Increasing Glucose 6-Phosphate Dehydrogenase Activity Restores Redox Balance in Vascular Endothelial Cells Exposed to High Glucose

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Zhang, Zhaoyun ^a,b   Yang, Zhihong ^a   Zhu, Bo ^d   Hu, Ji ^e   Liew, Chong Wee ^a   Zhang, Yingyi ^c   Leopold, Jane A ^c   Handy, Diane E ^c   Loscalzo, Joseph ^c   Stanton, Robert C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b FUDAN UNIVERSITY   (China)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d FIRST MILITARY MEDICAL UNIVERSITY   (China)

^e THE SECOND AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; PROTEIN KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA;

ADENOVIRUS INFECTION; ANIMAL CELL; ARTICLE; CELL DEATH; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; GENE SEQUENCE; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; ANTIOXIDANTS; CATTLE; CELL DEATH; CELL PROLIFERATION; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOTHELIAL CELLS; GLUCOSE; GLUCOSEPHOSPHATE DEHYDROGENASE; HUMANS; MODELS, BIOLOGICAL; NADPH OXIDASE; OLIGONUCLEOTIDES; OXIDATION-REDUCTION; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING;

EID: 84869767236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049128     Document Type: Article

References (52)

1. Fatokun AA, Stone TW, Smith RA, (2008) Oxidative stress in neurodegeneration and available means of protection. Front Biosci 13: 3288-3311.
2. Forbes JM, Coughlan MT, Cooper ME, (2008) Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 57: 1446-1454.
3. Lenzen S, (2008) Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans 36: 343-347.
4. Lubos E, Handy DE, Loscalzo J, (2008) Role of oxidative stress and nitric oxide in atherothrombosis. Front Biosci 13: 5323-5344.
5. Thomas SR, Witting PK, Drummond GR, (2008) Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal 10: 1713-1765.
6. Beisswenger PJ, Drummond KS, Nelson RG, Howell SK, Szwergold BS, et al. (2005) Susceptibility to diabetic nephropathy is related to dicarbonyl and oxidative stress. Diabetes 54: 3274-3281.
7. Maritim AC, Sanders RA, Watkins JB III, (2003) Diabetes, oxidative stress, and antioxidants: A review. Journal of Biochemistry and Molecular Toxicology 17: 24-38.
8. Okouchi M, Okayama N, Aw TY, (2005) Hyperglycemia potentiates carbonyl stress-induced apoptosis in naive PC-12 cells: relationship to cellular redox and activator protease factor-1 expression. Curr Neurovasc Res 2: 375-386.
9. Xu Y, Osborne BW, Stanton RC, (2005) Diabetes causes inhibition of glucose-6-phosphate dehydrogenase via activation of protein kinase A which contributes to oxidative stress in rat kidney cortex. American Journal of Physiology (Renal Physiology) 289: F1040-F1047.
10. Brownlee M, (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820.
11. Goh SY, Cooper ME, (2008) Clinical review: The role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab 93: 1143-1152.
12. Meister A, (1988) Glutathione metabolism and its selective modification. J Biol Chem 263: 17205-17208.
13. Kirkman HN, Rolfo M, Ferraris AM, Gaetani GF, (1999) Mechanisms of protection of catalase by NADPH. Kinetics and stoichiometry. Journal of Biological Chemistry 274: 13908-13914.
14. Fridovich I, (1997) Superoxide anion radical (O2-), superoxide dismutases, and related matters. J Biol Chem 272: 18515-18517.
15. Pigeolet E, Corbisier P, Houbion A, Lambert D, Michiels C, et al. (1990) Glutathione peroxidase, superoxide dismutase, and catalase inactivation by peroxides and oxygen derived free radicals. Mech Ageing Dev 51: 283-297.
