Roles of poly(ADP-ribose) polymerase activation in the pathogenesis of diabetes mellitus and its complications

Pharmacological Research

Volumn 52, Issue 1 SPEC. ISS., 2005, Pages 60-71

  Szabó, Csaba ^a,b  

^a INOTEK CORPORATION   (United States)

^b SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

Author keywords

Cardiomyopathy; Cytokines; Diabetes; Endothelium; Kidney; Neuropathy; Nitric oxide; Oxidative stress; Peroxynitrite; Poly(ADP ribose) polymerase; Retina

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DNA; GLUCOSE; INSULIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANTIOXIDANT ACTIVITY; AUTOIMMUNE DISEASE; BLOOD PRESSURE REGULATION; DIABETIC HYPERTENSION; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; DISEASE PREDISPOSITION; DNA DAMAGE; DNA STRAND BREAKAGE; DNA SYNTHESIS; DRUG INHIBITION; GLOMERULUS CAPILLARY; GLUCONEOGENESIS; GLYCATION; HUMAN; IMPAIRED GLUCOSE TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN SYNTHESIS; MITOCHONDRIAL MEMBRANE; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; QUALITY OF LIFE; RESPIRATORY CHAIN; REVIEW; VASCULAR ENDOTHELIUM;

EID: 19444377566     PISSN: 10436618     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phrs.2005.02.015     Document Type: Article

References (110)

1. L. Virág, and C. Szabó The therapeutic potential of poly(ADP-ribose) polymerase inhibitors Pharmacol Rev 54 2002 375 429
2. M.A. Atkinson, N.K. Maclaren, W.J. Riley, W.E. Winter, D.D. Fisk, and R.P. Spillar Are insulin autoantibodies markers for insulin-dependent diabetes mellitus? Diabetes 35 1986 894 898
3. S. Baekkeskov, H.J. Aanstoot, S. Christgau, A. Reetz, M. Solimena, and M. Cascalho Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase Nature 347 1990 151 156
4. C.C. Rerup Drugs producing diabetes through damage of the insulin secreting cells Pharmacol Rev 22 1970 485 518
5. A.A. Rossini, A.A. Like, W.L. Chick, M.C. Appel, and G.F. Cahill Jr. Studies of streptozotocin-induced insulitis and diabetes Proc Natl Acad Sci USA 74 1977 2485 2489
6. H. Kolb Mouse models of insulin dependent diabetes: low-dose streptozocin-induced diabetes and nonobese diabetic (NOD) mice Diab Metab Rev 3 1987 751 778
7. A.J. Bone, P.R. Hitchcock, D.J. Gwilliam, J.M. Cunningham, and J. Barley Insulitis and mechanisms of disease resistance: studies in an animal model of insulin dependent diabetes mellitus J Mol Med 77 1999 57 61
8. M. Prochazka, E.H. Leiter, D.V. Serreze, and D.L. Coleman Three recessive loci required for insulin-dependent diabetes in nonobese diabetic mice Science 237 1987 286 289
9. E.F. Lampeter, A. Signore, E.A. Gale, and P. Pozzilli Lessons from the NOD mouse for the pathogenesis and immunotherapy of human type 1 (insulin-dependent) diabetes mellitus Diabetologia 32 1989 703 708
10. L. Crisa, J.P. Mordes, and A. Rossini Autoimmune diabetes mellitus in the BB rat Diab Metab Rev 8 1992 4 37
11. R. Kleemann, H. Rothe, V. Kolb-Bachofen, Q.W. Xie, C. Nathan, and S. Martin Transcription and translation of inducible nitric oxide synthase in the pancreas of prediabetic BB rats FEBS Lett 328 1993 9 12
12. C. Suschek, K. Fehsel, K.D. Kroncke, A. Sommer, and V. Kolb-Bachofen Primary cultures of rat islet capillary endothelial cells. Constitutive and cytokine-inducible macrophagelike nitric oxide synthases are expressed and activities regulated by glucose concentration Am J Pathol 145 1994 685 695
