Cardiomyocyte apoptosis induced by short-term diabetes requires mitochondrial GSH depletion

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 289, Issue 2 58-2, 2005, Pages

  Ghosh, Sanjoy ^a   Pulinilkunnil, Thomas ^a   Yuen, Gloria ^a   Kewalramani, Girish ^a   An, Ding ^a   Qi, Dake ^a   Abrahani, Ashraf ^a   Rodrigues, Brian ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Caspase; Glutathione; Heart; Mitochondria; Oxidative stress

Indexed keywords

BUTHIONINE SULFOXIMINE; CASPASE 3; CASPASE 9; GLUTATHIONE; MALEIC ACID DIETHYL ESTER; REACTIVE OXYGEN METABOLITE; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVATION; GLUTATHIONE METABOLISM; HEART MITOCHONDRION; HYPERGLYCEMIA; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; STREPTOZOCIN DIABETES;

ANIMALS; APOPTOSIS; BUTHIONINE SULFOXIMINE; CASPASES; DIABETES MELLITUS, EXPERIMENTAL; GLUTATHIONE; MALE; MALEATES; MITOCHONDRIA, HEART; MYOCARDIUM; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RATS; RATS, WISTAR;

EID: 23744431987     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00038.2005     Document Type: Article

References (51)

1. Bishopric NH, Andreka P, Slepak T, and Webster KA. Molecular mechanisms of apoptosis in the cardiac myocyte. Curr Opin Pharmacol 1: 141-150, 2001.
2. Bonnefont-Rousselot D. Glucose and reactive oxygen species. Curr Opin Clin Nutr Metab Care 5: 561-568, 2002.
3. Cai L and Kang YJ. Cell death and diabetic cardiomyopathy. Cardiovasc Toxicol 3: 219-228, 2003.
4. Ceriello A, Quagliaro L, D'Amico M, Di Filippo C, Marfella R, Nappo F, Berrino L, Rossi F, and Giugliano D. Acute hyperglycemia induces nitrotyrosine formation and apoptosis in perfused heart from rat. Diabetes 51: 1076-1082, 2002.
5. Chernyak BV. Redox regulation of the mitochondrial permeability transition pore. Biosci Rep 17: 293-302, 1997.
6. Connaughton M, Kelly FJ, Haddock PS, Hearse DJ, and Shattock MJ. Ventricular arrhythmias induced by ischaemia-reperfusion are unaffected by myocardial glutathione depletion. J Mol Cell Cardiol 28: 679-688, 1996.
7. Dalle-Donne I, Rossi R, Giustarini D, Milzani A, and Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329: 23-38, 2003.
8. Darmaun D, Smith SD, Sweeten S, Sager BK, Welch S, and Mauras N. Evidence for accelerated rates of glutathione utilization and glutathione depletion in adolescents with poorly controlled type 1 diabetes. Diabetes 54: 190-196, 2005.
9. Das DK. Redox regulation of cardiomyocyte survival and death. Antioxid Redox Signal 3: 23-37, 2001.
10. Deneke SM, Lynch BA, and Fanburg BL. Transient depletion of lung glutathione by diethylmaleate enhances oxygen toxicity. J Appl Physiol 58: 571-574, 1985.
11. Ding C, He Q, and Li PA. Activation of cell death pathway after a brief period of global ischemia in diabetic and non-diabetic animals. Exp Neurol 188: 421-429, 2004.
12. Dominguez C, Ruiz E, Gussinye M, and Carrascosa A. Oxidative stress at onset and in early stages of type 1 diabetes in children and adolescents. Diabetes Care 21: 1736-1742, 1998.
13. Elhadd TA, Kennedy G, Hill A, McLaren M, Newton RW, Greene SA, and Belch JJ. Abnormal markers of endothelial cell activation-and oxidative stress in children, adolescents and young adults with type 1 diabetes with no clinical vascular disease. Diabetes Metab Res Rev 15: 405-411, 1999.
14. Fernandez-Checa JC, Kaplowitz N, Garcia-Ruiz C, Colell A, Miranda M, Mari M, Ardite E, and Morales A. GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect. Am J Physiol Gastrointest Liver Physiol 273: G7-G17, 1997.
