Neuronal cell death in the mammalian nervous system: The calmortin hypothesis

General Pharmacology

Volumn 27, Issue 3, 1996, Pages 407-419

  Bennett, Max R ^b   Huxlin, Krystel R ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NONE

Author keywords

Apoptosis; Axotomy; Calcium; Excitotoxicity; Hypoxia; Ischemia; Naturally occurring cell death; Necrosis; Neurons

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); BASIC FIBROBLAST GROWTH FACTOR; BRAIN DERIVED NEUROTROPHIN FACTOR; CALCIUM; CALCIUM ANTAGONIST; CALCIUM CHELATING AGENT; CALPAIN; FLURANIZINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NERVE GROWTH FACTOR; NEUROPROTECTIVE AGENT; NEUROTROPHIN 3; NEUROTROPHIN 4; SODIUM; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DEATH; CELL TYPE; DEVELOPMENT; HUMAN; HYPOTHESIS; HYPOXIA; ISCHEMIA; MAMMAL; NERVE CELL DEGENERATION; NERVE FIBER TRANSECTION; NERVOUS SYSTEM; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; THYMOCYTE;

EID: 0029895416     PISSN: 03063623     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-3623(95)02069-1     Document Type: Review

References (197)

1. Aguayo A. J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. In Synaptic Plasticity (edited by Coman C.W.). Gulford Press, New York, pp. 457-484.
2. Aguayo A. J., Rasminsky M., Bray G. M., Carbonetto S., McKerracher L., Villegas-Perez M. P., Vidal-Sanz M. and Carter D. A. (1991) Degenerative and regenerative responses of injured neurons in the central nervous system of adult mammals. Phil. Trans. R. Soc. Lond. B. 331, 337-343.
3. Alison M. R. and Saraf C. E. (1992) Apoptosis: a gene-directed programme of cell death. J. Royal Coll. Phys. Lond. 26, 25-35.
4. Allcutt D., Berry M. and Sievers J. (1984) A qualitative comparison of the reactions of retinal ganglion cells to optic nerve crush in neonatal and adult mice. Develop. Brain Res. 16, 231-240.
5. Barron K. D., Dentinger M. P., Krohel G., Easton S. K. and Mankes R. (1986) Qualitative and quantitative ultrastructural observations on retinal ganglion cell layer of rat after intraorbital optic nerve crush. J. Neurocytol. 15, 345-362.
6. 2+ and pH. Biochem. Biophys. Res. Commun. 186, 782-789.
7. 2+ concentration and DNA fragmentation. Cancer Res. 52, 1342-1346.
8. 2+ efflux mechanisms following depolarization evoked calcium transients in cultured rat sensory neurones. J. Physiol. 455, 567-583.
9. Berkelaar M., Clarke D. B., Wang Y.-C., Bray G. M. and Aguayo A. J. (1994) Axoytomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 14, 4368-4374.
10. 2+ levels in fish retinal ganglion cells. J. Neurophysiol. 72, 47-55.
11. Blaustein M. P., Ratzlaff R. W., Kendrick N. C. and Schweitzer E. S. (1978) Calcium buffering in presynaptic nerve terminals. I. Evidence for involvement of a nonmitochondrial ATP-dependent sequestration mechanism. J. Gen. Physiol. 72, 15-41.
12. Boje K. M. and Arora P. K. (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 587, 250-256.
13. Bowen I. D. Apoptosis or programmed cell death? (1993) Cell Biol. Interna. 17, 365-380.
14. Brake A. J., Wagenbach M. J. and Julius D. (1994) New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor. Nature 371, 519-523.
15. 2+ entry via AMPA/ KA receptors and excitotoxicity in cultured cerebellar Purkinje cells. J. Neurosci. 14, 187-197.
16. Bruckner G., Seeger G., Brauer K., Hartig W., Kacza J. and Bigl V. (1994) Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res. 658, 67-86.
17. Buisson A., Plotkine M. and Boulu R. G. (1992) The neuroprotective effect of nitric oxide in rat focal model of crebral ischemia. Br. J. Pharmac. 106, 766-767.