13. C. Southern, D. Schulster, and I.C. Green Inhibition of insulin secretion by interleukin-1 beta and tumour necrosis factor-alpha via an l-arginine-dependent nitric oxide generating mechanism FEBS Lett 276 1990 42 44
14. J.A. Corbett, J.L. Wang, M.A. Sweetland, J.R. Lancaster Jr., and M.L. McDaniel Interleukin 1 beta induces the formation of nitric oxide by beta-cells purified from rodent islets of Langerhans. Evidence for the beta-cell as a source and site of action of nitric oxide J Clin Invest 90 1992 2384 2391
15. M. Flodstrom, B. Tyrberg, D.L. Eizirik, and S. Sandler Reduced sensitivity of inducible nitric oxide synthase-deficient mice to multiple low-dose streptozotocin-induced diabetes Diabetes 48 1999 706 713
16. A. Rabinovitch, W.L. Suarez-Pinzon, O. Sorensen, and R.C. Bleackley Inducible nitric oxide synthase (iNOS) in pancreatic islets of nonobese diabetic mice: identification of iNOS-expressing cells and relationships to cytokines expressed in the islets Endocrinology 137 1996 2093 2099
17. W.L. Suarez-Pinzon, C. Szabó, and A. Rabinovitch Development of autoimmune diabetes in NOD mice is associated with the formation of peroxynitrite in pancreatic islet beta-cells Diabetes 46 1997 907 911
18. W.L. Suarez-Pinzon, J.G. Mabley, K. Strynadka, R.F. Power, C. Szabó, and A. Rabinovitch An inhibitor of inducible nitric oxide synthase and scavenger of peroxynitrite prevents diabetes development in NOD mice J Autoimmun 16 2001 449 455
19. G. Wu Nitric oxide synthesis and the effect of aminoguanidine and NG-monomethyl-l-arginine on the onset of diabetes in the spontaneously diabetic BB rat Diabetes 44 1995 360 364
20. J.A. Corbett, M.A. Sweetland, J.L. Wang, J.R. Lancaster, and M.L. McDaniel Jr. Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans Proc Natl Acad Sci USA 90 1993 1731 1735
21. D.L. Eizirik, S. Sandler, N. Welsh, M. Cetkovic-Cvrlje, A. Nieman, and D.A. Geller Cytokines suppress human islet function irrespective of their effects on nitric oxide generation J Clin Invest 93 1994 1968 1974
22. M.S. Khatim, G.M. Bahr, K.A. Gumaa, and K. Behbehani Effect of recombinant IL-1 isomers on fetal and adult islet cell function and replication Diab Res 8 1988 25 29
23. I.C. Green, J.M. Cunningham, C.A. Delaney, M.R. Elphick, J.G. Mabley, and M.H. Green Effects of cytokines and nitric oxide donors on insulin secretion, cyclic GMP and DNA damage: relation to nitric oxide production Biochem Soc Trans 22 1994 30 37
24. J. Radons, B. Heller, A. Burkle, B. Hartmann, M.L. Rodriguez, and K.D. Kroncke Nitric oxide toxicity in islet cells involves poly(ADP-ribose) polymerase activation and concomitant NAD+ depletion Biochem Biophys Res Commun 199 1994 1270 1277
25. K. Fehsel, A. Jalowy, S. Qi, V. Burkart, B. Hartmann, and H. Kolb Islet cell DNA is a target of inflammatory attack by nitric oxide Diabetes 42 1993 496 500
26. J.L. Bolaffi, G.G. Rodd, J. Wang, and G.M. Grodsky Interrelationship of changes in islet nicotine adeninedinucleotide, insulin secretion, and cell viability induced by interleukin-1 beta Endocrinology 134 1994 537 542
27. C.A. Delaney, M.H. Green, J.E. Lowe, and I.C. Green Endogenous nitric oxide induced by interleukin-1 beta in rat islets of Langerhans and HIT-T15 cells causes significant DNA damage as measured by the 'comet' assay FEBS Lett 333 1993 291 295
28. C.A. Delaney, D. Pavlovic, A. Hoorens, D.G. Pipeleers, and D.L. Eizirik Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells Endocrinology 138 1997 2610 2614
