NADPH oxidase activation by hyperglycaemia in cardiomyocytes is independent of glucose metabolism but requires SGLT1

Cardiovascular Research

Volumn 92, Issue 2, 2011, Pages 237-246

  Balteau, Magali ^a   Tajeddine, Nicolas ^a   De Meester, Carole ^a   Ginion, Audrey ^a   Des Rosiers, Christine ^b   Brady, Nathan R ^c   Sommereyns, Caroline ^a   Horman, Sandrine ^a   Vanoverschelde, Jean Louis ^a   Gailly, Philippe ^a   Hue, Louis ^a,d   Bertrand, Luc ^a   Beauloye, Christophe ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b MONTREAL HEART INSTITUTE   (Canada)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d DE DUVE INSTITUTE   (Belgium)

Author keywords

Glucose metabolism; Glucotoxicity; NADPH oxidase; Oxidative stress; SGLT

Indexed keywords

6 AMINONICOTINAMIDE; ALPHA METHYLGLUCOSIDE; GLUCOSE; GUANOSINE TRIPHOSPHATE; N ACETYLGLUCOSAMINE; PHLORIZIN; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM GLUCOSE COTRANSPORTER 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CONTROLLED STUDY; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HEART MUSCLE CELL; HYPERGLYCEMIA; INSULIN RESISTANCE; MALE; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; RAT; UPREGULATION;

6-AMINONICOTINAMIDE; ACETYLGLUCOSAMINE; ANIMALS; CELL DEATH; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; GLUCOSE; GLYCOSYLATION; HYPERGLYCEMIA; INSULIN RESISTANCE; MALE; MEMBRANE GLYCOPROTEINS; MYOCYTES, CARDIAC; NADPH OXIDASE; PENTOSE PHOSPHATE PATHWAY; PHLORHIZIN; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SODIUM-GLUCOSE TRANSPORTER 1;

EID: 80054122252     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr230     Document Type: Article

References (43)

