Molecular regulation of DNA damage-induced apoptosis in neurons of cerebral cortex

Cerebral Cortex

Volumn 19, Issue 6, 2009, Pages 1273-1293

  Martin, Lee J ^a   Liu, Zhiping ^a   Pipino, Jacqueline ^a   Chestnut, Barry ^a   Landek, Melissa A ^a  

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

Author keywords

Alzheimer's disease; ATM; Neonatal brain injury; P53; Parkinson's disease; Stroke

Indexed keywords

ABELSON KINASE; ATM PROTEIN; DNA; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); MITOCHONDRIAL PROTEIN; PIFITHRIN ALPHA; PROTEIN BAK; PROTEIN BAX; PROTEIN P53;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN CORTEX; CELL ACTIVATION; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME INHIBITION; IN VIVO STUDY; MITOCHONDRION; MOLECULAR DYNAMICS; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELLS, CULTURED; CEREBRAL CORTEX; DNA DAMAGE; MICE; NEURONS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 66549125541     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhn167     Document Type: Article

References (92)

1. Adamec E, Vonsattel JP, Nixon RA. 1999. DNA strand breaks in Alzheimer's disease. Brain Res. 849: 67-77.
2. Bendixen C, Thomsen B, Alsner J, Westergaard O. 1990. Camptothecin- stabilized topoisomerase I-DNA adducts cause premature termination of transcription. Biochemistry. 29: 5613-5619. (Pubitemid 20202289)
3. Bernardi P, Krauskopf A, Basso E, Petronilli V, Blalchy-Dyson E, Di Lisa F, Forte MA. 2006. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 273: 2077-2099.
4. Blasina A, Price BD, Turenne GA, McGowan CH. 1999. Caffeine inhibits the checkpoint kinase ATM. Curr Biol. 9: 1135-1138. (Pubitemid 29504487)
5. Bombrun A, Gerber P, Casi G, Terradillos O, Antonsson B, Halazy S. 2003. 3,6-Dibromocarbazole piperazine derivatives of 2-propanol as first inhibitors of cytochrome c release via bax channel modulation.J Med Chem. 46: 4365-4368. (Pubitemid 37238739)
6. Breunig JJ, Arellano JI, Macklis JD, Rakic P. 2007. Everything that glitters isn't gold: a critical review of postnatal neural precursor analysis. Cell Stem Cell. 1: 612-627. (Pubitemid 350215339)
7. Chao C, Saito S, Anderson Cw, Appella E, Xu Y. 2000. Phosphorylation of murine p53 at Ser-18 regulates the p53 response to DNA damage. Proc Natl Acad Sci USA. 97: 11936-11941.
8. Chen J, Jin K, Chen M, Pei W, Kawaguchi K, Greenberg DA, Simon RP. 1997. Early detection of DNA strand breaks in the brain after transient focal ischemia: implications for the role of DNA damage in apoptosis and neuronal cell death. J Neurochem. 69: 232-245. (Pubitemid 27274177)
9. Chen Y-H, Zhang Y-H, Zhang H-J, Liu D-Z, Gu M, Li J-Y, Wu F, Zhu X-Z, Li J, Nan F-J. 2006. Design, synthesis, and biological evaluation of isoquinoline-1,3,4,-trione derivative as potent caspase-3 inhibitors. J Med Chem. 49: 1613-1623. (Pubitemid 43376506)
10. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. 2004. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 303: 1010-1014. (Pubitemid 38209704)
11. Clark RSB, Chen M, Kochanek PM, Watkins SC, Jin KL, Draviam R, Nathaniel PD, Pinto R, Marion DW, Graham SH. 2001. Detection of single- and double-strand DNA breaks after traumatic brain injury in rats: comparison of in situ labeling techniques using DNA polymerase I, the Klenow fragment of DNA polymerase I, and terminal deoxynucleotidyl transferase. J Neurotrauma. 18: 675-689. (Pubitemid 32708985)