29. K.D. Kroncke, J. Funda, B. Berschick, H. Kolb, and V. Kolb-Bachofen Macrophage cytotoxicity towards isolated rat islet cells: neither lysis nor its protection by nicotinamide are beta-cell specific Diabetologia 34 1991 232 238
30. H. Kaneto, J. Fujii, H.G. Seo, K. Suzuki, T. Matsuoka, and M. Nakamura Apoptotic cell death triggered by nitric oxide in pancreatic beta-cells Diabetes 44 1995 733 738
31. J.M. Cunningham, J.G. Mabley, C.A. Delaney, and I.C. Green The effect of nitric oxide donors on insulin secretion, cyclic GMP and cyclic AMP in rat islets of Langerhans and the insulin-secreting cell lines HIT-T15 and RINm5F Mol Cell Endocrinol 102 1994 23 29
32. D.L. Eizirik, C.A. Delaney, M.H. Green, J.M. Cunningham, J.R. Thorpe, and D.G. Pipeleers Nitric oxide donors decrease the function and survival of human pancreatic islets Mol Cell Endocrinol 118 1996 71 83
33. V. Hadjivassiliou, M.H. Green, R.F. James, S.M. Swift, and H.A. Clayton Green IC insulin secretion, DNA damage, and apoptosis in human and rat islets of Langerhans following exposure to nitric oxide, peroxynitrite, and cytokines Nitric Oxide 2 1998 429 441
34. B. Heller, A. Burkle, J. Radons, E. Fengler, A. Jalowy, and M. Muller Analysis of oxygen radical toxicity in pancreatic islets at the single cell level Biol Chem Hoppe Seyler 375 1994 597 602
35. Y. Uchigata, H. Yamamoto, A. Kawamura, and H. Okamoto Protection by superoxide dismutase, catalase, and poly(ADP-ribose) synthetase inhibitors against alloxan- and streptozotocin-induced islet DNA strand breaks and against the inhibition of proinsulin synthesis J Biol Chem 257 1982 6084 6088
36. C. Szabó, and V.L. Dawson Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion Trends Pharmacol Sci 19 1998 287 298
37. P.S. Schein, D.A. Cooney, and M.L. Vernon The use of nicotinamide to modify the toxicity of streptozotocin diabetes without loss of antitumor activity Cancer Res 27 1967 2324 2332
38. H. Yamamoto, and H. Okamoto Protection by picolinamide, a novel inhibitor of poly (ADP-ribose) synthetase, against both streptozotocin-induced depression of proinsulin synthesis and reduction of NAD content in pancreatic islets Biochem Biophys Res Commun 95 1980 474 481
39. Y. Uchigata, H. Yamamoto, A. Kawamura, and H. Okamoto Protection by superoxide dismutase, catalase, and poly(ADP-ribose) synthetase inhibitors against alloxan- and streptozotocin-induced islet DNA strand breaks and against the inhibition of proinsulin synthesis J Biol Chem 257 1982 6084 6088
40. H. Okamoto, and H. Yamamoto DNA strand breaks and poly(ADP-ribose) synthetase activation in pancreatic islets - a new aspect to development of insulin-dependent diabetes and pancreatic B-cell tumors Princess Takamatsu Symp 13 1983 297 308
41. P. Masiello, T.L. Cubeddu, G. Frosina, and E. Bergamini Protective effect of 3-aminobenzamide, an inhibitor of poly(ADP-ribose) synthetase, against streptozotocin-induced diabetes Diabetologia 28 1985 683 686
42. P. Masiello, M. Novelli, V. Fierabracci, and E. Bergamini Protection by 3-aminobenzamide and nicotinamide against streptozotocin-induced beta-cell toxicity in vivo and in vitro Res Commun Chem Pathol Pharmacol 69 1990 17 32
43. K. Shima, M. Hirota, M. Sato, S. Numoto, and I. Oshima Effect of poly(ADP-ribose) synthetase inhibitor administration to streptozotocin-induced diabetic rats on insulin and glucagon contents in their pancreas Diab Res Clin Pract 3 1987 135 142
