Poly(ADP-ribose) polymerase activation in the reperfused myocardium

Cardiovascular Research

Volumn 61, Issue 3, 2004, Pages 471-480

  Szabó, Gábor ^a   Liaudet, Lucas ^b   Hagl, Siegfried ^a   Szabó, Csaba ^b,c  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b INOTEK CORPORATION   (United States)

^c SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

Author keywords

Heart; Oxidative stress; Peroxynitrite; Poly(ADP ribose) polymerase; Reperfusion injury

Indexed keywords

3 AMINOBENZAMIDE; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR;

CELL METABOLISM; CYTOTOXICITY; DNA STRAND BREAKAGE; ENERGY CONSUMPTION; ENZYME ACTIVATION; HEART MUSCLE INJURY; HEART MUSCLE REPERFUSION; HUMAN; INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; TISSUE INJURY;

ANIMALS; CELLS, CULTURED; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; MODELS, ANIMAL; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NIACINAMIDE; POLY(ADP-RIBOSE) POLYMERASES;

EID: 1142285446     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2003.09.029     Document Type: Review

References (78)

1. de Murcia G., Menissier de Murcia J. Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci. 19:1994;172-176.
2. de Murcia G., Schreiber V., Molinete M.et al. Structure and function of poly(ADP-ribose) polymerase. Mol. Cell. Biochem. 138:1994;15-24.
3. de Murcia J.M., Niedergang C., Trucco C.et al. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc. Natl. Acad. Sci. U. S. A. 94:1997;7303-7307.
4. Schreiber V., Hunting D., Trucco C.et al. A dominant-negative mutant of human poly(ADP-ribose) polymerase affects cell recovery, apoptosis and sister chromatid exchange following DNA damage. Proc. Natl. Acad. Sci. U. S. A. 92:1995;4753-4757.
5. Hauschildt S., Scheipers P., Bessler W.G., Mulsch A. Induction of nitric oxide synthase in L929 cells by tumour-necrosis factor alpha is prevented by inhibitors of poly(ADP-ribose) polymerase. Biochem. J. 288:1992;255-600.
6. Szabo C., Virag L., Cuzzocrea S.et al. Protection against peroxynitrite-induced fibroblast injury and arthritis development by inhibition of poly(ADP-ribose) synthase. Proc. Natl. Acad. Sci. U. S. A. 95:1998;3867-3872.
7. Le Page C., Sanceau J., Drapier J.C., Wietzerbin J. Inhibitors of ADP-ribosylation impair inducible nitric oxide synthase gene transcription through inhibition of NF kappa B activation. Biochem. Biophys. Res. Commun. 243:1998;451-457.
8. Oliver F.J., Menissier de Murcia J., Nacci C.et al. Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly(ADP-ribose) polymerase-1 deficient mice. EMBO J. 18:1999;4446-4454.
9. Zingarelli B., Salzman A.L., Szabó C. Genetic disruption of poly(ADP-ribose) synthetase inhibits the expression of P-selectin and intracellular adhesion molecule-1 in myocardial ischemia/reperfusion injury. Circ. Res. 83:1998;85-97.
10. Szabó G., Bährle S., Stumpf N.et al. Poly(ADP-ribose) polymerase inhibition reduces reperfusion injury after heart transplantation. Circ. Res. 90:2002;100-106.
11. Otsuka A., Hanafusa T., Miyagawa J., Kono N., Tarui S. Nicotinamide and 3-aminobenzamide reduce interferon-gamma-induced class II MHC (HLA-DR and -DP) molecule expression on cultured human endothelial cells and fibroblasts. Immunopharmacol. Immunotoxicol. 13:1991;263-280.