15. Fernandez-Checa JC, Ookhtens M, and Kaplowitz N. Effect of chronic ethanol feeding on rat hepatocytic glutathione. Compartmentation, efflux, and response to incubation with ethanol. J Clin Invest 80: 57-62, 1987.
16. Fiordaliso F, Bianchi R, Staszewsky L, Cuccovillo I, Doni M, Laragione T, Salio M, Savino C, Melucci S, Santangelo F, Scanziani E, Masson S, Ghezzi P, and Latini R. Antioxidant treatment attenuates hyperglycemia-induced cardiomyocyte death in rats. J Mol Cell Cardiol 37: 959-968, 2004.
17. Fiordaliso F, Leri A, Cesselli D, Limana F, Safai B, Nadal-Ginard B, Anversa P, and Kajstura J. Hyperglycemia activates p53 and p53-regulated genes leading to myocyte cell death. Diabetes 50: 2363-2375, 2001.
18. Fiordaliso F, Li B, Latini R, Sonnenblick EH, Anversa P, Leri A, and Kajstura J. Myocyte death in streptozotocin-induced diabetes in rats in angiotensin II-dependent. Lab Invest 80: 513-527, 2000.
19. Friesen C, Kiess Y, and Debatin KM. A critical role of glutathione in determining apoptosis sensitivity and resistance in leukemia cells. Cell Death Differ 11, Suppl 1: S73-S85, 2004.
20. Frustaci A, Kajstura J, Chimenti C, Jakoniuk I, Leri A, Maseri A, Nadal-Ginard B, and Anversa P. Myocardial cell death in human diabetes. Circ Res 87: 1123-1132, 2000.
21. Garcia-Ruiz C, Colell A, Morales A, Kaplowitz N, and Fernandez-Checa JC. Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial glutathione status in loss of mitochondrial function and activation of transcription factor nuclear factor-kappa B: studies with isolated mitochondria and rat hepatocytes. Mol Pharmacol 48: 825-834, 1995.
22. Gerard-Monnier D, Fougeat S, and Chaudiere J. Glutathione and cysteine depletion in rats and mice following acute intoxication with diethylmaleate. Biochem Pharmacol 43: 451-456, 1992.
23. Ghosh S, An D, Pulinilkunnil T, Qi D, Lau HC, Abraham A, Innis SM, and Rodrigues B. Role of dietary fatty acids and acute hyperglycemia in modulating cardiac cell death. Nutrition 20: 916-923, 2004.
24. Ghosh S, Qi D, An D, Pulinilkunnil T, Abrahani A, Kuo KH, Wambolt RB, Allard M, Innis SM, and Rodrigues B. Brief episode of STZ-induced hyperglycemia produces cardiac abnormalities in rats fed a diet rich in n-6 PUFA. Am J Physiol Heart Circ Physiol 287: H2518-H2527, 2004.
25. Ghosh S, Ting S, Lau H, Pulinilkunnil T, An D, Qi D, Abrahani MA, and Rodrigues B. Increased efflux of glutathione conjugate in acutely diabetic cardiomyocytes. Can J Physiol Pharmacol 82: 879-887, 2004.
26. Goossens V, Grooten J, De Vos K, and Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci USA 92: 8115-8119, 1995.
27. Green DR and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305: 626-629, 2004.
28. Green K, Brand MD, and Murphy MP. Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes 53, Suppl 1: S110-S118, 2004.
29. Griffith OW. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106: 207-212, 1980.
30. Griffith OW and Meister A. Origin and turnover of mitochondrial glutathione. Proc Natl Acad Sci USA 82: 4668-4672, 1985.
31. Higuchi Y, Otsu K, Nishida K, Hirotani S, Nakayama H, Yamaguchi O, Matsumura Y, Ueno H, Tada M, and Hori M. Involvement of reactive oxygen species-mediated NF-kappa B activation in TNF-alpha-induced cardiomyocyte hypertrophy. J Mol Cell Cardiol 34: 233-240, 2002.
32. Jain SK and McVie R. Effect of glycemic control, race (white vs. black), and duration of diabetes on reduced glutathione content in erythrocytes of diabetic patients. Metabolism 43: 306-309, 1994.