44. O. Bouix, M. Reynier, R. Guintrand-Hugret, and A. Orsetti Protective effect of gamma-hydroxybutyrate and nicotinamide on low-dose streptozotocin-induced diabetes in mice Horm Metab Res 27 1995 216 220
45. J. Mendola, J.R. Wright Jr., and P.E. Lacy Oxygen free-radical scavengers and immune destruction of murine islets in allograft rejection and multiple low-dose streptozocin-induced insulitis Diabetes 38 1989 379 385
46. J.G. Mabley, P. Jagtap, M. Perretti, S.J. Getting, A.L. Salzman, and L. Virag Anti-inflammatory effects of a novel, potent inhibitor of poly (ADP-ribose) polymerase Inflamm Res 50 2001 561 569
47. K. Yamada, K. Nonaka, T. Hanafusa, A. Miyazaki, H. Toyoshima, and S. Tarui Preventive and therapeutic effects of large-dose nicotinamide injections on diabetes associated with insulitis. An observation in nonobese diabetic (NOD) mice Diabetes 31 1982 749 753
48. S. Reddy, N.J. Bibby, and R.B. Elliott Early nicotinamide treatment in the NOD mouse: effects on diabetes and insulitis suppression and autoantibody levels Diab Res 15 1990 95 102
49. H. Nakajima, K. Yamada, T. Hanafusa, H. Fujino-Kurihara, J. Miyagawa, and A. Miyazaki Elevated antibody-dependent cell-mediated cytotoxicity and its inhibition by nicotinamide in the diabetic NOD mouse Immunol Lett 12 1986 91 94
50. B.A. O'Brien, B.V. Harmon, D.P. Cameron, and D.J. Allan Nicotinamide prevents the development of diabetes in the cyclophosphamide-induced NOD mouse model by reducing beta-cell apoptosis J Pathol 191 2000 86 92
51. G. Papaccio, E. Ammendola, and F.A. Pisanti Nicotinamide decreases MHC class II but not MHC class I expression and increases intercellular adhesion molecule-1 structures in non-obese diabetic mouse pancreas J Endocrinol 160 1999 389 400
52. C. Szabó, L.H. Lim, S. Cuzzocrea, S.J. Getting, B. Zingarelli, and R.J. Flower Inhibition of poly (ADP-ribose) synthetase attenuates neutrophil recruitment and exerts antiinflammatory effects J Exp Med 186 1997 1041 1049
53. J.Y. Kim, J.K. Chi, E.J. Kim, S.Y. Park, Y.W. Kim, and S.K. Lee Inhibition of diabetes in non-obese diabetic mice by nicotinamide treatment for 5 weeks at the early age J Korean Med Sci 12 1997 293 297
54. W.L. Suarez-Pinzon, J.G. Mabley, R. Power, C. Szabó, and A. Rabinovitch Poly(ADP-ribose) polymerase inhibition prevents spontaneous and recurrent autoimmune diabetes in NOD mice by inducing apoptosis of islet-infiltrating leukocytes Diabetes 52 2003 1683 1688
55. B.A. O'Brien, B.V. Harmon, D.P. Cameron, and D.J. Allan Beta-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model J Pathol 178 1996 176 181
56. B.A. O'Brien, B.V. Harmon, D.P. Cameron, and D.J. Allan Apoptosis is the mode of beta-cell death responsible for the development of IDDM in the nonobese diabetic (NOD) mouse Diabetes 46 1997 750 757
57. J.G. Mabley, W.L. Suarez-Pinzon, G. Hasko, A.L. Salzman, A. Rabinovitch, and E. Kun Inhibition of poly (ADP-ribose) synthetase by gene disruption or inhibition with 5-iodo-6-amino-1,2-benzopyrone protects mice from multiple-low-dose-streptozotocin-induced diabetes Br J Pharmacol 133 2001 909 919
58. D. Ferraris, R.P. Ficco, D. Dain, M. Ginski, S. Lautar, and K. Lee-Wisdom Design and synthesis of poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors. Part 4: biological evaluation of imidazobenzodiazepines as potent PARP-1 inhibitors for treatment of ischemic injuries Bioorg Med Chem 11 2003 3695 3707
