Gene expression induced by cerebral ischemia: An apoptotic perspective

Journal of Cerebral Blood Flow and Metabolism

Volumn 17, Issue 8, 1997, Pages 815-832

  MacManus, John P ^a   Linnik, Matthew D ^b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b SANOFI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; PROTEIN P53;

APOPTOSIS; BRAIN ISCHEMIA; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMAN; MITOCHONDRIAL RESPIRATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

EID: 0030813422     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/aj.jcbfm.9590266     Document Type: Review

References (130)

1. Alarcon RM, Rupnow BA, Graeber TG, Knox SJ, Giaccia AJ (1996) Modulation of c-myc activity and apoptosis in vivo. Cancer Res 56:4315-4319
2. Ankarcrona M, Dypbukt JM, Orrenhius S, Nicotera P (1996a) Calcineurin and mitochondrial function in glutamate-induced neuronal cell death. FEBS Lett 394:321-324
3. Ankarcrona M, Zhivotovsky B, Holmstrom T, Diana A, Eriksson JE, Orrenius S, Nicotera P (1996b) Lamm and β-tubulin fragmentation precede chromatin degradation in glutamate-induced neuronal apoptosis. Neuro Report 7:2659-2664
4. Asahi M, Hoshimaru M, Uemura Y, Tokime T, Kojima M, Ohtsuka T, Matsuura N, Aoki T, Shibahara K, Kikuchi H (1997) Expression of interleukin-1 beta converting enzyme gene family and bcl-2 gene family in the rat brain following permanent occlusion of the middle cerebral artery. J Cereb Blood Flow Metab 17:11-18
5. Barger SW, Mattson MP (1996) Induction of neuroprotective kappa B-dependent transcription by secreted forms of the Alzheimer's beta-amyloid precursor. Brain Res Mol Brain Res 40:116-126
6. Beg AA, Baltimore D (1996) An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274:782-784
7. Bhat RV DiRocco R, Marcy VR, Flood DG, Zhu Y, Dobrzanski P, Siman R, Scott R, Contreras PC, Miller M (1996) Increased expression of IL-1β converting enzyme in hippocampus after ischemia: selective localization in microglia. J Neurosci 16:4146-4154
8. Burkitt MJ, Milne L, Nicotera P, Orrenius S (1996) 1,10-phenanthroline stimulates internucleosomal DNA fragmentation in isolated rat-liver nuclei by promoting the redox activity of endogenous copper ions. Biochem J 313:163-169
9. Butterworth NJ, Dragunow M (1996) Medial septal cholinergic neurons express c-Jun but do not undergo DNA fragmentation after fornix-fimbria transections. Mol Brain Res 43:1-12
10. Casciola-Rosen L, Nicholson DW, Chong T, Rowan KR, Thornberry NA Miller DK, Rosen A (1996) Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J Exp Med 183:1957-1964
11. Charriault-Marlangue C, Margaill I, Represa A, Popovic, T, Plotkine M, Ben-Ari Y (1996) Apoptosis and necosis after reversible focal ischemia: an in situ DNA fragmentation analysis. J Cerebral Blood Flow Metab 16:186-194
12. Chen J, Zhu RL, Nakayama M, Kawaguchi K, Jin K, Stetler RA, Simon RP, Graham SH (1996) Expression of the apoptosis-effector gene, Bax is up-regulated in vulnerable hippocampal CA1 neurons following global ischemia. J Neurochem 67:64-71
13. Chen J, Graham SH, Nakayama M, Zhu RL, Jin K, Stetler RA Simon RP (1997) Apoptosis repressor genes Bcl-2 and Bcl-x-long are expressed in the rat brain following global ischemia. J Cereb Blood Flow Metab 17:2-10
