Mechanisms of nerve cell death: apoptosis or necrosis after cerebral ischaemia

International Review of Neurobiology

Volumn , Issue 40, 1996, Pages 1-25

  Chalmers Redman, R M E ^a   Fraser, A D ^a   Ju, W Y H ^a   Wadia, J ^a   Tatton, N A ^a   Tatton, W G ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33845197309     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0074-7742(08)60713-8     Document Type: Article

References (184)

1. Agard, D.A. & Sedat, J.W.(l 983) Three-dimensional architecture of a polytene nucleus. jYalure, 302,676-681.
2. Anderson, AJ., Su, J.H. & Cotman, C.W. (1996) DNA damage and apoptosis in Alzheimer's disease: colocalization with c-Jun immunoreactivity, relationship to brain area and the effect of postmortem delay. J.Neurosoci., 16, 1710-1719.
3. Anglade, P., Michel, P., Marquez.J., Mouatt-Prient, A., Ruberg, M. & Hirsch, E.G. et al. (1995) Apoptotic degeneration of nigral dopaminergic neurones in Parkinson's disease. Proc. Soc. Aeurosci., 21,489.3.
4. Baffy, G., Miyashita, T., Williamson, J.R. & Reed, J.C. (1993) Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning ofintracellular calcium and is blocked by enforced Bcl-2 oncoprotein production.J. Biol. Cian., 268, 6511-6519.
5. BaLxera, E., Bosca, L., Stauber, G., Gonzalez, A., Gonzalo, J.A. & Martinez, A. (1994) From apoptosis to autoimmunity: insights from signaling pathways leading to proliferation or programmed cell death. Immunol. Rev., 142, 53-91.
6. Baringaga, M. (1994) Neurotrophic factors enter the clinic. Science, 264, 772-774.
7. Batistatou, A. & Greene, L.A. (1993) Internucleosomal DNA cleavage and neuronal cell survival/death. J. Cell Bio., 122, 523-32.
8. Beal, M.F. (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann. Neural., 31, 119-130.
9. Beal, M.F., Hyman, T & Koroshetz, W. (1993) Do defects in mitochondrial energy metabolism underlie the pathology of neurodegenerative diseases? Trends jVeurosci., 16, 125-131.
10. Behl, G., Hove)-, L.d., Krajewski, S., Schubert, D. & Reed.J.C. (1993) BCL-2 prevents killing of neuronal cells by glutamate but not by amyloid beta protein. Biochein. Biophjs. Res. Commun., 197, 949-956.
11. Behl, C., Davis,J.B., Klier, EG. & Schubert, D. (1994) Amyloid beta peptide induces necrosis rather than apoptosis. Brain Res., 645, 253-264.
12. Behrens, MJ., Koh, J., Gwag, BJ, Canzoniero, L.M.T., Sensi, S.L. & Choi, D.W. (1994) Mitochondrial toxins induce cycloheximide-sensitivc neuronal death in murine cortical cultures. Soc. Xeurosci. Abst., 20, 248.
13. Beilharz, EJ., Williams, C.E., Dragunow, M., Sirimanne, E.S. & Gluckman, P.D. (1995)
14. Mechanisms of delayed cell death following hypoxic-ischaemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Brain Res. Mol. Brain Res., 29, 1-14.
15. Bernardes, C.F., Meyer-Fernandes, J.R., Basseres, D.S., Castilho, R.F. & Vercesi, A.E. (1994) Ca2+-dependent permeabilization of the inner mitochondria! membrane by 4,4'-diisothicyanatostilbene-2,2'-disulfonic acid (DIDS). Biochim. Biophys. Acta, 1188, 93-100.
16. Bonfoco, E., Ceccatelli, S., Manzo, L. & Nicotera, P. (1995a) Colchicine induces apoptosis in cerebellar granule cells. Exp. Cell. Res., 218, 189-200.
17. Bonfoco, E., Krainic, D., Ankarcrona, M., Nicotera, P. & Lipton, S.A. (1995b) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methylD-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. NtlAcad. Sei. USA, 92, 7162-7166.
18. Boniece, I.R. & \Vagner, J.A. (1993) Growth factors protect PC 12 cells against ischaemia by a mechanism that is independent of PKA, PKC, and protein synthesis. J. Xeurosci., 13, 4220-4228.
19. Bredesen, D.E. (1995) Neural apoptosis. Ann. Xeuml., 38, 839-851.
20. Brouillet, E., Jenkins, B.C., Hyman, B.T., Ferrante, RJ., Kowall, N.W. & Srivastave, R. et al. (1993) Age-dependent vulnerability of the striatum to the mitochondrial toxin 3-nitroproprionic acid. J. Neurochem., 60, 356-359.
21. Brugg, B., Michel, P.P., Agid, Y. & Ruberg, M. (1996) Ceramide induces apoptosis in cultured , mesencephalic neurones. J. Jfeurochem, 66, 733-739.
22. Chacon, E., Reece,J.M., Nieminen, A.L., Zahrebelsi, G., Herman, B. & Lemasters,JJ. (1994) Distribution of electrical potential, pH, free Ca2+, and volume inside cultured adult rabbit cardiac myocytes during chemical hypoxia: A multiparameter digitized confocal microscopic study. Biophys. J., 66, 942-952.
