Hyperhomocysteinemic diabetic cardiomyopathy: Oxidative stress, remodeling, and endothelial-myocyte uncoupling

Journal of Cardiovascular Pharmacology and Therapeutics

Volumn 10, Issue 1, 2005, Pages 1-10

  Tyagi, Suresh C ^a   Rodriguez, Walter ^a   Patel, Anuj M ^a   Roberts, Andrew M ^a   Falcone, Jeff C ^a   Passmore, John C ^a   Fleming, John T ^a   Joshua, Irving G ^a  

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

Author keywords

Diabetes mellitus; Edema; Extracellular matrix; Homocysteine; Matrix metalloproteinase; Microvascular permeability; Seizure; Stroke

Indexed keywords

CARDIAC TISSUE INHIBITOR OF METALLOPROTEINASE; GELATINASE B; GLUCOSE; INSULIN; MATRIX METALLOPROTEINASE; METALLOPROTEINASE INHIBITOR; PEROXIREDOXIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; THIOREDOXIN; TISSUE INHIBITOR OF METALLOPROTEINASE; UNCLASSIFIED DRUG;

BLOOD VESSEL PERMEABILITY; CARDIOMYOPATHY; DIABETES MELLITUS; DIASTOLE; EDEMA; ENDOTHELIUM; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FIBROSIS; HEART MUSCLE CELL; HUMAN; HYPERHOMOCYSTEINEMIA; KIDNEY CLEARANCE; MICROVASCULATURE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SEIZURE; STROKE;

CARDIOMYOPATHIES; DIABETIC ANGIOPATHIES; ENDOTHELIUM, VASCULAR; HUMANS; HYPERHOMOCYSTEINEMIA; OXIDATIVE STRESS;

EID: 17044372663     PISSN: 10742484     EISSN: None     Source Type: Journal    
DOI: 10.1177/107424840501000101     Document Type: Review

References (126)

