Diminished NADPH transhydrogenase activity and mitochondrial redox regulation in human failing myocardium

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 6-7, 2010, Pages 1138-1148

  Sheeran, Freya L ^a,b   Rydström, Jan ^c   Shakhparonov, Mikhail I ^d   Pestov, Nikolay B ^d   Pepe, Salvatore ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

Author keywords

Glutathione; Heart failure; Human; Mitochondria; Myocardium; NADPH transhydrogenase; Oxidative stress

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE TRANSHYDROGENASE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE EXPRESSION; HEART FAILURE; HEART LEFT VENTRICLE; HEART MUSCLE; HUMAN; HUMAN TISSUE; MITOCHONDRIAL RESPIRATION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SPECTROPHOTOMETRY; WESTERN BLOTTING;

CASE-CONTROL STUDIES; CITRIC ACID CYCLE; GENE EXPRESSION; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE REDUCTASE; HEART FAILURE; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MIDDLE AGED; MITOCHONDRIA; MYOCARDIUM; NADP; NADP TRANSHYDROGENASE; OXIDATION-REDUCTION;

EID: 77953810393     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.04.002     Document Type: Article

References (81)

1. Earle S.R., Anderson W.M., Fisher R.R. Evidence that reconstituted bovine heart mitochondrial transhydrogenase functions as a proton pump. FEBS Letters 1978, 91:21-24.
2. Pedersen A., Karlsson G.B., Rydström J. Proton-translocating transhydrogenase: an update of unsolved and controversial issues. J. Bioenerg. Biomembr. 2008, 40:463-473.
3. Rydström J. Mitochondrial NADPH, transhydrogenase and disease. Biochimica et Biophysica Acta 2006, 1757:721-726.
4. Bizouarn T., Fjellstrom O., Meuller J., Axelsson M., Bergkvist A., Johansson C., et al. Proton translocating nicotinamide nucleotide transhydrogenase from E. coli. Mechanism of action deduced from its structural and catalytic properties. Biochimica et Biophysica Acta 2000, 1457:211-228.
5. Jackson J.B., White S.A., Quirk P.G., Venning J.D. The alternating site, binding change mechanism for proton translocation by transhydrogenase. Biochemistry 2002, 41:4173-4185.
6. Sauer U., Canonaco F., Heri S., Perrenoud A., Fischer E. The soluble and membrane-bound transhydrogenases UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. Journal of Biological Chemistry 2004, 279:6613-6619.
7. Vogel R., Wiesinger H., Hamprecht B., Dringen R. The regeneration of reduced glutathione in rat forebrain mitochondria identifies metabolic pathways providing the NADPH required. Neuroscience Letters 1999, 275:97-100.
8. Holmgren A. Thioredoxin and glutaredoxin systems. Journal of Biological Chemistry 1989, 264:13963-13966.
9. Hoek J.B., Rydström J. Physiological roles of nicotinamide nucleotide transhydrogenase. Biochemical Journal 1988, 254:1-10.
10. O'Rourke B. Pathophysiological and protective roles of mitochondrial ion channels. Journal of Physiology 2000, 529:23-36.
11. Forte M., Bernardi P. Genetic dissection of the permeability transition pore. Journal of Bioenergetics and Biomembranes 2005, 37:121-128.
12. Arkblad E.L., Tuck S., Pestov N.B., Dmitriev R.I., Kostina M.B., Stenvall J., Tranberg M., Rydström J. A Caenorhabditis elegans mutant lacking functional nicotinamide nucleotide transhydrogenase displays increased sensitivity to oxidative stress. Free Radical Biology and Medicine 2005, 38:1518-1525.
13. Arkblad E.L., Egorov M., Shakhparonov M., Romanova L., Polzikov M., Rydström J. Expression of proton-pumping nicotinamide nucleotide transhydrogenase in mouse, human brain and C. elegans. Comparative Biochemistry and Physiology 2002, 133:13-21.
14. Humphrey G. The distribution and properties of transhydrogenase from animal tissues. Biochemical Journal 1957, 65:546-550.
15. Sheeran F.L., Pepe S. Energy deficiency in the failing heart: linking increased reactive oxygen species and disruption of oxidative phosphorylation rate. Biochim. Biophys. Acta 2006, 1757:543-552.
16. Damy T., Kirsch M., Khouzami L., Caramelle P., Le Corvoisier P., Roudot-Thoraval F., Dubois-Randé J.L., Hittinger L., Pavoine C., Pecker F. Glutathione deficiency in cardiac patients is related to the functional status and structural cardiac abnormalities. PLoS One 2009, 4:e4871.