23. Charriaut-Mariangue, C. & Ben-Ari, Y. (1995) A cautionary note on the use of the TUNEL stain to determine apoptosis. NeuroReport, 7, 61-64.
24. Charriaut-Mariangue, C., Margaill, I., Plotkine, M. & Ben-Ari, Y. (1995) Early endonuclease activation following reversible focal ischaemia in the rat brain. J. Cereb. Bl. Fl. Metab., 15, 385-388.
25. ChenJ., Graham, S.H., Chan, P.H., LanJ., Zhou, R.L. & Simon, R.P. (1995) bcl-2 is expressed in neurones that survive focal ischaemia in the rat. jVeuroReport, 6, 394-398.
26. Cheng, B. & Mattson, M.P. (1991) NGF and bFGF protect rat hippocampal and human cortical neurones against hypoglycémie damage by stabilizing calcium homeostasis. Neuron, 7, 1031-41.
27. Choi, D.W. (1995) Calcium: still center-stage in hypoxic-ischaemic neuronal death. Trends Xeurosci., 18, 58-60.
28. Choi, D.W. & Rotham, S.M. (1990) The role of glutamate neurotoxicity in hypoxic-ischaemic neuronal death. Ann. Rev. Neurosci., 13, 171-182.
29. Connor, J.R. & Menzies, S.L. (1995) Cellular management of iron in the brain. J JVeurol. Sei., 134, 33-34.
30. Cossarizza, A., Franceschi, C., Monti, D., Salvioli, S., Bellesia, E. & Rivabene, R. et al. (1995) Protective effect of N-acetylcysteine in tumour necrosis factor-alpha-induced apoptosis in U937 cells: the role of mitochondria. Exp. Cell Res., 220, 232-10.
31. Cotman, C.W. & Anderson, AJ. (1995) A potential role for apoptosis in neurodegeration and Alzheimer's disease. Mol.Neurobiol., 10, 19-45.
32. Cotman, C.W., Whittemore, E.R., Watt, J.A., Anderson, AJ. & Loo, D.T. (1994) Possible role or apoptosis in Alzheimer's disease. Ann.N.Y.Acad. Sei., 747, 36-49.
33. Darzynkiewicz, Z., Bruno, S., Del Bino, G., Gorczyca,W., Hotz, M.A. & Lassota, P. etal. (1992) Features of apoptotic cells measured by flow cytometry. Cylornelry, 13, 795-808.
34. Deckwerth, T.L. & Johnson, E.M.,Jr. (1993) Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurones deprived of nerve growth factor. J Cell. Bid., 123, 1207-1222.
35. Degirolami, U., Crowell, R.M. & Marcoux, F.W. (1984) Selective necrosis and total necrosis in focal cerebral ischaemia. Neuropathologic observations on experimental middle cerebral artery occlusion in the macaque monkey. J. Neuropathol. Exp. Neural., 43, 57-71.
36. Deshpande, J., Bergstedt, K., Linden, T., Kalimo, H. & Wieloch, T. (1992) Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischaemia: evidence against programmed cell death. Exp. Brain Res., 88, 91-105.
37. Dessi, E, Charriaut-Mariangue, C., Khrcstchatisky, M. & Ben-Ari, Y. (1993) Glutamateinduced neuronal death is not a programmed cell death in cerebellar culture. J. Neurochem., 60, 1953-1955.
38. Dessi, E, Pollard, H., Moreau, J., Ben-Ari, Y. & Charriaut-Mariangue, G. (1995) Cytosine arabinoside induces apoptosis in cerebellar neurones in culture. J. Neurochem., 64, 1980-1987.
39. Dipasquale, B., Marini, A.M. & Youle, RJ. (1991) Apoptosis and DNA degradation induced by l-methyl-4-phenylpryidinium in neurones. Biochem. Biophy. Res. Commun., 181,1442-1448.
40. Dragunow, M., Beilharz, E., Sirimanne, E., La\vlor, P., Williams, C. & Bravo, R. et al. (1994) Immediate-early gene protein expression in neurones undergoing delayed death, but not necrosis, following hypoxic-ischaemic injury to the young rat brain. Brain Res. Mol. Brain Res., 25, 19-33.
41. Dragunow, M., Faull, R.L., Lawlor, P., Beilharz, E.J., Singleton, K. & Walker, E.B., et al. (1995) In situ evidence for DNA fragmentation in Huntington's disease striatum and Alzheimeris disease temporal lobes. NeuroReport, 6, 1053-7.
42. Dragunow, M. & Preston, K. (1995) The role of inducible transcription factors in apoptotic nerve cell death. Brain Res. Rev., 21, 1-28.
43. Dragunow, M., Young, D., Hughes, P., MacGibbon, G., Lawlor, P. & Singleton, K. et al. (1993) Is c-Jun involved in nerve cell death following status epilepticus and hypoxic-ischaemic brain injury? Brain Res. Mol. Brain Res., 18, 347-52.
44. Eastman, A. (1993) Apoptosis: a product of programmed and unprogrammed cell death. Toxicol. Appl. Pharmacol., 121, 160-164.
45. Edwards, A.D., Yue, X., Squier, M.V., Thoresen, M., Cady, E.B. & Penrice, J. et al. (1995). Specific inhibition of apoptosis after cerebral hypoxia-ischaemia by moderate post-insult hypothermia.Biochem. & Biophys. Res. Commun., 217, 1193-1199.