18. Buja L. M., Eigenbrodt M. L. and Eigenbrodt E. H. (1993) Apoptosis and necrosis. Basic types and mechanisms of cell death. Arch. Pathol. Lab. Med. 117, 1208-1214.
19. Bursch W., Oberhammer F. and Schulte-Hermann R. (1992) Cell death by apoptosis and its protective role against disease. Trends Physiol. Sci. (TIPS) 13, 245-251.
20. Cajal R.y (1928) Degeneration and Regeneration of the Nervous System, Vols I and II, repr. 1959. Hafner, New York.
21. Campbell G. , Leiberman A. R., Anderson P. N. and Turmaine M. (1992) Regeneration of adult rat CNS axons into peripheral nerve autografts: ultrastructural studies of the early stages of axonal sprouting and regenerative axonal growth. J. Neurocyto. 21, 755-787.
22. Caner H., Collins J. L., Harris S. M., Kassell N. F. and Lee K. S. (1993) Attenuation of AMPA-induced neurotoxicity by a calpain inhibitor. Brain Res. 607, 354-356.
23. Carafoli E. (1991) The calcium pumping ATPase of the plasma membrane. Ann. Rev. Physiol. 53, 531-547.
24. Carmignoto G., Maffei L., Candeo P., Canella R. and Comelli C. (1989) Effect of NGF on the survival of rat retinal ganglion cells following optic nerve section. J. Neurosci. 9, 1263-1272.
25. Cheng B. and Mattson M. P. (1994) NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res. 640, 56-67.
26. Choi D. W. (1992) Excitotoxic cell death. J. Neurobiol. 23, 1261-1276.
27. Clarke P. G. H. (1990) Developmental cell death: morphological divesity and multiple mechanisms. Anal. Embryol. 181, 195-213.
28. Collazo D., Takahashi H. and McKay R. D. (1992) Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9, 643-656.
29. Collins F., Schmidt M. F., Guthrie P. B. and Kater S. B. (1991) Sustained increase in intracellular calcium promotes neuronal survival. J. Neurosci. 11, 2582-2587.
30. Collins M. K., Perkins G. R., Rodriguez-Tarduchy G., Nieto M. A. and Lopez-Rivas A. (1994) Growth factors as survival factors: regulation of apoptosis. BioEssays 16, 133-138.
31. Crompton T. (1991) IL-3 dependent cells die by apoptosis on removal of their growth factor. Growth Factors 4, 109-116.
32. Csernansky C. A., Canzoniero L. M., Sensi S. L., Yu S. P. and Choi D. W. (1994) Delayed application of aurintricarboxylic acid reduces glutamate-induced cortical neuronal injury. J. Neurosci. Res, 38, 101-108.
33. Cui Q. and Harvey A. R. (1994) NT-4/5 reduces naturally occuring retinal ganglion cell death in neonatal rats. NeuroReport 5, 1882-1884.
34. Dawson V. L., Dawson T. M., Bartley D. A., Uhl G. R. and Snyder S. H. (1993) Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661.
35. Dawson V. L., Dawson T. M., London E. D., Bredt D. S. and Snyder S. H. (1991) Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88, 6368-6371.
36. Desoize B. and Sen S. (1992) L'apoptose ou mort cellulaire programmée: concepts, mechanismes et apports en cancerologie. Bull. Cancer 79, 413-425.
37. Desoize B. (1995) Apoptose et mort cellulaire programmée. Bull Cancer. 82, 70-76.
38. Dessi F., Charriaut-Marlangue C., Khrestchatisky M. and Ben-Ari Y. (1993) Glutamate-induced neuronal death is not a programmed cell death in cerebel-lar culture. J. Neurochem. 60, 1953-1955.
39. Diener P. S. and Bregman B. S. (1994) Neurotrophic factors prevent the death of CNS neurons after spinal cord lesions in newborn rats. NeuroReport 5, 1913-1917.
40. Ding A. H., Nathan C. F.. and Stuehr D. J. (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal mac-rophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141, 2407-2412.