1. Tyagi SC. Homocyst(e)ine and heart disease: Pathophysiology of extracellular matrix. Clin Exp Hypertens 21:181-198, 1999
2. Yi P, Melnyk S, Pogribna M, Pogribny IP, et al. Increase in plasma homocysteine associated with parallel increase in plasma s-adenosylhomocysteine and lymphocyte DNA hypomethylation. J Biol Chem 275:29318-29323, 2000
3. McCully KS. Homocysteine and vascular disease. Nature Med 2:386-389, 1996
4. Mujumdar VS, Aru GM, Tyagi SC. Induction of oxidative stress by homocyst(e)ine impairs endothelial function. J Cell Biochem 82(3):491-500, 2001
5. Finkelstein JD. The metabolism of homocysteine: Pathways and regulation. Eur J Pediatr 157(S-2): S40-S44, 1998
6. Finkelstein JD. Methionine metabolism in mammals. J Nutr Biochem 1:228-237, 1990
7. Homocysteine Studies Collaboration: Homocysteine and risk of ischemic heart disease and stroke: A meta-analysis. JAMA 288(16):2015-2022, 2002
8. Klerk M, Verhoef P, Clarke R, et al. MTHFR 677C-T polymorphism and risk of coronary heart disease: A meta-analysis. JAMA 288(16):2023-2031, 2002
9. Wald DS, Law M, Morris JK. Homocysteine and cardiovascular disease: Evidence on causality from a meta-analysis. BMJ 325(7374):1202, 2002
10. Kaye JM, Stanton KG, McCann VJ, et al. Homocysteine, folate, methylene-tetrahydrofolate reducatse genotype and vascular morbidity in diabetic subjects. Clin Sci 102:631-637, 2002
11. Shcherbak NS, Shutskaya ZV, Sheidina AM, et al. Methylenetetrahydrofolate reductase gene polymorphism as a risk factor for diabetic nephropathy in IDDM patients. Molec Genet Metab 68:375-378, 1999
12. Davey SG, Ebrahim S. "Mendelian randomization": Can genetic epidemiology contribute to understanding environmental determinants of disease? Int J Epidemiol 32(1):1-22, 2003
13. Clarke R, Collins R. Can dietary supplements with folic acid or vitamin B6 reduce cardiovascular risk? Design of clinical trials to test the homocysteine hypothesis of vascular disease. J Cardiovas Risk 5(4):249-255, 1998
14. Schnyder G, Roffi M, Flammer Y, et al. Effect of homocysteine-lowering therapy with folic acid, vitamin B(12), and vitamin B(6) on clinical outcome after percutaneous coronary intervention: The Swiss Heart study: A randomized controlled trial. JAMA 288(8):973-979, 2002
15. Toole JF, Malinow MR, Chambless LE, et al. Lowering homocysteine in patients with ischemic stroke to prevent recurrent stroke, myocardial infarction, and death: The Vitamin intervention for Stroke Prevention (VISP) randomized controlled trial. JAMA 291(5):565-575, 2004
16. Fallon UB, Virtamo J, Young I, et al. Homocysteine and cerebral infarction in Finnish male smokers. Stroke 34(6):1359-1363, 2003
17. Graham IM, Daly LE, Refsum HM, et al. Plasma homocysteine as a risk factor for vascular disease. The European Concerted Action Project [see comments]. JAMA 277(22):1775-1781, 1997
18. Fallon UB, Elwood P, Ben-Shlomo Y, et al. Homocysteine and ischaemic stroke in men: The Caerphilly study. J Epidemiol Community Health 55(2):91-96, 2001
19. Audelin MC, Genest J Jr. Homocysteine and cardiovascular disease in diabetes mellitus. Atherosclerosis 159(2): 497-511, 2001
20. Fonseca VA, Fink UM, Kern PA. Insulin sensitivity and plasma homocysteine concentrations in non-diabetic obese and normal weight subjects. Atherosclerosis 167(1):105-109, 2003
21. Emoto M, Kanda H, Shoji T, et al. Impact of insulin resistance and nephropathy on homocysteine in type 2 diabetes. Diabetes Care 24(3):533-538, 2001
22. Giltay EJ, Hoogeveen EK, Elbers JM, et al. Insulin resistance is associated with elevated plasma total homocysteine levels in healthy, non-obese subjects. Atherosclerosis 139(1):197-198, 1998
23. Meigs JB, Jacques PF, Seihub J, et al. Fasting plasma homocysteine levels in the insulin resistance syndrome: The Framingham offspring study. Diabetes Care 24(8):1403-1410, 2001
24. Godsland IF, Rosankiewicz JR, Proudler AJ, Johnston DG. Plasma total homocysteine concentrations are unrelated to insulin sensitivity and components of the metabolic syndrome in healthy men. J Clin Endocrinol Metab 86(2):719-723, 2001
25. Rosolova H, Simon J, Mayer O Jr, et al. Unexpected inverse relationship between insulin resistance and serum homocysteine in healthy subjects. Physiol Res 51(1):93-98, 2002