46. Enokido, Y. & Hatanaka, H. (1994) [Neuronal cell death and apoptosis]. Can To Kagaku Rjoho, 21,615-620.
47. Farinelli, S.E. & Greene, L.A. (1996) Cell cycle blockers mimosine, ciclopirox, and deferoxamine prevent the death of PC 12 cells and postmitotic sympathetic neurones after removal of trophic support. J.Neurosci., 16, 1150-1162.
48. Ferrari, G., Yan, C.Y. & Greene, L.A. (1995).A-acerylcystine (D- and L-stereoisomers) prevents apoptotic death of neuronal cells. J.Neurosci., 15, 2857-2866.
49. Finnegan, K.T. & Karler, R. (1992) Role for protein synthesis in the neurotoxic effects of methamphetamine in mice and rats. Brain Res., 591, 160-164.
50. Forloni, G., Chiesa, R., Smiroldo, S., Verga, L., Salmona, M. & Tagliavini, F. et al. (1993) Apoptosis mediated neurotoxicity induced by chronic application of beta amyloid fragment 25-35. NeuroReport, 4, 523-526.
51. Frim, D.M., Simpson, J., Uhler, T.A., Short, M.P., Bossi, S.R. & Breakfield, X.O., et al. (1993) Striatal degeneration induced by mitochondrial blockade is prevented by biologically delivered NGF. J. Murosci. Res., 35, 452-458.
52. Garcia,J.H. & Kamijyo, Y. (1974) Cerebral infarction. Evolution of histopathological changes after occlusion of a middle cerebral artery in primates. J. Neuropathol. Exp. Neural., 33, 408-421.
53. Garcia, J.H., Chen, H., Li, Y, Zhang, Z.G., Lian, J. & Chen, S., et al. (1993) Progression from ischaemic injury to infarct following middle cerebral artery occlusion in the rat. Am. J. Pathol, 142,623-635.
54. Gobe, G.G. (1994) Apoptosis in brain and gut tissue of mice fed a seed preparation of the cycad Lepidozamia peroffskyana. Biochem. Bioptys. Res. Commun., 205, 327-33.
55. Greenlund, L.J.S., Deckwerth, T.L. & Johnson, E.M. (1995) Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron, 14,303-315.
56. Gschwind, M. & Huber, G. (1995) Apoptotic cell death induced by beta-amyloid 1-42 peptide is cell-type dependent. J. Neurochem., 65, 292-300.
57. Gwag, BJ., Lobner, D., Koh, J., We, M.B. & Choi, E.W. (1994) Blockade of glutamine receptors during oxygen glucose deprivation unmasks apoptosis in cultured cortical neurones. Soc. Neurosd. Abstr., 24, 248.
58. Hagg, T. & Varon, S. (1993) Ciliary neurotrophic factor prevents degeneration of adult rat substantia nigra dopaminergic neurones in tiro. Proc. NatlAcad. Sei. USA, 90, 6315-6319.
59. Hall, E.D., & McCall.J.M. (1994) Therapeutic potential of the lazeroids (21 aminosteroids) in acute CNS trauma, ischaemia and subarachnoid hemorrhage. Adv.Pharmacol., 28, 221-268.
60. Ham, J., Babij, C., Whitefield, J., Pfarr, C.M., Lallemand, D. & Yaniv, M., et al. (1995) A c-Jun dominant negative mutant protects sympathetic neurones against programmed cell death. Neuron, 14, 927-939.
61. Kara, A., Yoshimi, N., Hirose, Y, Ino, R, Tanaka, T. & Mori, H. (1995) DNA fragmentation in granular cells of human cerebellum following global ischaemia. Brain Res., 697, 247-250.
62. Hartley, A., StoneJ.M., Heron, C., Cooper,J.M. & Schapira, A.H. (1994) Complex I inhibitors induce dose-dependent apoptosis in PC 12 cells: relevance to Parkinson's disease. J. Neurochem., 63, 1987-90.
63. Hassouna, I., Wickert, H., Zimmermann, M. & Gillardon, F. (1996) Increase in bax expression in substantia nigra follo\ving l-methyl-4-phenyl-l,2,3,6-tetrahydropyridine (MPTP) treatment of mice. Neurosci. Letts., 204, 85-88.
64. Henderson, J.T., Seniuk, N.A., Richardson, P.M., Gaudie, J. & Roder, J.C. (1994) Systemic administration of ciliary neurotrophic factor induces cachexia in rodents. J. Clin. Invest., 93, 2632-2638.
65. Hengartner, M.O. & Horvitz, H.R. (1994) C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell, 76, 665-676.
66. Kennet, T.G., Bertoni, G., Richter, C. & Peterhans, E. (1993) Expression of Bcl-2 protein enhances the survival of mouse fibrosarcoid cells in tumour necrosis factor-mediated cytotoxicity. Cancer Res., 53, 1456-1460.
67. Hill, I.E., MacManuSjJ.R, Rasquinha, I. &Tour, U.I. (1995) DNA fragmentation indicative of apoptosis following unilateral cerebral hypoxia-ischaemia in the neonatal rat. Brain Res., 676, 398-103.
