Glucose-6-phosphate dehydrogenase-derived NADPH fuels superoxide production in the failing heart

Journal of Molecular and Cellular Cardiology

Volumn 41, Issue 2, 2006, Pages 340-349

  Gupte, Sachin A ^a   Levine, Robert J ^a   Gupte, Rakhee S ^a   Young, Martin E ^b   Lionetti, Vincenzo ^a,c   Labinskyy, Volodymyr ^a,c   Floyd, Beverly C ^a   Ojaimi, Caroline ^a   Bellomo, Michelle ^a   Wolin, Michael S ^a   Recchia, Fabio A ^a,c  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c SCUOLA SUPERIORE SANT ANNA   (Italy)

Author keywords

Glucose 6 phosphate; Heart failure; NADPH oxidase; Pentose phosphate pathway

Indexed keywords

6 AMINONICOTINAMIDE; ENZYME INHIBITOR; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLYCOPROTEIN GP 91; LUCIGENIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; PENTOSE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ADDITION REACTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CHEMOLUMINESCENCE; COMPARATIVE STUDY; CONTROLLED STUDY; DOG; ENZYME ACTIVATION; HEART FAILURE; HEART LEFT VENTRICLE; HEART MUSCLE; HEART PACING; HEART VENTRICLE ENDDIASTOLIC PRESSURE; HYPOTHESIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; TISSUE HOMOGENATE; UPREGULATION;

6-AMINONICOTINAMIDE; ANIMALS; BLOOD PRESSURE; CARDIAC PACING, ARTIFICIAL; DISEASE MODELS, ANIMAL; DOGS; ENZYME INHIBITORS; GLUCOSEPHOSPHATE DEHYDROGENASE; HEART FAILURE, CONGESTIVE; HUMANS; NADP; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; SUPEROXIDES; TERATOGENS; TIME FACTORS;

CANIS FAMILIARIS;

EID: 33746070800     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2006.05.003     Document Type: Article

References (40)

