Impact of glucose-6-phosphate dehydrogenase deficiency on the pathophysiology of cardiovascular disease

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 4, 2013, Pages

  Hecker, Peter A ^a   Leopold, Jane A ^b   Gupte, Sachin A ^c   Recchia, Fabio A ^d,e   Stanley, William C ^a  

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

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF SOUTH ALABAMA   (United States)

^d TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e SCUOLA SUPERIORE SANT ANNA   (Italy)

Author keywords

G6PD; Heart failure; NADPH; Oxidative stress; ROS

Indexed keywords

6 AMINONICOTINAMIDE; AMPHOTERICIN B; BENFOTIAMINE; CHOLESTEROL; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; POTASSIUM CHLORIDE; PRASTERONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE; XANTHINE OXIDASE;

ALBUMINURIA; ANTIOXIDANT ACTIVITY; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CHOLESTEROL SYNTHESIS; CYTOLOGY; DIABETES MELLITUS; GENE MUTATION; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HEART FAILURE; HEART INFARCTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE HYPERTROPHY; HEART LEFT VENTRICLE PRESSURE; HEART PROTECTION; HEART STRESS; HEART VENTRICLE OVERLOAD; HUMAN; HYPERTENSION; ISCHEMIC HEART DISEASE; KIDNEY FAILURE; METABOLIC DISORDER; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; VASCULAR DISEASE; VASODILATATION;

ANIMALS; CARDIOVASCULAR DISEASES; ENDOTHELIUM, VASCULAR; FEMALE; GLUCOSEPHOSPHATE DEHYDROGENASE DEFICIENCY; HEART; HUMANS; MALE; MICE; MUTATION; MYOCARDIUM; OXIDATIVE STRESS; RATS; REPERFUSION INJURY; SUPEROXIDES; THIAMINE;

EID: 84874088088     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00721.2012     Document Type: Review

References (115)

