Glucose-6-Phosphate Dehydrogenase and NADPH Redox Regulates Cardiac Myocyte L-Type Calcium Channel Activity and Myocardial Contractile Function

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Rawat, Dhwajbahadur K ^a   Hecker, Peter ^b   Watanabe, Makino ^c   Chettimada, Sukrutha ^a   Levy, Richard J ^d,e   Okada, Takao ^c   Edwards, John G ^d   Gupte, Sachin A ^a  

^a UNIVERSITY OF SOUTH ALABAMA   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d NEW YORK MEDICAL COLLEGE   (United States)

^e CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 AMINONICOTINAMIDE; ACETYL COENZYME A; ACONITATE HYDRATASE; ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; CALCIUM CHANNEL L TYPE; CHOLESTEROL; GAMMA GLUTAMYLTRANSFERASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE;

ADULT ANIMAL; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CARBON DIOXIDE TENSION; CELL ISOLATION; CONTROLLED STUDY; DIASTOLE; ENZYME ACTIVITY; ENZYME INHIBITION; HEART FUNCTION; HEART LEFT VENTRICLE DP-DT; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; ISOLATED HEART; M MODE ECHOCARDIOGRAPHY; MALE; METABOLIC PARAMETERS; METABOLISM; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PH; REGULATORY MECHANISM;

6-AMINONICOTINAMIDE; ANIMALS; CALCIUM CHANNELS, L-TYPE; ECHOCARDIOGRAPHY; GLUCOSEPHOSPHATE DEHYDROGENASE; GLUCOSEPHOSPHATE DEHYDROGENASE DEFICIENCY; MALE; MICE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; NADP; PENTOSE PHOSPHATE PATHWAY; RATS;

MUS;

EID: 84867167138     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045365     Document Type: Article

References (44)