41. Dragunow M., Belharz E., Sirimane E., Lawlor P., Williams C., Bravo R. and Gluckman P. (1994) Immediate-early gene protein expression in neurons undergoing delayed death but not necrosis, following hypoxic-ischaemic injury to the young rat brain. Mol. Brain Res. 25, 19-33.
42. Driscoll M. and Chalfie M. (1991) The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 349, 588-593.
43. +: Implications for neurode-generation. J. Neurochem. 63, 584-591.
44. Eastman A. and Barry M. A. (1992) The origins of DNA breaks: a consequence of DNA damage, DNA repair or apoptosis. Cancer Invest. 10, 229-240.
45. Eastman A., Barry M. A., Demarcq C., Li J. and Reynolds J. E. (1994) Endonucleases associated with apoptosis. In Apoptosis. (edited by Michich E. and Schimke R. T.). Plenum Press, New York, pp. 249-264.
46. Edwards S. N., Buckmaster A. E. and Tolkovsky A. M. (1991) The death programme in cultured sympathetic neurones can be suppressed at the post-translational level by nerve growth factor, cyclic AMP, and depolarization. J. Neurochem. 57, 2140-2143.
47. Eschweiler G. W. and Bahr M. (1993) Flunarizine enhances rat retinal ganglion cell survival after axotomy. J. Neurol. Sci. 116, 34-40.
48. Estus S., Zaks W. J., Freeman R. S., Gruda M., Bravo R. and Johnson E. M. (1994) Cultured gene expression in neurons during programmed cell death: identification of C-jun as necessary for neuronal apoptosis. J. Cell Biol. 127, 1717-1727.
49. Fawthrop D. J., Boobis A. R. and Davies D. S. (1991) Mechanisms of cell death. Arch. Toxicol. 65, 437-444.
50. Fernandes R. S. and Cotter T. G. (1994) Apoptosis or necrosis: intracellular levels of glutathione influence mode of cell death. Biochem. Pharmacol. 48, 675-681.
51. Ferrer I., Tortosa A., Blaco R., Martin F., Serrano T., Planas A. and Macaya A. (1994) Naturally occuring cell death in the developing cerebral cortex of the rat. Evidence of apoptosis-associated internucleosomal DNA fragmentation. Neurosci. Lett. 182, 77-79.
52. Flaccus A., Janetzko A., Tekotte R. K. and Margolis R. U. (1991) Immunocyto-chemical localisation of chondroitin 4- and 6-sulfates in developing rat cerebel-lum. J. Neurochem. 56, 1608-1615.
53. Frim D. M., Uhler T. A., Short M. P., Ezzedine Z. D., Klagsbrun M., Breakefield X. O. and Isacson O. (1993) Effects of biologically delivered NGF, BDNF and bFGF on striatal excitotoxic lesions. NeuroReport 4, 367-370.
54. Fukuda K., Kojiro M. and Chiu J. F. (1993) Demonstration of extensive chromatin cleavage in transplanted Morris hepatoma 7777 tissue: apoptosis or necrosis? Am. J. Pathol. 142, 935-946.
55. Galea E., Feinstein D. L. and Reis D. J. (1992) Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures. Proc. Nat. Acad. Sci. USA 89, 10945-10949.
56. Garcia-Valenzuela E., Gorczyca W., Darzynkiewicz Z. and Sharma S. C. (1994) Apoptosis in adult retinal ganglion cells after axotomy. J. Neurobiol. 25, 431-438.
57. Gerschenson L. E. and Rotello R. J. (1992) Apoptosis: a different type of cell death. FASEB J. 6, 2452-2455.
58. Glücksmann A. (1951) Cell death in normal vertebrate ontogeny. Biol. Rev. 26, 59-86.
59. Goldberg S. and Frank B. (1980) Will central nervous system axons in the adult mammal regenerate after bypassing a lesion? A study in the mouse and chick visual systems. Exp. Neuro. 70, 675-689.
60. Grotta J. (1993) Secular trends in stroke incidence and mortality. Stroke 24, 614.
61. Hall E. D. and Braughler J. M. (1989) Central nervous system trauma and stroke. II. Physiological and pharmacological evidence for involvement of oxygen radicals and lipid peroxidation. Free Rad. Biol. Med. 6, 303-313.
