Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia

Nature Medicine

Volumn 3, Issue 10, 1997, Pages 1089-1095

  Eliasson, Mikael J L ^a   Sampei, Kenji ^b   Mandir, Allen S ^a   Hurn, Patricia D ^b   Traystman, Richard J ^b   Bao, Jun ^a   Pieper, Andrew ^a   Wang, Zhao Qi ^c   Dawson, Ted M ^a   Snyder, Solomon H ^a   Dawson, Valina L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

POLY(ADENOSINE DIPHOSPHATE RIBOSE);

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN PROTECTION; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; DNA DAMAGE; FETUS; GENE DISRUPTION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANIMALS; BENZAMIDES; BRAIN; CELLS, CULTURED; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; DNA DAMAGE; ENZYME ACTIVATION; ENZYME INHIBITORS; HEMODYNAMIC PROCESSES; IMMUNITY, NATURAL; ISCHEMIC ATTACK, TRANSIENT; ISOQUINOLINES; MICE; MICE, KNOCKOUT; N-METHYLASPARTATE; NAD; NEURONS; NEUROTOXINS; NITRATES; NITRIC OXIDE; PIPERIDINES; POLY(ADP-RIBOSE) POLYMERASES;

EID: 0030842946     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1097-1089     Document Type: Article

References (47)

