Coupled calcium and zinc dyshomeostasis and oxidative stress in cardiac myocytes and mitochondria of rats with chronic aldosteronism

Journal of Cardiovascular Pharmacology

Volumn 53, Issue 5, 2009, Pages 414-423

  Kamalov, German ^a   Deshmukh, Prajwal A ^a   Baburyan, Narina Y ^a   Gandhi, Malay S ^a   Johnson, Patti L ^a   Ahokas, Robert A ^a   Bhattacharya, Syamal K ^a   Sun, Yao ^a   Gerling, Ivan C ^a   Weber, Karl T ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Calcium; Cardiac myocytes and mitochondria; Metal response element transcription factor 1; Metallothionein; Zinc; Zinc transporters

Indexed keywords

3 NITROTYROSINE; 4 HYDROXYNONENAL; ALDOSTERONE; AMLODIPINE; CALCITRIOL; CALCIUM; CALCIUM ION; CINACALCET; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; IPROTEIN ZIP1; MAGNESIUM ION; MALONALDEHYDE; METAL RESPONSE ELEMENT TRANSCRIPTION FACTOR 1; METALLOTHIONEIN I; PROTEIN; PROTEIN ZNT 1; SPIRONOLACTONE; UNCLASSIFIED DRUG; ZINC; ZINC BINDING PROTEIN; ZINC TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL RAT; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART PROTECTION; HYPERALDOSTERONISM; HYPERPARATHYROIDISM; HYPOCALCEMIA; HYPOMAGNESEMIA; MALE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ALDEHYDES; ALDOSTERONE; ALDOSTERONE ANTAGONISTS; AMLODIPINE; ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; GLUTATHIONE PEROXIDASE; HOMEOSTASIS; HYDROGEN PEROXIDE; HYPERALDOSTERONISM; MALE; METALLOTHIONEIN; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SPIRONOLACTONE; SUPEROXIDE DISMUTASE; TYROSINE; ZINC;

EID: 67650892013     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3181a15e77     Document Type: Article

References (57)

