The role of aryl hydrocarbon receptor signaling pathway in cardiotoxicity of acute lead intoxication in vivo and in vitro rat model

Toxicology

Volumn 306, Issue , 2013, Pages 40-49

  Ansari, Mushtaq A ^a   Maayah, Zaid H ^a   Bakheet, Saleh A ^a   El Kadi, Ayman O ^b   Korashy, Hesham M ^a  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cardiac hypertrophy; Cytochrome P4501A1; Gene expression; H9c2 cells; Lead nitrate; Rat cardiomyocyte

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BRAIN NATRIURETIC PEPTIDE; CREATINE KINASE; CYTOCHROME P450 1A1; LACTATE DEHYDROGENASE; LEAD; MESSENGER RNA; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; RESVERATROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOTOXICITY; CONTROLLED STUDY; GENE EXPRESSION; HEART FAILURE; HEART MUSCLE CELL; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LEAD POISONING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CREATINE KINASE; CYTOCHROME P-450 CYP1A1; HEART; HEART DISEASES; HISTOCYTOCHEMISTRY; L-LACTATE DEHYDROGENASE; LEAD; MALE; MYOCARDIUM; MYOCYTES, CARDIAC; MYOSIN HEAVY CHAINS; NATRIURETIC PEPTIDE, BRAIN; RANDOM ALLOCATION; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SIGNAL TRANSDUCTION; STILBENES;

EID: 84874569729     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.01.024     Document Type: Article

References (69)

