Mitochondrial MMP activation, dysfunction and arrhythmogenesis in hyperhomocysteinemia

Current Vascular Pharmacology

Volumn 6, Issue 2, 2008, Pages 84-92

  Moshal, Karni S ^a   Metreveli, Naira ^a   Frank, Iuliana ^a   Tyagi, Suresh C ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Calcium dynamics; Calpain; Cardiac NMDA R1; Cardiomyocytes; Channelopathies; Congestive heart failure; Cyclophilin D; Electrical remodeling; Extracellular matrix; Intracellular MMP; Mitochondrial permeability transition; Putative MMP (PUMP); Redox stress; Systolic diastolic dysfunction

Indexed keywords

CALCIUM; CALPAIN; CILAZAPRIL; CYCLOPHILIN D; DIZOCILPINE; GELATINASE B; HOMOCYSTEINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LEUPEPTIN; MATRIX METALLOPROTEINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR; VALSARTAN;

AMINO ACID ANALYSIS; ARRHYTHMOGENESIS; BRAIN TISSUE; CALCIUM CELL LEVEL; CELL MEMBRANE PERMEABILITY; CELL PERMEABILIZATION; CELLULAR DISTRIBUTION; CONGESTIVE HEART FAILURE; DIASTOLIC DYSFUNCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG MECHANISM; DRUG MEGADOSE; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HEART ARRHYTHMIA; HEART ATRIUM FIBRILLATION; HEART CONDUCTION; HEART FUNCTION; HEART MUSCLE CELL; HEART PERFORMANCE; HUMAN; HYPERHOMOCYSTEINEMIA; MITOCHONDRIAL MEMBRANE; NONHUMAN; PROTEIN FUNCTION; REDOX STRESS; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ENZYMOLOGY; HEART FAILURE; HEART MITOCHONDRION; METABOLISM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HEART FAILURE; HOMOCYSTEINE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; HYPERHOMOCYSTEINEMIA; MATRIX METALLOPROTEINASES; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

EID: 47249109410     PISSN: 15701611     EISSN: None     Source Type: Journal    
DOI: 10.2174/157016108783955301     Document Type: Review

References (74)

