Apoptosis in neurological disease

Neurosurgery

Volumn 42, Issue 3, 1998, Pages 555-574

  Savitz, Sean I ^a,b   Rosenbaum, Daniel M ^b  

^a Department of Neurology ^*  (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Bcl 2; Cerebral ischemia; Glioma; Interleukin 1 converting enzyme proteases; Neurodegenerative diseases; Oxidative stress; p53

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALZHEIMER DISEASE; APOPTOSIS; BRAIN ISCHEMIA; CANCER; DEGENERATIVE DISEASE; EPILEPSY; HUMAN; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NEUROLOGIC DISEASE; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; STROKE;

APOPTOSIS; HUMANS; NERVOUS SYSTEM DISEASES; NEURONS;

EID: 0031884393     PISSN: 0148396X     EISSN: None     Source Type: Journal    
DOI: 10.1097/00006123-199803000-00026     Document Type: Review

References (213)

1. Adcock I, Brown C, Kwon O, Barnes P: Oxidative stress induces NFxB DNA binding and inducible NOS mRNA in human epithelial cells. Biochem Biophys Res Commun 199:1518-1524,1994.
2. Allsopp T, VVyatt S, Paterson H, Davies A: The proto-oncogene bd-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell 73:295-307, 1993.
3. Altman J: Programmed cell death: The paths to suicide. Trends Neurosci 15:278-280, 1992.
4. Anderson AJ, Pike CJ, Cotman CW: Differential induction of immediate early gene proteins in cultured neurons by Aβ-amyloid (Aβ): Association of c-Jun with A-induced apoptosis. J Neurochem 65:1487-1498, 1995.
5. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P: Glutamate-induced neuronal death: A succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973, 1995.
6. Arends MJ, Morris RG, Wyllie AH: Apoptosis: The role of the endonuclease. Am J Pathol 136:593-608, 1990.
7. Bansal N, Houle A, Melnykovych G: Dexamethasone-induced killing of neoplastic cells of lymphoid derivation: Lack of early calcium involvement. J Cell Physiol 143:105-109, 1990.
8. Barry MA, Behnke CA, Eastman A: Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins, and hyperlhermia. Biochem Fharmacol 40:2353-2362,1990.
9. Barry MA, Reynolds J, Eastman A: Etoposide-induced apoptosis in human HL-60 cells is associated with intracelIular,Bcidification. Cancer Res 53:2349-2357, 1993.
10. Behl C, Davis J, Cole G, Schubert D: Vitamin E protects nerve cells from amyloid protein toxicity. Biochem Biophys Res Commun 186:944-950, 1992.
11. Behl C, Hovey LI, Krajewski S, Schubert D, Reed J: Bcl-2 prevents killing of neuronal cells by glutamate but not by amyloid protein. Biochem Biophys Res Commun 197:949-956, 1993.
12. Bertrand R, Solary E, O'Connor P, Kohn K, Pommier Y: Induction of a common pathway of apoptosis by staurosporine. Exp Cell Res 211:314-321, 1994.
13. Biggiogera M, Scherini E, Mares V: Ulrastructural cytochemistry of cis-dichlorodiammine platinum II induced apoptosis in immature rat cerebellum. Acta Histochem Cytochem 23:831838, 1990.
14. Bina-Stein M, Tritton T: Aurintricarboxylic acid is a nonspecific enzyme inhibitor. Mol Pharmacol 12:191-193, 1976.
15. Bissonnette R, Echeverri F, Mahboubi A, Green D: Apoptotic cell death induced by c-myc is inhibited by bd-2. Nature 359:554556, 1992.
16. Boe R, Gjertsen B, Vintèrmyr O, Houge G, Lanotte M, Doskeland S: The protein phosphatase inhibitor okadaic acid induces morphologic changes typical of apoptosis in mammalian cells. Exp Cell Res 195:237-246,1991.
17. Bogler O, Huang H-J, Cavenee VVK: Loss of wild-type p53 bestows a growth advantage on primary cortical astrocytes and facilitates in vitro transformation. Cancer Res 55:2746-2751, 1995.
18. Bogler O, Huang H-J, Kleihues P, Cavenee VVK: The p53 gene and its role in human brain tumors. Glia 15:308-327, 1995.
19. Boise LH, Gonzalez-Garcia M, Postem CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thomson CB: bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608, 1993.
20. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA: Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A 92:7162-7166, 1995.
21. Bruno S, Del Bino G, Lassota P, Giaretti W, Darzynkiewicz Z: Inhibitors of proteases prevent endonucleolysis accompanying apoptotic death in HL-60 leukemic cells and normal thymocytes. Leukemia 6:1113-1120, 1992.
22. Casaccia-Bonnefil P, Carter B, Dobrowsky R, Chao M: Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383:716-719,1996.
23. Charriaut-Marlangue C, Margaill I, Plotkine M, Ben-Ari Y: Early endonuclease activation following reversible focal ischemia in the rat brain. J Cereb Blood Flow Metab 15:385-388/1995.
24. Chittenden T, Harrington E, O'Connor R, Flemington C, Lutz R, Evan G, Guild B: Induction of apoptosis by the Bcl-2 homologue Bak. Nature 374:733-736, 1995.