12. Berger N.A., Sims J.L., Catino D.M., Berger S.J. Poly(ADP-ribose) polymerase mediates the suicide response to massive DNA damage: studies in normal and DNA-repair defective cells. Princess Takamatsu Symp. 13:1983;219-226.
13. Schraufstatter I.U., Hyslop P.A., Jackson J., Revak S.D., Cochrane C.C. Oxidant and protease injury of the lung. Bull. Eur. Physiopathol. Respir. 23:1987;297-302.
14. Sims J.L., Benjamin R.C. Alteration of poly(adenosine diphosphoribose) metabolism by ethanol: mechanism of action. Arch. Biochem. Biophys. 253:1987;357-366.
15. Tanuma S.I., Enomoto T., Yamada M.A. Changes in the level of poly ADP-ribosylation during a cell cycle. Exp. Cell. Res. 117:1978;421-430.
16. Kanai Y., Tanuma S., Sugimura T. Immunofluorescent staining of poly(ADP-ribose) in situ in HeLa cell chromosomes in the M phase. Proc. Natl. Acad. Sci. U. S. A. 78:1981;2801-2804.
17. Leduc Y., Lawrence J.J., de Murcia G., Poirier G.G. Cell cycle regulation of poly(ADP-ribose) synthetase in FR3T3 cells. Biochim. Biophys. Acta. 968:1988;275-282.
18. Bakondi E., Bai P., Bak I.et al. Role of poly(ADP-ribose) polymerase in contact hypersensitivity (Abstract). FASEB J. 16:2002;A674.
19. Freude B., Masters T.N., Robicsek F.et al. Apoptosis is initiated by myocardial ischemia and executed during reperfusion. J. Mol. Cell. Cardiol. 32:2000;197-208.
20. De Boer R.A., van Veldhuisen D.J., van Der Wijk J.et al. Additional use of immunostaining for active caspase 3 and cleaved actin and PARP fragments to detect apoptosis in patients with chronic heart failure. J. Card. Fail. 6:2000;330-337.
21. Virag L., Scott G.S., Cuzzocrea S., Marmer D., Salzman A.L., Szabo C. Peroxynitrite-induced thymocyte apoptosis: the role of caspases and poly(ADP-ribose) synthetase (PARS) activation. Immunology. 94:1998;345-355.
22. Herceg Z., Wang Z.Q. Failure of poly(ADP-ribose) polymerase cleavage by caspases leads to induction of necrosis and enhanced apoptosis. Mol. Cell. Biol. 19:1999;5124-5133.
23. Virág L., Szabó C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 54:2002;375-429.
24. Bowes J., Piper J., Thiemermann C. Inhibitors of the activity of poly(ADP-ribose) synthetase reduce the cell death caused by hydrogen peroxide in human cardiac myoblasts. Br. J. Pharmacol. 124:1998;1760-1766.
25. Flaherty J.T. Myocardial injury mediated by oxygen free radicals. Am. J. Med. 91:1991;3C79S-3C85S.
26. Kukreja R.C., Hess M.L. The oxygen free radical system: from equations through membrane-protein interaction to cardiovascular injury and protection. Cardiovasc. Res. 6:1992;641-655.
27. Wang P.H., Zweier J.L. Measurement of nitric oxide and peroxyntrite in the postischemic heart. Evidence for peroxynitrite mediated reperfusion injury. J. Biol. Chem. 271:1996;29223-29230.
28. Soriano F.G., Virag L., Jagtap P.et al. Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nat. Med. 7:2001;108-113.
29. Ferraris D., Ko Y.S., Pahutski T.et al. Design and synthesis of poly ADP-ribose polymerase-1 inhibitors: 2. Biological evaluation of aza-5[H]-phenanthridin-6-ones as potent, aqueous-soluble compounds for the treatment of ischemic injuries. J. Med. Chem. 46:2003;3138-3151.
30. Cosi C. New inhibitors of poly(ADP-ribose) polymerase and their potential therapeutic targets. Expert Opin. Ther. Pat. 12:2002;1047-1071.