14. Chinnaiyan AM, O'Rourke K, Lane BR, Dixit VM (1997) Interaction of CED-4 with CED-3 and CED-9: A molecular framework for cell death Science 275:1122-1126
15. Cobbs CS, Fenoy A, Bredt DS, Noble LJ (1997) Expression of nitric oxide synthase in the cerebral microvasculature after traumatic brain injury in the rat. Brain Res 336-338
16. Colicos MA, Dash PK (1996) Apoptotic morphology of dentate gyrus granule cells following experimental cortical impact injury in rats: possible role in spatial memory deficits. Brain Res 739:120-131
17. Collins MKL, Furlong IJ, Malde P, Ascaso R, Oliver J, Rivas AL (1996) An apoptotic endonuclease activated either by decreasing pH or by increasing calcium. J Cell Sci 109:2393-2399
18. Dawson VL, Kizushi VM, Huang PL, Snyder SH, Dawson TM (1996) Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci 16:2479-2487
19. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM Jr, Snider WD, Korsmeyer SJ (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17: 401-411
20. Didier M, Bursztajn S, Adamec E, Passani L, Nixon RA, Coyle JT, Wei JY, Berman SA (1996) DNA strand breaks induced by sustained glutamate excitotoxicity in primary neuronal cultures. J Neurosci 16:2238-2250
21. Du C, Hu R, Csernansky CA, Hsu CY, Choi DW (1996) Very delayed infarction after mild focal cerebral ischemia: a role for apoptosis? J Cereb Blood Flow Metab 16:195-201
22. Duckett CS, Nava VE, Gedrich RW, Clem RJ, Van-Dongen JL, Gilfillan MC, Shiels H, Hardwick JM, Thompson CB (1996) A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J 15:2685-2694
23. Eizenberg O, Faber-Elman A, Gottlieb E, Oren M, Rotter V, Schwartz M (1996) p53 plays a regulatory role in differentiation and apoptosis of central nervous system-associated cells. Mol Cell Biol 16:5178-5185
24. Enokido Y, Araki, 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
25. Enright H, Miller WJ, Hays R, Floyd RA, Hebbel RP (1996) Preferential targeting of oxidative base damage to internucleosomal DNA. Carcinogenesis 17:1175-1177
26. Fraser MJ, Tynan SJ, Papaioannou A, Ireland CM, Pittman SM (1996) Endo-exonuclease of human leukemic cells: evidence for a role in apoptosis. J Cell Sci 109:2343-2360
27. Friedlander RM, Gagliardini V, Hara H, Moskowitz MA, Yuan J (1996a) Neuronal apoptosis following activation of the ICE family is mediated by secreted mature IL-1β. Am Assn Neurol Surgeons Abstracts, p 7, 1996
28. Friedlander RM, Gagliardini V, Rotello RJ, Yuan J (1996b) Functional role of interleukin 1 beta (IL-1 beta) in IL-1 beta-converting enzyme-mediated apoptosis. J Exp Med 184:717-24
29. Geddes JW, Pettigrew LC, Holtz ML, Craddock SD, Maines MD (1996) Permanent focal and transient global cerebral ischemia increase glial and neuronal expression of heme oxygenase-1, but not heme oxygenase-2, protein in rat brain. Neurosci Lett 210:205-208
30. Gillardon F, Lenz C, Kuschinsky W, Zimmermann M (1996a) Evidence for apoptotic cell death in the choroid plexus following focal cerebral ischemia. Neurosci Lett 207:113-116