62. Hennig A., Krueger R., Mangoura D. and Schwartz N. B. (1992) Chondroitin sulfate proteoglycan expression during neuronal develoment. Cell Mol. Biol. 38, 585-593.
63. Henzi V. and MacDermott A. B. (1992) Characteristics and function of Ca(2+)- and inositoll,4,5-trisphosphate-releaseablestoresofCa2+ in neurons. Neuro-science 46, 251-273.
64. Hewett S. J., Csernansky C. A. and Choi D. W. (1994) Selective potentiation of NMDA-induced neuronal injury following induction of astrocytic iNOS. Neuron 13, 487-494.
65. Holmberg S. R., Cumming D. V., Kusama Y., Hearse D. J., Poole-Wilson P. A., Shattock M. J. and Williams A. J. (1991) Reactive oxygen species modify the structure and function of cardiac sarcoplasmic reticulum calcium-release channel. Cardioscience 2, 19-25.
66. Horsburgh G. M. and Sefton A. (1987) Cellular degeneration and synaptogenesis in the developing retina of the rat. J. Comp. Neurol. 263, 553-566.
67. Horvitz H. R., Ellis H. M. and Sternberg P. W. (1982) Programmed cell death in nematode development. Neurosc. Comment 1, 56-65.
68. Huxlin K. R., Carr R., Schulz M., Sefton A. and Bennett M. R. (1995a) Trophic effect of collicular proteoglycan on neonatal rat retinal ganglion cells in situ. Dev. Brain Res. 84, 77-88.
69. Huxlin K. R., Dreher B., Schulz M., Jervie Sefton A. and Bennett M. R. (1995b) Effect of collicular proteoglycan on the survival of adult rat retinal ganglion cells following axotomy. Eur. J. Neurosci. 7, 96-107.
70. Huxlin K. R., Sefton A. J., Schulz M. and Bennett M. R. (1993) Effect of proteoglycan purified from rat superior colliculus on the survival of murine retinal ganglion cells. Dev. Brain Res. 74, 207-217.
71. Iacopino A., Christakos S., German D., Sonsalla P. K. and Altar C. A. (1992) Calbindin-D28K-containing neurons in animal models of neurodegeneration: possible protection from excitotoxicity. Mol Brain Res. 13, 251-261.
72. Ilschner S. U. and Waring P. (1992) Fragmentation of DNA in the retina of chicken embryos coincides with retinal ganglion cell death. Biochem. Biophys. Res. Commun. 183, 1056-1061.
73. Inouye M., Tamaru M. and Kameyama Y. (1992) Effects of cycloheximide and actinomycin D on radiation-induced apoptotic cell death in the developing mouse cerebellum. Int. J. Rad. Biol. 61, 669-674.
74. Izumi Y., Benz A. M., Clifford D. B. and Zorumski C. F. (1992) Nitric oxide inhibitors attenuate N-methyl-D-aspartate excitotoxicity in rat hippocampal slices. Neurosci. Lett. 135, 227-230.
75. Jacobson M. (1991) Developmental Neurobiology. Plenum Press, New York, pp. 311-368.
76. Jacobson M. D., Burne J. F., King M. P., Miyashita T., Redd J. C. and Raff M. C. (1993) Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature 361, 365-369.
77. Jensen L. M., Zhang Y. and Shooter E. M. (1992) Steady state polypeptide modulations associated with nerve growth factor (NGF)-induced terminal differentiation and NGF deprivation-induced apoptosis in human neuro-blastoma cells. J. Biol. Chem. 267, 19325-19333.
78. 2+-ATPaSe inhibitor thapsigargin. Exp. Cell Res. 212, 84-92.
79. Johnson E. M., Koike T. and Franklin J. (1992) A "calcium set-point hypothesis" of neuronal dependence on neurotrophic factor. Exp. Neurol. 115, 163-166.
80. Johnson S. H., Kraimer J. M. and Graeber G. M. (1993) Effects of flunarizine on neurological recovery and spinal cord blood flow in experimental spinal cord ischemia in rabbits. Stroke 24, 1547-1553.
81. Kannan Y., Usami K., Okada M., Shimizu S. and Matsuda H. (1992) Nerve growth factor suppresses apoptosis of murine neutrophils. Biochem. Biochem. Biophys. Res. Commun. 186, 1050-1056.