31. Wayman Z., McDonald M.C., Thompson A.S., Threadgill M.D., Thiemermann C. 5-Aminoisoquinolinone, a potent inhibitor of poly(adenosine 5′- diphosphate ribose) polymerase, reduces myocardial infarct size. Eur. J. Pharmacol. 430:2001;93-100.
32. Faro R., Toyoda Y., McCully J.et al. Protective effect on regional myocardial function and infarct size induced by PJ34: a novel poly(ADP-ribose) synthetase inhibitor. Ann. Thorac. Surg. 73:2002;575-581.
33. Szabó G., Andrási T.B., Buhmann V.et al. Poly(ADP-ribose) polymerase (PARP) inhibition protects against myocardial and endothelial injury after hypothermic cardiac arrest. Circulation. 106(Suppl. I):2003;377-378. [Abstract].
34. Liaudet L., Szabó E., Timashpolsky L., Virág L., Cziráki A., Szabó C. Localizationof poly(ADP-ribose) polymerase (PARP) activation in a rat model of myocardial reperfusion injury: suppression of PARP activation and long-term morphological and functional improvement by 3-aminobenzamide. Br. J. Pharmacol. 133:2001;1424-1430.
35. Pieper A.A., Walles T., Wei G.et al. Myocardial postischemic injury is reduced by poly(ADP-ribose) polymerase-1 gene disruption. Mol. Med. 6:2000;271-282.
36. Yang Z., Zingarelli B., Szabo C. Effect of genetic disruption of poly(ADP-ribose) synthetase on delayed production of inflammatory mediators and delayed necrosis during myocardial ischemia-reperfusion injury. Shock. 13:2000;60-66.
37. Szabados E., Literati-Nagy P., Farkas B., Sumegi B. BGP-15, a nicotinic amidoxime derivate protecting heart from ischemia reperfusion injury through modulation of poly(ADP-ribose) polymerase. Biochem. Pharmacol. 59:2000;937-945.
38. Gilad E., Zingarelli B., Salzman A.L., Szabo C. Protection by inhibition of poly(ADP-ribose) synthetase against oxidant injury in cardiac myoblasts in vitro. J. Mol. Cell. Cardiol. 29:1997;2585-2597.
39. Bowes J., McDonald M.C., Piper J., Thiemermann C. Inhibitors of poly(ADP-ribose) synthetase protect rat cardiomyocytes against oxidant stress. Cardiovasc. Res. 41:1999;126-134.
40. Uchiyama T., Otani H., Okada T.et al. Nitric oxide induces caspase-dependent apoptosis and necrosis in neonatal rat cardiac myocytes. J. Mol. Cell. Cardiol. 34:2002;1049-1061.
41. Junod A.F., Jornot L., Petersen H. Differential effects of hyperoxia and hydrogen peroxide on DNA damage, polyadenosine diphosphate-ribose polymerase activity and nicotineamide adenine dinucleotide and adenosisne triphosphate contents in cultured endothelial cells and fibroblasts. J. Cell. Physiol. 140:1989;177-185.
42. Kirkland J.B. Lipid peroxidation, protein thiol oxidation and DNA damage hydrogen peroxide-induced injury to endothelial cells: role of activation of poly(ADP-ribose) polymerase. Biochim. Biophys. Acta. 1092:1994;319-325.
43. Zingarelli B., Cuzzocrea S., Zsengeller Z., Salzman A.L., Szabó C. Inhibition of poly(ADP ribose) synthetase protects against myocardial ischemia and reperfusion injury. Cardiovasc. Res. 36:1997;205-215.
44. Sharp C., Warren A., Oshima T., Williams L., Li J.H., Alexander J.S. Poly ADP ribose-polymerase inhibitors prevent the upregulation of ICAM-1 and E-selectin in response to Th1 cytokine stimulation. Inflammation. 25:2001;157-163.
45. Walisser J.A., Thies R.L. Poly(ADP-ribose) polymerase inhibition in oxidant-stressed endothelial cells prevents oncosis and permits caspase activation and apoptosis. Exp. Cell. Res. 251:1999;401-413.