17. Giordano F.J. Oxygen, oxidative stress, hypoxia, and heart failure. Journal of Clinical Investigation 2005, 115:500-508.
18. Ingwall J.S. Energy metabolism in heart failure and remodeling. Cardiovascular Research 2009, 81:412-419.
19. Rosca M.G., Hoppel C.L. New aspects of impaired mitochondrial function in heart failure. Journal of Bioenergetics and Biomembranes 2009, 41:107-112.
20. Shimomura K., Galvanovskis J., Goldsworthy M., Hugill A., Kaizak S., Lee A., Meadows N., Quwailid M.M., Rydström J., Teboul L., Ashcroft F., Croft R.D. Insulin secretion from β-cells is affected by deletion of nicotinamide nucleotide transhydrogenase. Methods in Enzymology 2009, 457:451-480.
21. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Analytical Biochemistry 1969, 27:502-522.
22. Bernocchi P., Ceconi C., Cargnoni A., Pedersini P., Curello S., Ferrari R. Extraction and assay of creatine phosphate, purine, and pyridine nucleotides in cardiac tissue by reversed-phase high-performance liquid chromatography. Analytical Biochemistry 1994, 222:374-379.
23. Marco E.J., Marco R. The use of 3-acetyl-pyridine adenine dinucleotide in the spectrophotometric assay of enzymatic activities coupled to dehydrogenases of unfavorable equilibrium. Analytical Biochemistry 1974, 62:472-477.
24. Ferrier B. An enzymatic cycling method for 3-acetylpyridine adenine dinucleotide to increase the sensitivity of enzymatic methods which employ this NAD analog. Analytical Biochemistry 1990, 186:229-232.
25. Persson B., Enander K., Tang H.L., Rydström J. Energy-linked nicotinamide nucleotie transhydrogenase. Properties of a proton-translocating mitochondrial transhydrogenase purified from beef heart by fast protein-liquid chromatography. Journal of Biological Chemistry 1984, 259:8626-8632.
26. Persson B., Hartog A., Rydström J., Berden J. NBD-Cl modification of essential residues in mitochondrial nicotinamide nucleotide transhydrogenase from bovine heart. Biochimica et Biophysica Acta 1988, 953:241-248.
27. Rydström J. Site-specific inhibitors of mitochondrial nicotinamide-nucleotide transhydrogenase. European Journal of Biochemistry 1972, 31:496-504.
28. Biagioli B., Scolletta S., Marchetti L., Tabucchi A., Carlucci F. Relationships between hemodynamic parameters and myocardial energy and antioxidant status in heart transplantation. Biomedicine & Pharmacotherapy 2003, 57:156-162.
29. Janssen M., Koster J.F., Bos E., de Jong J.W. Malondialdehyde and glutathione production in isolated perfused human and rat hearts. Circulation Research 1993, 73:681-688.
30. Richie J.P., Skowronski L., Abraham P., Leutzinger Y. Blood glutathione concentrations in a large-scale human study. Clinical Chemistry 1996, 42:64-70.
31. Luo J.-L., Hammarqvist F., Andersson K., Wernerman J. Surgical trauma decreases glutathione synthetic capacity in human skeletal muscle tissue. American Journal of Physiology 1998, 275:E359-E365.
32. Ferrari R., Alfieri O., Curello S., Ceconi C., Cargnoni A., Marzollo P., et al. Occurrence of oxidative stress during reperfusion of the human heart. Circulation 1990, 81:201-211.
33. Mezzetti A., Calafiore A.M., Lapenna D., Deslauriers R., Tian G., Salerno T.A., Verna A.M., Bosco G., Pierdomenico S.D., Caccurullo F. Intermittent antegrade warm cardioplegia reduces oxidative stress and improves metabolism of the ischemic-reperfused human myocardium. Journal of Thoracic & Cardiovascular Surgery 1995, 109:787-795.
34. Morishige N., Tashiro T., Yamada T., Kimura M. Retrograde continuous warm blood cardioplegia reduces oxidative stress during coronary artery bypass grafting. Annals of Thoracic & Cardiovascular Surgery 2002, 31-37.
35. Nagy N., Malik G., Tosaki A., Ho Y.-S., Maulik N., Das D.K. Overexpression of glutaredoxin-2 reduces myocardial cell death by preventing both apoptosis and necrosis. Journal of Molecular and Cellular Cardiology 2008, 44:252-260.
36. Hickman J., Barber R., Skaar E., Donohue T. Link between the membrane-bound pyridine nucleotide transhydrogenase and glutathione-dependent processes in Rhodobacter sphaeroides. Journal of Bacteriology 2002, 184:400-409.