1. Abdel Moneim A.E., Dkhil M.A., Al-Quraishy S. Effects of flaxseed oil on lead acetate-induced neurotoxicity in rats. Biol. Trace Elem. Res. 2011, 144:904-913.
2. Alhaider A.A., Korashy H.M., Sayed-Ahmed M.M., Mobark M., Kfoury H., Mansour M.A. Metformin attenuates streptozotocin-induced diabetic nephropathy in rats through modulation of oxidative stress genes expression. Chem. Biol. Interact. 2011, 192:233-242.
3. Alpert N.R., Mulieri L.A. Heat, mechanics, and myosin ATPase in normal and hypertrophied heart muscle. Fed. Proc. 1982, 41:192-198.
4. Alsaad A.M., Zordoky B.N., El-Sherbeni A.A., El-Kadi A.O. Chronic doxorubicin cardiotoxicity modulates cardiac cytochrome P450-mediated arachidonic acid metabolism in rats. Drug Metab. Dispos. 2012, 40:2126-2135.
5. Amodio-Cocchieri R., Arnese A., Prospero E., Roncioni A., Baruffo L., Ullucci R., Romano V. Lead in human blood from children living in Campania, Italy. J. Toxicol. Environ. Health 1996, 47:311-320.
6. ATSDR, 2007. Toxicological profile for lead. Agency for Toxic Substances and Disease Registry. U.S. Department of Health and Human Services.
7. ATSDR, 2011. The agency for toxic substances and disease registry, CDC. http://www.atsdr.cdc.gov/spl/.
8. Barbier O., Jacquillet G., Tauc M., Cougnon M., Poujeol P. Effect of heavy metals on, and handling by, the kidney. Nephron Physiol. 2005, 99:105-110.
9. Borlak J., Thum T. PCBs alter gene expression of nuclear transcription factors and other heart-specific genes in cultures of primary cardiomyocytes: possible implications for cardiotoxicity. Xenobiotica 2002, 32:1173-1183.
10. Buhl S.N., Jackson K.Y. Optimal conditions and comparison of lactate dehydrogenase catalysis of the lactate-to-pyruvate and pyruvate-to-lactate reactions in human serum at 25, 30, and 37 degrees C. Clin. Chem. 1978, 24:828-831.
11. CEPA, 2011. Canadian environmental protection act registry. http://www.ec.gc.ca/CEPARegistry/subs_list/Toxicupdate.cfm.
12. Cheng T.H., Liu J.C., Lin H., Shih N.L., Chen Y.L., Huang M.T., Chan P., Cheng C.F., Chen J.J. Inhibitory effect of resveratrol on angiotensin II-induced cardiomyocyte hypertrophy. Naunyn. Schmiedebergs Arch. Pharmacol. 2004, 369:239-244.
13. Choudhary D., Jansson I., Stoilov I., Sarfarazi M., Schenkman J.B. Metabolism of retinoids and arachidonic acid by human and mouse cytochrome P450 1b1. Drug Metab. Dispos. 2004, 32:840-847.
14. Cobanoglu U., Demir H., Sayir F., Duran M., Mergan D. Some mineral, trace element and heavy metal concentrations in lung cancer. Asian Pac. J. Cancer Prev. 2010, 11:1383-1388.
15. Denison M.S., Vella L.M., Okey A.B. Structure and function of the Ah receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin. Species difference in molecular properties of the receptors from mouse and rat hepatic cytosols. J. Biol. Chem. 1986, 261:3987-3995.
16. Denison M.S., Fisher J.M., Whitlock J.P. Protein-DNA interactions at recognition sites for the dioxin-Ah receptor complex. J. Biol. Chem. 1989, 264:16478-16482.
17. Elbekai R.H., El-Kadi A.O. Cytochrome P450 enzymes: central players in cardiovascular health and disease. Pharmacol. Ther. 2006, 112:564-587.
18. Factor-Litvak P., Slavkovich V., Liu X., Popovac D., Preteni E., Capuni-Paracka S., Hadzialjevic S., Lekic V., LoIacono N., Kline J., Graziano J. Hyperproduction of erythropoietin in nonanemic lead-exposed children. Environ. Health Perspect. 1998, 106:361-364.
19. Fatkin D., McConnell B.K., Mudd J.O., Semsarian C., Moskowitz I.G., Schoen F.J., Giewat M., Seidman C.E., Seidman J.G. An abnormal Ca(2+) response in mutant sarcomere protein-mediated familial hypertrophic cardiomyopathy. J. Clin. Invest. 2000, 106:1351-1359.
20. Gerhardsson L., Brune D., Nordberg G.F., Wester P.O. Multielemental assay of tissues of deceased smelter workers and controls. Sci. Total Environ. 1988, 74:97-110.
21. Goyer R.A. Lead toxicity: current concerns. Environ. Health Perspect. 1993, 100:177-187.
22. Haider U.G., Sorescu D., Griendling K.K., Vollmar A.M., Dirsch V.M. Resveratrol suppresses angiotensin II-induced Akt/protein kinase B and p70 S6 kinase phosphorylation and subsequent hypertrophy in rat aortic smooth muscle cells. Mol. Pharmacol. 2002, 62:772-777.
23. Harris D.E., Work S.S., Wright R.K., Alpert N.R., Warshaw D.M. Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro. J. Muscle Res. Cell Motil. 1994, 15:11-19.