1. Chen J, Mehta JL. Interaction of oxidized low-density lipoprotein and the renin-angiotensin system in coronary artery disease. Curr Hypertens Rep. 2006;8:139-143. (Pubitemid 43796691)
2. Chhokar VS, Sun Y, Bhattacharya SK, et al. Hyperparathyroidism and the calcium paradox of aldosteronism. Circulation. 2005;111:871-878.
3. Thomas M, Vidal A, Bhattacharya SK, et al. Zinc dyshomeostasis in rats with aldosteronism. Response to spironolactone. Am J Physiol Heart Circ Physiol. 2007;293:H2361-H2366. (Pubitemid 47605882)
4. Gandhi MS, Deshmukh PA, Kamalov G, et al. Causes and consequences of zinc dyshomeostasis in rats with chronic aldosteronism. J Cardiovasc Pharmacol. 2008;52:245-252.
5. 65zinc translocation in a rat model of chronic aldosteronism. J Cardiovasc Pharmacol. 2008;51:359-364.
6. Chhokar VS, Sun Y, Bhattacharya SK, et al. Loss of bone minerals and strength in rats with aldosteronism. Am J Physiol Heart Circ Physiol. 2004;287:H2023-H2026. (Pubitemid 39430739)
7. Smogorzewski M, Zayed M, Zhang YB, et al. Parathyroid hormone increases cytosolic calcium concentration in adult rat cardiac myocytes. Am J Physiol. 1993;264:H1998-H2006. (Pubitemid 23205973)
8. Fujita T, Palmieri GM. Calcium paradox disease: calcium deficiency prompting secondary hyperparathyroidism and cellular calcium overload. J Bone Miner Metab. 2000;18:109-125. (Pubitemid 30241105)
9. Gerling IC, Sun Y, Ahokas RA, et al. Aldosteronism: an immunostimulatory state precedes the proinflammatory/fibrogenic cardiac phenotype. Am J Physiol Heart Circ Physiol. 2003;285:H813-H821. (Pubitemid 36885915)
10. Ahokas RA, Warrington KJ, Gerling IC, et al. Aldosteronism and peripheral blood mononuclear cell activation. A neuroendocrine-immune interface. Circ Res. 2003;93:e124-e135.
11. 2 in peripheral blood mononuclear cells. Circulation. 2005;111:51-57.
12. Kristián T, Siesjö BK. Calcium in ischemic cell death. Stroke. 1998;29:705-718.
13. Sun Y, Zhang J, Lu L, et al. Aldosterone-induced inflammation in the rat heart. Role of oxidative stress. Am J Pathol. 2002;161:1773-1781. (Pubitemid 35265535)
14. Sun Y, Ramires FJA, Weber KT. Fibrosis of atria and great vessels in response to angiotensin II or aldosterone infusion. Cardiovasc Res. 1997;35:138-147. (Pubitemid 27374751)
15. Nickerson PA, Conran RM. Parathyroidectomy ameliorates vascular lesions induced by deoxycorticosterone in the rat. Am J Pathol. 1981;105:185-190. (Pubitemid 12241800)
16. Vidal A, Sun Y, Bhattacharya SK, et al. Calcium paradox of aldosteronism and the role of the parathyroid glands. Am J Physiol Heart Circ Physiol. 2006;290:H286-H294.
17. Nickerson PA. A low dose of a calcium antagonist (nitrendipine) ameliorates cardiac and renal lesions induced by DOC in the rat. Exp Mol Pathol. 1984;41:309-320.
18. Andrews GK. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol. 2000;59:95-104.
19. Andrews GK. Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals. 2001;14:223-237.
20. Liuzzi JP, Cousins RJ. Mammalian zinc transporters. Annu Rev Nutr. 2004;24:151-172.
21. Gaither LA, Eide DJ. Eukaryotic zinc transporters and their regulation. Biometals. 2001;14:251-270.
22. Brilla CG, Matsubara LS, Weber KT. Anti-aldosterone treatment and the prevention of myocardial fibrosis in primary and secondary hyperaldosteronism. J Mol Cell Cardiol. 1993;25:563-575. (Pubitemid 23208145)
23. Brilla CG, Pick R, Tan LB, et al. Remodeling of the rat right and left ventricle in experimental hypertension. Circ Res. 1990;67:1355-1364.
24. Brilla CG, Weber KT. Mineralocorticoid excess, dietary sodium and myocardial fibrosis. J Lab Clin Med. 1992;120:893-901.
25. Campbell SE, Janicki JS, Matsubara BB, et al. Myocardial fibrosis in the rat with mineralocorticoid excess: prevention of scarring by amiloride. Am J Hypertens. 1993;6:487-495.
26. Goodwin KD, Ahokas RA, Bhattacharya SK, et al. Preventing oxidative stress in rats with aldosteronism by calcitriol and dietary calcium and magnesium supplements. Am J Med Sci. 2006;332:73-78.
27. Selektor Y, Ahokas RA, Bhattacharya SK, et al. Cinacalcet and the prevention of secondary hyperparathyroidism in rats with aldosteronism. Am J Med Sci. 2008;335:105-110. (Pubitemid 351253405)
28. Mohanty JG, Jaffe JS, Schulman ES, et al. A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. J Immunol Methods. 1997;202:133-141.
29. Coeroli L, Renolleau S, Arnaud S, et al. Nitric oxide production and perivascular tyrosine nitration following focal ischemia in neonatal rat. J Neurochem. 1998;70:2516-2525. (Pubitemid 28252378)
30. Swaney JS, Roth DM, Olson ER, et al. Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression of adenylyl cyclase. Proc Natl Acad Sci U S A. 2005;102:437-442.