25. Choi DW: Ionic dependence of glutamate neurotoxicity in cortical cell culture. J Neurosci 7:369-379,1987.
26. Choi DW, Rothman SM: The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 13:171182, 1990.
27. Choi DW, Maulucci-Gedde M, Kriegstein AR: Glutamate neurotoxicity in cortical cell culture. J Neurosci 7:357-368, 1987.
28. Chopp M, Li Y, Zhang ZG, Freytag SO: p53 expression in brain after MCA occlusion in the rat. Biochem Biophys Res Commun 182:1201-1207,1992.
29. Clark MF, Apel IJ, Benedict MA, Eipers PG, Sumantran V, Gonzalez-Garcia M, Doedens M, Fukunaga N, Davidson B, Dick JE, Minn AJ, Boise LH, Thompson CB, Wicha M, Nunez G: A recombinant bcl-xs adenovirus selectively induces apoptosis in cancer cells but not in normal bone marrow cells. Proc Natl Acad Sci U S A 92:11024-11028, 1995.
30. Clark RS, Kochanek P, Chen J, Chen M, Zhu R, Simon R, Graham L: Expression of cell death regulatory proteins Cpp32, Bax, and Bcl-xl, after traumatic brain injury in rats. ] Cereb Blood Flow Metab 17[Suppl 1]:S22,1997 (abstr).
31. Cohen J, Duke R: Glucocorticoid activation of a calcium dependent endonuclease in thymocyte nuclei leads to cell death. J Immunol 132:38-42,1984.
32. Cohen G, Sun X-M, Snowden R, Dinsdale D, Skilleter D: Key morphological features of apoptosis may occur in the absence of internudeosomal DNA fragmentation. Biochem J 286:331-334,1992.
33. Coles H, Burne J, Raff M: Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor. Development 118:777-784, 1993.
34. Cortez SC, Mclntosh TK, Noble L: Experimental fluid percussion brain injury: Vascular disruption and neuronal and glial alterations. Brain Res 482:271-282, 1989.
35. Cotter T, Glynn JM, Echeverri F, Green DR: The induction of apoptosis by chemotherapeutic agents occurs in all phases of the cell cycle. Anticancer Res 12:773-780, 1992.
36. Couldwell WT, Gopalakrishna R, Hinton DR, He S, VVeiss M, Law RE, Apuzzo MLJ: Hypericin: A potential antiglioma therapy. Neurosurgery 35:705-710, 1994.
37. Couldwell WT, Hinton D, He S, Chen T, Sebat I, VVeiss M, Law R: PKC inhibitors induce apoptosis in human malignant glioma cell lines. FEES Lett 345:43-46, 1994.
38. Crumrine RC, Thomas AL, Morgan PF: Attenuation of p53 expression protects against focal ischémie damage in transgenic mice. J Cereb Blood Flow Metab 14:887-891, 1994.
39. Csernansky CA, Canzoniero LMT, Sensi SL, Yu SP, Choi DVV: Delayed application of aurintricarboxylic acid reduces glutamateinduced cortical neuronal injury. J Neurosci Res 38:101-108,1994.
40. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM, Snider VVD, Korsmeyer SJ: BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411, 1996.
41. Delia D, Aiello A, Lombard; L, Pelicci PG, Grignani F, Formelli F, Menard S, Costa A, Veronesi U, Pierotti MA: N-(4-Hydroxy. phenyl)retinamide induces apoptosis of malignant haemopoietic cell lines including those unresponsive to retinoic acid. Cancer Res 53:6036-6041,1993.
42. Dessi F, Charriaut-Marlangue C, Ben-Ari Y: Anisomycin and cycloheximide protect cerebellar neurons in culture from anoxia. Brain Res 581:323-326, 1992.
43. Dessi F, Charriaut-Marlangue C, Khrestchatisky M, Ben-Ari Y: Glutamate-induced neuronal death is not a programmed cell death in cerebellar culture. J Neurochem 60:1953-1955,1993.
44. Dole M, Nunez G, Merchant AK, Maybaum J, Rode CK, Bloch CA, Castle VP: Bcl-2 inhibits chemotherapy-induced apoptosis in neuroblastoma. Cancer Res 54:3253-3259, 1994.
45. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Butel JS, Bradley A: Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 356:215-221, 1992.
46. Dyson JED, Simmons DM, Daniel J, McLaughlin JM, Quirke P, Bird CC: Kinetic and physical studies of cell death induced by chemotherapeutic agents or hyperthermia. Cell Tissue Kinet 19:311-324,1986.
47. Ellison D, Steart P, Gatter K, Weller R: Apoptosis in cerebral astrocytic tumors and its relationship to expression of the bcl-2 and p53 proteins. Neuropathol AppI Neurobiol 21:352-361; 1995.
48. Esterbauer H, Schaur R, Zollner H: Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biol Med 11:81-128, 1991.
49. Evans D, Dive C: Effects of cisplatin on the induction of apoptosis in proliferating hepatoma cells and nonproliferating immature thymocytes. Cancer Res 53:2133-2139,1993.
50. Falcieri E, Martelli A, Bareggi R, Cataldi A, Cocco L: The protein kinase inhibitor staurosporine induces morphological changes typical of apoptosis in MOLT-4 cells without concomitant DNA fragmentation. Biochem Biophys Res Commun 193:19-25,1993.
