Deleterious activation of poly(ADP-ribose)polymerase-1 in brain after in vivo oxidative stress

Free Radical Research

Volumn 37, Issue 11, 2003, Pages 1201-1208

  Besson, Valérie C ^a   Margaill, Isabelle ^a   Plotkine, Michel ^a   Marchand Verrecchia, Catherine ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

3 Nitrotyrosine; Brain; Cell death; Oxidative stress; Peroxynitrite; Poly(ADP ribose)polymerase 1

Indexed keywords

3 AMINOBENZAMIDE; FREE RADICAL; MALONIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; POLY(ADENOSINE DIPHOSPHATE RIBOSE);

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN INJURY; BRAIN ISCHEMIA; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; CORPUS STRIATUM; DEGENERATIVE DISEASE; DRUG MECHANISM; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; MALE; MITOCHONDRION; NERVE CELL NECROSIS; NITROSATION; NONHUMAN; OXIDATIVE STRESS; RAT;

ANIMALS; APOPTOSIS; BENZAMIDES; BRAIN; BRAIN DISEASES; ENZYME ACTIVATION; IMMUNOHISTOCHEMISTRY; MALE; MALONATES; OXIDATIVE STRESS; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TYROSINE;

ANIMALIA;

EID: 0142242140     PISSN: 10715762     EISSN: None     Source Type: Journal    
DOI: 10.1080/10715760310001612568     Document Type: Article

References (67)