1. Vanoverschelde JL, Janier MF, Bakke JE, Marshall DR, Bergmann SR. Rate of glycolysis during ischemia determines extent of ischemic injury and functional recovery after reperfusion. Am J Physiol 1994;267:H1785-H1794. (Pubitemid 24363725)
2. Sodi-Pallares D, Testelli MR, Fishleder BL, Bisteni A, Medrano GA, Friedland C et al. Effects of an intravenous infusion of a potassium-glucose- insulin solution on the electrocardiographic signs of myocardial infarction. A preliminary clinical report. Am J Cardiol 1962;9:166-181.
3. Fath-Ordoubadi F, Beatt KJ. Glucose-insulin-potassium therapy for treatment of acute myocardial infarction: an overview of randomized placebo-controlled trials. Circulation 1997;96:1152-1156. (Pubitemid 27344217)
4. Mehta SR, Yusuf S, Diaz R, Zhu J, Pais P, Xavier D et al. Effect of glucose-insulin-potassium infusion on mortality in patients with acute ST-segment elevation myocardial infarction: the CREATE-ECLA randomized controlled trial. JAMA 2005;293:437-446.
5. Su H, Sun X, Ma H, Zhang HF, Yu QJ, Huang C et al. Acute hyperglycemia exacerbates myocardial ischemia/reperfusion injury and blunts cardioprotective effect of GIK. Am J Physiol Endocrinol Metab 2007;293:E629-E635. (Pubitemid 47358973)
6. Dyntar D, Sergeev P, Klisic J, Ambuhl P, Schaub MC, Donath MY. High glucose alters cardiomyocyte contacts and inhibits myofibrillar formation. J Clin Endocrinol Metab 2006;91:1961-1967.
7. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000;404:787-790. (Pubitemid 30212409)
8. Cai L, Li W, Wang G, Guo L, Jiang Y, Kang YJ. Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes 2002;51:1938-1948. (Pubitemid 34564309)
9. Fiordaliso F, Bianchi R, Staszewsky L, Cuccovillo I, Doni M, Laragione T et al. Antioxidant treatment attenuates hyperglycemia-induced cardiomyocyte death in rats. J Mol Cell Cardiol 2004;37:959-968. (Pubitemid 39446821)
10. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005;54:1615-1625. (Pubitemid 40770750)
11. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87:245-313. (Pubitemid 46209993)
12. Ceolotto G, Gallo A, Papparella I, Franco L, Murphy E, Iori E et al. Rosiglitazone reduces glucose-induced oxidative stress mediated by NAD(P)H oxidase via AMPKdependent mechanism. Arterioscler Thromb Vasc Biol 2007;27:2627-2633. (Pubitemid 350158915)
13. Quagliaro L, Piconi L, Assaloni R, Martinelli L, Motz E, Ceriello A. Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes 2003;52:2795-2804. (Pubitemid 37339710)
14. Gupte RS, Floyd BC, Kozicky M, George S, Ungvari ZI, Neito V et al. 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 2009;47:219-228.
15. Zuurbier CJ, Eerbeek O, Goedhart PT, Struys EA, Verhoeven NM, Jakobs C et al. Inhibition of the pentose phosphate pathway decreases ischemia-reperfusion- induced creatine kinase release in the heart. Cardiovasc Res 2004;62:145-153. (Pubitemid 38326820)
16. Kohler E, Barrach H, Neubert D. Inhibition of NADP dependent oxidoreductases by the 6-aminonicotinamide analogue of NADP. FEBS Lett 1970;6:225-228.
17. Hofgaard JP, Sigurdardottir KS, Treiman M. Protection by 6-aminonicotinamide against oxidative stress in cardiac cells. Pharmacol Res 2006;54:303-310. (Pubitemid 44233335)
18. Serpillon S, Floyd BC, Gupte RS, George S, Kozicky M, Neito V et al. 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 2009;297:H153-H162.
19. Banerjee SK, McGaffin KR, Pastor-Soler NM, Ahmad F. SGLT1 is a novel cardiac glucose transporter that is perturbed in disease states. Cardiovasc Res 2009;84: 111-118.
20. Bertrand L, Ginion A, Beauloye C, Hebert AD, Guigas B, Hue L et al. AMPK activation restores the stimulation of glucose uptake in an in vitro model of insulin-resistant cardiomyocytes via the activation of protein kinase B. Am J Physiol Heart Circ Physiol 2006; 291:H239-H250.
21. Bontemps F, Hue L, Hers HG. Phosphorylation of glucose in isolated rat hepatocytes. Sigmoidal kinetics explained by the activity of glucokinase alone. Biochem J 1978;174: 603-611.
22. Michal G. D-Glucose 6-phosphate and D-fructose 6-phosphate. In: Bergmeyer HU, ed. Methods of Enzymatic Analysis. Weinheim: Verlag Chemie; 1984. p191-198.
23. Keller D DK. Glycogen. In: Bergmeyer HU, ed. Methods of Enzymatic Analysis. Weinheim: Verlag Chemie; 1984. p11-18.
24. Bertrand L, Alessi DR, Deprez J, Deak M, Viaene E, Rider MH et al. Heart 6-phosphofructo-2-kinase activation by insulin results from Ser-466 and Ser-483 phosphorylation and requires 3-phosphoinositide-dependent kinase-1, but not protein kinase B. J Biol Chem 1999;274:30927-30933.
25. Akki A, Zhang M, Murdoch C, Brewer A, Shah AM. NADPH oxidase signaling and cardiac myocyte function. J Mol Cell Cardiol 2009;47:15-22.
26. Brandes RP. A radical adventure: the quest for specific functions and inhibitors of vascular NAPDH oxidases. Circ Res 2003;92:583-585. (Pubitemid 36417688)
27. Kuo M, Zilberfarb V, Gangneux N, Christeff N, Issad T. O-GlcNAc modification of FoxO1 increases its transcriptional activity: a role in the glucotoxicity phenomenon? Biochimie 2008;90:679-685.
28. Haltiwanger RS, Grove K, Philipsberg GA. Modulation of O-linked N-acetylglucosamine levels on nuclear and cytoplasmic proteins in vivo using the peptide O-GlcNAc-beta-Nacetylglucosaminidase inhibitor O-(2-acetamido-2-deoxy- D-glucopyranosylidene)amino-N-phenylcarbamate. J Biol Chem 1998;273:3611-3617. (Pubitemid 28109786)
29. Nishimura H, Zarnowski MJ, Simpson IA. Glucose transporter recycling in rat adipose cells. Effects of potassium depletion. J Biol Chem 1993;268:19246-19253. (Pubitemid 23270695)
30. Luiken JJ, Koonen DP, Willems J, Zorzano A, Becker C, Fischer Y et al. Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes 2002;51:3113-3119.
31. Wright EM, Loo DD, Hirayama BA. Biology of human sodium glucose transporters. Physiol Rev 2011;91:733-794.
32. Li Y, Li Y, Feng Q, Arnold M, Peng T. Calpain activation contributes to hyperglycaemia-induced apoptosis in cardiomyocytes. Cardiovasc Res 2009;84: 100-110.
33. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000;86:494-501. (Pubitemid 30165039)
34. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 2006;281:35137-35146. (Pubitemid 46036553)
35. Shen E, Li Y, Li Y, Shan L, Zhu H, Feng Q et al. Rac1 is required for cardiomyocyte apoptosis during hyperglycemia. Diabetes 2009;58:2386-2395.
36. Eggleston LV, Krebs HA. Regulation of the pentose phosphate cycle. Biochem J 1974; 138:425-435.
37. Fulop N, Marchase RB, Chatham JC. Role of protein O-linked N-acetyl-glucosamine in mediating cell function and survival in the cardiovascular system. Cardiovasc Res 2007; 73:288-297. (Pubitemid 44937687)
38. Ngoh GA, Facundo HT, Hamid T, Dillmann W, Zachara NE, Jones SP. Unique hexosaminidase reduces metabolic survival signal and sensitizes cardiac myocytes to hypoxia/reoxygenation injury. Circ Res 2009;104:41-49.
39. Jones SP. A bittersweet modification: O-GlcNAc and cardiac dysfunction. Circ Res 2005;96:925-926. (Pubitemid 40712790)
40. Champattanachai V, Marchase RB, Chatham JC. Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased protein-associated O-GlcNAc. Am J Physiol Cell Physiol 2007;292:C178-C187. (Pubitemid 46115129)
41. Luptak I, Yan J, Cui L, Jain M, Liao R, Tian R. Long-term effects of increased glucose entry on mouse hearts during normal aging and ischemic stress. Circulation 2007;116: 901-909. (Pubitemid 47300914)
42. O'Malley D, Reimann F, Simpson AK, Gribble FM. Sodium-coupled glucose cotransporters contribute to hypothalamic glucose sensing. Diabetes 2006;55:3381-3386. (Pubitemid 44923596)
43. Zhang M, Kho AL, Anilkumar N, Chibber R, Pagano PJ, Shah AM et al. Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 2006;113:1235-1243.