1. American Heart Association (Heart and stroke statistical update). Dallas, TX: American Heart Association 2000 2001; 31: 19-20.
2. Cowie MR, Mosterd A, Wood DA, Deckers JW, Poole-Wilson PA, Sutton GC, et al. The epidemiology of heart failure. Eur Heart J 1997; 18: 208-225.
3. Levy D, Larson MG, Vasan RS, Kannel WB, Ho KK. The progression from hypertension to congestive heart failure. JAMA 1996; 275: 1557-1562.
4. Wilhelmsen L, Rosengren A, Eriksson H, Lappas G. Heart failure in the general population of men. J Intern Med 2001; 249: 253-261.
5. Kenchaiah S, Evans JC, Levy D, Wilson PWF, Benjamin EJ, Larson MG, et al. Obesity and the risk of heart failure. N Engl J Med 2002; 347: 305-313.
6. Stevenson WG, Stevenson LW, Middlekauff HR, Fonarow GC, Hamilton MA, Woo MA, et al. Improving survival for patients with advanced heart failure: a study of 737 consecutive patients. J Am Coll Cardiol 1995; 26: 1417-1423.
7. Swynghedauw B. Molecular Mechanisms of Myocardial Remodeling. Physiol Rev 1999; 79: 215-262.
8. Colucci WS, Braunwald W. Path physiology of heart failure. In: E. Braunwald, D.P. Zipes and P. Libby, Editors, Heart Disease (6th ed); W B Saunders Company, Philadelphia, Pennsylvania 2001; 517-518.
9. Zucker IH, Wang W, Brändle M, Schultz HD, Patel KP. Neural regulation of sympathetic nerve activity in heart failure. Prog Cardiovasc Dis 1995; 37: 397-414.
10. Singh K, Communal C, Sawyer DB, Colucci WS. Adrenergic regulation of myocardial apoptosis. Cardiovasc Res 2000; 45: 713-719.
11. Li YF, Cornish KG, Patel KP. Alteration of NMDA NR[1] receptors within the paraventricular nucleus of hypothalamus in rats with heart failure. Circ Res 2003; 93(10): 990-7.
12. D'Amico M, Filippo C, Di Rossi F. Arrhythmias induced by myocardial ischemia-reperfusion are sensitive to ionotrophic excitatory amino acid receptor antagonists. Eur J Pharmacol 1999; 366: 167-174.
13. Herrmann M, Kindermann I, Muller S, Georg T, Kindermann M, Bohm M, et al. Relationship of plasma homocysteine with the severity of chronic heart failure. Clin Chem 2005; 51: 1512-1515.
14. Vasan RS, Beiser A, D'Agostino RB, Levy D, Selhub J, Jacques PF, et al. Plasma homocysteine and risk for congestive heart failure in adults without prior myocardial infarction. JAMA 2003; 289: 1251-1257.
15. Bollani G, Ferrari R, Bersatti F, Ferrari M, Cattaneo M, Zighetti MI, et al. A hyperhomocysteinemia study in a population with a familial factor for acute MI and SCD at a young age. Cardiologia 1999; 44: 75-81.
16. Albert C M, Rifai N, Stampfer MJ, Ridker PM. Prospective study of C-reactive protein, Hcy and plasma lipid levels as predictors of SCD. Circulation 2002; 105: 2595-2599.
17. Burke AP, Fonseca V, Kolodgie F, Zieske A, Fink L, Virmani R. Increased serum Hcy and SCD resulting from coronary atherosclerosis with fibrous plaques. Arterioscler Thromb Vasc Biol 2002; 22: 1936-1941.
18. Folbergrova J. NMDA and not non-NMDA receptor antagonists are protective against seizures induced by homocysteine in neonatal rats. Exp Neurol 1994; 130: 344-350.
19. DiMicco J, Monroe AJ. Stimulation of metabotropic glutamate receptors in the dorsomedial hypothalamus elevate heart rate in rats. Am J Physiol 1996; 270:1115-1121.
20. Gao X, Xu XB, Pang J, Zhang C, Ding JM, Peng X, et al. NMDA receptor activation induces mitochondrial dysfunction, oxidative stress and apoptosis in cultured neonatal rat cardio. Physiol Res 2007; 56: 559-569.
21. Razeghi P, Volpini KC, Wang ME, Youker KA, Stepkowski S, Taegtmeyer H. Mechanical unloading of the heart activates the calpain system. J Mol Cell Cardiol 2007; 42: 449-452.
22. Takahashi M, Tanonaka K, Yoshida H, Koshimizu M, Daicho T, Oikawa R, et al. Possible involvement of calpain activation in pathogenesis of chronic heart failure after acute myocardial infarction. J Cardiovasc Pharmacol 2006; 47: 413-421.
23. Goette A, Arndt M, Rocken C, Staack T, Bechtloff R, Reinhold D, et al. Calpains and cytokines in fibrillating human atria. Am J Physiol Heart Circ Physiol 2002; 283: 264-272.
24. Brundel BJ, Ausma J, van Gelder IC, Van der Want JJ, van Gilst WH, Crijns HJ, et al. Activation of proteolysis by calpains and structural changes in human paroxysmal and persistent atrial fibrillation. Cardiovasc Res 2002; 54: 380-389.
25. Delgado RM 3rd, Willerson JT. Pathophysiology of heart failure: a look at the future. Tex Heart Inst J 1999; 26: 28-33.