33. Kajstura J, Fiordaliso F, Andreoli AM, Li B, Chimenti S, Medow MS, Limana F, Nadal-Ginard B, Leri A, and Anversa P. IGF-1 overexpression inhibits the development of diabetic cardiomyopathy and angiotensin II-mediated oxidative stress. Diabetes 50: 1414-1424, 2001.
34. Kesavulu MM, Rao BK, Giri R, Vijaya J, Subramanyam G, and Apparao C. Lipid peroxidation and antioxidant enzyme status in type 2 diabetics with coronary heart disease. Diabetes Res Clin Pract 53: 33-39, 2001.
35. Kulisz A, Chen N, Chandel NS, Shao Z, and Schumacker PT. Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am J Physiol Lung Cell Mol Physiol 282: L1324-L1329, 2002.
36. Kupatt C, Hinkel R, Horstkotte J, Deiss M, von Bruhl ML, Bilzer M, and Boekstegers P. Selective retroinfusion of GSH and cariporide attenuates myocardial ischemia-reperfusion injury in a preclinical pig model. Cardiovasc Res 61: 530-537, 2004.
37. Li S, Li X, and Rozanski GJ. Regulation of glutathione in cardiac myocytes. J Mol Cell Cardiol 35: 1145-1152, 2003.
38. Lluis JM, Morales A, Blasco C, Colell A, Mari M, Garcia-Ruiz C, and Fernandez-Checa JC. Critical role of mitochondrial glutathione in the survival of hepatocytes during hypoxia. J Biol Chem 280: 3224-3232, 2005.
39. Marchetti P, Decaudin D, Macho A, Zamzami N, Hirsch T, Susin SA, and Kroemer G. Redox regulation of apoptosis: impact of thiol oxidation status on mitochondrial function. Eur J Immunol 27: 289-296, 1997.
40. Mishra R, Emancipator SN, Kern T, and Simonson MS. High glucose evokes an intrinsic proapoptotic signaling pathway in mesangial cells. Kidney Int 67: 82-93, 2005.
41. Murrant CL and Reid MB. Detection of reactive oxygen and reactive nitrogen species in skeletal muscle. Microsc Res Tech 55: 236-248, 2001.
42. Musallam L, Ethier C, Haddad PS, Denizeau F, and Bilodeau M. Resistance to Fas-induced apoptosis in hepatocytes: role of GSH depletion by cell isolation and culture. Am J Physiol Gastrointest Liver Physiol 283: G709-G718, 2002.
43. Plummer JL, Smith BR, Sies H, and Bend JR. Chemical depletion of glutathione in vivo. Methods Enzymol 77: 50-59, 1981.
44. Reers M, Smiley ST, Mottola-Hartshorn C, Chen A, Lin M, and Chen LB. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol 260: 406-417, 1995.
45. Rodrigues B, Cam MC, and McNeill JH. Myocardial substrate metabolism: implications for diabetic cardiomyopathy. J Mol Cell Cardiol 27: 169-179, 1995.
46. Santos DL, Palmeira CM, Seica R, Dias J, Mesquita J, Moreno AJ, and Santos MS. Diabetes and mitochondrial oxidative stress: a study using heart mitochondria from the diabetic Goto-Kakizaki rat. Mol Cell Biochem 246: 163-170, 2003.
47. Shen X, Zheng S, Thongboonkerd V, Xu M, Pierce WM Jr, Klein JB, and Epstein PN. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 287: E896-E905, 2004.
48. Shizukuda Y, Reyland ME, and Buttrick PM. Protein kinase C-delta modulates apoptosis induced by hyperglycemia in adult ventricular myocytes. Am J Physiol Heart Circ Physiol 282: H1625-H1634, 2002.
49. Singh A, Lee KJ, Lee CY, Goldfarb RD, and Tsan MF. Relation between myocardial glutathione content and extent of ischemia-reperfusion injury. Circulation 80: 1795-1804, 1989.
50. Srinivasan S, Stevens M, and Wiley JW. Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49: 1932-1938, 2000.
51. Turrens JF, Alexandre A, and Lehninger AL. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237: 408-414, 1985.