59. S. Takasawa, and H. Okamoto Pancreatic beta-cell death, regeneration and insulin secretion: roles of poly(ADP-ribose) polymerase and cyclic ADP-ribose Int J Exp Diab Res 3 2002 79 96
60. G.L. Wilson, N.J. Patton, J.M. McCord, D.W. Mullins, and B.T. Mossman Mechanisms of streptozotocin- and alloxan-induced damage in rat B cells Diabetologia 27 1984 587 591
61. C. Szabó, L. Virag, S. Cuzzocrea, G.S. Scott, P. Hake, and M.P. O'Connor Protection against peroxynitrite-induced fibroblast injury and arthritis development by inhibition of poly(ADP-ribose) synthase Proc Natl Acad Sci USA 95 1998 3867 3872
62. B. Heller, Z.Q. Wang, E.F. Wagner, J. Radons, A. Burkle, and K. Fehsel Inactivation of the poly(ADP-ribose) polymerase gene affects oxygen radical and nitric oxide toxicity in islet cells J Biol Chem 270 1995 11176 11180
63. Z.Q. Wang, B. Auer, L. Stingl, H. Berghammer, D. Haidacher, and M. Schweiger Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease Genes Dev 9 1995 509 520
64. V. Burkart, Z.Q. Wang, J. Radons, B. Heller, Z. Herceg, and L. Stingl Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozotocin Nat Med 5 1999 314 319
65. M. Masutani, H. Suzuki, N. Kamada, M. Watanabe, O. Ueda, and T. Nozaki Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes Proc Natl Acad Sci USA 96 1999 2301 2304
66. A.A. Pieper, D.J. Brat, D.K. Krug, C.C. Watkins, A. Gupta, and S. Blackshaw Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes Proc Natl Acad Sci USA 96 1999 3059 3064
67. C. Gonzalez, J. Menissier De Murcia, P. Janiak, J.P. Bidouard, C. Beauvais, and S. Karray Unexpected sensitivity of nonobese diabetic mice with a disrupted poly(ADP-ribose) polymerase-1 gene to streptozotocin-induced and spontaneous diabetes Diabetes 51 2002 1470 1476
68. E.A. Gale, P.J. Bingley, C.L. Emmett, and T. Collier European Nicotinamide Diabetes Intervention Trial (ENDIT) Group. European Nicotinamide Diabetes Intervention Trial (ENDIT): a randomised controlled trial of intervention before the onset of type 1 diabetes Lancet 363 2004 925 931
69. A.E. Caballero, S. Arora, R. Saouaf, S.C. Lim, P. Smakowski, and J.Y. Park Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes Diabetes 48 1999 1856 1862
70. H. Cai, and D.G. Harrison Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress Circ Res 87 2000 840 844
71. J. Calles-Escandon, and M. Cipolla Diabetes and endothelial dysfunction: a clinical perspective Endocr Rev 22 2001 36 52
72. F. Cosentino, and T.F. Luscher Endothelial dysfunction in diabetes mellitus J Cardiovasc Pharmacol 32 1998 S54 S61
73. J.A. Beckman Inhibition of protein kinase C beta prevents impaired endothelium-dependent vasodilation caused by hyperglycemia in humans Circ Res 90 2002 107 111
74. M. Brownlee Biochemistry and molecular cell biology of diabetic complications Nature 414 2001 813 820
75. A. Ceriello New insights on oxidative stress and diabetic complications may lead to a "causal" antioxidant therapy Diab Care 26 2003 1589 1596
76. F. Garcia Soriano, L. Virág, P. Jagtap, É. Szabó, J.G. Mabley, and L. Liaudet Diabetic endothelial dysfunction: the role of poly (ADP-ribose) polymerase activation Nat Med 7 2001 108 113
77. K.S. Park, J.H. Kim, M.S. Kim, J.M. Kim, S.K. Kim, and J.Y. Choi Effects of insulin and antioxidant on plasma 8-hydroxyguanine and tissue 8-hydroxydeoxyguanosine in streptozotocin-induced diabetic rats Diabetes 50 2001 2837 2841
