Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells

Journal of Clinical Investigation

Volumn 112, Issue 7, 2003, Pages 1049-1057

  Du, Xueliang ^a   Matsumura, Takeshi ^a   Edelstein, Diane ^a   Rossetti, Luciano ^a   Zsengellér, Zsuzsanna ^b   Szabó, Csaba ^b,c   Brownlee, Michael ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b INOTEK CORPORATION   (United States)

^c SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ADVANCED GLYCATION END PRODUCT; ANTISENSE OLIGODEOXYNUCLEOTIDE; COMPLEMENTARY DNA; DNA; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOSAMINE; INO 1001; MANGANESE SUPEROXIDE DISMUTASE; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE; ANTISENSE OLIGONUCLEOTIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SUPEROXIDE;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; AORTA; ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CATTLE; CONTROLLED STUDY; DIABETES MELLITUS; DNA STRAND BREAKAGE; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; HYPERGLYCEMIA; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; WESTERN BLOTTING; ANIMAL; CELL CULTURE; DIABETIC ANGIOPATHY; DNA DAMAGE; DRUG ANTAGONISM; METABOLISM; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANIMALS; CATTLE; CELLS, CULTURED; DIABETIC ANGIOPATHIES; DNA DAMAGE; ENDOTHELIUM, VASCULAR; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GLYCOSYLATION END PRODUCTS, ADVANCED; HEXOSAMINES; HYPERGLYCEMIA; MITOCHONDRIA; NF-KAPPA B; OLIGONUCLEOTIDES, ANTISENSE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN KINASE C; SUPEROXIDES;

EID: 85047691537     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI18127     Document Type: Article

References (46)