24. Holubarsch C., Goulette R.P., Litten R.Z., Martin B.J., Mulieri L.A., Alpert N.R. The economy of isometric force development, myosin isoenzyme pattern and myofibrillar ATPase activity in normal and hypothyroid rat myocardium. Circ. Res. 1985, 56:78-86.
25. Imig J.D., Zhao X., Capdevila J.H., Morisseau C., Hammock B.D. Soluble epoxide hydrolase inhibition lowers arterial blood pressure in angiotensin II hypertension. Hypertension 2002, 39:690-694.
26. Iqbal M., Dubey K., Anwer T., Ashish A., Pillai K.K. Protective effects of telmisartan against acute doxorubicin-induced cardiotoxicity in rats. Pharmacol. Rep. 2008, 60:382-390.
27. Kaul B., Sandhu R.S., Depratt C., Reyes F. Follow-up screening of lead-poisoned children near an auto battery recycling plant, Haina, Dominican Republic. Environ. Health Perspect. 1999, 107:917-920.
28. Kim D.H., Suh Y.S., Mun K.C. Tissue levels of malondialdehyde after passive smoke exposure of rats for a 24-week period. Nicotine Tob. Res. 2004, 6:1039-1042.
29. Kiriazis H., Kranias E.G. Genetically engineered models with alterations in cardiac membrane calcium-handling proteins. Annu. Rev. Physiol. 2000, 62:321-351.
30. Korashy H.M., El-Kadi A.O. Differential effects of mercury, lead and copper on the constitutive and inducible expression of aryl hydrocarbon receptor (AHR)-regulated genes in cultured hepatoma Hepa 1c1c7 cells. Toxicology 2004, 201:153-172.
31. Korashy H.M., El-Kadi A.O. Regulatory mechanisms modulating the expression of cytochrome P450 1A1 gene by heavy metals. Toxicol. Sci. 2005, 88:39-51.
32. Korashy H.M., El-Kadi A.O. The role of aryl hydrocarbon receptor in the pathogenesis of cardiovascular diseases. Drug Metab. Rev. 2006, 38:411-450.
33. Korashy H.M., El-Kadi A.O. The role of aryl hydrocarbon receptor and the reactive oxygen species in the modulation of glutathione transferase by heavy metals in murine hepatoma cell lines. Chem. Biol. Interact. 2006, 162:237-248.
34. Korashy H.M., El-Kadi A.O. The role of redox-sensitive transcription factors NF-kappaB and AP-1 in the modulation of the Cyp1a1 gene by mercury, lead, and copper. Free Radic. Biol. Med. 2008, 44:795-806.
35. Korashy H.M., Anwar-Mohamed A., Soshilov A.A., Denison M.S., El-Kadi A.O. The p38 MAPK inhibitor SB203580 induces cytochrome P450 1A1 gene expression in murine and human hepatoma cell lines through ligand-dependent aryl hydrocarbon receptor activation. Chem. Res. Toxicol. 2011, 24:1540-1548.
36. Korashy H.M., El-Kadi A.O. Transcriptional and posttranslational mechanisms modulating the expression of the cytochrome P450 1A1 gene by lead in HepG2 cells: a role of heme oxygenase. Toxicology 2012, 291:113-121.
37. Kvasnicka T., Kvasnicka J., Ceska R., Grauova B., Vrablik M. Increasing plasma levels of soluble cell adhesion molecules (sE-selectin, sP-selectin and sICAM-1) in overweight adults with combined hyperlipidemia. Sb. Lek. 2001, 102:473-477.
38. Laethem R.M., Halpert J.R., Koop D.R. Epoxidation of arachidonic acid as an active-site probe of cytochrome P-450 2B isoforms. Biochim. Biophys. Acta 1994, 1206:42-48.
39. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
40. Locher M.R., Razumova M.V., Stelzer J.E., Norman H.S., Moss R.L. Effects of low-level α-myosin heavy chain expression on contractile kinetics in porcine myocardium. Am. J. Physiol. Heart Circ. Physiol. 2011, 300:H869-H878.
41. Marttila M., Puhakka J., Luodonpaa M., Vuolteenaho O., Ganten U., Ruskoaho H. Augmentation of BNP gene expression in atria by pressure overload in transgenic rats harbouring human renin and angiotensinogen genes. Blood Press. 1999, 8:308-316.
42. Mikler J., Banovcin P., Jesenak M., Hamzikova J., Statelova D. Successful treatment of extreme acute lead intoxication. Toxicol. Ind. Health 2009, 25:137-140.
43. Mudipalli A. Lead hepatotoxicity & potential health effects. Indian J. Med. Res. 2007, 126:518-527.
44. Nebert D.W., Dalton T.P., Okey A.B., Gonzalez F.J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279:23847-23850.
45. Ng V.Y., Huang Y., Reddy L.M., Falck J.R., Lin E.T., Kroetz D.L. Cytochrome P450 eicosanoids are activators of peroxisome proliferator-activated receptor alpha. Drug Metab. Dispos. 2007, 35:1126-1134.
46. Sambrook J., Fritsch E.F., Maniatatis T. Molecular Cloning. A Laboratory Manual 1989, Cold Spring Harbour Laboratory Press, Plainview, NY. N. Ford (Ed.).
