Advertisement

PARP Activation and Necrotic Cell Death

Chapter
Part of the Cell Death in Biology and Diseases book series (CELLDEATH)

Abstract

Poly(ADP-ribose) polymerase (PARP) protein family consists of at least 17 members. They catalyze the chemical reaction termed polyADP-ribosylation, which functions to cleave nicotinamide adenine dinucleotide into ADP-ribose and nicotinamide mononucleotide (NAM), and transfer ADP-ribose to glutamate, aspartate, or lysine residues on substrate proteins to form poly(ADP-ribosyl)ated chains. PARP proteins play an essential role in chromatin organization, DNA repair, replication, and transcriptional regulation. Upon excessive DNA damage, PARP is hyperactivated and causes cell death. This chapter summarizes the molecular regulation of cell death by PARP.

Keywords

Mitochondrial Permeability Transition PARP Inhibitor Nicotinamide Adenine Dinucleotide Necrotic Cell Death PARP Activation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aguilar-Quesada R, Munoz-Gamez JA, Martin-Oliva D, Peralta A, Valenzuela MT, Matinez-Romero R, Quiles-Perez R, Menissier-de Murcia J, de Murcia G, Ruiz de Almodovar M, Oliver FJ (2007) Interaction between ATM and PARP-1 in response to DNA damage and sensitization of ATM deficient cells through PARP inhibition. BMC Mol Biol 8:29PubMedCentralPubMedCrossRefGoogle Scholar
  2. Alano CC, Tran A, Tao R, Ying W, Karliner JS, Swanson RA (2007) Differences among cell types in NAD(+) compartmentalization: a comparison of neurons, astrocytes, and cardiac myocytes. J Neurosci Res 85:3378–3385PubMedCrossRefGoogle Scholar
  3. Albert JM, Cao C, Kim KW, Willey CD, Geng L, Xiao D, Wang H, Sandler A, Johnson DH, Colevas AD, Low J, Rothenberg ML, Lu B (2007) Inhibition of poly(ADP-ribose) polymerase enhances cell death and improves tumor growth delay in irradiated lung cancer models. Clin Cancer Res 13:3033–3042PubMedCrossRefGoogle Scholar
  4. Alexander A, Cai SL, Kim J, Nanez A, Sahin M, MacLean KH, Inoki K, Guan KL, Shen J, Person MD, Kusewitt D, Mills GB, Kastan MB, Walker CL (2010) ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci U S A 107:4153–4158PubMedCentralPubMedCrossRefGoogle Scholar
  5. Andrabi SA, Kim NS, Yu SW, Wang H, Koh DW, Sasaki M, Klaus JA, Otsuka T, Zhang Z, Koehler RC, Hurn PD, Poirier GG, Dawson VL, Dawson TM (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci U S A 103:18308–18313PubMedCentralPubMedCrossRefGoogle Scholar
  6. Beneke S (2012) Regulation of chromatin structure by poly(ADP-ribosyl)ation. Front Genet 3:169PubMedCentralPubMedCrossRefGoogle Scholar
  7. Berger NA, Sims JL, Catino DM, Berger SJ (1983) Poly(ADP-ribose) polymerase mediates the suicide response to massive DNA damage: studies in normal and DNA-repair defective cells. Princess Takamatsu Symp 13:219–226PubMedGoogle Scholar
  8. Bianchi ME, Manfredi A (2004) Chromatin and cell death. Biochim Biophys Acta 1677:181–186PubMedCrossRefGoogle Scholar
  9. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A, Rubartelli A, Agresti A, Bianchi ME (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 22:5551–5560PubMedCentralPubMedCrossRefGoogle Scholar
  10. Christophe M, Nicolas S (2006) Mitochondria: a target for neuroprotective interventions in cerebral ischemia-reperfusion. Curr Pharm Des 12:739–757PubMedCrossRefGoogle Scholar
  11. Ciccia A, Elledge SJ (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40:179–204PubMedCentralPubMedCrossRefGoogle Scholar
  12. Cipriani G, Rapizzi E, Vannacci A, Rizzuto R, Moroni F, Chiarugi A (2005) Nuclear poly(ADP-ribose) polymerase-1 rapidly triggers mitochondrial dysfunction. J Biol Chem 280:17227–17234PubMedCrossRefGoogle Scholar