51. Fallen J, Cameron J: Interdigital cell death during limb development of the turtle and lizard with an interpretation of evolutionary significance. J Embryol 40:285-289, 1977.
52. Fearnhead HO, Chwalinski M, Snowden RT, Ormerod MG, Cohen GM: Dexamethasone and etoposide induce apoptosis in rat thymocytes from different phases of the cell cycle. Biochem Pharmacol 48:1073-1079,1994.
53. Ferguson D, Anderson T: Morphological evaluation of cell turnover in relation to the menstrual cycle in the 'resting' human breast. Br J Cancer 44:177-181, 1981.
54. Frade JM, Rodriguez-Tébar A, Barde Y: Induction of cell death by endogenous nerve growth factor through p75 receptor. Nature 383:166-168, 1996.
55. Gagliardini V, Femandez P, Lee R, Drexler H, Rotello R, Fishman M, Yuan J: Prevention of vertebrate neuronal death by the crinA gene. Science 263:826-828, 1994.
56. Gavrieli Y, Sherman Y, Ben-Sasson S: Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501, 1992.
57. Giordano DL, Murray M, Cunningham TJ: Naturally occurring neuron death in the optic layers of the superior colliculus of the postnatal rat. J Neurocytol 9:603-614, 1980.
58. Gong J, Li X, Darzynkiewicz Z: Different patterns of apoptosis of HL-60 cells induced by cycloheximide and camptothecin. J Cell Physiol 157:263-270, 1993.
59. Goto K, Ishige A, Sekiguchi K, Sugimoto A, Yuzurihara M, Aburada M, Hosoya E, Kogure K: Effects of cycloheximide on delayed neuronal death in rat hippocampus. Brain Res 534:299302, 1990.
60. Graeber T, Osmanian C, Jacks T, Housman D, Koch C, Löwe S, Giaccia A: Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumors. Nature 379:88-91, 1996.
61. Graeber T, Peterson J, Tsai M, Monica K, Fornace A, Giaccia A: Hypoxia induces accumulation of p53 protein, but activation of a Grphase checkpoint by low-oxygen conditions is independent of p53 status. Mol Cell Biol 14:6264-6277, 1994.
62. Greenlund L, Deckwerth T, Johnson E: Superoxide dismutase delays neuronal apoptosis: A role for reactive oxygen species in programmed neuronal death. Neuron 14:303-315, 1995.
63. Gunji H, Karbanda S, Kufe D: Induction of internucleosomal DNA fragmentation in human myeloid leukemia cells by 1-Darabinofuranosylcytosine. Cancer Res 51:741-743, 1991.
64. Ham J, Babij C, VVhitfield J, Pfarr C, Lalleman D, Yaniv M, Rubin LL: A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14:927-939, 1995.
65. Hamilton HB, Hinton DR, Law RE, Gopalakrishna R, Su YZ, Chen Z, VVeiss MH, Couldwell WT: Inhibition of cellular growth and induction of apoptosis in pituitary adenoma cell lines by the protein kinase C inhibitor hypericin: Potential therapeutic application. J Neurosurg 85:329-334,1996.
66. Hanabuchi S, Koyanagi M, Kawasaki A, Shinohara N, Matsuzawa A, Nishimura Y, Kobayashi Y, Yonehara S, Yagita H, Okumura F: Fas and its ligand in a general mechanism of T cell-mediated cytotoxicity. Proc Natl Acad Sci U S A 91:4930-4934,1994.
67. Harmon B, Takano YS, VVinterford CM, Pötten CS: Cell death induced by vincristine in the intestinal crypts of mice and in a human Burkitt's lymphoma cell line. Cell Prolif 25:523-536, 1992.
68. Hartley A, Stone J, Heron C, Cooper J, Schapira A: Complex I inhibitors induce dose-dependent apoptosis in PC12 cells: Relevance to Parkinson's disease. J Neurochem 63:1987-1990, 1994.
69. Hayes RL, Jenkins LW, Lyeth BG: Neurotransmitter-mediated mechanisms of traumatic brain injury: Acetylcholine and excitatory amino acids. J Neurotrauma 9[Suppl 1]:S173-S187, 1992.
70. Heintz N: Cell death and the cell cycle: A relationship between transformation and neurodegeneration? Trends Biol Sci 18:157159,1993.
71. Hengartner MO, Horvitz R: C. clcgans cell survival gene ced-9 encodes a functional homologue of the mammalian protooncogene bd-2. Cell 76:665-676, 1994.
72. Deleted in proof.
73. Hockenbery D, Oltvai Z, Yin X, Milliman C, Korsmeyer S: Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-251, 1993.
74. Hoehner J, Hedborg F, VVilklund H, Olsen L, Pahlman S: Cellular death in neuroblastoma: In situ correlation of apoptosis and bcl-2 expression. Int J Cancer 62:19-24, 1995.
75. Hopwood D, Levison D: Atrophy and apoptosis in the cyclical human endometrium. J Pathol 119:159-166, 1976.
76. Ikemoto H, Tani E, Matsumoto T, Nakano A, Furuyama J: Apo ptosis of human glioma cells in response to calphostin C, a specific protein kinase C inhibitor. J Neurosurg 83:1008-1016,1995.
77. Iwadate Y, Fujimoto S, Tagawa T, Namba H, Sueyoshi K, Hirose M, Sakiyama S: Association of p53 gene mutation with decreased chemosensitivity in human malignant gliomas. Int J Cancer 69:236-240, 1996.