1. Altenhofer S, Kleikers PW, Radermacher KA, Scheurer P, Rob Hermans JJ, Schiffers P, Ho H, Wingler K, Schmidt HH. The NOX toolbox: validating the role of NADPH oxidases in physiology and disease. Cell Mol Life Sci 69: 2327-2343, 2012.
2. Ata H, Rawat DK, Lincoln T, Gupte SA. Mechanism of glucose-6-phosphate dehydrogenase-mediated regulation of coronary artery contractility. Am J Physiol Heart Circ Physiol 300: H2054-H2063, 2011.
3. Babior BM. NADPH oxidase: an update. Blood 93: 1464-1476, 1999.
4. Batetta B, Bonatesta RR, Sanna F, Putzolu M, Mulas MF, Collu M, Dessi S. Cell growth and cholesterol metabolism in human glucose-6-phosphate dehydrogenase deficient lymphomononuclear cells. Cell Prolif 35: 143-154, 2002.
5. Beutler E. G6PD deficiency. Blood 84: 3613-3636, 1994.
6. Beutler E. Glucose-6-phosphate dehydrogenase deficiency: a historical perspective. Blood 111: 16-24, 2008.
7. Biaglow JE, Ayene IS, Koch CJ, Donahue J, Stamato TD, Tuttle SW. G6PD deficient cells and the bioreduction of disulfides: effects of DHEA, GSH depletion and phenylarsine oxide. Biochem Biophys Res Commun 273: 846-852, 2000.
8. Bing RJ, Gudbjarnason S, Tschopp H, Braasch W. Molecular changes in myocardial infarction in heart muscle. Ann NY Acad Sci 156: 583-593, 1969.
9. Boros LG, Puigjaner J, Cascante M, Lee WN, Brandes JL, Bassilian S, Yusuf FI, Williams RD, Muscarella P, Melvin WS, Schirmer WJ. Oxythiamine and dehydroepiandrosterone inhibit the nonoxidative synthesis of ribose and tumor cell proliferation. Cancer Res 57: 4242-4248, 1997.
10. Bukau B, Weissman J, Horwich A. Molecular chaperones and protein quality control. Cell 125: 443-451, 2006.
11. Cappellini MD, Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet 371: 64-74, 2008.
12. Ceylan-Isik AF, Wu S, Li Q, Li SY, Ren J. High-dose benfotiamine rescues cardiomyocyte contractile dysfunction in streptozotocin-induced diabetes mellitus. J Appl Physiol 100: 150-156, 2006.
13. Christians ES, Benjamin IJ. Proteostasis and REDOX state in the heart. Am J Physiol Heart Circ Physiol 302: H24-H37, 2012.
14. Cocco P, Todde P, Fornera S, Manca MB, Manca P, Sias AR. Mortality in a cohort of men expressing the glucose-6-phosphate dehydrogenase deficiency. Blood 91: 706-709, 1998.
15. Das DK. Redox regulation of cardiomyocyte survival and death. Antioxid Redox Signal 3: 23-37, 2001.
16. Dimmeler S, Zeiher AM. A "reductionist" view of cardiomyopathy. Cell 130: 401-402, 2007.
17. Doerries C, Grote K, Hilfiker-Kleiner D, Luchtefeld M, Schaefer A, Holland SM, Sorrentino S, Manes C, Schieffer B, Drexler H, Landmesser U. Critical role of the NAD(P)H oxidase subunit p47phox for left ventricular remodeling/dysfunction and survival after myocardial infarction. Circ Res 100: 894-903, 2007.
18. Efferth T, Fabry U, Glatte P, Osieka R. Increased induction of apoptosis in mononuclear cells of a glucose-6-phosphate dehydrogenase deficient patient. J Mol Med (Berl) 73: 47-49, 1995.
19. Efferth T, Fabry U, Osieka R. DNA damage and apoptosis in mononuclear cells from glucose-6-phosphate dehydrogenase-deficient patients (G6PD Aachen variant) after UV irradiation. J Leukoc Biol 69: 340-342, 2001.
20. Efferth T, Schwarzl SM, Smith J, Osieka R. Role of glucose-6-phosphate dehydrogenase for oxidative stress and apoptosis. Cell Death Differ 13: 527-528, 2006.
21. Eggleston LV, Krebs HA. Regulation of the pentose phosphate cycle. Biochem J 138: 425-435, 1974.
22. Fico A, Paglialunga F, Cigliano L, Abrescia P, Verde P, Martini G, Iaccarino I, Filosa S. Glucose-6-phosphate dehydrogenase plays a crucial role in protection from redox-stress-induced apoptosis. Cell Death Differ 11: 823-831, 2004.