1. Berger, N.A. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res. 101, 4-15 (1985).
2. Lautier, D., Lagueux, J., Thibodeau, J., Menard, L. & Poirier, G.G. Molecular and biochemical features of poly(ADP-ribose) metabolism. Mol. Cell. Biochem. 122, 171-193 (1993).
3. de Murcia, G. et al. Structure and function of poly(ADP-ribose) polymerase. Mol. Cell. Biochem. 138, 15-24 (1994).
4. Althaus, F.R. & Richter, C. ADP-ribosylation of proteins: Enzymology and biological significance. Mol. Biol. Biochem. Biophys. 37, 1-237 (1987).
5. de Murcia, G. & Menissier de Murcia, J. Poly(ADP-ribose) polymerase: A molecular nick-sensor. Trends Biochem. Sci. 19, 172-176 (1994).
6. Lipton, S.A. & Rosenberg, P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330, 613-622 (1994).
7. Meldrum, B. & Garthwaite, J. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol. Sci. 11, 379-387 (1990).
8. Choi, D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634 (1988).
9. Dawson, T.M. & Dawson, V.L. Protection of the brain from ischemia. in Cerebrovascular Disease (ed. Batjer, H.H.) 319-325 (Lippincott-Raven, Philadelphia, 1997).
10. Dawson, V.L., Dawson, T.M., London, E.D., Bredt, D.S. & Snyder, S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88, 6368-6371 (1991).
11. Dawson, V.L., Dawson, T.M., Bartley, D.A., Uhl, G.R. & Snyder, S.H. Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661 (1993).
12. Dawson, V.L., Kizushi, V.M., Huang, P.L., Snyder, S.H. & Dawson, T.M. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase deficient mice. J. Neurosci. 16, 2479-2487 (1996).
13. Iadecola, C. Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci. 20, 132-139 (1997).
14. Huang, Z. et al. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265, 1883-1885 (1994).
15. Beckman, J.S. & Crow, J.P. Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochem. Soc. Trans. 21, 330-334 (1993).
16. + depletion. Biochem. Biophys. Res. Commun. 199, 1270-1277 (1994).
17. Zhang, J., Dawson, V.L., Dawson, T.M. & Snyder, S.H. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263, 687-689 (1994).
18. Zhang, J., Pieper, A. & Snyder, S.H. Poly(ADP-ribose) synthetase activation: An early indicator of neurotoxic DNA damage. J. Neurochem. 65, 1411-1414 (1995).
19. Wang, Z.-Q. et al: Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9, 509-520 (1995).
20. Suto, M.J., Turner, W.R., Arundel-Suto, C.M., Werbel, L.M. & Sebolt-Leopold, J.S. Dihydroisoquinolinones: The design and synthesis of a new series of potent inhibitors of poly(ADP-ribose) polymerase. Anticancer Drug Des. 6, 107-117 (1991).
21. Banasik, M., Komura, H., Shimoyama, M. & Ueda, K. Specific inhibitors of poly(ADP-ribose) synthetase and mono(ADP-ribosyl)transferase. J. Biol. Chem. 267, 1569-1575 (1992).
22. Banasik, M. & Ueda, K. Inhibitors and activators of ADP-ribosylation reactions. Mol. Cell. Biochem. 138, 185-197 (1994).
23. Wang, Z.-Q. et al. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev. (in the press).
24. Chan, P.H., Chu, L., Chen, S.F., Carlson, E.J. St Epstein, C.J. Reduced neurotoxicity in transgenic mice overexpressing human copper-zinc-superoxide dismutase. Stroke 21 (Suppl.), III80-III82 (1990).
25. Choi, D.W. Cerebral hypoxia: Some new approaches and unanswered questions. J. Neurosci. 10, 2493-2501 (1990).
26. Dawson, T.M. & Snyder, S.H. Gases as biological messengers: Nitric oxide and carbon monoxide in the brain. J. Neurosci. 14, 5147-5159 (1994).
27. Sharkey, J. & Butcher, S.P. Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature 371, 336-339 (1994).
28. Kinouchi, H. et al. Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc. Natl. Acad. Sci. USA 88, 11158-11162 (1991).
29. Yang, G. et al. Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke 25, 165-170 (1994).
30. 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. (in the press).
31. Simpson, E.M. et al. Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nature Genet. 16, 19-27 (1997).
32. Takahashi, K., Greenberg, J.H., Jackson, P., Maclin, K. & Zhang, J. Effect of inhibition of poly(ADP-ribose) synthetase on focal cerebral ischemia in rats. Neurosci. Abstr. (in the press).
33. Mizumoto, K., Glascott, P.A., Jr. & Farber, J.L. Roles for oxidative stress and poly(ADP-ribosyl)ation in the killing of cultured hepatocytes by methyl methanesulfonate. Biochem. Pharmacol. 46, 1811-1818 (1993).
34. Heller, B. et al. Inactivation of the poly(ADP-ribose) polymerase gene affects oxygen radical and nitric oxide toxicity in islet cells. J. Biol. Chem. 270, 11176-11180 (1995).
35. 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. USA 94, 679-683 (1997).
36. Thies, R.L. & Autor, A.P. Reactive oxygen injury to cultured pulmonary artery endothelial cells: mediation by poly(ADP-ribose) polymerase activation causing NAD depletion and altered energy balance. Arch. Biochem. Biophys. 286, 353-363 (1991).
37. Hudak, B.B., Tufariello, J., Sokolowski, J., Maloney, C. & Holm, B.A. Inhibition of poly(ADP-ribose) polymerase preserves surfactant synthesis after hydrogen peroxide exposure. Am. J. Physiol. 269, L59-L64 (1995).
38. Kirkland, J.B. Lipid peroxidation, protein thiol oxidation and DNA damage in hydrogen peroxide-induced injury to endothelial cells: Role of activation of poly(ADP-ribose)polymerase. Biochim. Biophys. Acta 1092, 319-325 (1991).
39. Said, S.I., Berisha, H.I. & Pakbaz, H. Excitotoxicity in the lung: N-Methyl-D-aspartate-induced, nitric oxide-dependent, pulmonary edema is attenuated by vasoactive intestinal peptide and by inhibitors of poly(ADP-ribose) polymerase. Proc. Natl. Acad. Sci. USA 93, 4688-4692 (1996).
40. Szabo, C., Zingarelli, B., O'Connor, M. & Salzman, A.L. 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 (1996).
41. Szabo, C., Saunders, C., O'Connor, M. & Salzman, A.L. Peroxynitrite causes energy depletion and increases permeability via activation of poly(ADP-ribose) synthetase in pulmonary epithelial cells. Am. J. Respir. Cell. Mol. Mol. 16, 105-109 (1997).
42. Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. & Snyder, S.H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA 88, 7797-7801 (1991).
43. Bredt, D.S. et al. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7, 615-624 (1991).
44. Kaku, D.A., Goldberg, M.P. & Choi, D.W. Antagonism of non-NMDA receptors augments the neuroprotective effect of NMDA receptor blockade in cortical cultures subjected to prolonged deprivation of oxygen and glucose. Brain Res. 554, 344-337 (1991).
45. Monyer, H. et al. Oxygen or glucose deprivation-induced neuronal injury in cortical cell cultures is reduced by tetanus toxin. Neuron 8, 967-973 (1992).
46. Bederson, J.B. et al. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17, 1304-1308 (1986).
47. Kupper, J.H., van Gool, L., Muller, M. & Burkle, A. Detection of poly(ADP-ribose) polymerase and its reaction product poly(ADP-ribose) by immunocytochemistry. Histochem. J. 28, 391-395 (1996).