47. Savouret J.F., Berdeaux A., Casper R.F. The aryl hydrocarbon receptor and its xenobiotic ligands: a fundamental trigger for cardiovascular diseases. Nutr. Metab. Cardiovasc. Dis. 2003, 13:104-113.
48. Seddik L., Bah T.M., Aoues A., Brnderdour M., Silmani M. Dried leaf extract protects against lead-induced neurotoxicity in Wistar rats. Eur. J. Sci. Res. 2010, 42:139-151.
49. Selbst S.M., Henretig F.M., Pearce J. Lead encephalopathy. A case report and review of management. Clin Pediatr (Phila) 1985, 24. 280-282, 285.
50. Singh A.K. Neurotoxicity in rats chronically exposed to lead ingestion: measurement of intracellular concentrations of free calcium and lead ions in resting or depolarized brain slices. Neurotoxicology 1995, 16:133-138.
51. Sogawa K., Fujii-Kuriyama Y. Ah receptor, a novel ligand-activated transcription factor. J. Biochem. (Tokyo) 1997, 122:1075-1079.
52. Somers E. International agency for research on cancer. Can. Med. Assoc. J. 1985, 133:845-846.
53. Tezel H., Ertas O.S., Erakin C., Kayali A. Blood mercury levels of dental students and dentists at a dental school. Br. Dent. J. 2001, 191:449-452.
54. Thum T., Borlak J. Gene expression in distinct regions of the heart. Lancet 2000, 355:979-983.
55. Timchalk C., Lin Y., Weitz K.K., Wu H., Gies R.A., Moore D.A., Yantasee W. Disposition of lead (Pb) in saliva and blood of Sprague-Dawley rats following a single or repeated oral exposure to Pb-acetate. Toxicology 2006, 222:86-94.
56. Vakharia D.D., Liu N., Pause R., Fasco M., Bessette E., Zhang Q.Y., Kaminsky L.S. Effect of metals on polycyclic aromatic hydrocarbon induction of CYP1A1 and CYP1A2 in human hepatocyte cultures. Toxicol. Appl. Pharmacol. 2001, 170:93-103.
57. Vakharia D.D., Liu N., Pause R., Fasco M., Bessette E., Zhang Q.Y., Kaminsky L.S. Polycyclic aromatic hydrocarbon/metal mixtures: effect on PAH induction of CYP1A1 in human HEPG2 cells. Drug Metab. Dispos. 2001, 29:999-1006.
58. Waalkes M.P., Diwan B.A., Ward J.M., Devor D.E., Goyer R.A. Renal tubular tumors and atypical hyperplasias in B6C3F1 mice exposed to lead acetate during gestation and lactation occur with minimal chronic nephropathy. Cancer Res. 1995, 55:5265-5271.
59. Wadi S.A., Ahmad G. Effects of lead on the male reproductive system in mice. J. Toxicol. Environ. Health A 1999, 56:513-521.
60. Watkins S.J., Borthwick G.M., Arthur H.M. The H9C2 cell line and primary neonatal cardiomyocyte cells show similar hypertrophic responses in vitro. In Vitro Cell. Dev. Biol. Anim. 2011, 47:125-131.
61. Whitelaw M.L., Gustafsson J.A., Poellinger L. Identification of transactivation and repression functions of the dioxin receptor and its basic helix-loop-helix/PAS partner factor Arnt: inducible versus constitutive modes of regulation. Mol. Cell. Biol. 1994, 14:8343-8355.
62. Williams B.J., Hejtmancik M.R., Abreu M. Cardiac effects of lead. Fed. Proc. 1983, 42:2989-2993.
63. Wu A.H., Bowers G.N. Evaluation and comparison of immunoinhibition and immunoprecipitation methods for differentiating MB and BB from macro forms of creatine kinase isoenzymes in patients and healthy individuals. Clin. Chem. 1982, 28:2017-2021.
64. Xu M., Jin Y., Song Q., Wu J., Philbrick M.J., Cully B.L., An X., Guo L., Gao F., Li J. The endothelium-dependent effect of RTEF-1 in pressure overload cardiac hypertrophy: role of VEGF-B. Cardiovasc. Res. 2011, 90:325-334.
65. Yousif M.H., Benter I.F., Roman R.J. Cytochrome P450 metabolites of arachidonic acid play a role in the enhanced cardiac dysfunction in diabetic rats following ischaemic reperfusion injury. Auton. Autacoid. Pharmacol. 2009, 29:33-41.
66. Zordoky B.N., Aboutabl M.E., El-Kadi A.O. Modulation of cytochrome P450 gene expression and arachidonic acid metabolism during isoproterenol-induced cardiac hypertrophy in rats. Drug Metab. Dispos. 2008, 36:2277-2286.
67. Zordoky B.N., El-Kadi A.O. 2,3,7,8-Tetrachlorodibenzo-p-dioxin and beta-naphthoflavone induce cellular hypertrophy in H9c2 cells by an aryl hydrocarbon receptor-dependant mechanism. Toxicol. In Vitro 2010, 24:863-871.
68. Zordoky B.N., El-Kadi A.O. Effect of cytochrome P450 polymorphism on arachidonic acid metabolism and their impact on cardiovascular diseases. Pharmacol. Ther. 2010, 125:446-463.
69. Zordoky B.N., Anwar-Mohamed A., Aboutabl M.E., El-Kadi A.O. Acute doxorubicin toxicity differentially alters cytochrome P450 expression and arachidonic acid metabolism in rat kidney and liver. Drug Metab. Dispos. 2011, 39:1440-1450.