1. Nakajima T, Iwasawa K, Oonuma H, Morita T, Goto A, (1999) Antiarrhythmic effect and its underlying ionic mechanism of 17beta-estradiol in cardiac myocytes. Br J Pharmacol 127: 429-440.
2. Jiang C, Poole-Wilson PA, Sarrel PM, Mochizuki S, Collins P, (1992) Effect of 17 beta-oestradiol on contraction, Ca2+ current and intracellular free Ca2+ in guinea-pig isolated cardiac myocytes. Br J Pharmacol 106: 739-745.
3. Bai CX, Kurokawa J, Tamagawa M, Nakaya H, Furukawa T, (2005) Nontranscriptional regulation of cardiac repolarization currents by testosterone. Circulation 112: 1701-1710.
4. Michels G, Er F, Eicks M, Herzig S, Hoppe UC, (2006) Long-term and immediate effect of testosterone on single T-type calcium channel in neonatal rat cardiomyocytes. Endocrinology 147: 5160-5169.
5. Scragg JL, Jones RD, ChannerK S, Jones TH, Peers C, (2004) Testosterone is a potent inhibitor of L-type Ca(2+) channels. Biochem Biophys Res Commun 318: 503-506.
6. Hall J, Jones RD, Jones TH, Channer KS, Peers C, (2006) Selective inhibition of L-type Ca2+ channels in A7r5 cells by physiological levels of testosterone. Endocrinology 147: 2675-2680.
7. Gupte SA, Tateyama M, Okada T, Oka M, Ochi R, (2002) Epiandrosterone, a metabolite of testosterone precursor, blocks L-type calcium channels of ventricular myocytes and inhibits myocardial contractility. J Mol Cell Cardiol 34: 679-688.
8. Gordon G, Mackow MC, Levy HR, (1995) On the mechanism of interaction of steroids with human glucose 6-phosphate dehydrogenase. Arch Biochem Biophys 318: 25-29.
9. Gupte SA, Li KX, Okada T, Sato K, Oka M, (2002) Inhibitors of pentose phosphate pathway cause vasodilation: involvement of voltage-gated potassium channels. J Pharmacol Exp Ther 301: 299-305.
10. Gupte SA, Okada T, McMurtry IF, Oka M, (2006) Role of pentose phosphate pathway-derived NADPH in hypoxic pulmonary vasoconstriction. Pulm Pharmacol Ther 19: 303-309.
11. Gupte SA, Arshad M, Viola S, Kaminski PM, Ungvari Z, (2003) Pentose phosphate pathway coordinates multiple redox-controlled relaxing mechanisms in bovine coronary arteries. Am J Physiol Heart Circ Physiol 285: H2316-2326.
12. Jain M, Brenner DA, Cui L, Lim CC, Wang B, (2003) Glucose-6-phosphate dehydrogenase modulates cytosolic redox status and contractile phenotype in adult cardiomyocytes. Circ Res 93: e9-16.
13. Cocco P, Fadda D, Schwartz AG, (2008) Subjects expressing the glucose-6-phosphate dehydrogenase deficient phenotype experience a lower cardiovascular mortality. QJM 101: 161-163.
14. Drent M, Gorgels AP, Bast A, (2003) Cardiac failure associated with G6PD deficiency. Circ Res 93: e75.
15. Kohler E, Barrach H, Neubert D, (1970) Inhibition of NADP dependent oxidoreductases by the 6-aminonicotinamide analogue of NADP. FEBS Lett 6: 225-228.
16. Akuzawa-Tateyama M, Tateyama M, Ochi R, (1998) Low K+-induced hyperpolarizations trigger transient depolarizations and action potentials in rabbit ventricular myocytes. J Physiol 513: 775-786.
17. Tateyama M, Zong S, Tanabe T, Ochi R, (2001) Properties of voltage-gated Ca(2+) channels in rabbit ventricular myocytes expressing Ca(2+) channel alpha(1E) cDNA. Am J Physiol Cell Physiol 280: C175-182.
18. Lowry OH, Roberts NR, Kapphahn JI, (1957) The fluorometric measurement of pyridine nucleotides. J Biol Chem 224: 1047-1064.
19. Serpillon S, Floyd BC, Gupte RS, George S, Kozicky M, (2009) Superoxide production by NAD(P)H oxidase and mitochondria is increased in genetically obese and hyperglycemic rat heart and aorta before the development of cardiac dysfunction. The role of glucose-6-phosphate dehydrogenase-derived NADPH. Am J Physiol Heart Circ Physiol 297: H153-162.
20. Gupte RS, Floyd BC, Kozicky M, George S, Ungvari ZI, (2009) Synergistic activation of glucose-6-phosphate dehydrogenase and NAD(P)H oxidase by Src kinase elevates superoxide in type 2 diabetic, Zucker fa/fa, rat liver. Free Radic Biol Med 47: 219-228.
21. Balteau M, Tajeddine N, de Meester C, Ginion A, Des Rosiers C, (2011) NADPH oxidase activation by hyperglycaemia in cardiomyocytes is independent of glucose metabolism but requires SGLT1. Cardiovasc Res 92: 237-246.
22. Zuurbier CJ, Eerbeek O, Goedhart PT, Struys EA, Verhoeven NM, (2004) Inhibition of the pentose phosphate pathway decreases ischemia-reperfusion-induced creatine kinase release in the heart. Cardiovasc Res 62: 145-153.