26. Abbasi F, Facchini F, Humphreys MH, et al. Plasma homocysteine concentrations in healthy volunteers are not related to differences in insulin-mediated glucose disposal. Atherosclerosis 146(1):175-178, 1999
27. Buysschaert M, Dramais AS, Wallemacq PE, et al. Hyperhomocysteinemia in type 2 diabetes: Relationship to macroangiopathy, nephropathy, and insulin resistance. Diabetes Care 23(12):1816-1822, 2000
28. Bar-On H, Kidron M, Friedlander Y, et al. Plasma total homocysteine levels in subjects with hyperinsulinemia. J Intern Med 247(2):287-294, 2000
29. Fonseca VA, Mudaliar S, Schmidt B, et al. Plasma homocysteine concentrations are regulated by acute hyperinsulinemia in nondiabetic but not type 2 diabetic subjects. Metabolism 47(6):686-689, 1998
30. Pouwels MJ, den Heijer M, Blom HJ, et al. Improved insulin sensitivity and metabolic control in type 2 diabetes does not influence plasma homocysteine. Diabetes Care 26(5):1637-1639, 2003
31. Kark JD, Selhub J, Bostom A, et al. Plasma homocysteine and all-cause mortality in diabetes. Lancet 353(9168): 1936-1937, 1999
32. Hoogeveen EK, Kostense PJ, Jakobs C, et al. Hyperhomocysteinemia increases risk of death, especially in type 2 diabetes: 5-year follow-up of the Hoorn Study. Circulation 101(13):1506-1511, 2000
33. Becker A, Kostense PJ, Bos G, et al. Hyperhomocysteinaemia is associated with coronary events in type 2 diabetes. J Intern Med 253(3):293-300, 2003
34. Jeremy JY, Shukla N, Angelini GD. Homocysteine and cardiovascular disease in diabetes mellitus. Atherosclerosis 164(2):383-384, 2002
35. Shukia N, Thompson CS, Angelini GD, et al. Homocysteine enhances impairment of endothelium-dependent relaxation and guanosine cyclic monophosphate formation in aortae from diabetic rabbits. Diabetologia 45(9):1325-1331, 2002
36. Lin KY, Ito A, Asagami T, et al. Impaired nitric oxide synthase pathway in diabetes mellitus: Role of asymmetric dimethylarginine and dimethylarginine dimethylaminohyrolase (DDAH). Circulation 106:987-992, 2002
37. Selley ML. Homocysteine increase the production of asymmetric dimethylarginine in cultured neurons. J Neurosci Res 77:90-93, 2004
38. Dicker-Brown A, Fonseca VA. The effect of glucose and insulin on the activity of methylene tetrahydrofolate reductase and cystathionine-beta- synthase: Studies in hepatocytes. Atherosclerosis 158(2):297-301, 2001
39. Wollesen F, Brattstrom L, Refsum H, Ueland PM, Bergiund L, Beme C. Plasma total homocysteine and cysteine in relation to glomerular filtration rate in diabetes mellitus. Kidney Int 55(3):1028-1035, 1999
40. Fukagawa NK, Minaker KU, Young VR, et al. Insulin dose-dependent reductions in plasma amino acids in man. American Journal of Physiology 250(1):E13-E17, 1986
41. Tyagi SC, Smiley LM, Mujumdar VS, et al. Reduction-oxidation (redox) and vascular tissue level of homocyst(e)ine in human coronary atherosclerotic lesions and role in vascular extracellular matrix remodeling and vascular tone. Mol Cell Biochem 181:107-116, 1998
42. Daimon M, Susa S, Yamatani K, et al. Hyperglycemia is a factor for an increase in serum cemloplasmin in type 2 diabetes. Diabetes Care 21:1525-1528, 1998
43. Emsley A, Jeremy JY, Gomes G, et al. Copper interacts with homocysteine to inhibit nitric oxide formation in the rat isolated aorta. British Journal of Pharmacology 126:1034-1040, 1999
44. Starkebaum G, Harlan JM. Endothelial cell injury due to copper-catalyzed hydrogen peroxide generation from homocysteine. J Clinical Investigation 77:1370-1376, 1986
45. Sood HS, Hunt MJ, Tyagi SC. Peroxisome proliferator ameliorates endothelial dysfunction in a murine model of hyperhomocysteinemia. Am J Physiol Lung Cell Mol Physiol 284:L333-L341, 2003
46. Chen L, Xie QW, Nathan C. Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates. Mol Cell 1(6):795-805, 1998
47. Bryk R, Griffin P, Nathan C. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407(6801):211-215, 2000
48. Wong CM, Zhou Y, Ng RW, et al. Cooperation of yeast peroxiredoxins Tsa1p and Tsa2p in the cellular defense against oxidative and nitrosative stress. J Biol Chem 277(7):5385-5394, 2002
49. Barr SD, Gedamu L. Role of peroxidoxins in Leishmania chagasi survival. Evidence of an enzymatic defense against nitrosative stress. J Biol Chem 278(12): 10816-10823, 2003