31. Gillardon F, Lenz C, Waschke KF, Krajewski S, Reed JC, Zimmermann M, Kuschinsky W (1996b) Altered expression of Bcl-2, Bcl-X, Bax, and c-Fos colocalizes with DNA fragmentation and ischemic cell damage following middle cerebral artery occlusion in rats. Mol Brain Res 40:254-260
32. Gillardon F, Zimmermann M, Uhlmann E, Krajewski S, Reed JC, Klimaschewski L (1996c) Antisense oligodeoxynucleotides to bax mRNA promote survival of rat sympathetic neurons in culture. J Neurosci Res 43:726-734
33. Giordano JM, Mahadeo DK, He YY, Geist RT, Hsu C, Gutmann DH (1996) Increased expression of the neurofibromatosis 1 (NF1) gene product, neurofibromin, in astrocytes in response to cerebral ischemia. J Neurosci Res 43:246-253
34. Goodman Y, Mattson MP (1996) Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid beta-peptide toxicity. J Neurochem 66:869-872
35. Gottlieb RA, Nordberg J, Skowronski E, Babior BM (1996) Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc Natl Acad Sci USA 93:654-658
36. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379:88-91
37. Grilli M, Pizzi M, Memo M, Spano P (1996) Neuroprotection by aspirin and sodium salicylate through blockade of NF-kappaB activation. Science 274:1383-1385
38. Hara A, Iwai T, Niwa M, Uematsu T, Yoshimi N, Tanaka T, Mon H (1996) Immunohistochemical detection of Bax and Bcl-2 proteins in gerbil hippocampus following transient forebrain ischemia. Brain Res 1996:711:249-253
39. Hara H, Friedlander RM, Gagliardini V, Ayata C, Fink K, Huang Z, Shimizu-Sasamata M, Yuan J, Moskowitz MA (1997) Inhibition of interleukin 1β converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc Natl Acad Sci USA 94:2007-2012
40. Honkaniemi J, Massa SM, Breckinridge M, Sharp FR (1996a) Global ischemia induces apoptosis-associated genes in hippocampus. Mol Brain Res 42:79-88
41. Honkaniemi J, Sharp FR (1996b) Global ischemia induces immediate-early genes encoding zinc finger transcription factors. J Cereb Blood Flow Metab 16:557-565
42. Hughes PE, Alexi T, Yoshida T, Schreiber SS, Knusel B (1996) Excitotoxic lesion of rat brain with quinolinic acid induces expression of p53 messenger RNA and protein and p53-inducible genes Bax and Gadd-45 in brain areas showing DNA fragmentation. Neurosci 74:1143-1160
43. Iadecola C, Zhang F, Casey R, Clark HB, Ross ME (1996) Inducible nitric oxide synthase gene expression in vascular cells atter transient focal cerebral ischemia. Stroke 27:1373-1380
44. Jin K, Chen J, Kawaguchi K, Zhu RL, Stetler RA, Simon RP, Graham SH (1996) Focal ischemia induces expression of the DNA damage-inducible gene GADD45 in the rat brain. Neuroreport 7:1797-1802
45. Johnson TM, Yu, ZX, Ferrans VJ, Lowenstein RA, Finkel T (1996) Reactive oxygen species are downstream mediators of p53-dependent apoptosis. Proc Natl Acad Sci USA 93:11848-11852
46. Jordan J, Galindo MF, Prehn JHM, Weichselbaum RR, Beckett M, Ghadge GD, Roos RP, Leiden JM, and Miller RJ (1996) p53 expression induces apoptosis in hippocampal pyramidal neuron cultures. J Neurosci 17:1397-1405
47. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C (1997). Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc Natl Acad Sci USA 94:2642-2647.