  13. Cozzi A, Cipriani G, Fossati S, Faraco G, Formentini L, Min W, Cortes U, Wang ZQ, Moroni F, Chiarugi A (2006) Poly(ADP-ribose) accumulation and enhancement of postischemic brain damage in 110-kDa poly(ADP-ribose) glycohydrolase null mice. J Cereb Blood Flow Metab 26:684–695PubMedCrossRefGoogle Scholar
  14. Cregan SP, Dawson VL, Slack RS (2004) Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23:2785–2796PubMedCrossRefGoogle Scholar
  15. Culmsee C, Zhu C, Landshamer S, Becattini B, Wagner E, Pellecchia M, Blomgren K, Plesnila N (2005) Apoptosis-inducing factor triggered by poly(ADP-ribose) polymerase and Bid mediates neuronal cell death after oxygen-glucose deprivation and focal cerebral ischemia. J Neurosci 25:10262–10272PubMedCrossRefGoogle Scholar
  16. Cuzzocrea S, Wang ZQ (2005) Role of poly(ADP-ribose) glycohydrolase (PARG) in shock, ischemia and reperfusion. Pharmacol Res 52:100–108PubMedCrossRefGoogle Scholar
  17. Czura CJ, Wang H, Tracey KJ (2001) Dual roles for HMGB1: DNA binding and cytokine. J Endotoxin Res 7:315–321PubMedCrossRefGoogle Scholar
  18. D’Amours D, Desnoyers S, D’Silva I, Poirier GG (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342(Pt 2):249–268PubMedCentralPubMedCrossRefGoogle Scholar
  19. Dawson VL, Dawson TM (2004) Deadly conversations: nuclear-mitochondrial cross-talk. J Bioenerg Biomembr 36:287–294PubMedCrossRefGoogle Scholar
  20. Decker P, Muller S (2002) Modulating poly (ADP-ribose) polymerase activity: potential for the prevention and therapy of pathogenic situations involving DNA damage and oxidative stress. Curr Pharm Biotechnol 3:275–283PubMedCrossRefGoogle Scholar
  21. Ditsworth D, Zong WX, Thompson CB (2007) Activation of poly(ADP)-ribose polymerase (PARP-1) induces release of the pro-inflammatory mediator HMGB1 from the nucleus. J Biol Chem 282:17845–17854PubMedCentralPubMedCrossRefGoogle Scholar
  22. Dodoni G, Canton M, Petronilli V, Bernardi P, Di Lisa F (2004) Induction of the mitochondrial permeability transition by the DNA alkylating agent N-methyl-N′-nitro-N-nitrosoguanidine. Sorting cause and consequence of mitochondrial dysfunction. Biochim Biophys Acta 1658:58–63PubMedCrossRefGoogle Scholar
  23. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ (2011) Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331:456–461PubMedCentralPubMedCrossRefGoogle Scholar
  24. Fossati S, Cipriani G, Moroni F, Chiarugi A (2007) Neither energy collapse nor transcription underlie in vitro neurotoxicity of poly(ADP-ribose) polymerase hyper-activation. Neurochem Int 50:203–210PubMedCrossRefGoogle Scholar
  25. Fossati S, Formentini L, Wang ZQ, Moroni F, Chiarugi A (2006) Poly(ADP-ribosyl)ation regulates heat shock factor-1 activity and the heat shock response in murine fibroblasts. Biochem Cell Biol 84:703–712PubMedCrossRefGoogle Scholar
  26. Gibson BA, Kraus WL (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13:411–424PubMedCrossRefGoogle Scholar
  27. Goto W, Ota T, Morikawa N, Otori Y, Hara H, Kawazu K, Miyawaki N, Tano Y (2002) Protective effects of timolol against the neuronal damage induced by glutamate and ischemia in the rat retina. Brain Res 958:10–19PubMedCrossRefGoogle Scholar
  28. Guerriero JL, Ditsworth D, Catanzaro JM, Sabino G, Furie MB, Kew RR, Crawford HC, Zong WX (2011) DNA alkylating therapy induces tumor regression through an HMGB1-mediated activation of innate immunity. J Immunol 186(6):3517–3526PubMedCentralPubMedCrossRefGoogle Scholar
  29. Gurbuxani S, Schmitt E, Cande C, Parcellier A, Hammann A, Daugas E, Kouranti I, Spahr C, Pance A, Kroemer G, Garrido C (2003) Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor. Oncogene 22:6669–6678PubMedCrossRefGoogle Scholar