12. Cregan SP, Arbour NA, MacLaurin JG, Callaghan SM, Fortin A, Cheung ECC, Guberman DS, Park DS, Slack RS. 2004. p53 activation domain 1 is essential fro PUMA upregulation and p53-mediated neuronal cell death. J Neurosci. 24: 10003-10012. (Pubitemid 39463582)
13. Cregan SP, MacLaurin JG, Craig CG, Robertson GS, Nicholson DW, Park DS, Slack RS. 1999. Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons. J Neurosci.19: 7860-7869. (Pubitemid 30225784)
14. De la Monte SM, Sohn YK, Wands JR. 1997. Correlates of p53- and Fas (CD95)-mediated apoptosis in Alzheimer's disease. J Neurol Sci.152: 73-83. (Pubitemid 27469712)
15. D'Sa-Eipper C, Leonard JR, Putcha G, Zheng TS, Flavell RA, Rakic P,Kuida K, Roth KA. 2001. DNA damage-induced neural precursor cell apoptosis requires p53 and caspase 9 but neither Bax nor caspase 3. Development. 126: 137-146. (Pubitemid 32097941)
16. Dumaz N, Milne DM, Jardine LJ, Meek DW. 2001. Critical roles for the serine 20, but not the serine 15, phosphorylation site and for the polyproline domain in regulating p53 turnover. Biochem J.359: 469-1464
17. El-Mir M-Y, Detaille D, R-Villanueva G, Delgado-esteban M, Guigas B, Atrtia S, Fontaine E, Almeida A, Leverve X. 2008. Neuroprotective role of antidiabetic drug metformin against apoptotic cell death in primary cortical neurons. J Mol Neurosci. 34: 77-87.
18. Endokido Y, Araki T, Tanaka K, Aizawa S, Hatanaka H. 1996. Involvement of p53 in DNA strand break-induced apoptosis in postmitotic CNS neurons. Eur J Neurosci. 8: 1812-1821. (Pubitemid 26302277)
19. Figueroa-Masot XA, Hetman M, Higgins MJ, Kokot N, Xia Z. 2001. Taxol induces apoptosis in cortical neurons by a mechanism independent ofBcl-2 phosphorylation. J Neurosci. 21:46-57-- 46-67.
20. Giaccia AJ, Kastan MB. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12: 2973-2983. (Pubitemid 28469299)
21. Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, Parisi JE, Hyman BT. 1997. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol.41: 17-24. (Pubitemid 27057088)
22. Hedreen JC, Peyser CE, Folstein SE, Ross CA. 1991. Neuronal loss in layers V and VI ofcerebral cortex in Huntington's disease. Neurosci Lett. 133: 257-261.
23. Hetz C, Vite P-A, Bombrun A, Rostovtseva TK, Montessuit S, Hiver A, Schwarz MK, Chruch DJ, Kosrmeyer SJ, Martinou J-C, et al. 2005. Bax channel inhibitors prevent mitochondrion-mediated apoptosis and protect neurons in a model of global brain ischemia. J Biol Chem. 280: 42960-42970. (Pubitemid 43049259)
24. Hickson I, Zhao Y, Richardson CJ, Green SJ, Martin NMB, Orr AI, Reaper PM, Jackson SP, Curtin NJ, Smith GCM. 2004. Identification and characterization of a novel and specific inhibitor of the ataxia- telangiectasia mutated kinase ATM. Cancer Res. 64: 9152-9159. (Pubitemid 39665530)
25. Holinger EP, Chittenden T, Lutz RJ. 1999. Bak BH3 peptides antagonize Bcl-xL function and induce apoptosis through cytochrome c- independent activation of caspases. J Biol Chem. 274: 13298-13304.
26. Hou ST, MacManus JP. 2002. Molecular mechanisms of cerebral ischemia-induced neuronal death. Intl Rev Cytol. 221: 93-148. (Pubitemid 35429861)
27. Hsu YT, Wotter KG, Youle RJ. 1997. Cytosol-to-membrane redistribution of Bax and Bcl-X( L) during apoptosis. Proc. Natl. Acad. Sci. USA.94: 3668-3672.