1. Lewen, A., Matz, P. and Chan, P.H. (2000) "Free radical pathways in CNS injury", J. Neurotrauma 17, 871-890.
2. Chan, P.H. (2001) "Reactive oxygen radicals in signalling and damage in the ischemic brain", J. Cereb. Blood Flow Metab. 21, 2-14.
3. Gilgun-Sherki, Y., Melamed, E. and Offen, D. (2001) "Oxidative stress induced-neurodegenerative diseases: the need for antioxidants that penetrate the blood brain barrier", Neuropharmacology 40, 959-975.
4. Droge, W. (2002) "Free radicals in the physiological control of cell function", Physiol. Rev. 82, 47-95.
5. Love, S. (1999) "Oxidative stress in brain ischemia", Brain Pathol. 9, 119-131.
6. Pratico, D. and Delanty, N. (2000) "Oxidative injury in diseases of the central nervous system: focus on Alzheimer's disease", Am. J. Med. 109, 577-585.
7. Mates, J.M., Perez-Gomez, C. and Nunez de Castro, I. (1999) "Antioxidant enzymes and human diseases", Clin. Biochem. 32, 595-603.
8. Lautier, D., Lagueux, J., Thibodeau, J., Menard, L. and Poirier, G.G. (1993) "Molecular and biochemical features of poly (ADP-ribose) metabolism", Mol. Cell. Biochem. 122, 171-193.
9. D'Amours, D., Desnoyers, S., D'Silva, I. and Poirier, G.G. (1999) "Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions", Biochem. J. 342, 249-268.
10. Burkle, A. (2001) "Physiology and pathophysiology of poly(ADP-ribosyl)ation", Bioessays 23, 795-806.
11. Ha, H.C. and Snyder, S.H. (2000) "Poly(ADP-ribose) polymerase-1 in the nervous system", Neurobiol. Dis. 7, 225-239.
12. Pieper, A.A., Verma, A., Zhang, J. and Snyder, S.H. (1999) "Poly (ADP-ribose) polymerase, nitric oxide and cell death", Trends Pharmacol. Sci. 20, 171-181.
13. 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. Investig. 77, 1312-1320.
14. Schraufstatter, I.U., Hyslop, P.A., Hinshaw, D.B., Spragg, R.G., Sklar, L.A. and Cochrane, C.G. (1986) "Hydrogen peroxide-induced injury of cells and its prevention by inhibitors of poly(ADP-ribose) polymerase", Proc. Natl Acad. Sci. USA 83, 4908-4912.
15. Szabo, C., Zingarelli, B., O'Connor, M. and Salzman, A.L. (1996) "DNA strand breakage, activation of poly (ADP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite", Proc. Natl Acad. Sci. USA 93, 1753-1758.
16. Cookson, M.R., Ince, P.G. and Shaw, P.J. (1998) "Peroxynitrite and hydrogen peroxide induced cell death in the NSC34 neuroblastoma X spinal cord cell line: role of poly (ADP-ribose) polymerase", J. Neurochem. 70, 501-508.
17. 2-induced cell death in human glioma cells: role of lipid peroxidation and PARP activation", Neurochem. Res. 26, 337-343.
18. Cuzzocrea, S., Zingarelli, B. and Caputi, A.P. (1998) "Role of peroxynitrite and poly (ADP-ribosyl) synthetase activation in cardiovascular derangement induced by zymosan in the rat", Life Sci. 63, 923-933.
19. Szabo, C., Virag, L., Cuzzocrea, S., Scott, G.S., Hake, P., O'Connor, M.P., Zingarelli, B., Salzman, A. and Kun, E. (1998) "Protection against peroxynitrite-induced fibroblast injury and arthritis development by inhibition of poly(ADP-ribose) synthase", Proc. Natl Acad. Sci. USA 95, 3867-3872.
20. Endres, M., Scott, G.S., Salzman, A.L., Kun, E., Moskowitz, M.A. and Szabo, C. (1998) "Protective effects of 5-iodo-6-amino-1,2-benzopyrone, and inhibitor of poly(ADP-ribose) synthetase against peroxynitrite-induced glial damage and stroke development", Eur. J. Pharmacol. 351, 377-382.
21. Wallis, R.A., Panizzon, K.L., Henry, D. and Wasterlain, C.G. (1993) "Neuroprotection against nitric oxide injury with inhibitors of ADP- ribosylation", Neuroreport 5, 245-248.
22. Zhang, J., Dawson, V.L., Dawson, T.M. and Snyder, S.H. (1994) "Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity", Science 263, 687-689.
23. Abdelkarim, G.E., Gertz, K., Harms, C., Katchanov, J., Dirnagl, U., Szabo, C. and Endres, M. (2001) "Protective effects of PJ34, a novel, potent inhibitor of poly(ADP-ribose) polymerase (PARP) in in vitro and in vivo models of stroke", Int. J. Mol. Med. 7, 255-260.
24. Moroni, F., Meli, E., Peruginelli, F., Chiarugi, A., Cozzi, A., Picca, R., Romagnoli, P., Pellicciari, R. and Pellegrini-Giampietro, D.E. (2001) "Poly(ADP-ribose) polymerase inhibitors attenuate necrotic but not apoptotic neuronal death in experimental models of cerebral ischemia", Cell Death Differ. 8, 921-932.
25. Tasker, R.C., Sahota, S.K., Cotter, F.E. and Williams, S.R. (1998) "Early postischemic dantrolene-induced amelioration of poly(ADP-ribose)polymerase-related bioenergetic failure in neonatal rat brain slices", J. Cereb. Blood Flow Metab. 18, 1346-1356.