  30. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30:214–226PubMedCentralPubMedCrossRefGoogle Scholar
  31. Haince JF, Kozlov S, Dawson VL, Dawson TM, Hendzel MJ, Lavin MF, Poirier GG (2007) Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J Biol Chem 282:16441–16453PubMedCrossRefGoogle Scholar
  32. Hakme A, Wong HK, Dantzer F, Schreiber V (2008) The expanding field of poly(ADP-ribosyl)ation reactions. ‘Protein modifications: beyond the usual suspects’ review series. EMBO Rep 9:1094–1100PubMedCentralPubMedCrossRefGoogle Scholar
  33. Hanai S, Kanai M, Ohashi S, Okamoto K, Yamada M, Takahashi H, Miwa M (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc Natl Acad Sci U S A 101:82–86PubMedCentralPubMedCrossRefGoogle Scholar
  34. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774–785PubMedCrossRefGoogle Scholar
  35. Hassa PO, Haenni SS, Elser M, Hottiger MO (2006) Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev 70:789–829PubMedCentralPubMedCrossRefGoogle Scholar
  36. Hassa PO, Hottiger MO (2008) The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 13:3046–3082PubMedCrossRefGoogle Scholar
  37. Huang Q, Shen HM (2009) To die or to live: the dual role of poly(ADP-ribose) polymerase-1 in autophagy and necrosis under oxidative stress and DNA damage. Autophagy 5:273–276PubMedCrossRefGoogle Scholar
  38. Inoki K, Li Y, Xu T, Guan KL (2003) Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 17:1829–1834PubMedCentralPubMedCrossRefGoogle Scholar
  39. Jagtap P, Szabo C (2005) Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 4:421–440PubMedCrossRefGoogle Scholar
  40. Jesser M, Chypre C, Hog F, Mandel P (1993) Cytoplasmic poly(ADP-ribose)polymerase from mouse plasmacytoma free messenger ribonucleoprotein particles: purification and characterization. Biochem Biophys Res Commun 195:558–564PubMedCrossRefGoogle Scholar
  41. Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA (2006) Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci U S A 103:7136–7141PubMedCentralPubMedCrossRefGoogle Scholar
  42. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13:132–141PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kim MY, Zhang T, Kraus WL (2005) Poly(ADP-ribosyl)ation by PARP-1: ‘PAR-laying’ NAD+ into a nuclear signal. Genes Dev 19:1951–1967PubMedCrossRefGoogle Scholar
  44. Kofler J, Otsuka T, Zhang Z, Noppens R, Grafe MR, Koh DW, Dawson VL, de Murcia JM, Hurn PD, Traystman RJ (2006) Differential effect of PARP-2 deletion on brain injury after focal and global cerebral ischemia. J Cereb Blood Flow Metab 26:135–141PubMedCrossRefGoogle Scholar
  45. Kovacs K, Toth A, Deres P, Kalai T, Hideg K, Gallyas F Jr, Sumegi B (2006) Critical role of PI3-kinase/Akt activation in the PARP inhibitor induced heart function recovery during ischemia-reperfusion. Biochem Pharmacol 71:441–452PubMedCrossRefGoogle Scholar
  46. Langelier MF, Ruhl DD, Planck JL, Kraus WL, Pascal JM (2010) The Zn3 domain of human poly(ADP-ribose) polymerase-1 (PARP-1) functions in both DNA-dependent poly(ADP-ribose) synthesis activity and chromatin compaction. J Biol Chem 285:18877–18887PubMedCentralPubMedCrossRefGoogle Scholar
  47. Langelier MF, Servent KM, Rogers EE, Pascal JM (2008) A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation. J Biol Chem 283:4105–4114PubMedCrossRefGoogle Scholar
  48. Liu K, Mori S, Takahashi HK, Tomono Y, Wake H, Kanke T, Sato Y, Hiraga N, Adachi N, Yoshino T, Nishibori M (2007) Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J 21:3904–3916PubMedCrossRefGoogle Scholar