46. Mazzon E., De Sarro A., Caputi A.P., Cuzzocrea S. Role of tight junction derangement in the endothelial dysfunction elicited by exogenous and endogenous peroxynitrite and poly(ADP-ribose) synthetase. Shock. 18:2002;434-439.
47. Grupp I.L., Jackson T.M., Hake P., Grupp G., Szabó C. Protection against hypoxia-reoxygenation in the absence of poly(ADP-ribose) synthetase in isolated working hearts. J. Mol. Cell. Cardiol. 31:1999;297-303.
48. Thiemermann C., Bowes J., Myint F.P., Vane J.R. Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 94:1997;679-683.
49. Szabados E., Fischer G.M., Gallyas F. Jr., Kispal G., Sumegi B. Enhanced ADP-ribosylation and its diminution by lipoamide after ischemia-reperfusion in perfused rat heart. Free Radic. Biol. Med. 27:1999;1103-1113.
50. Docherty J.C., Kuzio B., Silvester J.A., Bowes J., Thiemermann C. An inhibitor of poly(ADP-ribose) synthetase activity reduces contractile dysfunction and preserves high energy phosphate levels during reperfusion of the ischaemic rat heart. Br. J. Pharmacol. 127:1999;1518-1524.
51. Bowes J., Ruetten H., Martorana P.A., Stockhausen H., Thiemermann C. Reduction of myocardial reperfusion injury by an inhibitor of poly(ADP-ribose) synthetase in the pig. Eur. J. Pharmacol. 359:1998;143-150.
52. Fiorillo C., Pace S., Ponziani V.et al. Poly(ADP-ribose) polymerase activation and cell injury in the course of rat heart heterotopic transplantation. Free Radic. Res. 36:2002;79-87.
53. Fiorillo C., Ponziani V., Giannini L.et al. Beneficial effects of poly(ADP-ribose) polymerase inhibition against the reperfusion injury in heart transplantation. Free Radic. Res. 37:2003;331-339.
54. Kahn T., Ruel M., Bianchi C., Szabó C., Sellke F.W. Poly(ADP-ribose) synthetase inhibition improves postischemic myocardial function after cardiopulmonary bypass. (Abstract) J. Am. Coll. Surg. 195:2002;S18. [Suppl.].
55. Liaudet L., Yang Z., Affar B., Szabó C. Myocardial ischemic preconditioning in rodents is dependent on poly(ADP-ribose) synthetase. Mol. Med. 7:2001;406-417.
56. Virag L., Salzman A.L., Szabo C. Poly(ADP-ribose) synthetase activation mediates mitochondrial injury during oxidant-induced cell death. J. Immunol. 161:1998;3753-3759.
57. Du L., Zhang X., Han Y.Y., Burke N.A.et al. Intra-mitochondrial poly(ADP-ribosylation) contributes to NAD+ depletion and cell death induced by oxidative stress. J. Biol. Chem. 278:2003;18426-18433.
58. Szabó C., Wong H.R., Bauer P.I.et al. Regulation of components of the inflammatory response by 5-iodo-6-amino-1,2-benzopyrone, and inhibitor of poly(ADP-ribose) synthetase and pleiotropic modifier of cellular signal pathways. Int. J. Oncol. 10:1997;1093-1101.
59. 2 and tumor necrosis factor-α activate intercellular adhesion molecule 1 (ICAM-1) gene transcription through distinct cis-regulatory elements within the ICAM-1 promoter. J. Biol. Chem. 270:1995;18966-18974.
60. Pieper A.A., Blackshaw S., Clements E.E.et al. Poly(ADP-ribosyl)ation basally activated by DNA strand breaks reflects glutamate-nitric oxide neurotransmission. Proc. Natl. Acad. Sci. U. S. A. 97:2000;1845-1850.
61. Simbulan-Rosenthal C.M., Ly D.H., Rosenthal D.S.et al. Misregulation of gene expression in primary fibroblasts lacking poly(ADP-ribose) polymerase. Proc. Natl. Acad. Sci. U. S. A. 97:2000;11274-11279.