1. Li J.M., and Shah A.M. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol, Regul Integr Comp Physiol 287 (2004) R1014-R1030
2. Dhalla N.S., Temsah R.M., and Netticadan T. Role of oxidative stress in cardiovascular diseases. J Hypertens 18 (2000) 655-673
3. Ballinger S.W. Mitochondrial dysfunction in cardiovascular disease. Free Radic Biol Med 38 (2005) 1278-1295
4. Berry C.E., and Hare J.M. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J Physiol 555 (2004) 589-606
5. Griendling K.K., Sorescu D., and Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86 (2000) 494-501
6. Cappola T.P., Kass D.A., Nelson G.S., Berger R.D., Rosas G.O., Kobeissi Z.A., et al. Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation 104 (2001) 2407-2411
7. Heymes C., Bendall J.K., Ratajczak P., Cave A.C., Samuel J.L., Hasenfuss G., et al. Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 41 (2003) 2164-2171
8. Maack C., Kartes T., Kilter H., Schafers H.J., Nickenig G., Bohm M., et al. Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment. Circulation 108 (2003) 1567-1574
9. Wolin M.S., Gupte S.A., and Oeckler R.A. Superoxide in the vascular system. J Vasc Res 39 (2002) 191-207
10. Dixon L.J., Morgan D.R., Hughes S.M., McGrath L.T., El-Sherbeeny N.A., Plumb R.D., et al. Functional consequences of endothelial nitric oxide synthase uncoupling in congestive cardiac failure. Circulation 107 (2003) 1725-1728
11. Stanley W.C., Recchia F.A., and Lopaschuk G.D. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85 (2005) 1093-1129
12. Osorio J.C., Stanley W.C., Linke A., Castellari M., Diep Q.N., Panchal A.R., et al. Impaired myocardial fatty acid oxidation and reduced protein expression of retinoid X receptor-alpha in pacing-induced heart failure. Circulation 106 (2002) 606-612
13. Davila-Roman V.G., Vedala G., Herrero P., de las Fuentes L., Rogers J.G., Kelly D.P., et al. Altered myocardial fatty acid and glucose metabolism in idiopathic dilated cardiomyopathy. J Am Coll Cardiol 40 (2002) 271-277
14. Lei B., Lionetti V., Young M.E., Chandler M.P., d'Agostino C., Kang E., et al. Paradoxical downregulation of the glucose oxidation pathway despite enhanced flux in severe heart failure. J Mol Cell Cardiol 36 (2004) 567-576
15. Razeghi P., Young M.E., Alcorn J.L., Moravec C.S., Frazier O.H., and Taegtmeyer H. Metabolic gene expression in fetal and failing human heart. Circulation 104 (2001) 2923-2931
16. Matsui R., Xu S., Maitland K.A., Hayes A., Leopold J.A., Handy D.E., et al. Glucose-6 phosphate dehydrogenase deficiency decreases the vascular response to angiotensin II. Circulation 112 (2005) 257-263
17. Gupte S.A., Kaminski P.M., Floyd B., Agarwal R., Ali N., Ahmad M., et al. Cytosolic NADPH may regulate differences in basal Nox oxidase-derived superoxide generation in bovine coronary and pulmonary arteries. Am J Physiol, Heart Circ Physiol 288 (2005) H13-H21
18. Lionetti V., Linke A., Chandler M.P., Young M.E., Penn M.S., Gupte S., et al. Carnitine palmitoyl transferase-I inhibition prevents ventricular remodeling and delays decompensation in pacing-induced heart failure. Cardiovasc Res 66 (2005) 454-461
19. Mohazzab K.M., and Wolin M.S. Sites of superoxide anion production detected by lucigenin in calf pulmonary artery smooth muscle. Am J Physiol 267 (1994) L815-L822
20. Ungvari Z., Csiszar A., Edwards J.G., Kaminski P.M., Wolin M.S., Kaley G., et al. Increased superoxide production in coronary arteries in hyperhomocysteinemia: role of tumor necrosis factor-alpha, NAD(P)H oxidase, and inducible nitric oxide synthase. Arterioscler Thromb Vasc Biol 23 (2003) 418-424
21. Kinugawa S., Huang H., Wang Z., Kaminski P.M., Wolin M.S., and Hintze T.H. A defect of neuronal nitric oxide synthase increases xanthine oxidase-derived superoxide anion and attenuates the control of myocardial oxygen consumption by nitric oxide derived from endothelial nitric oxide synthase. Circ Res 96 (2005) 355-362
22. Chalupsky K., and Cai H. Endothelial dihydrofolate reductase: critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 102 (2005) 9056-9061
23. Rey F.E., Cifuentes M.E., Kiarash A., Quinn M.T., and Pagano P.J. Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ Res 89 (2001) 408-414
24. Kohler E., Barrach H., and Neubert D. Inhibition of NADP dependent oxidoreductases by the 6-aminonicotinamide analogue of NADP. FEBS Lett 6 (1970) 225-228
25. 2. Am J Physiol 276 (1999) H235-H241
26. Radi R., Cosgrove T.P., Beckman J.S., and Freeman B.A. Peroxynitrite-induced luminol chemiluminescence. J Biochem 290 Pt 1 (1993) 51-57
27. Gupte S.A., Arshad M., Viola S., Kaminski P.M., Ungvari Z., Rabbani G., et al. Pentose phosphate pathway coordinates multiple redox-controlled relaxing mechanisms in bovine coronary arteries. Am J Physiol, Heart Circ Physiol 285 (2003) H2316-H2326
28. Blum J., and Fridovich I. Superoxide, hydrogen peroxide, and oxygen toxicity in two free-living nematode species. Arch Biochem Biophys 222 (1983) 35-43
29. Kauffman F.C., Brown J.G., Passonneau J.V., and Lowry O.H. Effects of changes in brain metabolism on levels of pentose phosphate pathway intermediates. J Biol Chem 244 (1969) 3647-3653
30. Gupte R.S., Weng Y., Liu L., and Lee M.Y. The second subunit of the replication factor C complex (RFC40) and the regulatory subunit (RIalpha) of protein kinase A form a protein complex promoting cell survival. Cell Cycle 4 (2005) 323-329
31. Mollnau H., Oelze M., August M., Wendt M., Daiber A., Schulz E., et al. Mechanisms of increased vascular superoxide production in an experimental model of idiopathic dilated cardiomyopathy. Arterioscler Thromb Vasc Biol (2005)
32. Gao W.D., Liu Y., and Marban E. Selective effects of oxygen free radicals on excitation-contraction coupling in ventricular muscle. Implications for the mechanism of stunned myocardium. Circulation 94 (1996) 2597-2604
33. MacFarlane N.G., and Miller D.J. Depression of peak force without altering calcium sensitivity by the superoxide anion in chemically skinned cardiac muscle of rat. Circ Res 70 (1992) 1217-1224
34. Siwik D.A., Pagano P.J., and Colucci W.S. Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am J Physiol, Cell Physiol 280 (2001) C53-C60
35. Shi Y., Baker J.E., Zhang C., Tweddell J.S., Su J., and Pritchard Jr. K.A. Chronic hypoxia increases endothelial nitric oxide synthase generation of nitric oxide by increasing heat shock protein 90 association and serine phosphorylation. Circ Res 91 (2002) 300-306
36. Gupte S.A., Tateyama M., Okada T., Oka M., and Ochi R. Epiandrosterone, a metabolite of testosterone precursor, blocks L-type calcium channels of ventricular myocytes and inhibits myocardial contractility. J Mol Cell Cardiol 34 (2002) 679-688
37. 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. Circ Res 93 (2003) e9-e16
38. Jain M., Cui L., Brenner D.A., Wang B., Handy D.E., Leopold J.A., et al. Increased myocardial dysfunction after ischemia-reperfusion in mice lacking glucose-6-phosphate dehydrogenase. Circulation 109 (2004) 898-903
39. Kletzien R.F., Harris P.K., and Foellmi L.A. Glucose-6-phosphate dehydrogenase: a "housekeeping" enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. FASEB J 8 (1994) 174-181
40. Eggleston L.V., and Krebs H.A. Regulation of the pentose phosphate cycle. Biochem J 138 (1974) 425-435