50. Farina AR, Tacconelli A, Cappabianca L, et al. Thioredoxin alters the MMP/TIMP balance and stimulates human SKNSH neuroblastoma cell invasion. Eur J Biochem 268(2):405-413, 2001
51. Oh JH, Chung AS, Steinbrenner H, et al. Thioredoxin secreted upon ultraviolet A irradiation modulates activities of matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-2 in human dermal fibroblasts. Arch Biochem Biophys 423:218-226, 2004
52. Hui TY, Sheth SS, Diffley JM, et al. Mice lacking thioredoxin interacting protein provide linking cellular redox state to appropriate response to nutritional signals. J Biol Chem 279(23):24387-24393, 2004
53. Shao LE, Tanaka T, Gribi R, Yu J. Thioredoxin-related regulation of NO/NOS activities. Ann NY Acta Sci 962:140-150, 2002
54. Wolff SP. Diabetes mellitus and free radical. Free radicals, transition metals and oxidative stress in the aetiology of diabetes mellitus and complications. Br Med Bull 49:642-652, 1993
55. West IC. Radical and oxidative stress in diabetes. Diabet Med 17:171-180, 2000
56. The Heart Outcome Prevention Evaluation Study Investigators: Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus, HOPE and MICRO-HOPE substudy. Lancet 355: 253-259, 2000
57. Brude IR, Finstad HS, Seljeflot I, et al. Plasma homocysteine concentration related to diet, endothelial function and mononuclear cell gene expression among male hyperlipidaemic smokers. Euro J Clin Invest 29:100-108, 1999
58. Lebovitz HE, Manerji MA. Insulin resistance and its treatment by thiazolidinediones. Recent Prog Horm Res 56:265-294, 2001
59. Itoh H, Doi K, Tanaka T, et al. Hypertension and insulin resistance: role of peroxisome proliferator-activated receptor gamma. Clin Exp Pharmacol Physiol 26: 558-560, 1999
60. Hunt MJ, Tyagi SC. Peroxisome proliferators compete and ameliorate homocysteine-mediated EE cells activation. Am J Physiol Cell Physiol 283:C1073-C1079, 2002
61. Ungvari Z, Pacher P, Rischak K, et al. Dysfunction of NO mediation in isolated rat arterioles with methionine-induced hyperhomocysteinemia. Artero Throm Vasc Biol 19:1899-1904, 1999
62. Cox MJ, Hawkins UA, Hoit BD, et al. Attenuation of oxidative stress and remodeling by cardiac inhibitor of metalloproteinase protein transfer. Circulation 109(17):2123-2128, 2004
63. Hoppeler H, Kayar SR. Capillary and oxidative capacity of muscles. News Physiol Sci 3:113-116, 1988
64. Roberts JT, Wearn JT. Quantitative changes in the capillary-muscle relationship in human hearts during normal growth and hypertrophy. Am Heart J 617-633, 1941
65. Hayden MR, Tyagi SC. Remodeling of the endocrine pancreas: The central role of amylin and insulin resistance. Southern Med J 93:24-28, 2000
66. Hayden MR, Tyagi SC. "A" is for amylin and Amyloid in type 2 diabetes mellitus. J Pancreas 2(4):124-139, 2001
67. Henderson AH, Lewis MJ, Shah AM, et al. Endothelium, endocardium, and cardiac contraction. Cardiovasc Res 26(4):305-308, 1992
68. Smith JA, Shah AM, Fort S, et al. The influence of endocardial endothelium on myocardial contraction. Trends Pharmacol Sci 13:113-116, 1992
69. Mebazaa A, Wetzel R, Cherian M, et al. Comparison between endothelial and great vessel endothelial cells: Morphology, growth, and prostaglandin release. Am J Physiol 268:H250-H259, 1995
70. Pinsky DJ, Patton S, Mesaros S, et al. Mechanical transduction of NO synthesis in the beating heart. Circ Res 81:372-379, 1997
71. Shah AM, Grocott-Mason RM, Pepper CB, Mebazaa A, Henderson AH, Lewis MJ, Paulus WJ. The cardiac endothelium: Cardioactive mediators. Prog Cardiovasc Dis 39(3):263-268, 1996
72. Scarabelli T, Stephanou A, Rayment N, et al. Apoptosis of endothelial cells precedes myocytes cell apoptosis in ischemia/reperfusion injury. Circulation 104:353-256, 2001
73. Fukuchi M, Watanabe J, Kumagai K, et al. Increased von Willebrand factor in the endocardium as a local predisposing factor for thrombogenesis in overloaded human atrial appendage. J Am Coll Cardiol 37:1436-1442, 2001
74. Wang J, Morgan JP. EE modulates myofilament Ca2+ responsiveness in aequorin-loaded ferret myocardium. Cir Res 70:754-760, 1992
75. Gattuso A, Mazza R, Pellegrino D, Tola B. Endocardial endothelium (EE) mediates luminal acetylcholine-nitric oxide signaling in isolated frog heart. Am J Physiol 276:H633-H641, 1999