68. Hockenbery, D., Nunez, G., Milliman, C., Schreiber, R.D. & Korsmeyer, S.J. (1990) Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature, 348, 334-336.
69. Hockenbery, D.M., Oltvai, Z.N., Yin, X.M., Milliman, C.L. & Korsmeyer, SJ. (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell, 75, 241-251.
70. Islam, R, Aftabuddin, M., Moriwaki, A. & Hori, Y. (1995) Detection of DNA damage induced by apoptosis in the rat brain following incomplete ischaemia. Neurosci. Letts. 188, 159-162.
71. Iwai, T., Hara, A., Niwa, M., Nozaki, M., Uematsu, T. & Sakai, R, et al. (l 995) Temporal profile of nuclear DNA fragmentation in situ in gerbil hippocampus following transient forebrain . ischaemia. Brain Res., 671, 305-8.
72. Jacobson, M.D., Burne, J.F., King, M.P., Miyashita, T, Reed, J.C. & Raff, M.C. (1993). Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature, 361, 365-9.
73. Janiak, F., Leber, B. & Andrews, DA V.(l 994) Assembly of Bcl-2 into microsomal and outer mitochondrial membranes. Biol. Chem., 269, 9842-9849.
74. Johnson, E.M.,Jr. (1994) Possible role of neuronal apoptosis in Alzheimer's disease. Neurobiol. Aging, 15 Suppl. 2, 5, 187-9.
75. Johnson, E.M., Greenland, L.J.S., Akins, P.T. & Hsu, C.Y. (1995) Neuronal apoptosis: Current understanding of molecular mechanisms and potential role in ischaemic brain injury. J. Neumtmuma, 12, 843-852.
76. Johnson, J. & Oppenheim, R. (1994) Neurotrophins. Keeping track of changing neurotrophic theory. PUTT. Biol., 4, 662-665.
77. Kerr,J.F.R., Wyllie, A.H. & Currie, A.R. (1972) Apoptosis: A basic biological phenomenon with wide ranging implications in tissue kinetics. Br. J. Cancer, 26, 239-257.
78. Kihara, S., Shiraishi, T., Nakagawa, S., Toda, K. & Tabuchi, K. (1994) Visualization of DNA double strand breaks in the gerbil hippocampal CA1 following transient ischaemia. Neurosci. Letts., 175, 133-136.
79. Kobayashi, Y., Saheki, T. & Shinozawa, T. (1994) Induction of PC 12 cell death, apoptosis, by a sialoglycopeptide from bovine brain. Biochem. Biophys. Res. Commun., 203, 1554-1559.
80. Koh, J.Y. & Cotman, C.W. (1992) Programmed cell death: its possible contribution to neurotoxicity mediated by calcium channel antagonists. Brain Res., 587, 233-240.
81. Kroemer, G., Petit, P., Xamzami, N., Vayssierre, J.L. & Mignotte, B. (1995) The biochemistry of programmed cell death. FASEB.J., 9, 1277-1287.
82. Kure, S., Tominaga, T., Yoshimotoo, T., Tada, K. & Narisawa, K. (1991) Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem. Biophys. Res. Commun., 179, 286-291.
83. Lassmann, H., Bancher, G., Breitschopf, H., WegielJ., Bobinski, M. &Jellinger, K., etal. (1995) Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol. Beil., 89, 35-11.
84. Laurence, M.S., Ho, D.Y, Sun, G.H., Steinberg, G.K. & Sapolsky, R.M. (1996) Over expression of bcl-2 with herpes simplex virus vectors protects CNS neurones against neurological insults in rilro and in riro.J.Neumsci., 16, 486-196.
85. Leppin, C., Finiels Marlier, F., Crawley, J.N., Montpied, P. & Paul, S.M. (1992) Failure of a protein synthesis inhibitor to modify glutamate receptor-mediated neurotoxicity in liio. Brain Res., 581, 168-170.
86. Li, Y, Chopp, M.,Jiang, N., Yao, F. & Zaloga, C. (1995a) Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab., 15, 389-97.
87. Li, Y, Chopp, M., Jiang, N. & Zaloga, C. (1995b) In situ detection of DNA fragmentation after focal cerebral ischaemia in mice. Brain Res. Mol. Brain Res., 28, 164-168.
88. Li, Y, Chopp, M.Jiang, N., Zhang, Z.G. & Zaloga, G. (1995e) Induction of DNA fragmentation after 10 to 20 minutes of focal cerebral ischaemia in rats. Stroke, 26, 1252-1257.
89. Li, Y, Sharov, VG., Jiang, N., Zaloga, C., Sabbah, H.N. & Chopp, M. (1995d) Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am. J. Pathoi, 146, 1045-1051.
90. Linnik, M.D., Zahos, P., Geschwind, M.D. & Federoff, HJ. (1995) Expression of bcl-2 from a defective herpes simplex virus-1 vector limits neuronal death in focal cerebral ischaemia. Stroke, 26, 1670-1674.
91. Linnik, M.D., Zobrist, R.H. & Hatfield, M.D. (1993) Evidence supporting a role for programmed cell death in focal cerebral ischaemia in rats. Stroke, 24, 2002-2008.