48. Kamme F, Wieloch T (1996) Induction of junD mRNA after transient forebrain ischemia in the rat. Effect of hypothermia. Mol Brain Res 43:51-56
49. Kayalar C, Ord T, Testa MP, Zhong LT, Bredesen DE (1996) Cleavage of actin by interleukin 1 beta-converting enzyme to reverse DNase I inhibition. Proc Natl Acad Sci USA 93:2234-2238
50. Kelley WJ, Burke RE (1996) Apoptotic neuron death in rat substantia nigra induced by striatal excitotoxic injury is developmentally dependent. Neurosci Lett 220:85-88
51. Khodarev NN, Ashwell JD (1996) An inducible lymphocyte nuclear Ca/Mg-dependent endonuclease associated with apoptosis. J Immunol 156:922-931
52. Kluck RM, Bossy-Wetzel E, Green DG, Newmeyer DD (1997) The release of cytochrome C from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132-1136
53. Koistinaho J, Pyykonen I, Keinanen R, Hokfelt T (1996) Expression of β-amyloid precursor protein mRNAs following transient focal ischaemia. Neuroreport 7:2727-2731
54. Kondo T, Sharp FR, Honkaniemi J, Mikawa S, Epstein CJ, Chan PH (1997) DNA fragmentation and prolonged expression of c-fos, c-jun, and hsp70 in kainic acid-induced neuronal cell death in transgenic mice overexpressing human CuZn-superoxide dismutase. J Cereb Blood Flow Metab 17:241-256
55. Krupinski J, Kumar P, Kumar S, Kaluza J (1996) Increased expression of TGF-B1 in brain tissue after ischemic stroke in humans. Stroke 27:852-857
56. Kuida K, Zheng TS, Na S, Kuan CY, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-372
57. Kuwabara K, Matsumoto M, Ikeda J, Hori O, Ogawa S, Maeda Y, Kitagawa K, Imuta N, Kinoshita T, Stern DM, Yanag, H, Kamada T (1996) Purification and characterization of a novel stress protein, the 150-kDa oxygen-regulated protein (ORP150), from cultured rat astrocytes and its expression in ischemic mouse brain. J Biol Chem 271:5025-5032
58. Lawrence MS, Ho DY, Sun GH, Steinberg GK, Sapolsky RM (1996) Overexpression of Bcl-2 with herpes simplex vectors protects CNS neurons against neurological insults in vitro and in vivo. J Neurosci 16:486-496
59. Lee PJ, Jiang BH, Chin BY, Iyer NV, Alam J, Semenza GL, Choi AMK (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 272:5375-5381
60. Li Y, Chopp M, Powers C (1997) Granule cell apoptosis and protein expression in hippocampal dentate gyrus after forebrain ischemia in rat. J Neurological Sci in press
61. Lin TN, Te J, Huang HC, Chi SI, Hsu CY (1997) Prolongation and enhancement of postischemic c-fos expression after fasting. Stroke 28:412-418
62. Liston P, Roy N, Tamai K, Lefebvre C, Baird S, Cherton-Horvat G, Farahani R, McLean M, Ikeda JE, MacKenzie A, Komeluk RG (1996) Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 379:349-353
63. Liu PK, Hsu CY, Dizdaroglu M, Floyd RA, Kow YW, Karakaya A, Rabow LE, Cui JK, (1996) Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia-reperfusion. J Neurosci 16:6795-6806
64. Liu W, Bi X, Tocco G, Baudry M, Schreiber SS (1996) Increased expression of cyclin D1 in the adult rat brain following kainic acid treatment. NeuroReport 7:2785-2789
65. Liu X, Kim CM, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome C. Cell 86:147-157
66. Liu ZG, Hsu H, Goeddel DV, Karin M (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87: 565-576
67. Loddick SA, MacKenzie A, Rothwell NJ (1996a) An ICE inhibitor, z-VAD-DCB attenuates ischaemic brain damage in the rat. Neuroreport 7:1465-1468
68. Loddick SA, Rothwell NJ (1996b) Neuroprotective effects of human recombinant interleukin-1 receptor antagonist in focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 16:932-940