28. Huang D, Shenoy A, Cui J, Huang W, Liu PK. 2000. In situ detection of AP sites and DNA strand breaks bearing 3'-phosphate termini in ischemic mouse brain. FASEB J. 14: 407-417. (Pubitemid 30086078)
29. Igata E, Inoue T, Ohtani-Fujita N, Sowa Y, Tsujimoto Y, Sakai T. 1999. Molecular cloning and functional analysis of the murine bax gene promoter. Gene. 238: 407-415. (Pubitemid 29446176)
30. Jeffers JR, Parganas E, Lee Y, Yang C, Wang J, Brennan J, MacLean KH,Han J, Chittenden T, Ihle JN, et al. 2003. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways.Cancer Cell. 4: 321-328. (Pubitemid 37329796)
31. Johnson MD, Kinoshita Y, Xiang H, Ghatan S, Morrison RS. 1999. Contribution of p53-dependent caspase activation to neuronal cell death declines with neuronal maturation. JNeurosci. 19: 2996-3006. (Pubitemid 29173996)
32. Johnston MV. 2004. Clinical disorders of brain plasticity. Brain Dev.26: 73-80. (Pubitemid 38229619)
33. Kannan K, Amariglio N, Rechavi G, Jakob-Hirsch J, Kela I, Kaminski N, Getz G, Domany E, Givol D. 2001. DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene.20: 2225-2234. (Pubitemid 32531280)
34. Kastan MB, Lim D-S. 2000. The many substrates and functions of ATM. Nat Mol Cell Biol. 1: 179-186.
35. Keramaris E, Hirao A, Slack RS, Mak TW, Park DS. 2003. Ataxia telangiectasia-mutated protein can regulate p53 and neuronal death independent of chk2 in response to DNA damage. J Biol Chem.278: 37782-37789. (Pubitemid 37175305)
36. Keramaris E, Stefanis L, MacLaurin J, Harada N, Takaku K, Ishikawa T-O, Taketa MM, Robertson GS, Nicholson DW, Slack RS, et al. 2000. Involvement of caspase 3 in apoptotic death of cortical neurons evoked by DNA damage. Mol Cell Neurosci. 15: 368-379. (Pubitemid 30266273)
37. Kharbanda S, Yuan Z-M, Weichselbaum R, Kufe D. 1998. Determination of cell fate by c-Abl activation in response to DNA damage. Oncogene. 17: 3309-3318. (Pubitemid 29043983)
38. Kindzelskii AL, Petty HR. 1999. Ultrasensitive detection of hydrogen peroxide-mediated DNA damage after alkaline single cell gel electrophoresis using occultation microscopy and TUNEL labeling. Mutat Res. 426: 11-22. (Pubitemid 29206467)
39. Komarov PG, Komarova EA, Kondratov RV, Christov-Teselkov K, Coon JS, Chernov MV, Gudkov AV. 1999. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science. 285: 1733-1737. (Pubitemid 29428873)
40. Kuan C-Y, Schoemer AJ, Lu A, Burns KA, Weng W-L, Williams MT, Strauss KI, Vorhees CV, Flavell RA, Davis RJ, et al. 2004. Hypoxia- ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci. 24: 10763-110722
41. Lee Y, Chong MJ, McKinnon PJ. 2001. Ataxia telangiectasia mutated- dependent apoptosis after genotoxic stress in the developing nervous system is determined by cellular differentiation status. J Neurosci. 21: 6687-6693. (Pubitemid 32781113)
42. Lesuisse C, Martin LJ. 2002a. Long-term culture of mouse cortical neurons as a model for neuronal development, aging, and death. J Neurobiol. 51: 9-23. (Pubitemid 34242501)
43. Lesuisse C, Martin LJ. 2002b. Immature and mature cortical neurons engage different apoptotic mechanisms involving caspase-3 and the MAP kinase pathway. J Cereb Blood Flow Metab. 22: 935-950. (Pubitemid 34831600)