23. Filosa S, Fico A, Paglialunga F, Balestrieri M, Crooke A, Verde P, Abrescia P, Bautista JM, Martini G. Failure to increase glucose consumption through the pentose-phosphate pathway results in the death of glucose-6-phosphate dehydrogenase gene-deleted mouse embryonic stem cells subjected to oxidative stress. Biochem J 370: 935-943, 2003.
24. Forgione MA, Loscalzo J, Holbrook M, Scribner AW, Palmisano J, Maxwell C, Baldwin C, Vita J. The A326G (A+) variant of the glucose-6-phosphate dehydrogenase gene is associated with endothelial dysfunction in African Americans (Abstract). J Am Coll Cardiol. 41, 249A. 2003.
25. Frazziano G, Champion HC, Pagano PJ. NADPH oxidase-derived ROS and the regulation of pulmonary vessel tone. Am J Physiol Heart Circ Physiol 302: H2166-H2177, 2012.
26. Frederiks WM, Kummerlin IP, Bosch KS, Vreeling-Sindelarova H, Jonker A, Van Noorden CJ. NADPH production by the pentose phosphate pathway in the zona fasciculata of rat adrenal gland. J Histochem Cytochem 55: 975-980, 2007.
27. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C. Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 109: 433-438, 2004.
28. Guan J, Mishra S, Falk RH, Liao R. Current perspectives on cardiac amyloidosis. Am J Physiol Heart Circ Physiol 302: H544-H552, 2012.
29. Gupte RS, Ata H, Rawat D, Abe M, Taylor MS, Ochi R, Gupte SA. Glucose-6-phosphate dehydrogenase is a regulator of vascular smooth muscle contraction. Antioxid Redox Signal 14: 543-558, 2011.
30. Gupte RS, Floyd BC, Kozicky M, George S, Ungvari ZI, Neito V, Wolin MS, Gupte SA. 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, 2009.
31. Gupte RS, Vijay V, Marks B, Levine RJ, Sabbah HN, Wolin MS, Recchia FA, Gupte SA. 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, 2007.
32. Gupte SA. Glucose-6-phosphate dehydrogenase: a novel therapeutic target in cardiovascular diseases. Curr Opin Investig Drugs 9: 993-1000, 2008.
33. Gupte SA. Targeting the pentose phosphate pathway in syndrome X-related cardiovascular complications. Drug Dev Res 71: 161-167, 2010.
34. Gupte SA, Levine RJ, Gupte RS, Young ME, Lionetti V, Labinskyy V, Floyd BC, Ojaimi C, Bellomo M, Wolin MS, Recchia FA. Glucose-6-phosphate dehydrogenase-derived NADPH fuels superoxide production in the failing heart. J Mol Cell Cardiol 41: 340-349, 2006.
35. Han CY, Umemoto T, Omer M, Den Hartigh LJ, Chiba T, Leboeuf R, Buller CL, Sweet IR, Pennathur S, Abel ED, Chait A. NADPH oxidase-derived reactive oxygen species increases expression of monocyte chemotactic factor genes in cultured adipocytes. J Biol Chem 287: 10379-10393, 2012.
36. Hayashi K, Kimata H, Obata K, Matsushita A, Fukata A, Hashimoto K, Noda A, Iwase M, Koike Y, Yokota M, Nagata K. Xanthine oxidase inhibition improves left ventricular dysfunction in dilated cardiomyopathic hamsters. J Card Fail 14: 238-244, 2008.
37. Hecker PA, Galvao TF, O'Shea KM, Brown BH, Henderson R Jr, Riggle H, Gupte SA, Stanley WC. High-sugar intake does not exacerbate metabolic abnormalities or cardiac dysfunction in genetic cardiomyopathy. Nutrition 28: 520-526, 2012.
38. Hecker PA, Lionetti V, Ribeiro RF Jr, Rastogi S, Brown BH, O'Connell KA, Cox JW, Shekar KC, Gamble D, Sabbah HN, Leopold JA, Gupte SA, Recchia FA, Stanley WC. Glucose 6-phosphate dehydrogenase deficiency increases redox stress and moderately accelerates the development of heart failure. Circ Heart Fail. First published on November 20, 2012; doi:10.1161/CIRCHEARTFAILURE. 112.969576.
39. Hecker PA, Mapanga RF, Kimar CP, Ribeiro RF Jr, Brown BH, O'Connell KA, Cox JW, Shekar KC, Asemu G, Essop MF, Stanley WC. Effects of glucose 6-phosphate-dehydrogenase deficiency on the metabolic and cardiac responses to obesogenic or high-fructose diets. Am J Physiol Endocrinol Metab 303: E959-E972, 2012.
40. Heymes C, Bendall JK, Ratajczak P, Cave AC, Samuel JL, Hasenfuss G, Shah AM. Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 41: 2164-2171, 2003.