23. Sanguinetti MC, Kass RS, (1984) Voltage-dependent block of calcium channel current in the calf cardiac Purkinje fiber by dihydropyridine calcium channel antagonists. Circ Res 55: 336-348.
24. Bean BP, (1984) Nitrendipine block of cardiac calcium channels: high-affinity binding to the inactivated state. Proc Natl Acad Sci U S A 81: 6388-6392.
25. Lee KS, Tsien RW, (1983) Mechanism of calcium channel blockade by verapamil, D600, diltiazem and nitrendipine in single dialysed heart cells. Nature 302: 790-794.
26. French-Mullen JM, Danks P, Spence KT, (1994) Neurosteroids modulate calcium currents in hippocampal CA1 neurons via a pertussis toxin-sensitive G-protein-coupled mechanism. J Neurosci 14: 1963-1977.
27. Arshad M, Vijay V, Floyd BC, Marks B, Sarabu MR, (2006) Thromboxane receptor stimulation suppresses guanylate cyclase-mediated relaxation of radial arteries. Ann Thorac Surg 81: 2147-2154.
28. Fearon IM, Palmer AC, Balmforth AJ, Ball SG, Mikala G, (1998) Inhibition of recombinant human cardiac L-type Ca2+ channel alpha1C subunits by 3-isobutyl-1-methylxanthine. Eur J Pharmacol 342: 353-358.
29. Koch SE, Bodi I, Schwartz A, Varadi G, (2000) Architecture of Ca(2+) channel pore-lining segments revealed by covalent modification of substituted cysteines. J Biol Chem 275: 34493-34500.
30. Hool LC, Arthur PG, (2002) Decreasing cellular hydrogen peroxide with catalase mimics the effects of hypoxia on the sensitivity of the L-type Ca2+ channel to beta-adrenergic receptor stimulation in cardiac myocytes. Circ Res 91: 601-609.
31. MacCarthy PA, Grieve DJ, Li JM, Dunster C, Kelly FJ, (2001) Impaired endothelial regulation of ventricular relaxation in cardiac hypertrophy: role of reactive oxygen species and NADPH oxidase. Circulation 104: 2967-2974.
32. Gupte SA, Kaminski PM, Floyd B, Agarwal R, Ali N, (2005) 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: H13-21.
33. Istvan ES, Palnitkar M, Buchanan SK, Deisenhofer J, (2000) Crystal structure of the catalytic portion of human HMG-CoA reductase: insights into regulation of activity and catalysis. EMBO J 19: 819-830.
34. Smeland TE, Nada M, Cuebas D, Schulz H, (1992) NADPH-dependent beta-oxidation of unsaturated fatty acids with double bonds extending from odd-numbered carbon atoms. Proc Natl Acad Sci U S A 89: 6673-6677.
35. Tsujikawa H, Song Y, Watanabe M, Masumiya H, Gupte SA, (2008) Cholesterol depletion modulates basal L-type Ca2+ current and abolishes its-adrenergic enhancement in ventricular myocytes. Am J Physiol Heart Circ Physiol 294: H285-292.
36. Lionetti V, Stanley WC, Recchia FA, (2011) Modulating fatty acid oxidation in heart failure. Cardiovasc Res 90: 202-209.
37. Gupte RS, Ata H, Rawat D, Abe M, Taylor MS, (2011) Glucose-6-phosphate dehydrogenase is a regulator of vascular smooth muscle contraction. Antioxid Redox Signal 14: 543-558.
38. Gupte SA, (2008) Glucose-6-phosphate dehydrogenase: a novel therapeutic target in cardiovascular diseases. Curr Opin Investig Drugs 9: 993-1000.
39. Kato T, Niizuma S, Inuzuka Y, Kawashima T, Okuda J, (2010) Analysis of metabolic remodeling in compensated left ventricular hypertrophy and heart failure. Circ Heart Fail 3: 420-430.
40. Gupte RS, Vijay V, Marks B, Levine RJ, Sabbah HN, (2007) Upregulation of glucose-6-phosphate dehydrogenase and NAD(P)H oxidase activity increases oxidative stress in failing human heart. J Card Fail 13: 497-506.
41. Gupte SA, Levine RJ, Gupte RS, Young ME, Lionetti V, (2006) Glucose-6-phosphate dehydrogenase-derived NADPH fuels superoxide production in the failing heart. J Mol Cell Cardiol 41: 340-349.
42. Assad RS, Atik FA, Oliveira FS, Fonseca-Alaniz MH, Abduch MC, (2011) Reversible pulmonary trunk banding. VI: Glucose-6-phosphate dehydrogenase activity in rapid ventricular hypertrophy in young goats. J Thorac Cardiovasc Surg 142: 1108-1113.
43. Zimmer HG, (1992) The oxidative pentose phosphate pathway in the heart: regulation, physiological significance, and clinical implications. Basic Res Cardiol 87: 303-316.
44. Zimmer HG, (1996) Regulation of and intervention into the oxidative pentose phosphate pathway and adenine nucleotide metabolism in the heart. Mol Cell Biochem 160-161: 101-109.