44. Lindahl T. 1993. Instability and decay of the primary structure of DNA.Nature. 362: 709-715.
45. MacDonald V, Halliday GM. 2002. Selective loss of pyramidal neurons inthe pre-supplementary motor cortex in Parkinson's disease. MovDisord. 17: 1166-1173. (Pubitemid 36041329)
46. Macleod MR, Ramage LE, McGregor A, Seckl JR. 2003. Reduced NMDA-induced apoptosis in neurons lacking ataxia telangiectasia mutated protein. NeuroReport. 14: 215-217. (Pubitemid 36308413)
47. Martin LJ. 2000. p53 is abnormally elevated and active in the CNS of patients with amyotrophic lateral sclerosis. Neurobiol Dis.7: 613-622. (Pubitemid 32044286)
48. Martin LJ. 2001. Neuronal cell death in nervous system development, disease, and injury. Int J Mol Med. 7: 455-478.
49. Martin LJ. 2008. Forthcoming. Mechanisms of neurodegeneration and therapeutics in animal models ofhypoxic-ischemic encephalopathy. In: Stevenson DK, Benitz WE, Sunshine P, editors. Fetal and neonatal brain brain injury. 4th ed. Cambridge: Cambridge University Press.
50. Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera- Cailliau C. 1998. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull. 46: 281-309. (Pubitemid 28294822)
51. Martin LJ, Liu Z. 2002. DNA damage profiling in motor neurons: a single- cell analysis by comet assay. Neurochem Res. 27: 1093-1104. (Pubitemid 35316105)
52. Martin LJ, Liu Z, Troncoso JC, Price DL. 2005. Neuronal cell death in human neurodegenerative diseases and their animal/cell models. In: Holcik M, LaCasse E, Korneluk R, MacKenzie A, editors. Apoptosis in health and disease. Cambridge: Cambridge University Press.p. 242-315.
53. Martin LJ, Price AC, McClendon KB, Al-Abdulla NA, Subramaniam JR, Wong PC, Liu Z. 2003. Early events of target deprivation/axotomy- induced neuronal apoptosis in vivo: oxidative stress, DNA damage, p53 phosphorylation and subcellular redistribution of death proteins. J Neurochem. 85: 234-247. (Pubitemid 36389713)
54. McArthur JC, BrewBJ, Nath A. 2005. Neurological complications of HIV infection. Lancet Neurol. 4: 543-555. (Pubitemid 41139976)
55. Miyashita T, Reed JC. 1995. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 80: 293-299.
56. Morris EJ, Geller HM. 1996. Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity. J Cell Biol. 134: 757-770. (Pubitemid 26269145)
57. Morrison RS, Kinoshita Y Johnson MD, Guo W, Garden GA. 2003. p53- dependent cell death signaling in neurons. Neurochem Res. 28: 15-27. (Pubitemid 36173223)
58. Mullaart E, Boerrigter METI, Ravid R, Swaab DF, Vijg J. 1990. Increased levels of DNA breaks in cerebral cortex of Alzheimer's disease patients. Neurobiol Aging. 11: 169-173. (Pubitemid 20181893)
59. Nakagawa K, Taya Y, Tamai K, Yamaizumi. 1999. Requirement of ATM in phosphorylation of the human p53 protein at serine 15 following DNA double-strand breaks. Mol Cell Biol. 19: 2828-2834. (Pubitemid 29144526)
60. Nakajima M, kashiwagi K, Ohta J, Furkawa S, Hayashi K, Kawashima T, Hayashi Y. 1994. Etoposide induces programmed death in neurons cultured from the fetal rat central nervous system. Brain Res.4: 350-352. (Pubitemid 24101305)
61. Narasimhaiah R, Tuchman A, Lin SL, Naegele JR. 2005. Oxidative damage and defective DNA repair is linked to apoptosis of migrating neurons and progenitors during cerebral cortex development in Ku70-deficient mice. Cereb Cortex. 15: 696-707. (Pubitemid 40696110)