92. Lithgow, T., van Driel, R., Bertram, J.F. & Strasser, A. (1994) The protein product of the oncogene bcl-2 is a component of the nuclear envelope, the endoplasmic reticulum, and the outer mitochondrial membrane. Cell Growth Differ., 5, 411-117.
93. Loo, D.T., Copani, A., Pike, C J., Whittemore, E.R., Walencewicz, AJ. & Cotman, C.W. (1993) Apoptosis is induced by beta-amyloid in cultured central nervous system neurones. Proc. Null Acad. Set. USA, 90, 7951-7955.
94. MacManus,J.P., Buchan, A.M., Hill, I.E., Rasquinha, I. & Preston, E. (1993) Global ischaemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci. Letts, 164,89-92.
95. MacManusJ.P., Hill, I.E., Huang, Z.G., Rasquinha, I., Xue, D. & Buchan, A.M. (1994) DNA
96. damage consistent with apoptosis in transient focal ischaemic neocortex. NeuroReport,-5, 493-496.
97. Martin, O.P., Schmidt, R.E., DiStephano, P.S., Lowry, O.K., Carter, J.G. & Johnson, E.M. (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell BioL, 106, 829-843.
98. Martin, R.L:, Lloyd, H.G. & Cowan, A.I. (1994) The early events of oxygen and glucose deprivation: setting the scene for neuronal death? Trends Neurosci., 17, 251-257.
99. Matsuyama, T., Hâta, R., Yamamoto, Y, Tagaya, M., Akita, H. & Uno, H., et al. (1995) Localization of Fas antigen mRNA induced in postischaemic murine forebrain by in situ hybridization. Mol. Brain Res., 34, 166-172.
100. Mattson, M.P. & Cheng, B. (1993) Growth factors protect neurones against excitotoxic/ischaemic damage by stabilizing calcium homeostasis. Stroke, 24.
101. Mattson, M.P., Rydel, R.E., Lieberburg, I. & Smith Swintosky, V.L. (1993a) Altered calcium signaling and neuronal injury: stroke and Alzheimer's disease as examples. Ann. NYAcad. Sei., 679,1-21.
102. Mattson, M.P. & Scheff, S.W. (1994) Endogenous neuroprotection factors and traumatic brain injury: mechanisms of action and implications for therapy.j'. Neuratmuma, 11, 3-33.
103. Mattson, M.P., Zhang, Y. & Böse, S. (1993b) Growth factors prevent mitochondrial dysfunction, loss of Ca2t homeostasis, and cell injury, but not ATP depletion in hippocampal neurones deprived of glucose. Exp. Neural., 121, 1-13.
104. Mehmet, H., Yue, X., Squier, M.V., Lorek, A., Cady, E. & Penrice, J., et al (1994) Increased apoptosis in the cingulate sulcus of newborn piglets following transient hypoxia-ischaemia is related to the degree of high energy phosphate depletion during the insult. Neurosci. Letts., 181, 121-125.
105. Mesner, P.W., Winters, T.R. & Green, S.H. (1992) Nerve gro\vth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurones. J. Cell BioL, 119, 1669-1680.
106. Migheli, A., Cavalla, P., Marino, S. & Schiffer, D. (1994) A study of apoptosis in normal and pathologic nervous tissue after in situ end-labelling of DNA strand breaks. J. Neuropathol. Exp.Neurol.,53,606-16.
107. Miller, R.G., Petajan, J.H., Bryan, W.W., Armon, C., Barohn, RJ. & Goodpasture, J.C., et al. (1996) A placebo-controlled trial of recombinant human ciliary neurotrophic (rhCNTF) factor in amylotrophic lateral sclerosis. Ann. Neural., 39, 256-260.
108. Mitchell, I.J., Lawson, S., Moser, B., Laidlaw, S.M., Cooper, AJ. & Walkinshaw, G. et al. (1994) Glutamate-induced apoptosis results in a loss of striatal neurones in the parkinsonian rat. Neuroscience, 63, 1-5.
109. Mochizuki, H., Nakamura, N., Nishi, K. & Mizuno, Y. (1994) Apoptosis is induced by 1-methyl4-phenylpyridinium ion (MPP+) in ventral mesencephalic-striatal co-culture in rat. Neurosci. Letts., 170, 191-194.
110. Monaghan, P., Robertson, D., Amos, A.S., Dyer, M.J.S., Mason, D.Y. & Greaves, M.F. (1992) Ultrastructural localization of Bcl-2 protein. J. Histochem. Cytochem., 40, 1819-1825.
111. Mukherjee, S.K., Yasharel, R., Klaidman, L.K., Hutchin, T.P. & AdamsJ.D. (1995) Apoptosis and DNA fragmentation as induced by tertiary butylhydroperoxide in the brain. Brain Res. Bul., 38, 595-604.
112. Muller, W.E., Schröder, H.C., Ushijima, H., Dapper, J. & Bormann, J. (1992) gp!20 of Hiv-1 induces apoptosis in rat cortical cell cultures: prevention by memantine. EUT. J. Pharmacol., 226, 209-14.
113. Mutisya, E.M., Bowling, A.C. & Beal, M.F. (1994) Cortical cytochrome oxidase activity is reduced in Alzheimer's disease. J. Neurochem., 63, 2179-2184.
114. Mutoh, T., Tokuda, A., Marini, A.M. & Fujiki, N. (1994) l-Methyl-4-phcnylpyridinum kills differentiated PC 12 cells with a concomitant change in protein phosphorylation. Brain Res., 661,51-55.