69. Lukkarinen J, Grohn OHJ, Sinevirta R, Jarvinen A, Kauppinen RA, Janne J, Alhonen LI (1997) Transgenic rats as models for studying the role of ornithine decarboxylase expression in permanent middle cerebral artery occlusion. Stroke 28:639-645
70. MacManus JP Rasquinha I, Tuor U, Preston Ed (1997) Detection of higher-order 50- and 10-kbp DNA fragments before apoptotic internucleosomal cleavage following transient cerebral ischemia. J Cereb Blood Flow Metab 17:376-387
71. Marchal G, Beaudouin V, Rioux P, de la Sayette V, le Doze F, Viader F, Derlon JM and Baron JC (1996) Prolonged persistence of substantial volumes of potentially viable brain tissue after stroke. Stroke 27:599-606
72. Marchetti P, Decaudin D, Macho A, Zamzami N, Hirsch T, Susin SA, Kroemer G (1997) Redox regulation of apoptosis: impact of thiol oxidation status on mitochondrial function. Eur J Immunol 27: 289-296
73. Marchetti P, Susin SA, Decaudin D, Gamen S, Castedo M, Hirsch T, Zamzami N, Naval J, Senik A, Kroemer G (1996) Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA. Cancer Res 56:2033-2038
74. Matsushima K, MacManus JP, Hakim AM (1997) Apoptosis is restricted to the thalamus in thiamine deficient rats. Neuroreport 8: 867-870
75. Minn AJ, Velez P, Schendel SL, Liang H, Muchmore SW, Fesik SW, Fill M, Thompson CB (1997) Bcl-x(L) forms an ion channel in synthetic lipid membranes. Nature 385:353-357
76. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, Schwartzkroin PA (1996) Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 16: 1337-1345
77. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SL, Ng SL, Fesik SW (1996) X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell. Nature 381:335-341
78. Murakami K, Kondo T, Chan PH (1997) Reperfusion following focal cerebral ischemia alters distribution of neuronal cell with DNA fragmentation in mice. Brain Res 751:160-164
79. Murphy AN, Bredesen DE, Cortopassi G, Wang E, Fiskum G (1996) Bcl-2 potentiates the maximal calcium uptake capacity of neural cell mitochondria. Proc Natl Acad Sci USA 93:9893-9898
80. Nakagomi T, Asai A, Kanemitsu H, Narita K, Kuchino Y, Tamura A, Kirino T (1996) Up-regulation of c-myc gene expression following focal ischemia in the rat brain. Neurol Res 18:559-563
81. Ostad M, Shu WP, Kong L, Liu BCS (1996) Ha-ras oncogene expression abrogates a pH dependent endonuclease activity of apoptosis in normal rat kidney cells. Cancer Lett 98:175-182
82. Panahian N, Yoshida T, Huang PL, Hedley-Whyte ET, Dalkara T, Fishman MC, Moskowitz MA (1996) Attenuated hippocampal damage after global cerebral ischemia in mice mutant in neuronal nitric oxide synthase. Neurosci 72:343-354
83. Pandey S, Walker PR, Sikorska M (1997) Identification of a novel 97 kDa endonuclease capable of internucleosomal DNA cleavage. Biochemistry 36:711-720
84. Park HJ, Makepeace CM, Lyons JC, Song CW (1996) Effect of intracellular acidity and ionomycin on apoptosis in HL-60 cells. Eur J Cancer 32A:540-546
85. Portera-Cailliau C, Price DL, Martin LJ (1997a) Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comparative Neurol 378:70-87
86. Portera-Cailliau C, Price DL, Martin LJ (1997b) Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. Comparative Neurol 378:88-104
87. Raghupathi R, McIntosh TK (1996) Regionally and temporally distinct patterns of induction of c-fos, c-jun and junB mRNAs following experimental brain injury in the rat. Mol Brain Res 37:134-144
88. Rao L, Perez D, White E (1996) Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol 135:1441-1455
89. Relton JK, Martin D, Thompson RC, Russel DA (1996) Peripheral administration of interleukin-1 receptor antagonist inhibits brain damage after focal cerebral ischemia in the rat. Exp Neurol 138: 206-213