62. Nechushtan A, Smith CL, Lamensdorf I, Yoon S-H, Youle RJ. 2001. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol. 153: 1265-1276. (Pubitemid 34289264)
63. Nieves-Neira W, Pommier Y. 1999. Apoptotic response to camptothecin and 7-hydroxystaurosporine (UCN-01) in the 8 human breast cancer cell lines of the NCI anticancer drug screen: multifactorial relationships with topoisomerase I, protein kinase, Bcl-2, p53, MDM- 2 and caspase pathways. Int J Cancer. 82: 396-404. (Pubitemid 29302981)
64. Nihei K, McKee AC, Kowall NW. 1993. Pattern of neuronal degeneration in motor cortex ofamyotrophic lateral sclerosis patients. Acta Neuropathol. 86: 55-64. (Pubitemid 23249074)
65. Nitiss JL, Wang JC. 1996. Mechanisms of cell killing by drugs that trap covalent complexes between DNA topoisomerases and DNA. Mol Pharmacol. 50: 1095-1102. (Pubitemid 26384847)
66. Northington FJ, Zelaya ME, O'Riordan DP, Blomgren K, Flock DL, Hagberg H, Ferriero DM, Martin LJ. 2007. Failure to complete apoptosis following neonatal hypoxia-ischemia manifests as ''continuum'' phenotype of cell death and occurs with multiple manifestations of mitochondrial dysfunction in rodent forebrain. Neuroscience. 149: 822-833. (Pubitemid 350130287)
67. Ohyagi Y, Asahara H, Chui D-H, Tsuruta Y, Sakae N, Miyoshi K, Yamada T, Kikuchi H, Taniwaki T, Murai H, et al. 2005. Intracellular Ab activates p53 promoter: a pathway to neurodegeneration in Alzheimer's disease. FASEB J. 19: 225-257.
68. Park DS, Morris EJ, Stefanis L, Troy CM, Shelanski ML, Geller HM, Greene LA. 1998. Multiple pathways of neuronal death induced by DNA-damaging agents, NGF deprivation, and oxidative stress.J Neurosci. 18: 830-840. (Pubitemid 28112906)
69. Pohl U, Wagenknecht B, Naumann U, Welleer M. 1999. p53 enhances Bak and CD95 expression in human malignant glioma cells but does not enhance CD95L-induced apoptosis. Cell Physiol Biochem.9: 29-37. (Pubitemid 29264201)
70. Portera-Cailliau C, Price DL, Martin LJ. 1997. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol. 378: 70-87. (Pubitemid 27057532)
71. Raina D, Mishra N, Kumar S, Kharbanda S, Saxena S, Kufe D. 2002. Inhibition of c-Abl with STI571 attenuates stress-activated protein kinase activation and apoptosis in the cellular response to 1-β- D-arabinofuranosylcytosine. Mol Pharmacol. 61: 1489-1495. (Pubitemid 34575758)
72. Rakic P. 2002. Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci. 3: 65-71. (Pubitemid 135706566)
73. Romero AA, Gross SR, Cheng KY, Goldsmith NK, Geller HM. 2003. An age-related increase in resistance to DNA damage-induced apopto- tic cell death is associated with development of DNA repair. J Neurochem. 84: 1275-1287. Sawada M, Hayes P, Matsuyama S. 2003. Cytoprotective membrane- permeable peptides designed from Bax-binding domain of Ku70.Nat Cell Biol. 5: 352-357. (Pubitemid 36343594)
74. Sawada M, Hayes P, Matsuyama S. 2003. Cytoprotective membrane- permeable peptides designed from Bax-binding domain of Ku70.Nat Cell Biol. 5: 352-357. (Pubitemid 36432301)
75. Schmidt T, Korner K, Karsunky H, Korsmeyer S, Muller R, Moroy T. 1999. The activity of the murine Bax promoter is regulated by Sp1/3 and E-box binding protein but not by p53. Cell Death Differ.6: 873-882. (Pubitemid 29488085)