41. Infanger DW, Cao X, Butler SD, Burmeister MA, Zhou Y, Stupinski JA, Sharma RV, Davisson RL. Silencing nox4 in the paraventricular nucleus improves myocardial infarction-induced cardiac dysfunction by attenuating sympathoexcitation and periinfarct apoptosis. Circ Res 106: 1763-1774, 2010.
42. Izumo K, Horiuchi M, Komatsu M, Aoyama K, Bandow K, Matsuguchi T, Takeuchi M, Takeuchi T. Dehydroepiandrosterone increased oxidative stress in a human cell line during differentiation. Free Radic Res 43: 922-931, 2009.
43. Jain M, Brenner DA, Cui L, Lim CC, Wang B, Pimentel DR, Koh S, Sawyer DB, Leopold JA, Handy DE, Loscalzo J, Apstein CS, Liao R. Glucose-6-phosphate dehydrogenase modulates cytosolic redox status and contractile phenotype in adult cardiomyocytes. Circ Res 93: e9-e16, 2003.
44. Jain M, Cui L, Brenner DA, Wang B, Handy DE, Leopold JA, Loscalzo J, Apstein CS, Liao R. Increased myocardial dysfunction after ischemia-reperfusion in mice lacking glucose-6-phosphate dehydrogenase. Circulation 109: 898-903, 2004.
45. Katare R, Caporali A, Emanueli C, Madeddu P. Benfotiamine improves functional recovery of the infarcted heart via activation of prosurvival G6PD/Akt signaling pathway and modulation of neurohormonal response. J Mol Cell Cardiol 49: 625-638, 2010.
46. Katare RG, Caporali A, Oikawa A, Meloni M, Emanueli C, Madeddu P. Vitamin B1 analog benfotiamine prevents diabetes-induced diastolic dysfunction and heart failure through Akt/Pim-1-mediated survival pathway. Circ Heart Fail 3: 294-305, 2010.
47. Ko CH, Li K, Li CL, Ng PC, Fung KP, James AE, Wong RP, Gu GJ, Fok TF. Development of a novel mouse model of severe glucose-6-phosphate dehydrogenase (G6PD)-deficiency for in vitro and in vivo assessment of hemolytic toxicity to red blood cells. Blood Cells Mol Dis 47: 176-181, 2011.
48. Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci USA 107: 15565-15570, 2010.
49. Lee JW, Choi AH, Ham M, Kim JW, Choe SS, Park J, Lee GY, Yoon KH, Kim JB. G6PD up-regulation promotes pancreatic beta-cell dysfunction. Endocrinology 152: 793-803, 2011.
50. Leopold JA, Cap A, Scribner AW, Stanton RC, Loscalzo J. Glucose-6-phosphate dehydrogenase deficiency promotes endothelial oxidant stress and decreases endothelial nitric oxide bioavailability. FASEB J 15: 1771-1773, 2001.
51. Leopold JA, Dam A, Maron BA, Scribner AW, Liao R, Handy DE, Stanton RC, Pitt B, Loscalzo J. Aldosterone impairs vascular reactivity by decreasing glucose-6-phosphate dehydrogenase activity. Nat Med 13: 189-197, 2007.
52. Leopold JA, Loscalzo J. Oxidative enzymopathies and vascular disease. Arterioscler Thromb Vasc Biol 25: 1332-1340, 2005.
53. Leopold JA, Zhang YY, Scribner AW, Stanton RC, Loscalzo J. Glucose-6-phosphate dehydrogenase overexpression decreases endothelial cell oxidant stress and increases bioavailable nitric oxide. Arterioscler Thromb Vasc Biol 23: 411-417, 2003.
54. Levy HR, Christoff M. A critical appraisal of the effect of oxidized glutathione on hepatic glucose 6-phosphate dehydrogenase activity. Biochem J 214: 959-965, 1983.
55. Long WK, Wilson SW, Frenkel EP. Associations between red cell glucose-6-phosphate dehydrogenase variants and vascular diseases. Am J Hum Genet 19: 35-53, 1967.
56. Longo L, Vanegas OC, Patel M, Rosti V, Li H, Waka J, Merghoub T, Pandolfi PP, Notaro R, Manova K, Luzzatto L. Maternally transmitted severe glucose 6-phosphate dehydrogenase deficiency is an embryonic lethal. EMBO J 21: 4229-4239, 2002.
57. Luzzatto L, Notaro Malaria R. Protecting against bad air. Science 293: 442-443, 2001.
58. Maloyan A, Sanbe A, Osinska H, Westfall M, Robinson D, Imahashi K, Murphy E, Robbins J. Mitochondrial dysfunction and apoptosis underlie the pathogenic process in alpha-B-crystallin desmin-related cardiomyopathy. Circulation 112: 3451-3461, 2005.