78. D. Anderson, T.W. Yu, J. Wright, and C. Ioannides An examination of DNA strand breakage in the comet assay and antioxidant capacity in diabetic patients Mutat Res 398 1998 151 161
79. S. Astley, A. Langrish-Smith, S. Southon, M. Sampson, and Vitamin E supplementation and oxidative damage to DNA and plasma LDL in type 1 diabetes Diab Care 22 1999 1626 1631
80. Y. Dincer, T. Akcay, H. Ilkova, Z. Alademir, and G. Ozbay DNA damage and antioxidant defense in peripheral leukocytes of patients with Type I diabetes mellitus Mutat Res 527 2003 49 55
81. F.G. Soriano, J.G. Mabley, P. Pacher, L. Liaudet, and C. Szabó Rapid reversal of the diabetic endothelial dysfunction by pharmacological inhibition of poly(ADP-ribose) polymerase Circ Res 89 2001 684 691
82. P. Pacher, L. Liaudet, F.G. Soriano, J.G. Mabley, É. Szabó, and C. Szabó The role of poly(ADP-ribose) polymerase in the development of myocardial and endothelial dysfunction in diabetes mellitus Diabetes 51 2002 514 521
83. Y. Fukuda, H. Teragawa, K. Matsuda, T. Yamagata, H. Matsuura, and K. Chayama Tetrahydrobiopterin restores endothelial function of coronary arteries in patients with hypercholesterolaemia Heart 87 2002 264 269
84. T.J. Guzik, N.E. West, E. Black, D. McDonald, C. Ratnatunga, and R. Pillai Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors Circ Res 86 2000 85 90
85. M. Pannirselvam, S. Verma, T.J. Anderson, and C.R. Triggle Cellular basis of endothelial dysfunction in small mesenteric arteries from spontaneously diabetic (db/db -/-) mice: role of decreased tetrahydrobiopterin bioavailability Br J Pharmacol 136 2002 255 263
86. L. Piconi, L. Quagliaro, R. Da Ros, R. Assaloni, D. Giugliano, and K. Esposito Intermittent high glucose enhances ICAM-1, VCAM-1, E-selectin and interleukin-6 expression in human umbilical endothelial cells in culture: the role of poly(ADP-ribose)polymerase J Thromb Haemost 2 2004 1453 1459
87. X. Du, T. Matsumura, D. Edelstein, L. Rossetti, Z. Zsengeller, and C. Szabó Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells J Clin Invest 112 2003 1049 1057
88. Z. Zsengeller, J.G. Mabley, and C. Szabó High glucose induced endothelial dysfunction: mitochondrial uncoupling inhibits DNA single strand breakage and PARP activation FASEB J 18 2004 A1185
89. D.S. Bell Heart failure: the frequent, forgotten, and often fatal complication of diabetes Diab Care 26 2003 2433 2441
90. B.V. Bui, J.A. Armitage, M. Tolcos, M.E. Cooper, and A.J. Vingrys ACE inhibition salvages the visual loss caused by diabetes Diabetologia 46 2003 401 408
91. H. Cai, K.K. Griendling, and D.G. Harrison The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases Trends Pharmacol Sci 24 2003 471 478
92. M.J. Mihm, S.K. Wattanapitayakul, S.F. Piao, D.G. Hoyt, and J.A. Bauer Effects of angiotensin II on vascular endothelial cells: formation of receptor-mediated reactive nitrogen species Biochem Pharmacol 65 2003 1189 1197
93. S.K. Wattanapitayakul, D.M. Weinstein, B.J. Holycross, and J.A. Bauer Endothelial dysfunction and peroxynitrite formation are early events in angiotensin-induced cardiovascular disorders FASEB J 14 2000 271 278
94. C. Szabó, P. Pacher, Z. Zsengeller, A. Vaslin, K. Komjati, and R. Benko Angiotensin II-mediated endothelial dysfunction: role of poly(ADP-ribose) polymerase activation Mol Med 10 2004 28 35