1. The Diabetes Control and Complications Trial Research Group. 1993. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N. Eng. J. Med. 329:977-986.
2. UK Prospective Diabetes Study (UKPDS) Group. 1998. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet. 352:837-853.
3. Wei, M., Gaskill, S.P., Haffner, S.M., and Stem, M.P. 1998. Effects of diabetes and level of glycemia on all-cause and cardiovascular mortality. The San Antonio Heart Study. Diabetes Care. 21:1167-1172.
4. Brownlee, M. 2001. Biochemistry and molecular cell biology of diabetic complications. Nature. 414:813-820.
5. Nishikawa, T., et al. 2000. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 404:787-790.
6. Du, X.L., et al. 2000. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc. Natl. Acad. Sci. U. S. A. 97:12222-12226.
7. Molina y Vedia, L., et al. 1992. Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation. J. Biol. Chem. 267:24929-24932.
8. McDonald, L.J., and Moss, J. 1993. Stimulation by nitric oxide of an NAD linkage to glyceraldehyde-3-phosphate dehydrogenase. Proc. Natl. Acad. Sci. U. S. A. 90:6238-6241.
9. Brune, B., and Lapetina, E.G. 1995. Protein thiol modification of glyceraldehyde-3-phosphate dehydrogenase as a target for nitric oxide signaling. Genet. Eng. (N. Y.). 17:149-164.
10. Garcia, S.F., et al. 2001. Diabetic endothelial dysfunction: the role of poly (ADP-ribose) polymerase activation. Nat. Med. 7:108-113.
11. Mabley, J.G., et al. 2001. Anti-inflammatory effects of a novel, potent inhibitor of poly (ADP-ribose) polymerase. Inflamm. Res. 50:561-569.
12. Jagtap, P., et al. 2002. Novel phenanthridinone inhibitors of poly (adenosine 5′-diphosphate-ribose) synthetase: potent cytoprotective and antishock agents. Crit. Care Med. 30:1071-1082.
13. Shimoda, K., et al. 2003. Effect of poly (ADP-ribose) synthetase inhibition on burn and smoke inhalation injury in the sheep. Am. J. Physiol. Lung Cell. Mol. Physiol. 285:L240-L249.
14. Khan, T.A., et al. 2003. Poly(ADP-ribose) synthetase inhibition improves postischemic myocardial function after cardioplegia-cardiopulmonary bypass. J. Am. Coll. Surg. 197:270-277.
15. Tao, Y., Howlett, A., and Klein, C. 1994. Nitric oxide regulation of glyceraldehyde-3-phosphate dehydrogenase activity in Dictyostelium discoideum cells and lysates. Eur. J. Biochem. 224:447-454.
16. Schraufstatter, I.U., Hinshaw, D.B., Hyslop, P.A., Spragg, R.G., and Cochrane, C.G. 1986. Oxidant injury of cells DNA strand-breaks activate polyadenosine diphosphate-ribose polymerase and lead to depletion of nicotinamide adenine dinucleotide. J. Clin. Invest. 77:1312-1320.
17. Rossetti, L., and Hu, M. 1993. Skeletal muscle glycogenolysis is more sensitive to insulin than is glucose transport/phosphorylation. Relation to the insulin-mediated inhibition of hepatic glucose production. J. Clin. Invest. 92:2963-2974.
18. Shinohara, M., et al. 1998. Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J. Clin. Invest. 101:1142-1147.
19. Hammes, H.P., et al. 2003. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat. Med. 9:294-299.
20. Kurose, I., et al. 1997. CD18/ICAM-1-dependent oxidative NF-κB activation leading to nitric oxide production in rat Kupffer cells cocultured with syngeneic hepatoma cells. J. Clin. Invest. 99:867-878.
21. Manna, S.K., Zhang, H.J., Yan, T., Oberley, L.W., and Aggarwal, B.B. 1998. Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-κB and activated protein-1. J. Biol. Chem. 273:13245-13254.
22. Virag, L., and Szabo, C. 2002. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 54:375-429.
23. Harnmes, H.P., Martin, S., Federlin, K., Geisen, K., and Brownlee, M. 1991. Aminoguanidine treatment inhibits the development of experimental diabetic retinopathy. Proc. Natl. Acad. Sci. U. S. A. 88:11555-11558.
24. Ishii, H., et al. 1996. Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor. Science. 272:728-731.
25. Lee, A.Y., Chung, S.K., and Chung, S.S. 1995. Demonstration that polyol accumulation is responsible for diabetic cataract by the use of transgenic mice expressing the aldose reductase gene in the lens. Proc. Natl. Acad. Sci. U. S. A. 92:2780-2784.
26. Nakamura, S., et al. 1997. Progression of nephropathy in spontaneous diabetic rats is prevented by OPB-9195, a novel inhibitor of advanced glycation. Diabetes. 46:895-899.
27. Soulis-Liparota, T., Cooper, M., Papazoglou, D., Clarke, B., and Jerums, G. 1991. Retardation by aminoguanidine of development of albuminutia, mesangial expansion, and tissue fluorescence in streptozocin-induced diabetic rat. Diabetes. 40:1328-1334.
28. Pieper, G.M., and Riaz-ul-Haq. 1997. Activation of nuclear factor-κB in cultured endothelial cells by increased glucose concentration: prevention by calphostin C. J. Cardiovasc. Pharmacol. 30:528-532.
29. Sirovet, M.A. 1997. Role of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in normal cell function and in cell pathology. J. Cell. Biochem. 66:133-140.
30. Mazzola, J.L., and Sirover, M.A. 2002. Alteration of intracellular structure and function of glyceraldehyde-3-phosphate dehydrogenase: a common phenotype of neurodegenerative disorders? Neurotoxicology. 23:603-609.
31. Sawa, A. 1997. Glyceraldehyde-3-phosphate dehydrogenase: nuclear translocation participates in neuronal and nonneuronal cell death. Proc. Natl. Acad. Sci. U. S. A. 94:11669-11674.
32. Schmitz, H.D. 2001. Reversible nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase upon serum depletion. Eur. J. Cell. Biol. 80:419-427.
33. Krynetski, E.Y. et al. 2003. A nuclear protein complex containing high mobility group proteins B1 and B2, heat shock cognate protein 70, ERp60, and glyceraldehyde-3-phosphate dehydrogenase is involved in the cytotoxic response to DNA modified by incorporation of anticancer nucleoside analogues. Cancer Res. 63:100-106.
34. Brune, B., and Lapetina, E.G. 1996. Nitric oxide-induced covalent modification of glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase. Methods Enzymol. 269:400-407.
35. Eliasson, M.J., et al. 1997. Poly (ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med. 3:1089-1095.
36. Ha, H.C., Hester, L.D., and Snyder, S.H. 2002. Poly (ADP-ribose) polymerase-1 dependence of stress-induced transcription factors and associated gene expression in glia. Proc. Natl. Acad. Sci. U. S. A. 99:3270-3275.
37. Hassa, P.O., Covic, M., Hasan, S., Imhof, R., and Hottiger, M.O. 2001. The enzymatic and DNA binding activity of PARP-1 are not required for NF-κB coactivator function. J. Biol. Chem. 276:45588-45597.
38. Pieper, A.A., et al. 2000. Myocardial postischemic injury is reduced by polyADPribose polymerase-1 gene disruption. Mol. Med. 6:271-282.
39. Pacher, P., et al. 2002. The role of poly (ADP-ribose) polymerase activation in the development of myocardial and endothelial dysfunction in diabetes. Diabetes. 51:514-521.
40. Soriano, F.G., Pacher, P., Mabley, J., Liaudet, L., and Szabo, C. 2001. Rapid reversal of the diabetic endothelial dysfunction by pharmacological inhibition of poly (ADP-ribose) polymerase. Circ. Res. 89:684-691.
41. Wakasaki, H., et al. 1997. Targeted overexpression of protein kinase C beta2 isoform in myocardium causes cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 94:9320-9325.
42. Beckman, J.A., Goldfine, A.B., Gordon, M.B., Garrett, L.A., and Creager, M.A. 2002. Inhibition of protein kinase C beta prevents impaired endothelium-dependent vasodilation caused by hyperglycemia in humans. Circ. Res. 90:107-111.
43. Du, X.L., et al. 2001. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J. Clin. Invest. 108:1341-1348. doi:10.1172/JCI200111235.
44. Koya, D., et al. 2000. Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J. 14:439-447.
45. Bucciarelli, L.G., et al. 2002. RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation. 106:2827-2835.
46. Park, L., et al. 1998. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat. Med. 4:1025-1031.