115. Myers, K.M., Fiskum, G., Uu, Y.B., Simmens, S.J., Bredesen, D.E. & Murphy, A.N. (1995) Bcl2 protects neural cells from cyanide/aglyccmia-induced lipid oxidation, mitochondrial injury, and loss of viability. J. Neurochem., 65, 2432-2440.
116. Nakai, M., Takeda, A., Cleary, M.L. & Endo, T. (1993) The bcl-2 protein is inserted into the outer membrane but not into the inner membrane of rat liver mitochondria in titro. Biochem. Biophjs. Res. Commun., 196, 233-239.
117. Newmeyer, D.D., Farschon, D.M. & Reed, J.C. (1994) Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell, 79, 353-364.
118. Nicholls, D.G. & Ferguson, SJ. (1992) Bioenergetics 2. London: Academic Press.
119. Nitatori, T., Sato, N., Waguri, S.,Karasawa, Y., Araki, H. & Shibanai, K. etal. (1995) Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischaemia is apoptosis.j'. j\eurosci., 15, 1001-1011.
120. Okamoto, M., Matsumoto, M., Ohtsuki, T., Taguchi, A., Mikoshiba, K. & Yanagihara, T. etal. (1993) Internucleosomal DNA cleavage involved in ischaemia-induced neuronal death. Biochem. Biophjs. Res. Commun., 196, 1356-1362.
121. Olanow, C.W., Hauser, R.A., Gauger, L., Malapira, T., Koller, W. & HubbleJ. etal. (1995) The effect of deprenyl and levodopa on the progression of Parkinson's disease. Ann. jYeurol., 38, 771-777.
122. Oltvai, Z.N. & Korsmeyer, SJ. (1994) Checkpoints of dueling dimers foil death wishes. Cell, 79, 189-192.
123. Oo, T.F., Henchcliffe, C. & Burke, R.E. (1995) Apoptosis in substantia nigra following developmental hypoxic-ischaemic injury.Neuroscience, 69, 893-901.
124. Oppenheim, R.W. (1989) The neurotrophic theory and naturally occurring motoneurone death. Trends Jfeurosri., 12, 252-255.
125. Oppenheim, R.W. (1991) Cell death during the development of the nervous system. Ann. Rev. Aeurosd., 14, 1356-1362.
126. Oppenheim, R.W., Frevelte, D., Tytell, M. & Homma, S. (1990) Naturally occurring and induced neuronal death in the chick embryo in mo requires protein and RNA synthesis: evidence for the role of cell death genes. Dee. Biol., 138, 104-113.
127. Parkinson, S.G. (1993) Effects oftocopherol and deprenyl on the progression of disability in early Parkinson's disease. JfewEngl.J. Med., 328, 176-183.
128. Pechan, P.A., Yoshida, T, Panahian, N., Moskowitz, M.A. & Breakefield, X.O. (1995) Genetically modified fibroblasts producing NGF protect hippocampal neurones after ischaemia in the rat.NeuroReport, 6, 669-672.
129. Petit, P.X., Lecoeur, H., Zorn, E., Dauguet, C., Mignotte, B. & Gougeon, M.L. (1995) Alterations in mitochondrial structure and function are early events of dexamethasoneinduced thymocyte apoptosis.J. Cell Biol., 130, 157-167.
130. Petito, C.K. & Roberts, B. (1995a) Effect of postmortem interval on in situ end-labelling of DNA oligonucleosomes.,7. Neuropathol, Exp. Neural., 54, 761-765.
131. Petito, C.K. & Roberts, B. (1995b) Evidence of apoptotic cell death in HIV encephalitis [see comments]. Am. J. Pathol, 146, 1121-1130.
132. Pollard, H., Cantagrel, S., Charriaut-Mariangue, C., Moreau,J. & Ben Ari, Y. (1994) Apoptosis associated DNA fragmentation in epileptic brain damage.NeuroReport, 5, 1053-1055.
133. Portera-Cailliau, C., Hedreen,J.C., Price, D.L. & Koliatsos, V.E. (1995a) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci., 15, 3775-3787.
134. Portera-Cailliau, C., Hedreen.J.C., Price, D.L. & Koliatsos, YE. (1995b) Evidence for apoptotic cell death in Huntingdon's disease and excototic animal models. J. Neurosci., 15, 3775-3787.
135. Prhen, J.H., Bindokas, V.P., Marcuccilli, C.J., Krajewski, S., ReedJ.C. & Miller, RJ. (1994) Regulation of neuronal Bcl2 protein expression and calcium homcostasis by transforming
136. growth factor type beta confers wide-ranging protection on rat hippocampal neurones. Proc. NatlAcad. Sa. USA, 91, 12599-12603.
137. RafT, M.C., Barres, B.A., Burnc, J.E, Coles, H.S., Ishizaki, Y. &Jacobson, M.D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system. Science, 262, 695-700
138. ReedJ.C. (1994) Bcl-2 and the Regulation of Programmed Cell Death. J. CellBiol., 124, 1-6.
139. Regan, R.F., Panter, S.S.,Witz, A., Tilly, J.L. & GifTard, R.G. (1995) Ultrastructure of excitotoxic neuronal death in murine cortical culture. Brain Res., 705, 188-198.