16. Kalinina EV, Chernov NN, Saprin AN, (2008) Involvement of thio-, peroxi-, and glutaredoxins in cellular redox-dependent processes. Biochemistry (Mosc) 73: 1493-1510.
17. Kletzien RF, Harris PKW, Foellmi LA, (1994) Glucose-6-phosphate dehydrogenase: a "housekeeping" enzyme subject to tissue-specific regulation by hormones, nutrients, and oxident stress. FASEB J 8: 174-181.
18. Leopold JA, Cap A, Scribner AW, Stanton RC, Loscalzo J, (2001) Glucose 6-phosphate dehydrogenase deficiency promotes endothelial oxidant stress and decreases nitiric oxide bioavailability. FASEB J 15: 1771-1773.
19. Martini G, Ursini MV, (1996) A new lease of life for an old enzyme. BioEssays 18: 631-637.
20. Stanton RC, Seifter JL, Boxer DC, Zimmerman E, Cantley LC, (1991) Rapid release of bound glucose-6-phosphate dehydrogenase by growth factors. J Biol Chem 266: 12442-12448.
21. Tian W-N, Braunstein LD, Apse K, Pang J, Rose M, et al. (1999) Importance of glucose 6-phosphate dehydrogenase activity in cell death. Amer J Physiol (Cell) 276: C1121-C1131.
22. Tian W-N, Braunstein LD, Pang J, Stuhlmeier K, Xi Q-C, et al. (1998) Importance of glucose 6-phosphate dehydrogenase activity for cell growth. J Biol Chem 273: 10609-10617.
23. Zhang Z, Apse K, J P, Stanton RC, (2000) High glucose inhibits glucose 6-phosphate dehydrogenase via cAMP in aortic endothelial cells. J Biol Chem 275: 40042-40047.
24. Ding H, Aljofan M, Triggle CR, (2007) Oxidative stress and increased eNOS and NADPH oxidase expression in mouse microvessel endothelial cells. J Cell Physiol 212: 682-689.
25. Nakagami H, Kaneda Y, Ogihara T, Morishita R, (2005) Endothelial dysfunction in hyperglycemia as a trigger of atherosclerosis. Curr Diabetes Rev 1: 59-63.
26. Sheu ML, Chiang CK, Tsai KS, Ho FM, Weng TI, et al. (2008) Inhibition of NADPH oxidase-related oxidative stress-triggered signaling by honokiol suppresses high glucose-induced human endothelial cell apoptosis. Free Radic Biol Med 44: 2043-2050.
27. Zhang Z, Apse K, Pang J, Stanton RC, (2000) High glucose inhibits glucose-6-phosphate dehydrogenase via cAMP in aortic endothelial cells. J Biol Chem 275: 40042-40047.
28. Diaz-Flores M, Ibanez-Hernandez MA, Galvan RE, Gutierrez M, Duran-Reyes G, et al. (2006) Glucose-6-phosphate dehydrogenase activity and NADPH/NADP+ ratio in liver and pancreas are dependent on the severity of hyperglycemia in rat. Life Sci 78: 2601-2607.
29. Ulusu NN, Sahilli M, Avci A, Canbolat O, Ozansoy G, et al. (2003) Pentose phosphate pathway, glutathione-dependent enzymes, and antioxidant defense during oxidative stress in diabetic rodent brain and peripheral organs: Effects of stobadine and vitamin E. Neurochemical Research 28: 815-823.
30. Kuroda A, Saito K, Tanaka H, (1990) Histochemical studies on the conduction system of diabetic rat hearts. Arch Histol Cytol 53: 193-198.
31. Tarach JS, (1978) Some histochemical observations on the myocardial metabolism in experimental conditions. Part I. Acta Histochem 61: 257-272.
32. Calvo JC, Biella de Souza Valle L, Baranao JL, Tesone M, Charreau EH, (1979) NADPH generating enzymes in Leydig cells from diabetic rats. Horm Metab Res 11: 161-164.
33. Muggeo M, Moghetti P, Querena M, Cacciatori V, Zoppini G, et al. (1993) Mononuclear leukocytes from obese patients with type II diabetes have reduced activity of hexokinase, 6-phosphofructokinase and glucose-6-phosphate dehydrogenase. Horm Metab Res 25: 160-164.
34. VanderJagt DJ, Harrison JM, Ratliff DM, Hunsaker LA, Vander Jagt DL, (2001) Oxidative stress indices in IDDM subjects with and without long-term diabetic complications. Clin Biochem 34: 265-270.