78. Jacobson MD, Burne JF, Raff MC: Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J 13:18991910, 1994.
79. Jarvis VVD, Turner AJ, Povirk LF, Traylor RS, Grant S: Induction of apoptotic DNA fragmentation and cell death in HL-60 human promyelocytic leukemia cells by pharmacological inhibitors of protein kinase C. Cancer Res 54:1707-1714,1994.
80. Johnson EM, Greenland LS, Akins FT, Hsu CY: Neuronal apoptosis: Current understanding of molecular mechanisms and potential role in ischémie brain injury. J Neurotrauma 12:843-852,1995.
81. Kane D, Sarafian T, Anton R, Hahn H, Gralla E, Valentine J, Ord T, Bredesen D: Bcl-2 inhibition of neural death: Decreased generation of reactive oxygen species. Science 262:1274-1276,1993.
82. Kerr JFR: Shrinkage necrosis: A distinct mode of cellular death. J Pathol 105:13-20, 1971.
83. Kerr J, Winterford C, Harmon B: Apoptosis: Its significance in cancer and cancer therapy. Cancer 73:2013-2026, 1994.
84. Kerr J, Wyllie A, Currie A: Apoptosis: A basic biological phenomenon with wide ranging implications in tissue kinetics. Br J Cancer 26:239-257, 1972.
85. Kessler J, Ludlam VV, Freidin M, Hall D, Michaelson M, Spray D, Batter D: Cytokine-induced programmed cell death of cultured sympathetic neurons. Neuron 11:1123-1132, 1993.
86. Kihara S, Shiraishi T, Nakagawa S, Toda K, Tabuchi K: Visualization of DNA double strand breaks in the gerbil hippocampal CA1 following transient ischemia. Neurosci Lett 175:133-136,1994.
87. Kirino T: Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57-69,1982.
88. Kizaki H, Ohnishi Y, Azuma Y, Mizuno Y, Ohsaka F: 1-β-DArabinosylcytosine and 5-azacytidine induce internucleosomal DNA fragmentation and cell death in thymocytes. Immunopharmacology 24:219-227,1992.
89. Koh J, Wie MB, Gwag BJ, Sensi SL, Canzoniero LM, Demaro J, Csernansky C, Choi DW: Staurosporine induced neuronal apoptosis. Exp Neurol 135:153-159,1995.
90. Kokunai T, Sawa H, Tamaki N: Localization of apoptotic cells in situ of brain tumors. Brain Tumor Pathol 12:15-21, 1995.
91. Krajewski S, Mai JK, Krajewska M, Sikorska M, Mossakowski MJ, Reed JC: Upregulation of Bax protein levels in neurons following cerebral ischemia. J Neurosci 15:6364-6376, 1995.
92. Krishna M, Smith TVV, Recht LD: Expression of bcl-2 in reactive and neoplastic astrocytes: Lack of correlation with presence or degree of malignancy. J Neurosurg 83:1017-1022,1995.
93. Kruman I, Bruce-Keller A, Bredesen D, Waeg G, Mattson M: Evidence that 4-hydroxynonenal mediates oxidative stressinduced neuronal apoptosis. J Neurosci 17:5089-5100, 1997.
94. Kuida K, Lippeke JA, Ku G, Harding MW, Livingston DJ, Michael SSS, Flavel RA: Altered cytokine export and apoptosis in mice deficient in ICE. Science 267:2000-2003,1995.
95. Kure S, Tominaga T, Yoshimoto T, Tada K, Narisawa K: Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem Biophys Res Commun 179:39-15, 1991.
96. Le WD, Colom LV, Xie WJ, Smith RG, Alexianu M, Appel SH: Cell death induced by β-amyloid 1-10 in MES 23.5 hybrid clone: The role of nitric oxide and NMDA-gated channel activation leading to apoptosis. Brain Res 686:49-60,1995.
97. Ledda-Columbano G, Coni P, Gaa G, Manenti G, Columbano A: Rapid induction of apoptosis in rat liver by cycloheximide. Am J Pathol 140:545-549, 1992.
98. Lennon SV, Martin SJ, Cotter TG: Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell Prolif 24:203-214, 1991.
99. Li Y, Chopp M, Jiang N, Yao F, Zaloga C: Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 15:389-397,1995.
100. Li Y, Chopp M, Jiang N, Zhang ZG, Zaloga C: Induction of DNA fragmentation after 10 to 120 minutes of focal cerebral ischemia in rats. Stroke 26:1252-1258, 1995.
101. Li Y, Sharov VG, Jiang N, Zalong C, Sabbah HN, Chopp M: Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am J Pathol 146: 1045-1051, 1995.
102. Linnik MD, Zahos P, Geschwind MD, Federoff HJ: Expression of bcl-2 from a defective herpes simplex virus-1 vector limits neuronal death in focal cerebral ischemia. Stroke 26:1670-1675,1995.
103. Linnik MD, Zobrist R, Hatfield M: Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2009, 1993.
104. Liu Y, Bhalla K, Hill C, Priest DG: Evidence for involvement of tyrosine phosphorylation in taxol-induced apoptosis in a human ovarian tumor cell line. Biochem Pharmacol 48:1265-1272,1994.