140. 2+: their relationship to apoptosis and oncogenesis. FEBS Letts., 325, 104-107.
141. Richter, C., Gogvadze, V, Laffranchi, R., Schlapbach, R., Schweizer, M. & Suter, M. et al. (1995) Oxidants in mitochondria: from physiology to diseases. Biochem. BiophysActa, 1271, 67-74.
142. Richter, C. & Kass, G.E.N. (1991) Oxidative stress in mitochondria: its relationship to cellular calcium homeostasis, cell death, proliferation, and differentiation. Chan.-Biol. Interact, 77, 1-23.
143. Roberts-Lewis, J.M., Marcy, V.R., Zhao, Y, Vaught, J.L., Siman, R. & Lewis, M.E. (1993). Aurintricarboxylic acid protects hippocampal neurones from NMDA- and ischaemiainduced toxicity in liïo.J.Neurochem., 61, 378-381.
144. Rosenbaum, D.M., Michaelson, M., Batter, O.K., Doshi, P. & KesslerJ.A. (1994) Evidence for hypoxia-induced, programmed cell death of cultured neurones. Ann. Neural., 36, 864-870.
145. RothsteinJ.D., Bristol, L.A., Hosier, B., Brown, R.H.Jr. & Kuncl, R.W. (1994) Chronic inhibition of Superoxide dismutase produces apoptotic death of spinal neurones. Proc. Natl Acad. Sei USA, 91,4155-1159.
146. Rukenstein, A., Rydel, R.E. & Greene, L.A. (1991) Multiple agents rescue PC12 cells from serum-free cell death by translation- and transcription-independent mechanisms. J. Neuwsci., 11,2552-2563.
147. Schlingensiepen, K.H., Wollnik, E, Kunst, M., Schlingensiepen, R., Herdegen, T. & Brysch, W. (1994) The role ofjun transcription factor expression and phosphorylation in neuronal differentiation, neuronal cell death, and plastic adaptations in vii'O. Cell Mol. Neurobiol, 14, 487-505.
148. Schulze-OsthofT, K., Bakker, A.C., Vanhaesebroeck, B., Beyaert, R.Jacob, W.A. & Fiers, W. (1992) Cytotoxic activity of tumour necrosis factor is mediated by early damage of mitochondrial functions. J. Biol. Chem., 267, 5317-5323.
149. Sei, Y, Von Lubitz, K.J., Basile, A.S., Borner, M.M., Lin, R.C. & Skolnick, P. et al. (1994) Internucleosomal DNA fragmentation in gerbil hippocampus following forebrain ischaemia. Neurosci. Letts., 171, 179-182.
150. Sendtner, M., Arakawa, Y, Stockli, K.A., Kreutzberg, G.W. & Thoenen, H. (1991) Effect of ciliary neurotrophic factor (CNTF) on motoneurone survival. [Review.] J. Cell Sei., Supplement, 15, 103-109.
151. Sendtner, M., Holtmann, B., Kolbeck, R., Thoenen, H. & Barde, Y.-A. (1992a) Brain-derived neurotrophic factor prevents the death of motoneurones in newborn rats after nerve section. Nature, 360, 757-759.
152. Sendtner, M., Schmalbruch, H., Stockli, K.A., Carroll, P., Kreutzberg, G.W. & Thoenen, H. (1992b) Ciliary neurotrophic factor prevents degeneration of motor neurones in mouse mutant progressive motor neuroneopathy. Nature, 358, 502-504.
153. Shaw, P. (1994) Deconvolution in 3D optical microscopy. Histochem. J., 26, 687-694.
154. Shigeno, T., Yamasaki, Y. & Kato, G. (1990) Reduction of delayed neuronal death by inhibition of protein synthesis. Neurosd. Letts., 120, 117-119.
155. Slater, A.E, Nobel, C.S. & Orrenius, S. (1995a) The role of intracellular oxidants in apoptosis. Biochim. Biophys. Acta, 1271, 59-62.
156. Slater, A.F.G., Stefan, C., Nobel, I.,van den Dobbelsteen, DJ. & Orrenius. S. (1995b) Signalling mechanisms and oxidative stress in apoptosis. Toxicol. Letts., 82-3, 149-153.
157. Smale, G., Nichols, N.R., Brady, D.R., Finch, C.E. & Horion, W.E., Jr. (1995) Evidence for apoptotic cell death in Alzheimer's disease. Exp. Neurol., 133, 225-230.
158. Smets, L.A., Van den BergJ., Acton, D., Top, B., Van Rooij, H. & Verwijsjanssen, M. (1994) BCL-2 expression and mitochondrial activity in leukemic cells with different sensitivity to glucocorticoid-induced apoptosis. Blood, 84, 1613-1619.
159. Steinberg, R.H. (1994) Survival factors in retinal degenerations. Curr. Opin. Neurobiol., 4, 515-524.
160. Su, J.H., Anderson, A.J., Cummings, BJ. & Cotman, C.W. (1994) Immunohistochemical evidence for apoptosis in Alzheimer's disease. NeuroReport, 5, 2529-2533.