76. Tyagi SC, Smiley LM, Mujumdar VS. Homocyst(e)ine impairs endocardial endothelial function. Can J Physiol Pharmacol 77:950-957, 1999
77. Tyagi SC, Hoit BD. Metalloproteinase in myocardial adapatation and maladaptation. Cardiovasc Pharmaol Therapeut 7(4):241-246, 2002
78. Tyagi SC. Proteinases and myocardial extracellular matrix turnover. Mol Cell Biochem 168:1-12, 1997
79. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of MMPs: Structure, function, and biochemistry. Circ Res 92(8):827-839, 2003
80. Stamenkovic I. Extracellular matrix remodeling: The role of matrix metalloproteinases. J Pathol 200:448-464, 2003
81. Shastry S, Tyagi SC. Homocysteine induces metalloproteinase and shedding of β-1 integrin in microvessel endothelial cells. J Cell Biochem 93:207-213, 2004
82. Hunt MJ, Aru GM, Hayden MR, et al. Induction of oxidative stress and disintegrin metalloproteinase in human heart end-stage failure. Am J Physiol 283(2):L239-L245, 2002 (editorial on this paper, L237-L238)
83. Tyagi SC, Lewis K, Pikes D, et al. Stretch induced membrane type matrix metalloproteinases and tissue plasminogen activator in cardiac fibroblast cells. J Cell Physiol 176:374-382, 1998
84. Tyagi SC, Hayden MR. Role of nitric oxide in matrix remodeling in diabetes and heart failure. Heart Fail Rev 8:23-28, 2003
85. Mujumdar VS, Aru GM, Tyagi SC. Induction of oxidative stress by homocyst(e)ine impairs endothelial function. J Cell Biochem 82(3):491-500, 2001
86. Kern TS, Tang J, Mizutani M, et al. Response of capillary cell death to aminoguanidine predicts the development of retinopathy: Comparison of diabetes and galactosemia. Invest Ophthalmol 41(12):3972-3978, 2000
87. Miller A, Mujumdar V, Shek E, et al. Hyperhomocysteinemia induces multiorgan damage. Heart Vessels 15(3):135-143, 2000
88. Miller A, Mujumdar V, Palmer L, et al. Reversal of endocardial endothelial dysfunction by folic acid in homocysteinemic hypertensive rats. Am J Hyperten 15:157-163, 2002
89. Warley A, Powell JM, Skepper JN. Capillary surface area is reduced and tissue thickness from capillaries to myocytes is increased in LV of STZ-diabetic rats. Diabetologia 38:413-421, 1995
90. Di Bello V, Giampietro O, Matteucci E, et al. Ultrasonic video-densitometric analysis in type I diabetic myocardium. Coron Artey Dis 7(12):895-901, 1996
91. Sokolov EI, Zaichikova OS, Tsyplenkova VG. Ultrastructure of the myocardium in patients with cardiac pathology complicated by diabetes mellitus. Arkh Patol 60(1):49-54, 1998
92. Dhalla NS, Pierce GN, Innes IR, et al. Pathogenesis of cardiac dysfunction in diabetes mellitus. Can J Cardiol 1(4):263-281, 1985
93. Abe T, Ohga Y, Tabayashi N, et al. LV diastolic dysfunction in type 2 DM model rats. Am J Physiol 282:H138-H148, 2002
94. Thompson EW. Structural manifestations of diabetic cardiomyopathy in the rat and its reversal by insulin treatment. Am J Anat 182:270-282, 1988
95. Avendano GF, Agarwal RK, Bashey RI. Effects of glucose intolerance on myocardial function and collagen-linked glycation. Diabetes 48:1443-1447, 1999
96. Turk Z, Misur I, Turk N, et al. Rat tissue collagen modified by advanced glycation: Co-relation with duration of diabetes and glycemic control. Clin Chem Lab Med 37:813-820, 1999
97. Katayama S, Abe M, Negishi K, et al. Reciprocal changes in LV collagen alpha 1 chain gene expression between type I and IV in spontaneously diabetic rats. Diabetes Res Clin Pract 26:163-169, 1994
98. Mizushige K, Yao L, Noma T, et al. Alteration in LV diastolic filling and accumulation of myocardial collagen at insulin-resistant prediabetic stage of a type 2 diabetic rat model. Circulation 101:899-907, 2000
99. He Q, Spiro MJ. Isolation of rat heart endothelial cells and pericytes: Evaluation of their role in the formation of ECM components. J Mol Cell Cardiol 27(5):1173-1183, 1995
100. Ryan ME, Usman A, Ramamurthy NS, et al. Excessive matrix metalloproteinase activity in diabetes: Inhibition by tetracycline analogues with zinc reactivity. Curr Med Chem 8(3):305-316, 2001
101. Kwan CY, Wang RR, Beazley JS, et al. Alterations of elastin and elastase-like activities in aortas of diabetic rats. Biochim Biophys Acta 967:322-325, 1988
