Combined therapy with PJ34, a poly(ADP-ribose)polymerase inhibitor, reduces tissue plasminogen activator-induced hemorrhagic transformations in cerebral ischemia in mice

Fundamental and Clinical Pharmacology

Volumn 27, Issue 4, 2013, Pages 393-401

  Haddad, Marianne ^a   Beray Berthat, Virginie ^a   Coqueran, Bérard ^a   Plotkine, Michel ^a   Marchand Leroux, Catherine ^a   Margaill, Isabelle ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Brain hemorrhage; Cerebral ischemia; Hemorrhagic transformation; PJ34; Poly(ADP ribose) polymerase PARP; Recombinant tissue plasminogen activator rtPA

Indexed keywords

ALTEPLASE; GELATINASE A; GELATINASE B; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HEMORRHAGE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROLOGIC EXAMINATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BRAIN ISCHEMIA; ENZYME INHIBITORS; HEMORRHAGE; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MATRIX METALLOPROTEINASES; MICE; MIDDLE CEREBRAL ARTERY; PHENANTHRENES; POLY(ADP-RIBOSE) POLYMERASES; RECOMBINANT PROTEINS; TISSUE PLASMINOGEN ACTIVATOR;

EID: 84879554666     PISSN: 07673981     EISSN: 14728206     Source Type: Journal    
DOI: 10.1111/j.1472-8206.2012.01036.x     Document Type: Article

References (61)