62. Ha H.C., Hester L.D., Snyder S.H. Poly(ADP-ribose) polymerase-1 dependence of stress-induced transcription factors and associated gene expression in glia. Proc. Natl. Acad. Sci. U. S. A. 99:2002;3270-3275.
63. Szabó C., Lim L.H.K., Cuzzocrea S.et al. Inhibition of poly(ADP-ribose) synthetase attenuates neutrophil recruitment and exerts antiinflammatory effects. J. Exp. Med. 186:1997;1041-1049.
64. Zingarelli B., Szabó C., Salzman A.L. Blockade of poly(ADP-ribose) synthetase inhibits neutrophil recruitment, oxidant generation, and mucosal injury in murine colitis. Gastroenterology. 116:1999;335-345.
65. Szabo C., Cuzzocrea S., Zingarelli B., O'Connor M., Salzman A.L. Endothelial dysfunction in a rat model of endotoxic shock. Importance of the activation of poly(ADP-ribose) synthetase by peroxynitrite. J. Clin. Invest. 100:1997;723-735.
66. De Murcia G., Shall S. From DNA damage and stress signaling to cell death; polyADP-ribosylation reactions. 2000;Oxford Univ. Press, Oxford.
67. Szabados E., Fischer G.M., Toth K.et al. Role of reactive oxygen species and poly-ADP-ribose polymerase in the development of AZT-induced cardiomyopathy in rat. Free Radic. Biol. Med. 26:1999;309-317.
68. Skuta G., Fischer G.M., Janaky T.et al. Molecular mechanism of the short-term cardiotoxicity caused by 2′,3′-dideoxycytidine (ddC): modulation of reactive oxygen species levels and ADP-ribosylation reactions. Biochem. Pharmacol. 58:1999;1915-1925.
69. Pacher P., Liaudet L., Mabley J., Komjati K., Szabo C. Pharmacologic inhibition of poly(adenosine diphosphate-ribose) polymerase may represent a novel therapeutic approach in chronic heart failure. J. Am. Coll. Cardiol. 40(5):2002 (Sep. 4);1006-1016.
70. Pacher P., Cziraki A., Mabley J.G., Liaudet L., Papp L., Szabo C. Role of poly(ADP-ribose) polymerase activation in endotoxin-induced cardiac collapse in rodents. Biochem. Pharmacol. 64:2002;1785-1791.
71. Pacher P., Liaudet L., Soriano F.G., Mabley J.G., Szabo E., Szabo C. The role of poly(ADP-ribose) polymerase activation in the development of myocardial and endothelial dysfunction in diabetes. Diabetes. 51:2002;514-521.
72. Szabo C., Zanchi A., Komjati K.et al. 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.
73. Oikawa A., Tohda H., Kanai M., Miwa M., Sugimura T. Inhibitors of poly(adenosine diphosphate ribose) polymerase induce sister chromatid exchanges. Biochem. Biophys. Res. Commun. 97:1999;1311-1316.
74. Simbulan-Rosenthal C.M., Haddad B.R.et al. Chromosomal aberrations in PARP(-/-) mice: genome stabilization in immortalized cells by reintroduction of poly(ADP-ribose) polymerase cDNA. Proc. Natl. Acad. Sci. U. S. A. 96:1999;13191-13196.
75. Smulson M.E., Simbulan-Rosenthal C.M., Boulares A.H.et al. Roles of poly(ADP-ribosyl)ation and PARP in apoptosis, DNA repair, genomic stability and functions of p53 and E2F-1. Adv. Enzyme Regul. 40:2000;183-215.
76. Nagele A. Poly(ADP-ribosyl)ation as a fail-safe, transcription- independent, suicide mechanism in acutely DNA-damaged cells: a hypothesis. Radiat. Environ. Biophys. 34:1995;251-254.
77. Cleaver J.E., Park S.D. Enhanced ligation of repair sites under conditions of inhibition of poly(ADP-ribose) synthesis by 3-aminobenzamide. Mutat. Res. 173:1986;287-290.
78. Borek C., Morgan W.F., Ong A., Cleaver J.E. Inhibition of malignant transformation in vitro by inhibitors of poly(ADP-ribose) synthesis. Proc. Natl. Acad. Sci. U. S. A. 81:1984;243-247.