J., Koprowski, S. L., Lough, J., Hu, N., and Smith, S. M. (2006b). Trichloroethylene exposure during cardiac valvuloseptal morphogenesis alters cushion formation and cardiac, hemodynamics in the avian embryo. Environ. Health Perspect. 114, 842-847.
12. Dugard, P. H. (2000). Effects of trichloroethylene (TCE) on an in vitro chick atrioventricular canal culture. Toxicol. Sci. 56, 437-438.
13. Fu, J. D., Li, J., Tweedie, D., Yu, H. M., Chen, L., Wang, R., Riordon, D. R., Brugh, S. A., Wang, S. Q., Boheler, K. R., et al. (2006). Crucial role of the sarcoplasmic reticulum in the developmental regulation of Ca2+ transients and contraction in cardiomyocytes derived from embryonic stem cells. FASEB J. 20, 181-183.
14. Go, L. O., Moschella, M. C., Watras, J., Handa, K. K., Fyfe, B. S., and Marks, A. R. (1995). Differential regulation of two types of intracellular calcium release channels during end-stage heart failure. J. Clin. Invest. 95, 888-894.
15. Goldberg, S. J., Lebowitz, M. D., Graver, E. J., and Hicks, S. (1990). An association of human congenital cardiac malformations and drinking water contaminants. J. Am. Coll. Cardiol. 16, 155-164.
16. Goldberg, S. J., Dawson, B. V., Johnson, P. D., Hoyme, H. E., and Utreich, J. B. (1992). Cardiac teratogenicity of dichloroethylene in a chick model. Pediatr. Res. 32, 23-26.
17. Groenendijk, B. C., Hierck, B. P., Gittenberger-De Groot, A. C., and Poelmann, R. E. (2004). Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos. Dev. Dyn. 230, 57-68.
18. Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
19. Haghighi, K., Schmidt, A. G., Hoit, B. D., Brittsan, A. G., Yatani, A., Lester, J. W., et al. (2001). Superinhibition of sarcoplasmic reticulum function by phospholamban induces cardiac contractile failure. J. Biol. Chem. 276, 24145-24152.
20. Hardin, B. D., Ketman, B. J., and Brent, R. L. (2005). Trichloroethylene and dichloroethylene: A critical review of teratogenicity. Birth Defects Res. A Clin. Mol. Teratol. 73, 931-955.
21. Hasenfuss, G., Reinecke, H., Studer, R., Meyer, M., Pieske, B., Holtz, J., Holubarsch, C., Posival, H., Just, H., and Drexler, H. (1994). Relation between myocardial function and expression of sarcoplasmic reticulum Ca(2+)-ATPase in failing and nonfailing human myocardium. Circ. Res. 75, 434-442.
22. He, L., Marecki, J. C., Sererro, G., Simmen, F. A., Ronis, M. J. J., and Badger, T. M. (2007). Dose-dependent effects of alcohol on insulin signaling: Partial explanation for biphasic alcohol impact on human health. Mol. Endocrinol. 21, 2541-2550.
23. Hobai, I. A., and O'Rourke, B. (2001). Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation 103, 1577-1584.
24. Ji, Y., Lalli, M. J., Babu, G. J., Xu, Y., Kirkpatrick, D. L., Liu, L. H., Chiamvimonvat, N., Walsh, R. A., Shull, G. E., and Periasamy, M. (2000). Disruption of a single copy of the SERCA2 gene results in altered Ca2+ homeostasis and cardiomyocyte function. J. Biol. Chem. 275, 38073-38080.
25. Johnson, P. D., Dawson, B. V., and Goldberg, S. J. (1998). A review: Trichloroethylene metabolites: Potential cardiac teratogens. Environ. Health Perspect. 106(Suppl. 4), 995-999.
26. Lalli, M. J., Yong, J., Prasad, V., Hashimoto, K., Plank, D., Babu, G. J., Kirkpatrick, D., Walsh, R. A., Sussman, M., Yatani, A., et al. (2001). Sarcoplasmic reticulum Ca(2+) atpase (SERCA) 1a structurally substitutes for SERCA2a in the cardiac sarcoplasmic reticulum and increases cardiac Ca(2+) handling capacity. Circ. Res. 89, 160-167.
27. Lehnart, S. E., Schillinger, W., Pieske, B., Prestle, J., Just, H., and Hasenfuss, G. (1998). Sarcoplasmic reticulum proteins in heart failure. Ann. N. Y. Acad. Sci. 853, 220-230. (Review).
28. Lehnart, S. E., Wehrens, X. H., Kushnir, A., and Marks, A. R. (2004). Cardiac ryanodine receptor function and regulation in heart disease. Ann. N. Y. Acad. Sci. 1015, 144-159. (Review).
29. Loeber, C. P., Hendrix, M. J., Diez De Pinos, S., and Goldberg, S. J. (1988). Trichloroethylene: A cardiac teratogen in developing chick embryos. Pediatr. Res. 24, 740-744.
30. Marks, A. R., Priori, S., Memmi, M., Kontula, K., and Laitinen, P. J. (2002). Involvement of the cardiac ryanodine receptor/calcium release channel in catecholaminergic polymorphic ventricular tachycardia. J. Cell. Physiol. 190, 1-6.