37. Aon M., Cortassa S., Maack C., O'Rourke B. Sequential opening of mitochondrial ion channels as a function of glutathione redox thiol status. Journal of Biological Chemistry 2007, 282:21889-21900.
38. Sharov V.G., Todor A., Khanal S., Imai M., Sabbah H.N. Cyclosporine A attenuates mitochondrial permeability transition and improves mitochondrial respiratory function in cardiomyocytes isolated from dogs with heart failure. Journal of Molecular and Cellular Cardiology 2007, 42:150-158.
39. Sazanov L., Jackson J.B. Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenase operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Letters 1994, 344:109-116.
40. Hancock J., Desikan R., Neill S. Does the redox status of cytochrome c act as a fail-safe mechanism in the regulation of programmed cell death?. Free Radical Biology and Medicine 2001, 31:697-703.
41. Green D., Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004, 305:626-629.
42. Schafer F., Buettner G. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biology and Medicine 2001, 30:1191-1212.
43. Meredith M.J., Reed D.J. Status of the mitochondrial pool of glutathione in the isolated hepatocyte. Journal of Biological Chemistry 1982, 257:3747-3753.
44. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiological Reviews 1979, 59:527-605.
45. Rebrin I., Kamzalov S., Sohal R.S. Effects of age and caloric restriction on glutathione redox state in mice. Free Radical Biology and Medicine 2003, 35:626-635.
46. Radi R., Turrens J.F., Chang L.Y., Bush K.M., Crapo J.D., Fremman B.A. Detection of catalase in beef heart mitochondria. Journal of Biological Chemistry 1991, 266:22028-22034.
47. Dickinson D.A., Forman H.J. Glutathione in defense and signaling: Lessons from a small thiol. Annals of the New York Academy of Sciences 2002, 973:488-504.
48. 2+ efflux. Biochimica et Biophysica Acta 1990, 1035:300-305.
49. Vogel R., Jennemann G., Seitz J., Wiesinger H., Hamprecht B. Mitochondrial malic enzyme: purification from bovine brain, generation of an antiserum and immunocytochemical localization in neurons of rat brain. Journal of Neurochemistry 1998, 71:844-852.
50. Jain A., Martensson J., Stole E., Auld P.A., Meister A. Glutathione deficiency leads to mitochondrial damage in brain. Proceedings of the National Academy of Sciences of the United States of America 1991, 88:1913-1917.
51. Ceconi C., Curello S., Cargnoni A., Ferrari R., Albertini A., Visioli O. The role of glutathione status in the protection against ischaemic and reperfusion damage: effects of N-acetyl cysteine. Journal of Molecular and Cellular Cardiology 1988, 20:5-13.
52. Zhang J., Jin B., Li L., Block E.R., Patel J.M. Nitric oxide-induced persistent inhibition and nitrosylation of active site cysteine residues of mitochondrial cytochrome-c oxidase in lung endothelial cells. American Journal of Physiology 2005, 288:C840-C849.
53. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 1980, 106:207-212.
54. Scheubel R., Tostlebe M., Simm A., Rohrbach S., Prondzinsky R., Gellerich F., et al. Dysfunction of mitochondrial respiratory chain complex I in human failing myocardium is not due to disturbed mitochondrial gene expression. Journal of the American College of Cardiology 2002, 40:2174-2181.
55. Jarreta D., Orus J., Barrientos A., Miro O., Roig E., Heras M., et al. Mitochondrial function in heart muscle from patients with idiopathic dilated cardiomyopathy. Cardiovascular Research 2000, 45:860-865.
56. Quigley A.F., Kapsa R.M., Esmore D., Hale G., Byrne E. Mitochondrial respiratory chain activity in idiopathic dilated cardiomyopathy. Journal of Cardiac Failure 2000, 6:47-55.
57. Sharov V., Todor A., Silverman N., Goldstein S., Sabbah H. Abnormal mitochondrial respiration in failed human myocardium. Journal of Molecular and Cellular Cardiology 2000, 32:2361-2367.
58. Heymes C., Bendall J., Ratajczak P., Cave A., Samuel J., Hasenfuss G., Shah A.M. Increased myocardial NADPH oxidase activity in human heart failure. Journal of the American College of Cardiology 2003, 41:2164-2171.
59. Ide T., Tsutsui H., Kinugawa S., Utsumi H., Kang D., Hattori N., et al. Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circulation Research 1999, 85:857-863.