1. Hacke W., Donnan G., Fieschi C. et al.Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet (2004) 363 768-774.
2. NINDS (The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group). Tissue plasminogen activator for acute ischemic stroke. N. Engl. J. Med. (1995) 333, 1581-1587.
3. Rosamond W., Flegal K., Friday G. et al.Heart disease and stroke statistics-2007 update: a report from the american heart association statistics committee and stroke statistics subcommittee. Circulation (2007) 115 e69-e171.
4. Hacke W., Kaste M., Bluhmki E. et al.Thrombolysis with alteplase 3 to 4.5hours after acute ischemic stroke. N. Engl. J. Med. (2008) 359 1317-1329.
5. Derex L., Nighoghossian N.Intracerebral haemorrhage after thrombolysis for acute ischaemic stroke: an update. J. Neurol. Neurosurg. Psychiatry (2008) 79 1093-1099.
6. Schreiber V., Dantzer F., Ame J.C., de Murcia G.Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. (2006) 7 517-528.
7. Pacher P., Szabo C.Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. Am. J. Pathol. (2008) 173 2-13.
8. Love S., Barber R., Wilcock G.K.Neuronal accumulation of poly(ADP-ribose) after brain ischaemia. Neuropathol. Appl. Neurobiol. (1999) 25 98-103.
9. Love S., Barber R., Wilcock G.K.Neuronal death in brain infarcts in man. Neuropathol. Appl. Neurobiol. (2000) 26 55-66.
10. Giansanti V., Dona F., Tillhon M., Scovassi A.I.PARP inhibitors: new tools to protect from inflammation. Biochem. Pharmacol. (2010) 80 1869-1877.
11. Jagtap P., Szabo C.Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat. Rev. Drug Discov. (2005) 4 421-440.
12. Nguewa P.A., Fuertes M.A., Valladares B., Alonso C., Perez J.M.Poly(ADPribose) polymerases: homology, structural domains and functions. novel therapeutical applications. Prog. Biophys. Mol. Biol. (2005) 88 143-172.
13. Peralta-Leal A., Rodriguez-Vargas J.M., Aguilar-Quesada R. et al.PARP inhibitors: new partners in the therapy of cancer and inflammatory diseases. Free Radic. Biol. Med. (2009) 47 13-26.
14. Tentori L., Portarena I., Graziani G.Potential clinical applications of poly(ADPribose) polymerase (PARP) inhibitors. Pharmacol. Res. (2002) 45 73-85.
15. Chiarugi A.Poly(ADP-ribosyl)ation and stroke. Pharmacol. Res. (2005) 52 15-24.
16. Komjati K., Besson V.C., Szabo C.Poly(ADP-ribose)polymerase inhibitors as potential therapeutic agents in stroke and neurotrauma. Curr. Drug Targets CNS Neurol. Disord. (2005) 4 179-194.
17. Eliasson M.J., Sampei K., Mandir A.S. et al.Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med. (1997) 3 1089-1095.
18. Endres M., Wang Z.Q., Namura S., Waeber C., Moskowitz M.A.Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J. Cereb. Blood Flow Metab. (1997) 17 1143-1151.
19. Crome O., Doeppner T.R., Schwarting S., Muller B., Bahr M., Weise J.Enhanced poly(ADP-ribose) polymerase-1 activation contributes to recombinant tissue plasminogen activator-induced aggravation of ischemic brain injury in vivo. J. Neurosci. Res. (2007) 85 1734-1743.
20. Moroni F., Chiarugi A.Post-ischemic brain damage: targeting PARP-1 within the ischemic neurovascular units as a realistic avenue to stroke treatment. FEBS J. (2009) 276 36-45.
21. Lenzser G., Kis B., Snipes J.A. et al.Contribution of poly(ADP-ribose) polymerase to postischemic blood-brain barrier damage in rats. J. Cereb. Blood Flow Metab. (2007) 27 1318-1326.
22. Haddad M., Beray-Berthat V., Coqueran B. et al.Reduction of hemorrhagic transformation by PJ34, a poly(ADP-ribose)polymerase inhibitor, after permanent focal cerebral ischemia in mice. Eur. J. Pharmacol. (2008) 588 52-57.
23. Koh S.H., Chang D.I., Kim H.T. et al.Effect of 3-aminobenzamide, PARP inhibitor, on matrix metalloproteinase-9 level in plasma and brain of ischemic stroke model. Toxicology (2005) 214 131-139.
24. Clark W.M., Lessov N.S., Dixon M.P., Eckenstein F.Monofilament intraluminal middle cerebral artery occlusion in the mouse. Neurol. Res. (1997) 19 641-648.
25. Paxinos G., Franklin K.B.J.The mouse brain in stereotaxic coordinates. Academic press ed. Academic press, San Diego, 2001.
26. Murata Y., Rosell A., Scannevin R.H., Rhodes K.J., Wang X., Lo E.H.Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke (2008) 39 3372-3377.
27. Zhang L., Chopp M., Jia L., Cui Y., Lu M., Zhang Z.G.Atorvastatin extends the therapeutic window for tPA to 6h after the onset of embolic stroke in rats. J. Cereb. Blood Flow Metab. (2009) 29 1816-1824.
28. Ishiguro M., Mishiro K., Fujiwara Y. et al.Phosphodiesterase-III inhibitor prevents hemorrhagic transformation induced by focal cerebral ischemia in mice treated with tPA. PLoS One (2010) 5 e15178.
29. Hall E.D.High-dose glucocorticoid treatment improves neurological recovery in headinjured mice. J. Neurosurg. (1985) 62 882-887.
30. Caplan L.R.Hemorrhage into embolic brain infarcts. Pharmacotherapy (1999) 19 125-127.
31. Golanov E.V., Reis D.J.Contribution of cerebral edema to the neuronal salvage elicited by stimulation of cerebellar fastigial nucleus after occlusion of the middle cerebral artery in rat. J. Cereb. Blood Flow Metab. (1995) 15 172-174.
32. Bradford M.M.A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. (1976) 72 248-254.