59. Maron BA, Zhang YY, Handy DE, Beuve A, Tang SS, Loscalzo J, Leopold JA. Aldosterone increases oxidant stress to impair guanylyl cyclase activity by cysteinyl thiol oxidation in vascular smooth muscle cells. J Biol Chem 284: 7665-7672, 2009.
60. Matsui R, Xu S, Maitland KA, Hayes A, Leopold JA, Handy DE, Loscalzo J, Cohen RA. Glucose-6 phosphate dehydrogenase deficiency decreases the vascular response to angiotensin II. Circulation 112: 257-263, 2005.
61. -/- mice. Arterioscler Thromb Vasc Biol 26: 910-916, 2006.
62. McLendon PM, Robbins J. Desmin-related cardiomyopathy: an unfolding story. Am J Physiol Heart Circ Physiol 301: H1220-H1228, 2011.
63. Meldrum NU, Tarr HL. The reduction of glutathione by the Warburg-Christian system. Biochem J 29: 108-115, 1935.
64. Mellor K, Ritchie RH, Meredith G, Woodman OL, Morris MJ, Delbridge LM. High-fructose diet elevates myocardial superoxide generation in mice in the absence of cardiac hypertrophy. Nutrition 26: 842-848, 2010.
65. Meloni L, Manca MR, Loddo I, Cioglia G, Cocco P, Schwartz A, Muntoni S, Muntoni S. Glucose-6-phosphate dehydrogenase deficiency protects against coronary heart disease. J Inherit Metab Dis 31: 412-417, 2008.
66. Mesbah-Namin SA, Nemati A, Tiraihi T. Evaluation of DNA damage in leukocytes of G6PD-deficient Iranian newborns (Mediterranean variant) using comet assay. Mutat Res 568: 179-185, 2004.
67. Morelli A, Benatti U, Gaetani GF, De Flora A. Biochemical mechanisms of glucose-6-phosphate dehydrogenase deficiency. Proc Natl Acad Sci USA 75: 1979-1983, 1978.
68. Muntoni S, Batetta B, Dessi S, Muntoni S, Pani P. Serum lipoprotein profile in the Mediterranean variant of glucose-6-phosphate dehydrogenase deficiency. Eur J Epidemiol 8, Suppl 1: 48-53, 1992.
69. Muntoni S, Muntoni S. Gene-nutrient interactions in G6PD-deficient subjects-implications for cardiovascular disease susceptibility. J Nutrigenet Nutrigenomics 1: 49-54, 2008.
70. Naylor CE, Rowland P, Basak AK, Gover S, Mason PJ, Bautista JM, Vulliamy TJ, Luzzatto L, Adams MJ. Glucose 6-phosphate dehydrogenase mutations causing enzyme deficiency in a model of the tertiary structure of the human enzyme. Blood 87: 2974-2982, 1996.
71. Ng HP, Wang YF, Lee CY, Hu ML. Toxicological and antioxidant effects of short-term dehydroepiandrosterone injection in young rats fed diets deficient or adequate in vitamin E. Food Chem Toxicol 37: 503-508, 1999.
72. Niazi GA. Glucose-6-phosphate dehydrogenase deficiency and diabetes mellitus. Int J Hematol 54: 295-298, 1991.
73. Nichols KD, Kirby GM. Expression of cytochrome P450 2A5 in a glucose-6-phosphate dehydrogenase-deficient mouse model of oxidative stress. Biochem Pharmacol 75: 1230-1239, 2008.
74. Nogueira M, Garcia G, Mejuto C, Freire M. Regulation of the pentose phosphate cycle. Cofactor that controls the inhibition of glucose-6-phosphate dehydrogenase by NADPH in rat liver. Biochem J 239: 553-558, 1986.
75. Oshikawa J, Kim SJ, Furuta E, Caliceti C, Chen GF, McKinney RD, Kuhr F, Levitan I, Fukai T, Ushio-Fukai M. Novel role of p66Shc in ROS-dependent VEGF signaling and angiogenesis in endothelial cells. Am J Physiol Heart Circ Physiol 302: H724-H732, 2012.
76. Park J, Choe SS, Choi AH, Kim KH, Yoon MJ, Suganami T, Ogawa Y, Kim JB. Increase in glucose-6-phosphate dehydrogenase in adipocytes stimulates oxidative stress and inflammatory signals. Diabetes 55: 2939-2949, 2006.
77. Park J, Chung JJ, Kim JB. New evaluations of redox regulating system in adipose tissue of obesity. Diabetes Res Clin Pract 77, Suppl 1: S11-S16, 2007.
78. Park J, Rho HK, Kim KH, Choe SS, Lee YS, Kim JB. Overexpression of glucose-6-phosphate dehydrogenase is associated with lipid dysregulation and insulin resistance in obesity. Mol Cell Biol 25: 5146-5157, 2005.