90. Roffler-Tarlov S, Brown JJG, Tarlov E, Stolarov J, Chapman DL, Alexiou M, Papaioannou VE (1996) Programmed cell death in the absence of c-Fos and c-Jun. Development 122:1-9
91. Sakhi S, Gilmore W, Tran ND, Schreiber SS (1996) p53-deficient mice are protected against adrenalectomy-induced apoptosis. NeuroReport 8:233-235
92. Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, Eberstadt M, Yoon HS, Shuker SB, Chang BS, Minn AJ, Thompson CB, Fesik SW (1997) Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275:983-986
93. Schindler KS, Latham CB, Roth KA (1997) bax deficiency prevents the increased cell death of immature neurons in bcl-x-deficient mice. J Neurosci 17:3112-3119
94. Schmidt-Kastner R, Fliss H, Hakim AM (1997) Subtle neuronal death in striatum after short forebrain ischemia in rats detected by in situ end-labeling for DNA damage. Stroke 28:163-170
95. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, Giallongo A (1996) Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor-1. J Biol Chem 271:32529-32537
96. Slack RS, Belliveau DJ, Rosenberg M, Atwal J, Lochmuller H, Aloyz R, Haghighi A, Lach B, Seth P, Cooper E, and Miller FD (1996) Adenovirus-mediated gene transfer of the tumor suppressor p53 induces apoptosis in postmitotic neurons. J Cell Biol 135:1085-1096
97. Sloviter RS, Dean E, Sollas AL, Goodman JH (1996) Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol 366:516-533
98. Song Q, Burrows SR, Smith G, Lees-Miller SP, Kumar S, Chan DW, Trapani JA, Alnemri E, Litwack G, Lu H, Moss DJ, Jackson S, Lavin MF. Interleukin-1 beta-converting enzyme-like protease cleaves DNA-dependent protein kinase in cytotoxic T cell killing. J Exp Med 184:619-626
99. States BA, Honkaniemi J, Weinstein PR, Sharp FR (1996) DNA fragmentation and HSP70 protein inducion in hippocampus and cortex occurs in separate neurons following permanent middle cerebral arter occlusions. J Cereb Blood Flow Metab 16:1165-1175
100. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 184: 1331-1341
101. Takahashi A, Alnemri ES, Lazebnik YA, Fernandes-Alnemri T, Litwack G, Moir RD, Goldman RD, Poirier GG, Kaufmann SH, Earnshaw WC (1996a) Cleavage of lamin A by Mch2 alpha but not CPP32: multiple interleukin 1 beta-converting enzyme-related proteases with distinct substrate recognition properties are active in apoptosis. Proc Natl Acad Sci USA 93:8395-8400
102. Takahashi, A, Musy, P-Y, Martins LM, Poirier GG Moyer RW. Earnshaw WC (1996b) CrmA/SPI-2 inhibition of an endogenous ICE-related protease responsible for lamin A cleavage and apoptotic nuclear fragmentation. J Biol Chem 271:32487-32490
103. Takeda A, Kimpara T, Onodera H, Itoyama Y, Shibahara S, Kogure K (1996) Regional difference in induction of heme oxygenase-1 protein following rat transient forebrain ischemia. Neurosci Lett 205: 169-172
104. Terai K, Matsuo A, McGeer EG, McGeer PL (1996a) Enhancement of immunoreactivity for NF-kappaB in human cerebral infarctions. Brain Res 739:343-349
105. Terai K, Matsuo A, McGeer PL (1996b) Enhancement of immunore-activity for NF-kappa B in the hippocampal formation and cerebral cortex of Alzheimer's disease. Brain Res 735:159-168
106. Tobita M, Nagano I, Nakamura S, Itoyama Y, Kogure K (1995) DNA single-strand breaks in postischemic gerbil brain detected by in situ nick translation procedure. Neurosci Lett 200:129-132
107. Tomasevic G, Subberod P, Wieloch M, Wieloch T (1996) DNA damage and repair: changes in the tumor suppressor protein p53 and the proliferative nuclear antigen (PCNA) in the rat brain following transient cerebral ischemia. In: Pharmacology of Cerebral Ischemia 1996, (Krieglestein J, Oberpichler-Schwenk H, eds) Wissenschaftliche Verlagsgesellschaft mbH, Stuttgart, pp 1-5.