31. Marx, S. O., Reiken, S., Hisamatsu, Y., Jayaraman, T., Burkhoff, D., Rosemblit, N., and Marks, A. R. (2000). PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): Defective regulation in failing hearts. Cell 101, 365-376.
32. Mercadier, J. J., Lompre, A. M., Duc, P., Boheler, K. R., Fraysse, J. B., Wisnewsky, C., Allen, P. D., Komajda, M., and Schwartz, K. (1990). Altered sarcoplasmic reticulum Ca2(+)-ATPase gene expression in the human ventricle during end-stage heart failure. J. Clin. Invest. 85, 305-309.
33. Mishima, N., Hoffman, S., Hill, E. G., and Krug, E. L. (2006). Chick embryos exposed to trichloroethylene in an ex ovo culture model show selective defects in early endocardial cushion tissue formation. Birth Defects Res. A Clin. Mol. Teratol. 76, 517-527.
34. Moorman, A. F., Schumacher, C. A., de Boer, P. A., Hagoort, J., Bezstarosti, K., van den Hoff, M. J., Wagenaar, G. T., Lamers, J. M., Wuytack, F., Christoffels, V. M., et al. (2000). Presence of functional sarcoplasmic reticulum iti the developing heart and its confinement to chamber myocardium. Dev. Biol. 223, 279-290.
35. NCHS. (2004). Deaths: Final repTrt for 2004. Available at: http://www.cdc.gov/nchs/products/pubs/pubd/hestats/finaldeaths04/ finaldeaths04.htm. Accessed on July 10, 2007.
36. NRC. (2006). Assessing the Human Health Risks of Trichloroethylene: Key scientific Issues. National Academies Press, Washington, D.C.
37. Opie, L. H. (2004). In Heart Physiology: From Cell to Circulation, 4th edn. Lippincott Williams & Wilkins, Philadelphia.
38. Ou, J., Ou, Z., McCarver, D. G., Hines, R. N., Oldham, K. T., Ackerman, A. W., and Pritchard, K. A., Jr. (2003). Trichloroethylene decreases heat shock protein 90 interactions with endothelial nitric oxide synthase: Implications for endothelial Cell proliferation. Toxicol. Sci. 73 90-97.
39. Periasamy, M., and Janssen, P. M. (2008). Molecular basis of diastolic dysfunction. Heart Fail. Clin 4, 13-21.
40. Periasamy, M., Reed, T. D., Liu, L. H., Ji, Y., Loukianov, E., Paul, R. J., Nieman, M. L., Riddle, T., Duffy, J. J., Doetschman, T., et al. (1999). Impaired cardiac performance in heterozygous mice with a null mutation in the sarco(endo)plasmic reticulum, Ca2+-ATPase isoform, 2 (SERCA2) gene. J. Biol. Chem. 274, 2556-2562.
41. Pieske, B., Maier, L. S., Bets, D. M., and Hasenfuss, G. (1999). Ca2+ handling and sarcoplasmic reticulum Ca2+ content in isolated failing and nonfailing human myocardium. Circ. Res. 85, 38-46.
42. Prasad, V., Okunade, G. W., Miller, M. L., and Shun, G. E. (2004). Phenotypes of SERCA and PMCA knockout mice. Biochem. Biophys. Res. Commun. 322, 1192-1203. (Review).
43. Reiken, S., Gaburjakova, M., Guatimosim, S., Gomez, A. M., D'Armiento, J., Burkhoff, D., Wang, J., Vassort, G., Lederer, W. J., Marks, A. R., et al. (2003). Protein kinase A phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. Role of phosphatases and response to isoproterenol. J. Biol. Chem. 278, 444-453.
44. Runyan, R. B., Potts, J. D., Sharma, R. V., Loeber, C. P., Chiang, J. J., and Bhalla, R. C. (1990). Signal transduction of a tissue interaction during embryonic heart development. Cell Regul. 1 301-313.
45. Selmin, O., Thome, P. A., Caldwell, P. T., Johnson, P. D., and Runyan, R. B. (2005). Effects of trichloroethylene and its metabolite trichloroacetic acid on the expression of vimentin in the rat H9c2 Cell line. Cell Biol. Toxicol. 21, 83-95.
46. Selmin, O., Thorne, P. A., Caldwell, P. T., and Taylor, M. R. (2008). Trichloroethylene and Trichloroacetic Acid Regulate Calcium Signaling Pathways in Marine Embryonal Carcinoma Cells P19. Cardiovascular Toxicology. doi:10.1007/s 12012-008-9014-2.
47. Ver Heyen, M., Heymans, S., Antoons, G., Reed, T., Periasamy, M., Awede, B., Lebacq, J., Vangheluwe, P., Dewerchin, M., Collett, D., et al. (2001). Replacement of the muscle-speciftc sarcoplasmic reticulum. Ca(2+)-ATPase isoform SERCA2a by the nonmuscle SERCA2b homologue causes mild concentric hypertrophy and impairs contraction-relaxation of the heart. Circ. Res. 89, 838-846.
48. Watson, R. E., Jacobson, C. F., Williams, A. L., Howard, W. B., and DeSesso, J. M. (2006). Trichloroethylene-contaminated drinking water and congenital heart defects: A critical analysis of the literature. Reprod. Toxicol. 21, 117-147. (Review).