26. Endres, M., Wang, Z.Q., Namura, S., Waeber, C. and Moskowitz, M.A. (1997) "Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase", J. Cereb. Blood Flow Metab. 17, 1143-1151.
27. Tokime, T., Nozaki, K., Sugino, T., Kikuchi, H., Hashimoto, N. and Ueda, K. (1998) "Enhanced poly(ADP-ribosyl)ation after focal ischemia in rat brain", J. Cereb. Blood Flow Metab. 18, 991-997.
28. Takahashi, K., Pieper, A.A., Croul, S.E., Zhang, J., Snyder, S.H. and Greenberg, J.H. (1999) "Post-treatment with an inhibitor of poly(ADP-ribose) polymerase attenuates cerebral damage in focal ischemia", Brain Res. 829, 46-54.
29. Ducrocq, S., Benjelloun, N., Plotkine, M., Ben-Ari, Y. and Charriaut-Marlangue, C. (2000) "Poly(ADP-ribose) synthase inhibition reduces ischemic injury and inflammation in neonatal rat brain", J. Neurochem. 74, 2504-2511.
30. Mésenge, C., Verrecchia, C., Charriaut-Marlangue, C., Boulu, R.G. and Plotkine, M. (1999) "Peroxynitrite-PARS pathway activation following traumatic brain injury in mice", J. Cereb. Blood Flow Metab. 19, S390.
31. LaPlaca, M.C., Zhang, J., Raghupathi, R., Li, J.H., Smith, F., Bareyre, F.M., Snyder, S.H., Graham, D.I. and McIntosh, T.K. (2001) "Pharmacologic inhibition of poly(ADP-ribose) polymerase is neuroprotective following traumatic brain injury in rats", J. Neurotrauma 18, 369-376.
32. Satchell, M.A., Zhang, X., Kochanek, P.M., Dixon, C.E., Jenkins, L.W., Melick, J., Szabo, C. and Clark, R.S. (2003) "A dual role for poly-ADP-ribosylation in spatial memory acquisition after traumatic brain injury in mice involving NAD depletion and ribosylation of 14-3-3gamma", J. Neurochem. 85, 697-708.
33. Cosi, C. and Marien, M. (1999) "Implication of poly (ADP-ribose) polymerase (PARP) in neurodegeneration and brain energy metabolism. Decreases in mouse brain NAD+ and ATP caused by MPTP are prevented by the PARP inhibitor benzamide", Ann. NY Acad. Sci. 890, 227-239.
34. Scott, G.S., Hake, P., Kean, R.B., Virag, L., Szabo, C. and Hooper, D.C. (2001) "Role of poly(ADP-ribose) synthetase activation in the development of experimental allergic encephalomyelitis", J. Neuroimmunol. 117, 78-86.
35. Chiarugi, A. (2002) "Inhibitors of poly(ADP-ribose)polymerase-1 suppress transcriptional activation in lymphocytes and ameliorate autoimmune encephalomyelitis in rats", Br. J. Pharmacol. 137, 761-770.
36. Schulz, J.B., Henshaw, D.R., Siwek, D., Jenkins, B.G., Ferrante, R.J., Cipolloni, P.B., Kowall, N.W., Rosen, B.R. and Beal, M.F. (1995) "Involvement of free radicals in excitotoxicity in vivo", J. Neurochem. 64, 2239-2247.
37. Ferger, B., Eberhardt, O., Teismann, P., de Groote, C. and Schulz, J.B. (1999) "Malonate-induced generation of reactive oxygen species in rat striatum depends on dopamine release but not on NMDA receptor activation", J. Neurochem. 73, 1329-1332.
38. Paxinos, G. and Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates (Academic press, San Diego).
39. Golanov, E.V. and Reis, D.J. (1995) "Contribution of cerebral oedema to the neuronal salvage elicited by stimulation of cerebellar fastigial nucleus after occlusion of the middle cerebral artery in rats", J. Cereb. Blood Flow Metab. 15, 172-174.
40. Virag, L. and Szabo, C. (2002) "The therapeutic potential of poly(ADP-ribose) polymerase inhibitors", Pharmacol. Rev. 54, 375-429.
41. Beckman, J.S. (1996) "Oxidative damage and tyrosine nitration from peroxynitrite", Chem. Res. 9, 836-844.
42. Eiserich, J.P., Hristova, M., Cross, C.E., Jones, A.D., Freeman, B.A., Halliwell, B. and van der Vliet, A. (1998) "Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils", Nature 391, 393-397.
43. Eliasson, M.J., Sampei, K., Mandir, A.S., Hurn, P.D., Traystman, R.J., Bao, J., Pieper, A., Wang, Z.Q., Dawson, T.M., Snyder, S.H. and Dawson, V.L. (1997) "Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia", Nat. Med. 3, 1089-1095.
44. Ame, J.C., Rolli, V., Schreiber, V., Niedergang, C., Apiou, F., Decker, P., Muller, S., Hoger, T., Ménissier-de Murcia, J. and de Murcia, G. (1999) "PARP-2, a novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase", J. Biol. Chem. 274, 17860-17868.
45. Sallmann, F.R., Vodenicharov, M.D., Wang, Z.Q. and Poirier, G.G. (2000) "Characterization of sPARP-1. An alternative product for PARP-1 gene with poly(ADP-ribose) polymerase activity independent of DNA strand breaks", J. Biol. Chem. 275, 15504-15511.
46. Kickhoefer, V.A., Siva, A.C., Kedersha, N.L., Inman, E.M., Ruland, C., Streuli, M. and Rome, L.H. (1999) "The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase", J. Cell. Biol. 146, 917-928.