26. Nagase H, Woessner J Jr. Matrix metalloproteinases. J Biol Chem 1999; 274: 21491-21494.
27. Mujumdar VS, Smiley LM, Tyagi SC. Activation of matrix metalloproteinase dilates and decreases cardiac tensile strength. Int J Cardiol 2001; 79: 277-286.
28. Thomas CV, Coker ML, Zellner JL, Handy JR, Crumbley AJ 3rd, Spinale FG. Increased matrix metalloproteinase activity and selective upregulation in LV myocardium from patients with end-stage dilated cardiomyopathy. Circulation 1998; 97: 1708-1715.
29. Spinale FG, Coker ML, Heung LJ, Bond BR, Gunasinghe HR, Etoh T, et al. A matrix metalloproteinase induction/activation system exists in the human left ventricular myocardium and is upregulated in heart failure. Circulation 2000; 102: 1944-1949.
30. Iwanaga Y, Aoyama T, Kihara Y, Onozawa Y, Yoneda T, Sasayama S. Excessive activation of matrix metalloproteinases coincides with left ventricular remodeling during transition from hypertrophy to heart failure in hypertensive rats. J Am Coll Cardiol 2002; 39: 1384-1391.
31. Reinhardt D, Sigusch HH, Hensse J, Tyagi SC, Korfer R, Fiqulla HR. Cardiac remodeling in end stage heart failure: upregulation of matrix metalloproteinase (MMP) irrespective of the underlying disease, and evidence for a direct inhibitory effect of ACE inhibitors on MMP. Heart 2002; 88: 525-530.
32. Shastry S, Hayden MR, Luchessi PA, Tyagi SC. Matrix metalloproteinase in left ventricular remodeling and heart failure. Curr Cardiol Rep 2003; 5: 200-204.
33. Moshal KS, Tyagi N, Moss V, Henderson B, Steed M, Ovechkin A, et al. Early induction of matrix metalloproteinase-9 transduces signaling in human heart end stage failure. J Cell Mol Med 2005; 9: 704-713.
34. Moshal KS, Tyagi N, Henderson B, Ovechkin AV, Tyagi SC. Protease-activated receptor and endothelial-myocyte uncoupling in chronic heart failure. Am J Physiol Heart Circ Physiol 2005; 288: 2770-2777.
35. Sood HS, Cox M J, Tyagi SC. Generation of Nitrotyrosine Precedes the Activation of Matrix Metalloproteinase in Left Ventricle of Hyperhomocystenemia Rats. Antioxidant Redox Signal 2002; 45: 799-804.
36. Adalbert R, Engelhardt JI, Siklos L. Hcy application disrupts calcium homeostasis and induces degeneration of spinal motor neurons in vivo. Acta Neuropathologica 2002; 103: 428-436.
37. Mujumdar VS, Hayden MR, Tyagi SC. Homocysteine induces calcium secondary messenger in vascular smooth muscle cells. J Cell Physiol 2000; 183: 28-36.
38. Moshal KS, Singh M, Sen U, Rosenberger DS, Henderson B, Tyagi N, et al. Homocysteine-mediated activation and mitochondrial translocation of calpain regulates MMP-9 in MVEC. Am J Physiol Heart Circ Physiol 2006; 291: 2825-2835.
39. Li YF, Cornish KG, Patel KP. Alteration of NMDA NR1 receptors within the paraventricular nucleus of hypothalamus in rats with heart failure. Circ Res 2003; 93: 990-7.
40. Nakamichi N, Ohno H, Kuramoto N, Yoneda Y. Dual mechanisms of Ca(2+) increases elicited by N-methyl-D-aspartate in immature and mature cultured cortical neurons. J Neurosci Res 2002; 67:275-283.
41. Schinder AF, Olson EC, Spitzer NC, Montal M. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 1996; 16: 6125-6133.
42. Kraine D, Bai G, Okamoto S, Carlos M. Synergistic activation of the NMDA receptor subunit 1 promoter by myocyte enhancer factor 3C and sp1. J Biol Chem 1998; 273: 26218-26224.
43. Huang CF, Su MJ. Positive inotropic action of NMDA receptor antagonist (+)-MK801 in rat heart. J Biomed Sci 1999; 6: 387-398.
44. Chen H, Fitzgerald R, Brown AT. Identification of Hcy receptor in the peripheral endothelial and its role in proliferation. J Vasc Surg 2005; 41: 853-860.
45. Qureshi I, Chen H, Brown AT. Hcy-induced vascular dysregulation is mediated by the NMDA receptor. Vasc Med 2005; 10: 215-223.
46. Gill SS, Pulido OM, Mueller RW, McGuire PF. Molecular and immunochemical characterization of the ionotropic glutamate receptors in the rat heart. Brain Res Bull 1998; 46: 429-434.
47. Gill SS, Pulido OM, Mueller RW, McGuire PF. Immunochemical localization of the metabotropic glutamate receptors in the rat heart. Brain Res Bull 1999; 48: 143-146.
48. Tyagi SC, Smiley LM, Mujumdar VS. Homocyst(e)ine impairs endocardial endothelial function. Canad J Physiol Pharmacol 1999; 77: 950-957.
49. 2+ sparks. Cell Calcium 1999; 20: 129-140.
50. Koss KL, Kranias EG. Phospholamban: A prominent regulator of cardiac contractility. Circ Res 1996; 79: 1059-1063.