60. Sam F., Kerstetter D., Pimental D., Mulukutla S., Tabaee A., Bristow M., Colucci W., Sawyer D. Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. Journal of Cardiac Failure 2005, 11:473-480.
61. Nakamura K., Kusano K., Nakamura Y., Kakishita M., Ohta K., Nagase S., et al. Carvedilol decreases elevated oxidative stress in human failing myocardium. Circulation 2002, 105:2867-2871.
62. Mallat Z., Phillip I., Lebret M. Elevated levels of 8-iso-prostaglandin F2a in pericardial fluid of patients with heart failure: a potential role for in vivo oxidant stress in ventricular dilatation and progression to heart failure. Circulation 1998, 97:1536-1539.
63. Jain M., Brenner D.A., Cui L., Lim C.C., Wang B., Pimentel D.R., et al. Glucose-6-phosphate dehydrogenase modulates cytosolic redox status and contractile phenotype in adult cardiomyocytes. Circulation Research 2003, 93:e9-e16.
64. Chernyak B. Redox regulation of the mitochondrial permeability transition pore. Bioscience Reports 1997, 17:293-302.
65. Costantini P., Chernyak B., Petronilli V., Bernardi P. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. Journal of Biological Chemistry 1996, 271:6746-6751.
66. Petronilli V., Costantini P., Scorrano L., Colonna R., Passamonti S., Bernardi P. The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols, Increase of the gating potential by oxidants and its reversal by reducing agents. Journal of Biological Chemistry 1994, 269:16638-16642.
67. Romashko D., Marban E., O'Rourke B. Subcellular metabolic transients and mitochondrial redox waves in heart cells. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:1618-1623.
68. Aon M., Cortassa S., Marban E., O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. Journal of Biological Chemistry 2003, 278:44735-44744.
69. Mak S., Lehotay D., Yazdanpanah M., Azevedo E., Liu P., Newton G. Unsaturated aldehydes including 4-OH-nonenal are elevated in patients with congestive heart failure. Journal of Cardiac Failure 2000, 6:108-114.
70. Belch J., Bridges A., Scott N., Chopra M. Oxygen free radicals and congestive heart failure. British Heart Journal 1991, 65:245-248.
71. McMurray J., McLay J., Chopra M., Bridges A., Belch J. Evidence for enhanced free radical activity in chronic congestive heart failure secondary to coronary artery disease. American Journal of Cardiology 1990, 65:1261-1262.
72. Kim S.Y., Park J.-W. Cellular defense against singlet oxygen-induced oxidative damage by cytosolic NADP+-dependent isocitrate dehydrogenase. Free Radical Res. 2003, 37:309-316.
73. Forsmark-Andree P., Persson B., Radi R., Dallner G., Ernster L. Oxidative modification of nicotinamide nucleotide transhydrogenase in submitochondrial particles. Archives of Biochemistry and Biophysics 1996, 336:113-120.
74. Lee C.-P., Ernster L. Studies of the energy-transfer system of submitochondrial particles: Competition between oxidative phosphorylation and the energy-linked nicotinamide-adenine dinucleotide transhydrogenase reaction. European Journal of Biochemistry 1968, 3:385-390.
75. Rydström J., Teixeira da Cruz A., Ernster L. Factors governing the kinetics and steady-state of the mitochondrial nicotinamide nucleotide transhydrogenase system. European Journal of Biochemistry 1970, 17:56-62.
76. Rydström J., Teixeira da Cruz A., Ernster L. Steady-state kinetics of mitochondrial nicotinamide nucleotide transhydrogenase. The energy-linked reaction. European Journal of Biochemistry 1971, 23:212-219.
77. Rydström J. Site-specific inhibitors of mitochondrial nicotinamide-nucleotide transhydrogenase. European Journal of Biochemistry 1972, 31:496-504.
78. Teixeira da Cruz A., Rydström J., Ernster L. Steady-state kinetics of mitochondrial nicotinamide nucleotide translocase, The nonenergy-linked reaction. European Journal of Biochemistry 1971, 23:203-211.
79. Lee S.M., Koh H.-J., Park D.-C., Song B.J., Huh T.-L., Park J.-W. Cytosolic NADP+-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radical Biology and Medicine 2002, 32:1185-1196.
80. Zhu G., Golding G.B., Dean A.M. The selective cause of an ancient adaptation. Science 2005, 307:1279-1282.
81. Freeman H., Shimomura K., Horner E., Cox R., Ashcroft F. Nicotinamide nucleotide transhydrogenase: a key role in insulin secretion. Cell Metabolism 2006, 3:35-45.