76. Shaikh AY, Martin LJ. 2002. DNA base-excision repair enzyme apurinic/ apyrimidinic endonuclease/redox factor-1 is increased and competent in brain and spinal cord of individuals with amyotrophic lateral sclerosis. Neuromolecular Med. 2: 47-60. (Pubitemid 37012509)
77. Shimizu S, Konishi A, Kodama T, Tsujimoto Y. 2000. BH4 domain of antiapoptotic Bcl-2 members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc Natl Acad Sci USA. 97: 3100-3105. (Pubitemid 30183262)
78. Shimizu S, Narita M, Tsujimoto Y. 1999. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial VDAC. Nature. 399: 483-487. (Pubitemid 29258855)
79. Slack RS, Belliveau DJ, Rosenberg M, Atwal J, Lochmuller H, Aloyz R, Haghighi A, Lach B, Seth P, Cooper E, et al. 1996. Adenovirus- mediated gene transfer of the tumor suppressor, p53, induces apoptosis in postmitotic neurons. J Cell Biol. 135: 1085-1096. (Pubitemid 26403780)
80. Stefanis L, Park DS, Friedman WJ, Greene LA. 1999. Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J Neurosci. 19: 6235-6247. (Pubitemid 29347424)
81. Strom E, Sathe S, Kamarov PG, Chernova OB, Pavlovska I, Shyshynova I, Bosykh DA, Burdelya LG, Macklis RM, Skaliter R, et al. 2006. Small- molecule inhibitor of p53-binding to mitochondria protects mice from gamma radiation. Nat Chem Biol. 2: 474-479. (Pubitemid 44266309)
82. Sze C-I, Troncoso JC, Kawas C, Mouton P, Price DL, Martin LJ. 1997. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease.J Neuropathol Exp Neurol. 56: 993-1944
83. Thornborrow EC, Patel S, Mastropietro AE, Schwartzfarb EM, Manfredi JJ. 2002. A conserved intronic response element mediates direct p53-dependent transcriptional activation of both the human and murine bax genes. Oncogene. 21: 990-999. (Pubitemid 34174511)
84. Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu J-C, Sasaki YF. 2000. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing.Environ Mol Mutagen. 35: 206-221. (Pubitemid 30196665)
85. Wang G-Q, Gastman BR, Wieckowski E, Goldstein LA, Gambotto A, Kim T-H, Fang B, Rabinovitz A, Yim XM, Rabinowich H. 2001. A role for mitochondrial Bak in apoptotic response to anticancer drugs. J Biol. Chem. 276: 34307-34317.
86. Wong HK, Fricker M, Wyttenbach A, Villunger A, Michalak EM, Strasser A, Tolkovsky AM. 2005. Mutually exclusive subsets of BH3-only protein are activated by p53 and c-Jun N-terminal kinase/ c-Jun signaling pathways during cortical neuron apoptosis induced by arsenite. Mol Cell Biol. 25: 8732-8747. (Pubitemid 41369190)
87. Wyttenbach A, Tolkovsky AM. 2006. The BH3-only protein Puma is both necessary and sufficient for neuronal apoptosis induced by DNA damage in sympathetic neurons. J Neurochem. 96: 1213-1226.
88. Xiang H, Hochman DW, Sava H, Fujwara T, Schwartzkroin PA,Morrison RS. 1996. Evidence for p53-mediated modulation of neuronal viability. J Neurosci. 16: 6753-6765. (Pubitemid 26359359)
89. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS. 1998. Bax involvement in p53-mediated neuronal cell death. J Neurosci. 18: 1363-1373. (Pubitemid 28082421)
90. Yang Y, Geldmacher DS, Herrup K. 2001. DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci. 21: 2661-2668. (Pubitemid 32298208)
91. 1-42 through p53 and Bax in cultured primary human neurons. J Cell Biol. 156: 519-529. (Pubitemid 40246773)
92. 1-42 through p53 and Bax in cultured primary human neurons. J Cell Biol. 156: 519-529. (Pubitemid 34839899)