47. Smith, S., Giriat, I., Schmitt, A. and de Lange, T. (1998) "Tankyrase, a poly(ADP-ribose) polymerase at human telomeres", Science 282, 1484-1487.
48. Kaminker, P.G., Kim, S.H., Taylor, R.D., Zebarjadian, Y., Funk, W.D., Morin, G.B., Yaswen, P. and Campisi, J. (2001) "TANK2, a new TRF1-associated poly(ADP-ribose)polymerase, causes rapid induction of cell death upon overexpression", J. Biol. Chem. 276, 35891-35899.
49. Pieper, A.A., Blackshaw, S., Clements, E.E., Brat, D.J., Krug, D.K., White, A.J., Pinto-Garcia, P., Favit, A., Conover, J.R., Snyder, S.H. and Verma, A. (2000) "Poly(ADP-ribosyl)ation basally activated by DNA strand breaks reflects glutamate-nitric oxide neurotransmission", Proc. Natl Acad. Sci. USA 97, 1845-1850.
50. Chatterjee, P.K., Cuzzocrea, S. and Thiemermann, C. (1999) "Inhibitors of poly (ADP-ribose) synthetase protect rat proximal tubular cells against oxidant stress", Kidney Int. 56, 973-984.
51. Bowes, J., Ruetten, H., Martorana, P.A., Stockhausen, H. and Thiemermann, C. (1998) "Reduction of myocardial reperfusion injury by an inhibitor of poly (ADP-ribose) synthetase in the pig", Eur. J. Pharmacol. 359, 143-150.
52. Zingarelli, B., Cuzzocrea, S., Zsengeller, Z., Salzman, A.L. and Szabo, C. (1997) "Protection against myocardial ischemia and reperfusion injury by 3-aminobenzamide, an inhibitor of poly(ADP-ribose) synthetase", Cardiovasc. Res. 36, 205-215.
53. Schulz, J.B., Huang, P.L., Matthews, R.T., Passov, D., Fishman, M.C. and Beal, M.F. (1996) "Striatal malonate lesions are attenuated in neuronal nitric oxide synthase knockout mice", J. Neurochem. 67, 430-433.
54. Schulz, J.B., Matthews, R.T., Jenkins, B.G., Ferrante, R.J., Siwek, D., Henshaw, D.R., Cipolloni, P.B., Mecocci, P., Kowall, N.W. and Rosen, B.R. (1995) "Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo", J. Neurosci. 15, 8419-8429.
55. Takahashi, K., Greenberg, J.H., Jackson, P., Maclin, K. and Zhang, J. (1997) "Neuroprotective effects of inhibiting poly(ADP-ribose) synthetase on focal cerebral ischemia in rats", J. Cereb. Blood Flow Metab. 17, 1137-1142.
56. Milam, K.M. and Cleaver, J.E. (1984) "Inhibitors of poly(adenosine diphosphate-ribose) synthesis: effect on other metabolic processes", Science 223, 589-591.
57. Zingarelli, B., O'Connor, M., Wong, H., Salzman, A.L. and Szabo, C. (1996) "Peroxynitrite-mediated DNA strand breakage activates poly-adenosine diphosphate ribosyl synthetase and causes cellular energy depletion in macrophages stimulated with bacterial lipopolysaccharide", J. Immunol. 156, 350-358.
58. Bowes, J. and Thiemermann, C. (1998) "Effects of inhibitors of the activity of poly(ADP-ribose) synthetase on the liver injury caused by ischaemia-reperfusion: a comparison with radical scavengers", Br. J. Pharmacol. 124, 1254-1260.
59. Szabo, C. and Dawson, V.L. (1998) "Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion", Trends Pharmacol. Sci. 19, 287-298.
60. Beal, M.F., Brouillet, E., Jenkins, B., Rosen, B. and Hyman, B.T. (1993) "Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate", J. Neurochem. 61, 1147-1150.
61. Henshaw, R., Jenkins, B.G., Schulz, J.B., Ferrante, R.J., Kowall, N.W., Rosen, B.R. and Beal, M.F. (1994) "Malonate produces striatal lesions by indirect NMDA receptor activation", Brain Res. 647, 161-167.
62. Whalen, M.J., Clark, R.S., Dixon, C.E., Robichaud, P., Marion, D.W., Vagni, V., Graham, S.H., Virag, L., Hasko, G., Stachlewitz, R., Szabo, C. and Kochanek, P.M. (1999) "Reduction of cognitive and motor deficits after traumatic brain injury in mice deficient in poly(ADP-ribose) polymerase", J. Cereb. Blood Flow Metab. 19, 835-842.
63. Halliwell, B. (2001) "Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment", Drugs Aging 18, 685-716.
64. Cosi, C., Colpaert, F., Koek, W., Degryse, A. and Marien, M. (1996) "Poly(ADP-ribose) polymerase inhibitors protect against MPTP-induced depletions of striatal dopamine and cortical noradrenaline in C57B1/6 mice", Brain Res. 729, 264-269.
65. Mandir, A.S., Przedborski, S., Jackson-Lewis, V., Wang, Z.Q., Simbulan-Rosenthal, C.M., Smulson, M.E., Hoffman, B.E., Guastella, D.B., Dawson, V.L. and Dawson, T.M. (1999) "Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism", Proc. Natl Acad. Sci. USA 96, 5774-5779.
66. Love, S., Barber, R. and Wilcock, G.K. (1999) "Neuronal accumulation of poly(ADP-ribose) after brain ischaemia", Neuropathol. Appl. Neurobiol. 25, 98-103.
67. Love, S., Barber, R. and Wilcock, G.K. (1999) "Increased poly(ADP-ribosyl)ation of nuclear proteins in Alzheimer's disease", Brain 122, 247-253.