35. Chiu DT, Liu TZ, (1997) Free Radical and Oxidative Damage in Human Blood Cells. J Biomed Sci 4: 256-259.
36. Costagliola C, (1990) Oxidative state of glutathione in red blood cells and plasma of diabetic patients: in vivo and in vitro study. Clin Physiol Biochem 8: 204-210.
37. Kamal K, Du W, Mills I, Sumpio BE, (1998) Antiproliferative effect of elevated glucose in human microvascular endothelial cells. J Cell Biochem 71: 491-501.
38. Xu Y, Osborne BW, Stanton RC, (2005) Diabetes causes inhibition of glucose-6-phosphate dehydrogenase via activation of PKA, which contributes to oxidative stress in rat kidney cortex. Am J Physiol Renal Physiol 289: F1040-1047.
39. Costa Rosa LF, Curi R, Murphy C, Newsholme P, (1995) Effect of adrenaline and phorbol myristate acetate or bacterial lipopolysaccharide on stimulation of pathways of macrophage glucose, glutamine and O2 metabolism. Evidence for cyclic AMP-dependent protein kinase mediated inhibition of glucose-6-phosphate dehydrogenase and activation of NADP+-dependent 'malic' enzyme. Biochem J 310 (Pt 2) (): 709-714.
40. Frey RS, Ushio-Fukai M, Malik A, (2008) NADPH Oxidase-Dependent Signaling in Endothelial Cells: Role in Physiology and Pathophysiology. Antioxid Redox Signal.
41. Nauseef WM, (2008) Biological roles for the NOX family of NADPH oxidases. Journal of Biological Chemistry 283: 16961-16965.
42. Selemidis S, Sobey CG, Schmidt HH, Wingler K, Drummond GR, (2008) NADPH oxidases in the vasculature: Molecular features, roles in disease and pharmacological inhibition. Pharmacol Ther 120: 254-291.
43. Hwang J, Ing MH, Salazar A, Lassegue B, Griendling K, et al. (2003) Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: implication for native LDL oxidation. Circ Res 93: 1225-1232.
44. Bayraktutan U, Blayney L, Shah AM, (2000) Molecular characterization and localization of the NAD(P)H oxidase components gp91-phox and p22-phox in endothelial cells. Arterioscler Thromb Vasc Biol 20: 1903-1911.
45. Kim JS, Diebold BA, Babior BM, Knaus UG, Bokoch GM, (2007) Regulation of Nox1 activity via protein kinase A-mediated phosphorylation of NoxA1 and 14-3-3 binding. J Biol Chem 282: 34787-34800.
46. Muzaffar S, Jeremy JY, Sparatore A, Del Soldato P, Angelini GD, et al. (2008) H(2)S-donating sildenafil (ACS6) inhibits superoxide formation and gp91(phox) expression in arterial endothelial cells: role of protein kinases A and G. Br J Pharmacol 155: 984-994.
47. Muzaffar S, Shukla N, Bond M, Newby AC, Angelini GD, et al. (2008) Exogenous Hydrogen Sulfide Inhibits Superoxide Formation, NOX-1 Expression and Rac(1) Activity in Human Vascular Smooth Muscle Cells. J Vasc Res 45: 521-528.
48. Nogueira-Machado JA, Lima e Silva FC, Cunha EP, Calsolari MR, Costa DC, et al. (2006) Modulation of the production of reactive oxygen species (ROS) by cAMP-elevating agents in granulocytes from diabetic patients: an Akt/PKB-dependent phenomenon. Diabetes Metab 32: 331-335.
49. Leopold JA, Walker J, Scribner AW, Voetsch B, Zhang YY, et al. (2003) Glucose-6-phosphate dehydrogenase modulates vascular endothelial growth factor-mediated angiogenesis. J Biol Chem 278: 32100-32106.
50. Stanton RC, Seifter JL, (1988) Epidermal growth factor rapidly activates the hexose monophosphate shunt in kidney cells. Am J Physiol 254: C267-271.
51. Rask-Madsen C, King GL, (2008) Differential regulation of VEGF signaling by PKC-alpha and PKC-epsilon in endothelial cells. Arterioscler Thromb Vasc Biol 28: 919-924.
52. Greindling K, Minieri C, Ollerenshaw J, Alexander R, (1994) Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circulation Research 74: 1141-1148.