  49. Mangerich A, Burkle A (2011) How to kill tumor cells with inhibitors of poly(ADP-ribosyl)ation. Int J Cancer 128:251–265PubMedCrossRefGoogle Scholar
  50. Masmoudi A, el-Fetouaki J, Weltin D, Belhadj O, Mandel P (1993) Association of mitochondrial ADP-ribosyl transferase activity with the DNA-protein complex. Biochem Mol Biol Int 29:77–83PubMedGoogle Scholar
  51. Muller S, Scaffidi P, Degryse B, Bonaldi T, Ronfani L, Agresti A, Beltrame M, Bianchi ME (2001) New EMBO members’ review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J 20:4337–4340PubMedCentralPubMedCrossRefGoogle Scholar
  52. Munoz-Gamez JA, Rodriguez-Vargas JM, Quiles-Perez R, Aguilar-Quesada R, Martin-Oliva D, de Murcia G, Menissier de Murcia J, Almendros A, Ruiz de Almodovar M, Oliver FJ (2009) PARP-1 is involved in autophagy induced by DNA damage. Autophagy 5:61–74PubMedCrossRefGoogle Scholar
  53. Muthumani K, Choo AY, Zong WX, Madesh M, Hwang DS, Premkumar A, Thieu KP, Emmanuel J, Kumar S, Thompson CB, Weiner DB (2006) The HIV-1 Vpr and glucocorticoid receptor complex is a gain-of-function interaction that prevents the nuclear localization of PARP-1. Nat Cell Biol 8:170–179PubMedCentralPubMedCrossRefGoogle Scholar
  54. Palfi A, Toth A, Kulcsar G, Hanto K, Deres P, Bartha E, Halmosi R, Szabados E, Czopf L, Kalai T, Hideg K, Sumegi B, Toth K (2005) The role of Akt and mitogen-activated protein kinase systems in the protective effect of poly(ADP-ribose) polymerase inhibition in Langendorff perfused and in isoproterenol-damaged rat hearts. J Pharmacol Exp Ther 315:273–282PubMedCrossRefGoogle Scholar
  55. Raucci A, Palumbo R, Bianchi ME (2007) HMGB1: a signal of necrosis. Autoimmunity 40:285–289PubMedCrossRefGoogle Scholar
  56. Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jaattela M, Penninger JM, Garrido C, Kroemer G (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3:839–843PubMedCrossRefGoogle Scholar
  57. Sanges D, Comitato A, Tammaro R, Marigo V (2006) Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors. Proc Natl Acad Sci U S A 103:17366–17371PubMedCentralPubMedCrossRefGoogle Scholar
  58. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191–195PubMedCrossRefGoogle Scholar
  59. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517–528PubMedCrossRefGoogle Scholar
  60. Seth R, Yang C, Kaushal V, Shah SV, Kaushal GP (2005) p53-dependent caspase-2 activation in mitochondrial release of apoptosis-inducing factor and its role in renal tubular epithelial cell injury. J Biol Chem 280:31230–31239PubMedCrossRefGoogle Scholar
  61. Sevigny M, Garnier P, Kauppinen T, Swanson R (2003) Heat shock-induced Hsp70 expression in murine astrocytes does not require poly(ADP-ribose) polymerase activity. Cell Physiol Biochem 13:297–300PubMedCrossRefGoogle Scholar
  62. Sims JL, Berger SJ, Berger NA (1983) Poly(ADP-ribose) Polymerase inhibitors preserve nicotinamide adenine dinucleotide and adenosine 5′-triphosphate pools in DNA-damaged cells: mechanism of stimulation of unscheduled DNA synthesis. Biochemistry 22:5188–5194PubMedCrossRefGoogle Scholar
  63. Skulachev VP (2006) Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11:473–485PubMedCrossRefGoogle Scholar
  64. Suh J, Payvandi F, Edelstein LC, Amenta PS, Zong WX, Gelinas C, Rabson AB (2002) Mechanisms of constitutive NF-kappaB activation in human prostate cancer cells. Prostate 52:183–200PubMedCrossRefGoogle Scholar
  65. Tapodi A, Debreceni B, Hanto K, Bognar Z, Wittmann I, Gallyas F Jr, Varbiro G, Sumegi B (2005) Pivotal role of Akt activation in mitochondrial protection and cell survival by poly(ADP-ribose)polymerase-1 inhibition in oxidative stress. J Biol Chem 280:35767–35775PubMedCrossRefGoogle Scholar