33. Kaur J., Zhao Z., Klein G.M., Lo E.H., Buchan A.M.The neurotoxicity of tissue plasminogen activator. J. Cereb. Blood Flow Metab. (2004) 24 945-963.
34. Meng W., Wang X., Asahi M. et al.Effects of tissue type plasminogen activator in embolic versus mechanical models of focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. (1999) 19 1316-1321.
35. Orset C., Macrez R., Young A.R. et al.Mouse model of in situ thromboembolic stroke and reperfusion. Stroke (2007) 38 2771-2778.
36. Yagi K., Kitazato K.T., Uno M. et al.Edaravone, a free radical scavenger, inhibits MMP-9-related brain hemorrhage in rats treated with tissue plasminogen activator. Stroke (2009) 40 626-631.
37. Christou I., Alexandrov A.V., Burgin W.S. et al.Timing of recanalization after tissue plasminogen activator therapy determined by transcranial doppler correlates with clinical recovery from ischemic stroke. Stroke (2000) 31 1812-1816.
38. Alexandrov A.V., Burgin W.S., Demchuk A.M., El-Mitwalli A., Grotta J.C.Speed of intracranial clot lysis with intravenous tissue plasminogen activator therapy: sonographic classification and short-term improvement. Circulation (2001) 103 2897-2902.
39. STAIR. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke (1999) 30, 2752-2758.
40. Soriano F.G., Virag L., Szabo C.Diabetic endothelial dysfunction: role of reactive oxygen and nitrogen species production and poly(ADP-ribose) polymerase activation. J. Mol. Med. (2001) 79 437-448.
41. Couturier J.Y., Ding-Zhou L., Croci N., Plotkine M., Margaill I.3-aminobenzamide reduces brain infarction and neutrophil infiltration after transient focal cerebral ischemia in mice. Exp. Neurol. (2003) 184 973-980.
42. Iwashita A., Tojo N., Matsuura S. et al.A novel and potent poly(ADP-ribose) polymerase-1 inhibitor, FR247304 (5-chloro-2-[3-(4-phenyl-3, 6-dihydro-1(2H)-pyridinyl)propyl]-4(3H)-quinazolinone), attenuates neuronal damage in in vitro and in vivo models of cerebral ischemia. J. Pharmacol. Exp. Ther. (2004) 310 425-436.
43. Takahashi K., Pieper A.A., Croul S.E., Zhang J., Snyder S.H., Greenberg J.H.Post-treatment with an inhibitor of poly(ADP-ribose)polymerase attenuates cerebral damage in focal ischemia. Brain Res. (1999) 829 46-54.
44. Abdelkarim G.E., Gertz K., Harms C. et al.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. (2001) 7 255-260.
45. Haddad M., Rhinn H., Bloquel C. et al.Anti-inflammatory effects of PJ34, a poly(ADP-ribose) polymerase inhibitor, in transient focal cerebral ischemia in mice. Br. J. Pharmacol. (2006) 149 23-30.
46. Burggraf D., Martens H.K., Dichgans M., Hamann G.F.Matrix metalloproteinase (MMP) induction and inhibition at different doses of recombinant tissue plasminogen activator following experimental stroke. Thromb. Haemost. (2007) 98 963-969.
47. Candelario-Jalil E., Yang Y., Rosenberg G.A.Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience (2009) 158 983-994.
48. Jin R., Yang G., Li G.Molecular insights and therapeutic targets for blood-brain barrier disruption in ischemic stroke: critical role of matrix metalloproteinases and tissue-type plasminogen activator. Neurobiol. Dis. (2010) 38 376-385.
49. Kelly M.A., Shuaib A., Todd K.G.Matrix metalloproteinase activation and blood brain barrier breakdown following thrombolysis. Exp. Neurol. (2006) 200 38-49.
50. Lapchak P.A., Chapman D.F., Zivin J.A.Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke (2000) 31 3034-3040.
51. Pfefferkorn T., Rosenberg G.A.Closure of the blood-brain barrier by matrix metalloproteinase inhibition reduces rtPA-mediated mortality in cerebral ischemia with delayed reperfusion. Stroke (2003) 34 2025-2030.
52. Sumii T., Lo E.H.Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke (2002) 33 831-836.
53. Tsuji K., Aoki T., Tejima E. et al.Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke (2005) 36 1954-1959.
54. Wang X., Rosell A., Lo E.H.Targeting extracellular matrix proteolysis for hemorrhagic complications of tPA stroke therapy. C.N.S. Neurol. Disord. Drug Targets (2008) 7 235-242.
55. Copin J.C., Bengualid D.J., Da Silva R.F., Kargiotis O., Schaller K., Gasche Y.Recombinant tissue plasminogen activator induces blood-brain barrier breakdown by a matrix metalloproteinase-9-independent pathway after transient focal cerebral ischemia in mouse. Eur. J. Neurosci. (2011) 34 1085-1092.
56. Kauppinen T.M., Swanson R.A.Poly(ADP-ribose) polymerase-1 promotes microglial activation, proliferation, and matrix metalloproteinase-9-mediated neuron death. J. Immunol. (2005) 174 2288-2296.
57. Siao C.J., Tsirka S.E.Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J. Neurosci. (2002) 22 3352-3358.
58. Yepes M., Roussel B.D., Ali C., Vivien D.Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends Neurosci. (2009) 32 48-55.
59. Cuadrado E., Ortega L., Hernandez-Guillamon M. et al.Tissue plasminogen activator (t-PA) promotes neutrophil degranulation and MMP-9 release. J. Leukoc. Biol. (2008) 84 207-214.
60. Koh S.H., Park Y., Song C.W. et al.The effect of PARP inhibitor on ischaemic cell death, its related inflammation and survival signals. Eur. J. Neurosci. (2004) 20 1461-1472.
61. Zhang R.L., Zhang C., Zhang L. et al.Synergistic effect of an endothelin type A receptor antagonist, S-0139, with rtPA on the neuroprotection after embolic stroke. Stroke (2008) 39 2830-2836.