79. Paulin R, Meloche J, Jacob MH, Bisserier M, Courboulin A, Bonnet S. Dehydroepiandrosterone inhibits the Src/STAT3 constitutive activation in pulmonary arterial hypertension. Am J Physiol Heart Circ Physiol 301: H1798-H1809, 2011.
80. Persico MG, Viglietto G, Martini G, Toniolo D, Paonessa G, Moscatelli C, Dono R, Vulliamy T, Luzzatto L, D'Urso M. Isolation of human glucose-6-phosphate dehydrogenase (G6PD) cDNA clones: primary structure of the protein and unusual 5= non-coding region. Nucleic Acids Res 14: 2511-2522, 1986.
81. Porras AG, Olson JS, Palmer G. The reaction of reduced xanthine oxidase with oxygen. Kinetics of peroxide and superoxide formation. J Biol Chem 256: 9006-9103, 1981.
82. Pretsch W, Charles DJ, Merkle S. X-linked glucose-6-phosphate dehydrogenase deficiency in Mus musculus. Biochem Genet 26: 89-103, 1988.
83. Rajasekaran NS, Connell P, Christians ES, Yan LJ, Taylor RP, Orosz A, Zhang XQ, Stevenson TJ, Peshock RM, Leopold JA, Barry WH, Loscalzo J, Odelberg SJ, Benjamin IJ. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 130: 427-439, 2007.
84. Rajasekaran NS, Firpo MA, Milash BA, Weiss RB, Benjamin IJ. Global expression profiling identifies a novel biosignature for protein aggregation R120GCryAB cardiomyopathy in mice. Physiol Genomics 35: 165-172, 2008.
85. Rajasekaran NS, Varadharaj S, Khanderao GD, Davidson CJ, Kannan S, Firpo MA, Zweier JL, Benjamin IJ. Sustained activation of nuclear erythroid 2-related factor 2/antioxidant response element signaling promotes reductive stress in the human mutant protein aggregation cardiomyopathy in mice. Antioxid Redox Signal 14: 957-971, 2011.
86. Rawat DK, Hecker P, Watanabe M, Chettimada S, Levy RJ, Okada T, Edwards JG, Gupte SA. Glucose-6-phosphate dehydrogenase and NADPH redox regulates cardiac myocyte L-type calcium channel activity and myocardial contractile function. PLoS One 7: e45365, 2012.
87. Ray R, Murdoch CE, Wang M, Santos CX, Zhang M, om-Ruiz S, Anilkumar N, Ouattara A, Cave AC, Walker SJ, Grieve DJ, Charles RL, Eaton P, Brewer AC, Shah AM. Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arterioscler Thromb Vasc Biol 31: 1368-1376, 2011.
88. Saeed TK, Hamamy HA, Alwan AA. Association of glucose-6-phosphate dehydrogenase deficiency with diabetes mellitus. Diabet Med 2: 110-112, 1985.
89. Salvemini F, Franze A, Iervolino A, Filosa S, Salzano S, Ursini MV. Enhanced glutathione levels and oxidoresistance mediated by increased glucose-6-phosphate dehydrogenase expression. J Biol Chem 274: 2750-2757, 1999.
90. Sanada S, Komuro I, Kitakaze M. Pathophysiology of myocardial reperfusion injury: preconditioning, postconditioning, and translational aspects of protective measures. Am J Physiol Heart Circ Physiol 301: H1723-H1741, 2011.
91. Sanders S, Smith DP, Thomas GA, Williams ED. A glucose-6-phosphate dehydrogenase (G6PD) splice site consensus sequence mutation associated with G6PD enzyme deficiency. Mutat Res 374: 79-87, 1997.
92. Sanna F, Bonatesta RR, Frongia B, Uda S, Banni S, Melis MP, Collu M, Madeddu C, Serpe R, Puddu S, Porcu G, Dessi S, Batetta B. Production of inflammatory molecules in peripheral blood mononuclear cells from severely glucose-6-phosphate dehydrogenase-deficient subjects. J Vasc Res 44: 253-263, 2007.
93. Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C, Luedike P, Michaelis UR, Weissmann N, Dimmeler S, Shah AM, Brandes RP. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res 110: 1217-1225, 2012.
94. Schwartz HP, Haberman BE, Ruddy RM. Hyperbilirubinemia: current guidelines and emerging therapies. Pediatr Emerg Care 27: 884-889, 2011.
95. Serpillon S, Floyd BC, Gupte RS, George S, Kozicky M, Neito V, Recchia F, Stanley W, Wolin MS, Gupte SA. 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-H162, 2009.