105. Liu Y, Joshua D, Williams G, Smith C, Gordon J, MacLennan I: Mechanism of antigen-driven selection in germinal centers. Nature 342:929-931, 1989.
106. Lockshin R, Zakeri Z: Programmed cell death and apoptosis, in Tomei LD, Cope FO (eds): Apoptosis: The Molecular Basis of Cell Death. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory, 1991, pp 47-59.
107. Loo D, Copani A, Pike C, Whittemore E, VValencewicz A, Cotman C: Apoptosis is induced by -amyloid in cultured central nervous system neurons. Proc Natl Acad Sci U S A 90:7951-7955,1993.
108. Louis J, Magal E, Takayama S, Varon S: CNTF protection of oligodendrocytes against natural and tumor necrosis factorinduced death. Science 259:689-692, 1993.
109. Lowe SVV, Ruley HE, Jacks T, Housman DE: p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74:957-967, 1993.
110. MacManus JP, Hill IE, Huang ZG, Rasquinha I, Xue D, Buchan AM: DNA damage consistent with apoptosis in transient focal ischémie neocortex. Neuroreport 5:493-496,1994.
111. Maldonado V, Melendez J, Gonzalez H, Ortega A: Internucleosomal DNA cleavage in HeLa cells exposed to cisplatin. Biochem Mol Biol Int 37:691-696, 1995.
112. Mariotti A, Marcora E, Bunone G, Costa A, Veronesi U, Pierotti MA, Delia Valle G: N-(4-Hydroxyphenyl)retinamide: A potent inducer of apoptosis in human neuroblastoma cells. J Natl Cancer Inst 86:1245-1247,1994.
113. Mark R, Lovell M, Markesberg VV, Uchida K, Mattson M: A role for 4-hydroxynonenal in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J Neurochem 68: 255-264, 1997.
114. Martelli A, Canonero R, Cavanna M, Ceredelli M, Marinari U: Cytotoxic and genotoxic effects of five N-alkanals in primary cultures of rat and human hepatocytes. Mutât Res 323:121-126,1994.
115. Martin S: Protein or RNA synthesis inhibition induces apoptosis of mature human CD4+ T cell blasts. Immunol Lett 35:125-134,1993.
116. Martin S, Green D: Protease activation during apoptosis: Death by a thousand cuts? Cell 82:1-20, 1995.
117. Martin DP, Ito A, Horigome K, Lampe PA, Johnson EM: Biochemical characterization of programmed cell death in NGFdeprived sympathetic neurons. J Neurobiol 23:1205-1220,1992.
118. Martin DP, Schmidt E, DiStefano P, Lowry O, Carter J, Johnson E: Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 106:829-844, 1988.
119. Martin DP, Wallace T, Johnson E: Cytosine arabinoside kills postmitotic neurons in a fashion resembling trophic factor deprivation: Evidence that a deoxycytidine-dependent process may be required for nerve growth factor signal transduction. J Neurosci 10:184-193, 1990.
120. Martinou JC, Dubois-Dauphin M, Staple JK, Rodriguez I, Frankowski H, Missotten M, Albertini P, Talabot D, Catsicas S, Pietra C, Huarte J: Overexpression of Bcl-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017-1030, 1994.
121. McConkey DJ, Hartzell P, Nicotera P, Orrenius S: Calciumactivated DNA fragmentation kills immature thymocytes. FASEB J 3:1843-1849,1989.
122. Deleted in proof.
123. Meikrantz W, Gisselbrecht S, Tarn SW, Schlegel R: Activation of cyclin A-dependent protein kinases during apoptosis. Proc Natl Acad Sci U S A 91:3754-3758, 1994.
124. Meldrum B, Garthwaite J: Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol Sci 11:379387, 1990.
125. Mesner P, Winters T, Green S: Nerve growth factor withdrawalinduced cell death in neuronal PC12 cells resembles that in sympathetic neurons. J Cell Biol 119:1669-1680, 1992.
126. Miura M, Zhu H, Rotello R, Hartwieg E, Yuan J: Induction of apoptosis in fibroblasts by IL-l-converting enzyme, a mammalian homologue of the'C. elegnns cell death gene ced-3. Cell 75:653-660, 1993.
127. Miyashita T, Reed JC: Bcl-2 oncoprotein blocks chemotherapyinduced apoptosis in a human leukemia cell line. Blood 81:151157, 1993.
128. Miyashita T, Reed JC: Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299,1995.
129. Mizumoto K, Rothman R, Farberm J: Programmed cell death (apoptosis) of mouse fibroblasts is induced by the topoisomerase II inhibitor etoposide. Mol Pharmacol 46:890-895, 1994.
130. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, Schwartzkroin PA: Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 16:1337-1345, 1996.
131. Mountz J, Wu J, Cheng J, Zliou T: Autoimmune disease: A problem of defective apoptosis. Arthritis Rheum 37:1415-1420,1994.
132. Murphy TH, Schnaar RL, Coyle JT: Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake. FASEB J 4:1624-1633, 1990.
133. Nakagawa S, Shiraishi T, Kihara S, Tabuchi K: Detection of DNA strand breaks associated with apoptosis in human brain tumors. Virchows Arch 427:175-179,1995.
134. Nakajima M, Kashiwagi K, Ohta J, Furukawa S, Hayashi K, Kawashima T, Hayashi Y: Etoposide induces programmed cell death in neurons cultured from the fetal rat central nervous system. Brain Res 641:350-352, 1994.