31. Tomlinson JW, Sinha B, Bujalska I, et al. Expression of 11β-hydroxysteroid dehydrogenase type 1 in adipose tissue is not increased in human obesity. J Clin Endocrinol Metab. 2002;87:5630-5635. (Pubitemid 36034370)
32. 2+ current in mice. J Physiol. 2005;569(pt 1):153-162.
33. Rossier MF, Lesouhaitier O, Perrier E, et al. Aldosterone regulation of T-type calcium channels. J Steroid Biochem Mol Biol. 2003;85:383-388. (Pubitemid 37011114)
34. Mak IT, Zhang J, Weglicki WB. Cytoprotective properties of nisoldipine and amlodipine against oxidative endothelial cell injury. Ann N Y Acad Sci. 2000;899:403-406. (Pubitemid 30352804)
35. Katakai K, Liu J, Nakajima K, et al. Nitric oxide induces metallothionein (MT) gene expression apparently by displacing zinc bound to MT. Toxicol Lett. 2001;119:103-108. (Pubitemid 32304371)
36. St. Croix CM, Wasserloos KJ, Dineley KE, et al. Nitric oxide-induced changes in intracellular zinc homeostasis are mediated by metallothionein/ thionein. Am J Physiol Lung Cell Mol Physiol. 2002;282:L185-L192.
37. 2+ release. Proc Natl Acad Sci U S A. 2003;100:13952-13957.
38. Khatai L, Goessler W, Lorencova H, et al. Modulation of nitric oxide-mediated metal release from metallothionein by the redox state of glutathione in vitro. Eur J Biochem. 2004;271:2408-2416. (Pubitemid 38813571)
39. 2+ signaling: old guests, new functions. Pflugers Arch. 2007;455:375-396.
40. 2+ and 5-aminolevulinic acid-derived oxyradicals promote injury to isolated mitochondria? Free Radic Biol Med. 1995;19:381-390.
41. Aon MA, Cortassa S, Maack C, et al. Sequential opening of mitochondrial ion channels as a function of glutathione redox thiol status. J Biol Chem. 2007;282:21889-21900. (Pubitemid 47195754)
42. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta. 2006;1757:509-517.
43. Costello LC, Guan Z, Franklin RB, et al. Metallothionein can function as a chaperone for zinc uptake transport into prostate and liver mitochondria. J Inorg Biochem. 2004;98:664-666. (Pubitemid 38369294)
44. 2+ loads in cortical neurons. Neurobiol Dis. 2002;10:100-108.
45. Guan Z, Kukoyi B, Feng P, et al. Kinetic identification of a mitochondrial zinc uptake transport process in prostate cells. J Inorg Biochem. 2003;97:199-206. (Pubitemid 37152444)
46. Feng W, Cai J, Pierce WM, et al. Metallothionein transfers zinc to mitochondrial aconitase through a direct interaction in mouse hearts. Biochem Biophys Res Commun. 2005;332:853-858. (Pubitemid 40745191)
47. Chanoit G, Lee S, Xi J, et al. Exogenous zinc protects cardiac cells from reperfusion injury by targeting mitochondrial permeability transition pore through inactivation of glycogen synthase kinase-3beta. Am J Physiol Heart Circ Physiol. 2008;295:H1227-H1233.
48. Aon MA, Cortassa S, O'Rourke B. Percolation and criticality in a mitochondrial network. Proc Natl Acad Sci U S A. 2004;101:4447-4452.
49. Slodzinski MK, Aon MA, O'Rourke B. Glutathione oxidation as a trigger of mitochondrial depolarization and oscillation in intact hearts. J Mol Cell Cardiol. 2008;45:650-660.
50. Lossnitzer K, Janke J, Hein B, et al. Disturbed myocardial calcium metabolism: a possible pathogenetic factor in the hereditary cardiomyopathy of the Syrian hamster. Recent Adv Stud Cardiac Struct Metab. 1975;6:207-217.
51. Bhattacharya SK, Johnson PL, Thakar JH. Reversal of impaired oxidative phosphorylation and calcium overloading in the in vitro cardiac mitochondria of CHF-146 dystrophic hamsters with hereditary muscular dystrophy. J Neurol Sci. 1993;120:180-186.
52. Palmieri GM, Nutting DF, Bhattacharya SK, et al. Parathyroid ablation in dystrophic hamsters. Effects on Ca content and histology of heart, diaphragm, and rectus femoris. J Clin Invest. 1981;68:646-654.
53. Bhattacharya SK, Palmieri GM, Bertorini TE, et al. The effects of diltiazem in dystrophic hamsters. Muscle Nerve. 1982;5:73-78.
54. Crawford AJ, Bhattacharya SK. Excessive intracellular zinc accumulation in cardiac and skeletal muscles of dystrophic hamsters. Exp Neurol. 1987;95:265-276.
55. Kanai A, Epperly M, Pearce L, et al. Differing roles of mitochondrial nitric oxide synthase in cardiomyocytes and urothelial cells. Am J Physiol Heart Circ Physiol. 2004;286:H13-H21. (Pubitemid 38049457)
56. Cai L. Diabetic cardiomyopathy and its prevention by metallothionein: experimental evidence, possible mechanisms and clinical implications. Curr Med Chem. 2007;14:2193-2203. (Pubitemid 47578157)
57. Karagulova G, Yue Y, Moreyra A, et al. Protective role of intracellular zinc in myocardial ischemia/reperfusion is associated with preservation of protein kinase C isoforms. J Pharmacol Exp Ther. 2007;321:517-525. (Pubitemid 46624490)