96. Shao D, Oka S, Brady CD, Haendeler J, Eaton P, Sadoshima J. Redox modification of cell signaling in the cardiovascular system. J Mol Cell Cardiol 52: 550-558, 2012.
97. Soliman H, Gador A, Lu YH, Lin G, Bankar G, Macleod KM. Diabetes-induced increased oxidative stress in cardiomyocytes is sustained by a positive feedback loop involving Rho kinase and PKCbeta2. Am J Physiol Heart Circ Physiol 303: H989-H1000, 2012.
98. Spencer NY, Yan Z, Boudreau RL, Zhang Y, Luo M, Li Q, Tian X, Shah AM, Davisson RL, Davidson B, Banfi B, Engelhardt JF. Control of hepatic nuclear superoxide production by glucose 6-phosphate dehydrogenase and NADPH oxidase-4. J Biol Chem 286: 8977-8987, 2011.
99. Stanton RC. Glucose-6-phosphate dehydrogenase, nadph, and cell survival. IUBMB Life 64: 362-369, 2012.
100. Stanton RC, Seifter JL, Boxer DC, Zimmerman E, Cantley LC. Rapid release of bound glucose-6-phosphate dehydrogenase by growth factors. Correlation with increased enzymatic activity. J Biol Chem 266: 12442-12448, 1991.
101. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101: 6062-6067, 2004.
102. Takizawa T, Huang IY, Ikuta T, Yoshida A. Human glucose-6-phosphate dehydrogenase: primary structure and cDNA cloning. Proc Natl Acad Sci USA 83: 4157-4161, 1986.
103. Tian WN, Braunstein LD, Apse K, Pang J, Rose M, Tian X, Stanton RC. Importance of glucose-6-phosphate dehydrogenase activity in cell death. Am J Physiol Cell Physiol 276: C1121-C1131, 1999.
104. Tian WN, Braunstein LD, Pang J, Stuhlmeier KM, Xi QC, Tian X, Stanton RC. Importance of glucose-6-phosphate dehydrogenase activity for cell growth. J Biol Chem 273: 10609-10617, 1998.
105. Tome ME, Johnson DB, Samulitis BK, Dorr RT, Briehl MM. Glucose 6-phosphate dehydrogenase overexpression models glucose deprivation and sensitizes lymphoma cells to apoptosis. Antioxid Redox Signal 8: 1315-1327, 2006.
106. Tsutsui H, Kinugawa S, Matsushima S. Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol 301: H2181-H2190, 2011.
107. Wan GH, Tsai SC, Chiu DT. Decreased blood activity of glucose-6-phosphate dehydrogenase associates with increased risk for diabetes mellitus. Endocrine 19: 191-195, 2002.
108. Wiesenfeld SL, Petrakis NL, Sams BJ, Collen MF, Cutler JL. Elevated blood pressure, pulse rate and serum creatinine in Negro males deficient in glucose-6-phosphate dehydrogenase. N Engl J Med 282: 1001-1002, 1970.
109. World Health Organization Working Group. Glucose-6-phosphate dehydrogenase deficiency. WHO Working Group. Bull World Health Organ 67: 601-611, 1989.
110. Xia Y, Dawson VL, Dawson TM, Snyder SH, Zweier JL. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci USA 93: 6770-6774, 1996.
111. Xu Y, Zhang Z, Hu J, Stillman IE, Leopold JA, Handy DE, Loscalzo J, Stanton RC. Glucose-6-phosphate dehydrogenase-deficient mice have increased renal oxidative stress and increased albuminuria. FASEB J 24: 609-616, 2010.
112. Zhang H, Limphong P, Pieper J, Liu Q, Rodesch CK, Christians E, Benjamin IJ. Glutathione-dependent reductive stress triggers mitochondrial oxidation and cytotoxicity. FASEB J 26: 1442-1451, 2012.
113. Zhang M, Brewer AC, Schroder K, Santos CX, Grieve DJ, Wang M, Anilkumar N, Yu B, Dong X, Walker SJ, Brandes RP, Shah AM. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci USA 107: 18121-18126, 2010.
114. Zhang X, Min X, Li C, Benjamin IJ, Qian B, Zhang X, Ding Z, Gao X, Yao Y, Ma Y, Cheng Y, Liu L. Involvement of reductive stress in the cardiomyopathy in transgenic mice with cardiac-specific overexpression of heat shock protein 27. Hypertension 55: 1412-1417, 2010.
115. Zhang Z, Liew CW, Handy DE, Zhang Y, Leopold JA, Hu J, Guo L, Kulkarni RN, Loscalzo J, Stanton RC. High glucose inhibits glucose-6-phosphate dehydrogenase, leading to increased oxidative stress and beta-cell apoptosis. FASEB J 24: 1497-1505, 2010.