135. Negri C, Bernardi R, Braghetti A, Ricotti GC, Scovassi AI: The effect of chemotherapeutic drug VP-16 on poly(ADP-ribosylation) in apoptotic HeLa cells. Carcinogenesis 14:2559-2564,1993.
136. Nieto MA, Gonzalez A, Lopez-Rivas A, Diaz-Espada F, Gambon F: IL-2 protects T lymphocytes from glucocorticoid-induced DNA fragmentation and cell death. J Immunol 143:4166-4170, 1989.
137. Oberhammer F: Apoptotic death in epithelial cells: Cleavage of DNA to 300 and/or 500 kb fragments prior to or in absence of internudeosomal fragmentation. EMBO J 12:3679-3684, 1993.
138. Okamoto-Kubo S, Nishio K, Keike Y, Yoshida M, Ohmori T, Saijo B: Apoptosis induced by etoposide in small-cell lung cancer cell lines. Cancer Chemother Pharmacol 33:385-390, 1994.
139. Olney J: Brain lesion, obesity and other disturbances in mice treated with monosodium glutamate. Science 164:719-721,1969.
140. Oltvai Z, Milliman C, Korsmeyer S: Bcl-2 heterodimerizes in vivo with a conserved homologue, Bax, that accelerates cell death. Cell 74:609-619,1993.
141. Oppenheim RVV, Prevette D, Tytell M, Homma S: Naturally occurring and induced neuronal death in the chick embryo in vivo requires protein and RNA synthesis: Evidence for the role of cell death genes. Dev Biol 138:104-113,1990.
142. Ormerod MG, Orr RM, Peacock JH: The role of apoptosis in cell killing by cisplatin: A flow cytometric study. Br J Cancer 69:93100, 1994.
143. Patsouris E, Davaki P, Kapranos N, Davaris P, Papageorgiou K: A study of apoptosis in brain tumors by in situ end-labeling methods. Clin Neuropathol 15:337-341, 1996.
144. Petito CK, Feldmann E, Pulsinelli WA, Plum F: Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 37:1281-1286, 1987.
145. Pierce G, Lewellyn A, Parchment R: Mechanism of programmed cell death in the blastocyst. Proc Natl Acad Sci U S A 86:36543658, 1989.
146. Pilar G, Landmesser L: Ultrastructural differences during embryonic cell death in normal and peripherally deprived ciliary ganglia. J Cell Biol 68:339-356, 1976.
147. Pollard H, Cantagrel S, Charriaut-Marlangue C, Moreau J, Ben Ari Y: Apoptosis associated DNA fragmentation in epileptic brain damage. Neuroreport 5:1053-1055,1994.
148. Pollard H, Charriaut-Marlangue C, Cantagrel S, Represa A, Robain O, Moreau J, Ben-Ari Y: Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience 63:7-18, 1994.
149. Posner A, Raser KJ, Hajimohammadreza I, Yuen PVV, Wang KK: Aurintricarboxylic acid is an inhibitor of inn- and m-calpain. Biochem Mol Biol Int 36:291-299, 1995.
150. Potten CC: Extreme sensitivity of some intestinal crypt cells to X and y irradiation. Nature 269:518-521, 1977.
151. Potten C: What is an apoptotic index measuring? A commentary. Br J Cancer 74:1743-1748, 1996.
152. Rabizadeh S, Gralla E, Borchelt D, Gwinn R, Valentine J, Sisodia S, Wong P, Lee M, Hahn H, Bredesen D: Mutations associated with ALS convert Superoxide dismutase from an anti-apoptotic gene to a pro-apoptotic gene: Studies in yeast and neural cells. Proc Natl Acad Sci U S A 92:3024-3028, 1995.
153. Rabizedah S, Oh J, Zhong L, Yang J, Bitler C, Butcher L, Bredesen D: Induction of apoptosis by the low affinity NGF receptor. Science 261:345-348, 1993.
154. Raff MC: Social control on cell survival and cell death. Nature 356:397-400, 1992.
155. Raff MC, Barres B, Burne J, Coles H, Ishizaki Y, Jacobson M: Programmed cell death and the control of cell survival: Lessons from the nervous system. Cell 262:695-699,1993.
156. Ratan R, Murphy T, Baraban J: Macromolecular synthesis inhibitors prevent oxidative stress-induced apoptosis in embryonic cortical neurons by shunting cysteine from protein synthesis to glutathione. J Neurosci 14:4385-1392, 1994.
157. Ratan R, Murphy 1, Baraban ]: Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 62:1-4, 1994.
158. Ray S, Ponnathpur V, Huang Y, Tang C, Mahoney ME, Ibrado AM, Bullock G, Bhalla K: 1-D-Arabinofuranosylcytosine-, mitoxantrone-, and paclitaxel-induced apoptosis in HL-60 cells: Improved method for detection of internucleosomal DNA fragmentation. Cancer Chemother Pharmacol 34:365-371, 1994.
159. Rink A, Fung KM, Trojanowski JQ, Lee VM, Neugebauer E, Mclntosh TK: Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am J Pathol 147:15751583, 1995.
160. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Reagan J, Deng H-X, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston S, Berger R, Tanzi R, Halperin J, Herzfeldt B, Van den Bergh R, Hung W-Y, Bird T, Deng G, Mulder D, Smyth C, Laing N, Soriano E, Pericak-Vance M, Haines J, Ronleau G, Gusella J, Horuitz HR, Brown R: Mutations in Cu/Zn Superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62,1993.
161. Rosenbaum D, Kalberyg J, Kessler J: Superoxide dismutase ameliorates neuronal death from hypoxia in culture. Stroke 25:857863,1994.
162. Rosenbaum DM, Michaelson M, Batter D, Doshi P, Kessler J: Evidence of hypoxia-induced, programmed cell death of cultured neurons. Ann Neurol 36:864-870, 1994.
163. Rothman SM, Olney JW: Excitotoxicity and the NMDA receptor. Trends Neurosci 10:299-302, 1987.
164. Sakaguchi Y, Stephens LC, Makino M, Kaneko T, Strebet FR, Danhauser LL, Jenkins GN, Bull JM: Apoptosis in normal tissues induced by 5-fluorouracil: Comparison between bolus injection and prolonged infusion. Anticancer Res 14:1489-1492,1994.
165. Sanderson C: The mechanism of T cell mediated cytotoxicity: Morphological studies of cell death by time-lapse microcinematography. Proc R Soc Lond [Biol] 192:241-255,1976.
166. Sandstrom PA, Roberts B, Folks T, Buttke TM: HIV gene expression enhances T cell susceptibility to hydrogen peroxideinduced apoptosis. AIDS Res Hum Retrovir 9:1107-1113, 1993.
167. Sandstrom PA, Tebbey PW, Van Cleave S, Buttke TM: Lipid hydroperoxides induce apoptosis in T cells displaying a HIVassociated glutathione peroxidase deficiency. J Biol Chem 269: 798-601, 1994.
168. Sarafian T, Bredesen D: Invited commentary: Is apoptosis mediated by reactive oxygen species? Free Radical Res Commun 2:1-8, 1994.
169. Schapira A: Evidence for mitochondrial dysfunction in Parkinson's disease: A critical appraisal. Mov Disord 9:125-138, 1994.
170. Schapira A, Cooper J, Dexter D, Clark J, Jenner P, Marsden C: Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 54:823-827,1990.
171. Schiffer D, Cavalla P, Chio A, Giordana M, Marino S, Mauro A, Migheli A: Tumor cell proliferation and apoptosis in medulloblastoma. Acta Neuropathol 87:362-370, 1994.
172. Schwartz L, Smith S, Jones M, Osborne B: Do all programmed cell deaths occur via apoptosis? Proc Natl Acad Sci USA 90:980-984, 1993.
173. Scott S, Davies A: Inhibition of protein synthesis prevents cell death in sensory and parasympathetic neurons deprived of neurotrophic factor in vitro. J Neurobiol 21:630-638,1990.
174. Searle L: An electron microscopy study of the mode of cell death induced by cancer-chemotherapeutic agents in populations of proliferating normal and neoplastic cells. J Pathol 116: 129-138, 1975.
175. Shchepotin IB, Soldatenkov V, Buras RR, Nauta RJ, Shabahang M, Evans SR: Apoptosis of human primary and metastatic colon adcnocarcinoma cell lines in vitro induced by 5-fluorouraciI, verapamil, and hyperthermia. Anticancer Res 14:1027-1031, 1994.
176. Shi L, Kraut RP, Aebersold R, Greenberg AH: A natural killer cell granule' protein that induces DNA fragmentation and apoptosis. J Exp Med 175:553-566,1992.
177. Siesjo BK: Calcium-mediated processes in neuronal degeneration. Ann N Y Acad Sci 747:140-161,1994.
178. Smith C, Williams G, Kingston R, Jenkinson E, Owen J: Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature 337:181-184,1989.
179. Sulston JE, Horvitz HR: Post-embryonic cell lineages of the nematode C. clcgans. Dev Biol 82:110-156,1977.
180. Tachibana O, Lampe J, Kleihues P, Ohgaki H: Preferential expression of Fas/APOl (CD95) and apoptotic cell death in perinecrotic cells of glioblastoma multiforme. Acta Neuropathol 92:431-434, 1996.
181. Takano Y, .Harmon B, Kerr J: Apoptosis induce'd by mild hyperthermia in human and murine cell lines: A study using electron microscopy and DNA gel electrophoresis. J Pathol 163:329-336, 1991. .
182. Takei N, Endo Y: Calcium ionophore-induced apoptosis in cultured embryonic rat cortical neurons. Brain Res 652:65-70,1994.
183. Terai C, Kornbluth RS, Pauza CD, Richman DD, Carson AD: Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HFV-1. J Clin Invest 87:1710-1715,1991.
184. Tymianski M, Tator CH: Normal and abnormal calcium homeostasis in neurons: A basis for the pathophysiology of traumatic and ischémie central nervous system injury. Neurosurgery 38:1176-1195,1996.
185. Vallbo C, Bergenheim T, Bergh A, Grankvist K, Henriksson R: DNA fragmentation induced by the antimitotic drug estramustine in malignant rat glioma but not in normal brain, suggesting an apoptotic cell death. Br J Cancer 71:717-720, 1995.
186. Vaux D, Cory S, Adams J: bcl-2 gene promotes haemopoietic cell survival and cooperates with c-tnyc to immortalize pre-B-cells. Nature 335:440-442, 1988.