  66. Thomassin H, Niedergang C, Mandel P (1985) Characterization of the poly(ADP-ribose) polymerase associated with free cytoplasmic mRNA-protein particles. Biochem Biophys Res Commun 133:654–661PubMedCrossRefGoogle Scholar
  67. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR (2005) The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201:1135–1143PubMedCentralPubMedCrossRefGoogle Scholar
  68. Ulloa L, Messmer D (2006) High-mobility group box 1 (HMGB1) protein: friend and foe. Cytokine Growth Factor Rev 17:189–201PubMedCrossRefGoogle Scholar
  69. van Wijk SJ, Hageman GJ (2005) Poly(ADP-ribose) polymerase-1 mediated caspase-independent cell death after ischemia/reperfusion. Free Radic Biol Med 39:81–90PubMedGoogle Scholar
  70. Veres B, Gallyas F Jr, Varbiro G, Berente Z, Osz E, Szekeres G, Szabo C, Sumegi B (2003) Decrease of the inflammatory response and induction of the Akt/protein kinase B pathway by poly-(ADP-ribose) polymerase 1 inhibitor in endotoxin-induced septic shock. Biochem Pharmacol 65:1373–1382PubMedCrossRefGoogle Scholar
  71. Virag L (2005a) The expanding universe of poly(ADP-ribosyl)ation. Cell Mol Life Sci 62:719–720PubMedCrossRefGoogle Scholar
  72. Virag L (2005b) Structure and function of poly(ADP-ribose) polymerase-1: role in oxidative stress-related pathologies. Curr Vasc Pharmacol 3:209–214PubMedCrossRefGoogle Scholar
  73. Virag L, Szabo C (2002) The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 54:375–429PubMedCrossRefGoogle Scholar
  74. Wang H, Yu SW, Koh DW, Lew J, Coombs C, Bowers W, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J Neurosci 24:10963–10973PubMedCrossRefGoogle Scholar
  75. Xu Y, Huang S, Liu ZG, Han J (2006) Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/TRAF2-mediated JNK1 activation. J Biol Chem 281:8788–8795PubMedCrossRefGoogle Scholar
  76. Ying W, Alano CC, Garnier P, Swanson RA (2005) NAD+ as a metabolic link between DNA damage and cell death. J Neurosci Res 79:216–223PubMedCrossRefGoogle Scholar
  77. Ying W, Garnier P, Swanson RA (2003) NAD + repletion prevents PARP-1-induced glycolytic blockade and cell death in cultured mouse astrocytes. Biochem Biophys Res Commun 308:809–813PubMedCrossRefGoogle Scholar
  78. Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, Dawson VL (2006) Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci U S A 103:18314–18319PubMedCentralPubMedCrossRefGoogle Scholar
  79. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297:259–263PubMedCrossRefGoogle Scholar
  80. Yuan M, Siegel C, Zeng Z, Li J, Liu F, McCullough LD (2009) Sex differences in the response to activation of the poly (ADP-ribose) polymerase pathway after experimental stroke. Exp Neurol 217:210–218PubMedCrossRefGoogle Scholar
  81. Zhang J (2003) Are poly(ADP-ribosyl)ation by PARP-1 and deacetylation by Sir2 linked? Bioessays 25:808–814PubMedCrossRefGoogle Scholar
  82. Zhang S, Lin Y, Kim YS, Hande MP, Liu ZG, Shen HM (2007) c-Jun N-terminal kinase mediates hydrogen peroxide-induced cell death via sustained poly(ADP-ribose) polymerase-1 activation. Cell Death Differ 14:1001–1010PubMedCrossRefGoogle Scholar
  83. Zong WX, Ditsworth D, Bauer DE, Wang ZQ, Thompson CB (2004) Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 18:1272–1282PubMedCentralPubMedCrossRefGoogle Scholar
  84. Zong WX, Thompson CB (2006) Necrotic death as a cell fate. Genes Dev 20:1–15PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Molecular Genetics & MicrobiologyStony Brook UniversityStony BrookUSA

Personalised recommendations