161. Takahashi, A. & Earnshaw, W.C. (1996) ICE-related proteases in apoptosis. Cur. Opin. Gen. & Dev., 6, 50-55.
162. Tatton, W.G., Ju, WJ.H., Wadia, J. & Tatton, N.A. (1996) Reduction of neuronal apoptosis by small molecules: promise for new approaches to neurological therapy.In Neuroprotection and Neundegeneration (eds Olanow, W., Youdim, M. & Jenner, P.), pp. 209-229. Academic Press Ltd, London.
163. Tatton, W.G., Ju, W.Y., Holland, O.P., Tai, C. & Kwan, M. (1994). (-)-Deprenyl reduces PG12 cell apoptosis by inducing new protein synthesis. J. Neurochem., 63, 1572-1575.
164. Thomas, L.B., Gates, DJ., Richfield, E.K., TF, O.B., SchweitzerJ.B. & Steindler, D.A. (1995) DNA end labelling (TUNEL) in Huntington's disease and other neuropathological conditions. Exp. Neural., 133, 265-272.
165. Tipton, K.F. & Singer, T.P. (1993) Advances in our understanding of the mechanisms of the neurotoxicity of MPTP and related compounds. J. Neurochem., 61, 1191-1207.
166. Tobita, M., Nagano, I., Nakamura, S., Itoyama, Y. & Kogure, K. (1995) DNA single-strand breaks in postischaemic gerbil brain detected by in silu nick translation procedure. Neurosci. Letts., 200, 129-132.
167. Troy, C.M. & Shelanski, M.L. (1994) Down-regulation of copper/zinc Superoxide dismutase causes apoptotic death in PC12 neuronal cells. Proc. NatlAcad. Set. USA. 91, 6384-6387.
168. Tso, M.O., Zhang, C., Abler, A.S., Chang, C.J., Wong, F. & Chang, G.Q. et al. (1994) Apoptosis leads to photoreceptor degeneration in inherited retinal dystrophy of RCS rats. Invest. Ophthalmol. Vis. Sei., 35, 2693-2699.
169. van de Water, B., ZoeteweijJ.R, De Bont, HJ., Mulder, G.J. & NagelkerkeJ.E (1994) Role of mitochondrial Ca2in the oxidative stress-induced dissipation of the mitochondrial membrane potential. J. Biol. Chem., 269, 14546-14552.
170. Vayssiere,J.L., Petit, P.X., Risler, Y. & Mignotte, B. (1994) Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with simian virus 40. Proc. NatlAcad. Sei USA 91,11 752-11 756.
171. Volpe, B.T., Wessel, T.C., Mukherjee, B. & Federoff, H.J. (1995) Temporal pattern of internucleosomal DNA fragmentation in the striatum and hippocampus after transient forebrain ischaemia. Neurosci. Letts, 186, 157-160.
172. Walkinshaw, G. & Waters, C.M. (1994) Neurotoxin-induced cell death in neuronal PC 12 cells is mediated by induction of apoptosis. Neuroscience 63, 975-987.
173. Watt, J.A., Pike CJ., Walencewicz Wasserman, AJ. & Cotman, C.W. (1994) Ultrastructural analysis of beta-amyloid-induced apoptosis in cultured hippocampal neurones Brain Res., 661, 147-156.
174. Wolvetang, EJ.Johnson, K.L., Krauer, K., Ralph, SJ. & Linnane, A.W. (1994) Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Letts, 339, 40-44.
175. Wyllie, A.H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature, 284, 555-556.
176. Wyllie, A.H. (1987) Cell death.Int. Rev. Cylol, 17, 755-785.
177. Yan, C.Y., Ferrari, G. & Greene, L.A. (1995) .A-acetylcysteine-promoted survival of PC12 cells is glutathione-independent but transcription-dependent. J. Biol. Chem., 270, 26827-26832.
178. Yoshiyama, Y, Yamada, T., Asanuma, K. & Asahi, T. (1994) Apoptosis related antigen, Le(Y) and nick-end labelling are positive in spinal motor neurones in amyotrophic lateral sclerosis. Ada jVeuropathol. Berl., 88, 207-211.
179. Zamzami, N., Marchetti, P., Castedo, M., Decaudin, D., Macho, A. &
180. Zamzami, N., Marchetti, P., Castedo, M., Zanin, C., Vayssiere, J.L. & Petit, P.X. et al. (1995) Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in lii-o.J. Exp. Med., 181, 1661-1672.
181. Zhang, F., Richardson, P.M., Holland, D.P., Guo, G. & Tatton, W.G. (1995) CNTF or (-)-deprenyl in immature rats: survival of axotomized facial motoneurones and weight loss. J. Murosci. Res., 40, 564-570.
182. Zhang, Y, Tatsuno, T., CarneyJ.M. & Mattson, M.P. (1993) Basic FGF, NGF, and IFGs protect hippocampal and cortical neurones against iron-induced degeneration. J. Cereb. Blood How Metab., 13, 378-388.
183. Ziv, I., Melamed, E., Nardi,_N., Luria, D., Achiron, A. & Offen, D. (1994) Dopamine induces apoptosis-like cell death in cultured chick sympathetic neurones. Meurosci. Letts. 170, 136-140.
184. Zsnagy, I., Steiber, J. & Jeney, F. (1995) Induction of age pigment accumulation in the brain cells of young male rats through iron-injection into the cerebrospinal fluid. Gerontology 41, 145-156.