187. VValton M, Whysong D, O'Connor PM, Hockenbery D, Korsmeyer SJ, Kohn KVV: Constitutive expression of human Bcl-2 modulates nitrogen mustard- and camptothecin-induced apoptosis. Cancer Res 53:1853-1861,1993.
188. Wang YW, Forrester K, Yeh H, Feitelson MA, Gu JM, Harris CC: Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3. Proc Nail Acad Sci U S A 91:2230-2234,1994.
189. Wang L, Miura M, Bergeron L, Zhu H, Yuan J: Ich-l, an ke/ccd-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78:739-750, 1994.
190. Wang XW, Yeh H, Schaffer L, Roy R, Moncollin V, Egly JM, Wang Z, Friedberg EC, Evans MK, Taffe BG, Bohr VA, Weeda G, Hoeijmakers JHJ, Forrester K, Harris CC: p53 modulation of TFllH-associated nucleotide excision repair activity. Nature Genet 10:188-195, 1995.
191. Weiler M, Malipiero U, Rensing-Ehl A, Barr P, Fontana A: Fas/ APO-1 gene transfer for human malignant glioma. Cancer Res 55:2936-2944,1995.
192. Whittemore E, Loo D, Cotman C: Exposure to hydrogen peroxide induces cell death via apoptosis in cultured rat cortical neurons. Neuroreport 5:1485-1488, 1994.
193. Williams G, Smith C, Spooncer E, Dexter T, Taylor D: Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature 343:76-79, 1990.
194. Wood K, Youle R: The role of free radicals and p53 in neuron apoptosis in vivo. J Neurosci 15:5851-5857, 1995.
195. Wu J, Ye Z, Darras B: Frequency of p53 tumor suppressor gene mutations in human primary brain tumors. Neurosurgery 33: 824-830, 1993.
196. Wyllie A: Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284: 555-556,1980.
197. Wyllie A: Chromntin cleavage in apoptosis: Association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol 142:67-77, 1984.
198. Wyllie A, Kerr J, Currie A: Cell death: The significance of apo. ptosis. Int Rev Cytol 68:251-307, 1980.
199. Yang J, Liu X, Challa K, Kirn CN, Ibrado AM, Cai J, Peng T, Jones DP, Wang X: Prevention of apoptosis by W-2: Release of cytochrome c from mitochondria blocked. Science 275:1129-1132,1997.
200. Yang E, Zha J, Jockei J, Boise L, Thompson C, Korsmeyer S: Bad, a heterodimeric partner for Bcl-xl and Bcl-2, displaces Bax and promotes cell death. Cell 80:285-291, 1995.
201. Yin C, Knudson M, Korsmeyer S, Dyke T: Bax suppresses tumorigenesis and stimulates apoptosis in vivo. Nature 385:637640,1997.
202. Yin D, Kondo S, Bamett G, Morimura T, Takeuchi J: Tumor necrosis factor a induces p53-dependent apoptosis in rat glioma cells. Neurosurgery 37:758-762,1995.
203. Yin XM, Oltvai ZN, Korsmeyer SJ: BH1 and BH2 domains of bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-333, 1994.
204. Deleted in proof.
205. Yoshioka A, Tanaka S, Hiraoka O, Kayama Y, Hirota Y, Ayusawa D, Seno T, Garrctt C, Wataya Y: Deoxyribonudeoside triphosphate imbalance: 5-Fluorodeoxyuridine-induced DMA double-strand breaks in mouse FM3A cells and the mechanism of death. J Biol Chem 262:8235-8241,1987.
206. Yu J, Sena-Esteves M, Paulus W, Breakefield X; Reeves S: Retroviral delivery and tetracycline-dependent expression of IL-lconverting enzyme (ICE) in a rat glioma model provides controlled induction of apoptotic death in tumor cells. Cancer Res 56:5423-5427,1996.
207. Yuan J: Transducing signals of life and death. Curr Opin Cell Biol 9:247-251, 1997.
208. Yuan JY, Horvitz HR: The Cnenorliabditis ekgans genes ccd-3 and ced-4 act autonomously to cause programmed cell death. Dev Biol 138:33-41, 1990.
209. Yuan J, Horvitz R: The Caenorlmbditis ekgans cell death gene cerf-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 116:309-320,1992.
210. Yuan J, Shaham S, Ledoux S, Ellis H, Horvitz R: The C. clegans cell death gene cf-3 encodes a protein similar to mammalian interleukin-l-bi'frt-converting enzyme. Cell 74:641-652, 1993.
211. Zeevalk G, Schoepp D, Nicklas W: Aurintricarboxylic acid prevents NMDA-mediated excitotoxicity: Evidence for its action as an NMDA receptor antagonist. J Neurochem 61:386-389, 1993.
212. Zhong LT, Sarafian T, Kane DJ, Charles AC, Mäh SP, Edwards RH, Bredesen DE: Bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl Acad Sci USA 90:45334537,1993.
213. Ziv I, Melamed E, Nardi N, Luria D, Achiron A, Offen D, Barzilai A: Dopamine induces apoptosis-like cell death in cultured chick sympathetic neurons: A possible novel pathogenetic mechanism in Parkinson's disease. Neurosci Lett 170:136-140, 1994.