51. Gwathmey JK, Copelas L, MacKinnon R, Schoen FJJ, Feldman MD, Grossman W, et al. Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ Res 1987; 61: 70-76.
52. 2+-ATPase gene expression in the human ventricle during end-stage heart failure. J Clin Invest 1990; 85: 305-309.
53. Tyagi N, Ovechkin AV, Lominadze D, Moshal KS, Tyagi SC. Mitochondrial mechanism of microvascular endothelial cells apoptosis in hyperhomocysteinemia. J Cell Biochem 2006; 98:1150-1162.
54. Perez-de-Arce K, Foncea R, Leighton F. Reactive oxygen species mediates homocysteine-induced mitochondrial biogenesis in human endothelial cells: modulation by antioxidants. Biochem Biophys Res Commun 2005; 338:1103-1119.
55. Austin RC, Sood SK, Dorward AM, Singh G, Shaughnessy SG, Pamidi S, et al. Homocysteine-dependent alterations in mitochondrial gene expression, function and structure. J Biol Chem 1998; 273: 30808-30817.
56. Sabbah HN, Sharov VG, Riddle JM, Kono T, Lesch M, Goldstein S. Mitochondrial abnormalities in myocardium of dogs with chronic heart failure. J Mol Cell Cardiol 1992; 24: 1333-1347.
57. Halestrap AP. Mitochondrial permeability: Dual role for the ADP/ATP translocator? Nature 2004; 430: 983.
58. Halestrap A. Biochemistry: A pore way to die. Nature 2005; 434: 578-579.
59. Fareh S, Villemaire C, Nattel S. Importance of refractoriness heterogeneity in the enhanced vulnerability to atrial fibrillation induction caused by tachycardia-induced atrial electrical remodeling. Circulation 1998; 83: 2202-2209.
60. Liu L, Nattel S. Differing sympathetic and vagal effects on atrial fibrillation in dogs: role of refractoriness heterogeneity. Am J Physiol 1997; 273: 805-816.
61. Jayachandran JV, Sih HJ, Winkle W, Zipes DP, Hutchins GD, Olgin JE. Atrial fibrillation produced by prolonged rapid atrial pacing is associated with heterogeneous changes in atrial sympathetic innervation. Circulation 2000; 101: 1185-1191.
62. Leistad E, Aksnes G, Verburg E, Christensen G. Atrial contractile dysfunction after short-term atrial fibrillation is reduced by verapamil but increased by BAY K8644. Circulation 1996; 93: 1747-1754.
63. Manning WJ, Silverman DI, Katz SE, Riley MF, Come PC, Doherty RM, et al. Impaired left atrial mechanical function after cardioversion: relation to the duration of atrial fibrillation. J Am Coll Cardiol 1994; 23: 1535-1540.
64. Ausma J, Wijffels M, Thone F, Wouters L, Allisse M, Borgers M. Structural changes of atrial myocardium due to sustained atrial fibrillation in the goat. Circulation 1997;96:3157-3163.
65. Brundel BJ, Kampinga HH, Henning RH. Calpain inhibition prevents pacing-induced cellular remodeling in a HL-1 myocyte model for atrial fibrillation. Cardiovasc Res 2004; 62: 521-528.
66. Li Y, Li W, Gong Y, Li B, Liu W, Han W, et al. The effects of cilazapril and valsartan on the mRNA and protein expressions of atrial calpains and atrial structural remodeling in atrial fibrillation dogs. Basic Res Cardiol 2007; 102: 245-56.
67. Schulz R. Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rational and therapeutic approaches. Annu Rev Pharmacol Toxicol 2007; 47: 211-242.
68. Wang W, Schulze C, Suarez-Pinzon W, Dyck J, Sawaicki G, Schulz R, et al. Intracellular action of MMP-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 2002; 106: 1543-1549.
69. McCawley JL, Matrisian LM. Matrix metalloproteinases: they are not just for matrix anymore! Curr Opin Biol 2001; 13: 534-540.
70. Aguilar HI, Botla R, Arora AS, Bronk SF, Gores GJ. Induction of the mitochondrial permeability transition by protease activity in rats: a mechanism of hepatocyte necrosis. Gastroenterology 1996; 110: 558-66.
71. Pacher P, Ungvari Z, Kecskemeti V. Electrophysiological effects of homocysteine in isolated rat right ventricular papillary muscles and left atria. Gen Pharmacol 1999; 32: 439-443.
72. + currents by homocysteine in rat ventricular myocytes, J Cardiovasc Electrophysiol 2001; 12: 175-182.
73. Kumagai K, Nakashima H, Saku K. The HMG-CoA reductase inhibitor atorvastatin prevents artial fibrillation by inhibiting inflammation in a canine sterile pericarditis model. Cardiovasc Res 2004; 62:105-111.
74. Chiu JH, Abdelhadi RH, Chung MK, Gurm HS, Marrouche NF, Saliba WI, et al. Effect of statin therapy on risk of ventricular arrhythmia among patients with coronary artery disease and an implanatable cardiovascular-defibrillator. Am J Cardiol 2005; 95: 490-491.