102. Senior RM, Griffin GL, Eliszar CJ, et al. Human 92- and 72-kilodalton type IV collagenases are elastases. J Biol Chem 266:7870-7875, 1991
103. Aimes RT, Quigley JP. MMP-2 is an interstitial collagenase. J Biol Chem 270:5872-5876, 1995
104. Rucklidge GJ, Milne G, McGaw BA, et al. Turnover rates of different collagen types measured by isotope ratio mass spectrometery. Biochim Biophys Acta 11:1156-1157, 1992
105. Nolte RT, Wisely GB, Westin S, et al. Ligand binding and co-activator assembly of the proliferator-activated receptor-gamma. Nature 395:137-143, 1998
106. Zhang X, Li H, Jin H, Ebin Z, et al. Effects of homocysteine on endothelial nitric oxide production. Am J Physiol 279:F671-F678, 2000
107. Salas A, Panes J, Elizalde JL, et al. Mechanisms responsible for enhanced inflammatory response to ischemia-reperfusion in diabetes. Am J Physiol 275:H1773-H1781, 1998
108. Starkebaum G, Harlan JM. Endothelial cell injury due to copper-catalyzed hydrogen peroxide generation from homocysteine. J Clin Invest 77:1370-1376, 1986
109. Konecky N, Malinow MR, Tunick PA, et al. Correlation between plasma homocysteine and aortic atherosclerosis. Am Heart J 133:534-540, 1997
110. Rolland PH, Friggi A, Barlatier A, et al. Hyperhomocysteinemia-induced vascular damage in the minipigs. Captopril-hydrochlorothiazide combination prevents elastic alterations. Circulation 91:1161-1174, 1995
111. Marx N, Sukhova G, Murphy C, et al. Macrophages in human atheroma contain PPARgamma: Differentiation-dependent peroxisomal proliferator-activated receptor gamma(PPARgamma) expression and reduction of MMP-9 activity through PPARgamma activation in mononuclear phagocytes in vitro. Am J Pathol 153:17-23, 1998
112. Blane GF. Comparative toxicity and safety profile of fenofibrate and other fibric acid derivatives. Am J Med 83:26-36, 1987
113. Dierkes J, Westphal S, Luley S. Serum homocysteine increases after therapy with fenollbrate or bezafibrate. Lancet 354:219-220, 1999
114. Bissonnette R, Treacy E, Rozen R, et al. Fenofibrate raises plasma homocysteine levels in the fasted and fed states. Atherosclerosis 155:455-462, 2001
115. Kajstura J, Fiordaliso F, Andreoli AM, et al. IGF-1 overexpression inhibits the development of diabetic cardiomyopathy and angII-mediated oxidative stress. Diabetes 50:1414-1424, 2001
116. Rosen R, Du X, Tschope D. Role of ROS for vascular dysfunction in the diabetic hearts. Mol Cell Biochem 188:103-111, 1998
117. Radomski A, Sawicki G, Oison DM, et al. The role of nitric oxide and metalloproteinases in the pathogenesis of hyperoxia-induced lung injury in newborn rats. Brit J Pharmacol 125:1455-1462, 1998
118. Sood HS, Cox MJ, Tyagi SC. Generation of nitrotyrosine precedes the activation of matrix metalloproteinase in left ventricle of hyperhomocysteinemic rats. Antioxid Redox Signal 4(5):799-804, 2002
119. Tyagi SC, Campbell SE, Reddy HK, et al. Matrix metalloproteinase activity expression in infarcted, noninfarcted and dilated cardiomyopathic human hearts. Mol Cell Biochem 155:13-21, 1996
120. Tyagi SC, Haas SJ, Kumar SG, et al. Post-transcriptional regulation of extracellular matrix metalloproteinase in human heart end-stage failure secondary to ischemic cardiomyopathy. J Mol Cell Cardiol 28:1415-1428, 1996
121. Hackam DG, Peterson JC, Spence JD. What level of plasma homocysteine should be treated? Am J Hyperten 13:105-110, 2000
122. Schnyder G, Roffi M, Pin R, et al. Decreased rate of coronary restenosis after lowering of plasma homocysteine levels. N Eng J Med 345:1593-1600, 2001
123. Pavia C, Ferrer I, Valls C, et al. Total homocysteine in patients with type I diabetes Diabetes Care 23:84-87, 2000
124. Wang Y, Jones JF, Jeggo RD, et al. Effect of pulmonary C-fibre afferent stimulation on cardiac vagal neurones in the nucleus ambiguus in anaesthetized cats. J Physiol 526(Pt 1):157-165, 2000
125. Barger PM, Brandt JM, Leone TC, et al. Deactivation of peroxisome proliferator-activated receptor-alpha during cardiac hypertrophic growth. J Clin Invest 105: 1723-1730, 2000
126. Yamamoto K, Ohki R, Lee RT, et al. Peroxisome proliferator-activated receptor gamma activators inhibit cardiac hypertrophy in cardiac myocytes. Circulation 104: 1670-1675, 2001