95. C. Szabó, A. Zanchi, K. Komjati, P. Pacher, A.S. Krolewski, and W.C. Quist Poly(ADP-ribose) polymerase is activated in subjects at risk of developing type 2 diabetes and is associated with impaired vascular reactivity Circulation 106 2002 2680 2686
96. C.Y. Xiao, M. Chen, Z. Zsengellér, and C. Szabó Poly(ADP-ribose) polymerase contributes to the development of myocardial infarction in diabetic rats and regulates the nuclear translocation of apoptosis-inducing factor J Pharmacol Exp Ther 310 2004 498 504
97. B. Zingarelli, A.L. Salzman, and C. Szabó Genetic disruption of poly (ADP ribose) synthetase inhibits the expression of P-selectin and intercellular adhesion molecule-1 in myocardial ischemia-reperfusion injury Circ Res 83 1998 85 94
98. E. Szabó, T.S. Kern, L. Virag, J. Mabley, and C. Szabó Evidence for poly(ADP-ribose) polymerase activation in the diabetic retina FASEB J 15 2001 A942
99. I.G. Obrosova, A.G. Minchenko, R.N. Frank, G.M. Seigel, Z. Zsengeller, and P. Pacher Poly(ADP-ribose) polymerase inhibitors counteract diabetes- and hypoxia-induced retinal vascular endothelial growth factor (VEGF) overexpression Int J Mol Med 14 2004 55 64
100. L. Zheng, C. Szabó, and T.S. Kern Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-kappaB Diabetes 53 2004 2960 2967
101. J.G. Mabley, Y. Feng, F. Hagen, J. Lin, M. Brownlee, and C. Szabó Poly(ADP-ribose) polymerase and diabetic retinopathy FASEB J 18 2004 A1189
102. G. Wahlberg, L.A. Carlson, J. Wasserman, and A. Ljungqvist Protective effect of nicotinamide against nephropathy in diabetic rats Diab Res 2 1985 307 312
103. A.G. Minchenko, M.J. Stevens, L. White, O.I. Abatan, K. Komjáti, and P. Pacher Diabetes-induced overexpression of endothelin-1 and endothelin receptors in the rat renal cortex is mediated via poly(ADP-ribose) polymerase activation FASEB J 17 2003 1514 1516
104. F. Li, C. Szabó, P. Pacher, G.J. Southan, O.I. Abatan, and T. Charniauskaya Evaluation of orally actrive poly(ADP-ribose) polymerase inhibitor in streptozotocin-diabetic rat model of early peripheral neuropathy Diabetologia 47 2004 710 717
105. I.G. Obrosova, F. Li, O.I. Abatan, K. Komjáti, P. Pacher, and C. Szabó Role for poly (ADP-ribose) polymerase activation in diabetic neuropathy Diabetes 53 2004 711 720
106. T. Kuchmerovska, I. Shymanskyy, G. Donchenko, M. Kuchmerovskyy, L. Pakirbaieva, and A. Klimenko Poly(ADP-ribosyl)ation enhancement in brain cell nuclei is associated with diabetic neuropathy J Diab Complications 18 2004 198 204
107. S. Cuzzocrea, B. Pisano, L. Dugo, A. Ianaro, P. Maffia, and N.S. Patel Rosiglitazone, a ligand of the peroxisome proliferator activated receptor-gamma, reduces acute inflammation Eur J Pharmacol 483 2004 79 93
108. R. Da Ros, R. Assaloni, and A. Ceriello The preventive anti-oxidant action of thiazolidinediones: a new therapeutic prospect in diabetes and insulin resistance Diab Med 21 2004 1249 1252
109. I.G. Obrosova, M.J. Stevens, P. Pacher, Z. Zsengeller, D. Larkin, and C. Szabó Aldose reductase inhibition counteracts oxidative/nitrosative stress and poly(ADP-ribose) polymerase activation in two tissue-sites for diabetic complications FASEB J 18 2004 A1186
110. C. Szabó, J.G. Mabley, S.M. Moeller, R. Shimanovich, P. Pacher, and L. Virag Pathogenetic role of peroxynitrite in the development of diabetes and diabetic vascular complications: studies with FP15, a novel potent peroxynitrite decomposition catalyst Mol Med 8 2002 571 580