108. Tsang SY, Tam SC, Bremner I, Burkitt MJ (1996) Copper-1,10-phenanthroline induces internucleosomal DNA fragmentation in HepG2 cells, resulting from direct oxidation by the hydroxyl radical. Biochem 7317:13-16
109. Tseng MT, Chan SA, Reid KH, Iyer VG (1997) Fos-like immunore-activity in rat hippocampal neurons following transient global ischemia. Neurol Res 19:89-91
110. Uren AG, Pakusch M, Hawkins CJ, Puis KL, Vaux DL (1996) Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc Natl Acad Sci USA 93:4974-4978
111. Van Antwerp DJ, Martin SJ Kafri T, Green DR, Verma IM (1996) Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274:787-789.
112. van Lockeren Campagne M, and Gill R (1996) Ultrastructural morphological changes are not characteristic of apoptotic cell death following focal cerebral ischaemia in the rat. Neurosci Lett 213: 111-114
113. Walton M, Lawlor P, Sirimanne E, Williams C, Gluckman P, Dragunow M (1996a) Loss of Ref-1 protein expression precedes DNA fragmentation in apoptotic neurons. Mol Brain Res 44:167-170
114. Walton M, Young D, Sirimanne E, Dodd J, Christie D, Williams C, Gluckman P, Dragunow M (1996b) Induction of clusterin in the immature brain following a hypoxic-ischemic injury. Mol Brain Res 39:137-152
115. Wang CY, Mayo MW, Baldwin AS Jr (1996) TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274:784-787
116. Waterhouse N, Kumar S, Song Q, Strike P, Sparrow L, Dreyfuss G, Alnemri ES, Litwack G, Lavin M, Watters D (1996) Heteronuclear ribonucleoproteins C1 and C2, components of the spliceosome, are specific targets of interleukin 1 beta-converting enzyme-like proteases in apoptosis. J Biol Chem 271:29335-29341
117. Weiss S, Cataltepe O, Cole AJ (1996) Anatomical studies of DNA fragmentation in rat brain after systemic kainate administration. Neurosci 74:541-551
118. Wiener CM, Booth G, Semenza GL (1996) In vivo expression of mR-NAs encoding hypoxia-inducible factor-1. Biochem Biophys Res Commun 225:485-4 88
119. Wiessner C, Vogel P, Neumann-Haefelin T, Hossmann KA (1996) Molecular correlates of delayed neuronal death following transient forebrain ischemia in the rat. Acta Neurochir Suppl 66:1-7
120. Wilson TM, Rivkees SA, Deutsch WA, and Kelley MR (1996) Differential expression of the apurinic/apyrimidic endonuclease (APE/ref-1) multifunctional DNA base excision repair gene during fetal development and in adult rat brain and testis. Mut Res 362:237-248
121. Wu D, Wallen WD, Nunez G (1997) Interaction and regulation of subcellular localization of CED-4 by CED-9. Science 275:1126-1129
122. Wyllie AH, Kerr JFR, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68:251-306
123. Xiang H, Hochman DW, Saya H, Fujiwara T, Schwartzkroin PA, Morrison RS (1996) Evidence for p53-mediated modulation of neuronal viability. J Neurosci 16:6753-6765
124. Xu DG, Korneluk RG, Tamai K, Wigle N, Hakim A, MacKenzie A, Robertson GS (1997) Distribution of neuronal apoptosis inhibitory protein-like immunoreactivity in the rat central nervous system. J Comparative Neurol 382:247-259
125. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome C from mitochondria blocked. Science 275:1129-1132
126. Yoon YS, Kim JW, Kang DW, Kim YS, Choi KH, Joe CO (1996) Poly(ADP-ribosyl)ation of histone HI correlates with internucleosomal DNA fragmentation during apoptosis. J Biol Chem 271: 9129-9134
127. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G (1996) Mitochondrial control of apoptosis. J Exp Med 183:1533-1544
128. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ (1996) Serine phosnhorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87:619-28
129. Zhang F, Casey RM, Ross ME, Iadecola C (1996) Aminoguanidine ameliorates and L-arginine worsens brain damage from intraluminal middle cerebral artery occlusion. Stroke 27:317-323
130. Zhu W, Cowie A, Wasfy GW, Penn LZ, Leber B, Andrews DW (1996) Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J 15:4130-4141