82. Kerr J. F. R., Wyllie A. H. and Currie A. R. (1972) Apoptosis: a basic biological phenomenon with wide ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
83. Kilbourn R. G. and Belloni P. (1990) Endothelial cell production of nitrogen oxides in response to interferon gamma in combination with tumor necrosis factor, interleukin-1, or endotoxin. J. Natl. Cancer Inst. 82, 726-728.
84. Koch R. A. and Barish M. E. (1994) Perturbation of intracellular calcium and hydrogen ion regulation in cultured mouse hippocampal neurons by reduction of the sodium ion concentration gradient. J. Neurosci. 14, 2585-2593.
85. Kocsis J.D., R and M.N., Chen B., Waxsman S.G. and Pourcho R.(1993) Kainate elicits elevated nuclear calcium signals in retinal neurons via calcium-induced calcium release. Brain Res. 616, 273-282.
86. Koh J. Y. and Cotman C. W. (1992) Programmed cell death: its possible contribution to neurotoxicity mediated by calcium channel antagonists. Brain Res. 587, 233-240.
87. 2+ determine nerve growth factor dependence of sympathetic ganglion cells. Proc. Natl. Acad. Sci. USA 86, 6421-6425.
88. Kolleger H., McBean G. J. and Tipton K. F. (1993) Reduction of striatal N-methyl-D-aspartate toxicity by inhibition of NO synthesis. Biochem. Pharmac. 45, 260-264.
89. Korsmeyer S. J., Shutter J. R., Veis D. J., Merry D. E. and Oltvai Z. N. (1993) Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin. Cancer Biol. 4, 327-332.
90. Kowarski D., Shuman H., Somlyo A. P. and Somlyo A. V. (1985) Calcium release by noradrenaline from central sarcoplasmic reticulum in rabbit main pulmonary artery. J. Physiol. 366, 153-175.
91. Kozak A., Nikodijevic B., Yavin E. and Guroff G. (1992) Intracellular calcium levels regulate the actions of nerve growth factor on calcium uptake in PC 12 cells. J. Neurosci. Res. 33, 30-36.
92. Kressel M. and Groscurth P. (1994) Distinction of apoptotic and necrotic cell death by in situ labelling of fragmented DNA. Cell Tiss. Res. 278, 549-556.
93. Leber S. M., Breedlove S. M. and Sanes J. R. (1990) Lineage arrangement and death of clonally related motorneurons in chick spinal cord. J. Neurosci. 10, 2451-2462.
94. Leybaert L. and De Ley G. (1994) Intersitial and tissue cations and electrical potential after experimental spinal cord injury. Exp. Brain Res. 100, 369-375.
95. Lieberman A. R. (1974) Some factors affecting retrograde neuronal responses to axonal lesions. In Essays on the Nervous System. (Edited by Bellairs, R and Gray, E. G.), Clarendon Press, Oxford, pp. 71-105.
96. Linnik M. D., Zobrist R. H. and Hatfield M. D. (1993) Evidence supporting a role for programmed cell death in focal cerebral ischaemia in rats. Stroke 24, 2002-2008.
97. Lipton S. A., Choi Y. B., Pan Z. H., Lei S. Z., Chen H. S., Sucher N. J., Loscalzo J., Singel D. J. and Stamler J. S. (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364, 626-632.
98. Lobner D. and Lipton P. (1993) Intracellular calcium levels and calcium fluxes in the CA1 region of the rat hippocampal slice during in vitro ischemia: relationship to electrophysiological cell damage. J. Neurosci. 13, 4861-4871.
99. Lowenstein D. H., Chan P. H. and Miles M. F. (1991) The stress protein response in cultured neurons: characterization and evidence for a protective role in excitotoxicity. Neuron 7, 1053-1060.
100. Lytton J., Westlin M. and Hanley M. R. (1991) Thapsigargininhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266, 17067-17071.
101. Maiese K., Boniece I. R., Skurat K. and Wagner J. A. (1993a) Protein kinases modulate the sensitivity of hippocampal neurons to nitric oxide toxicity and anoxia. J. Neurosci. Res. 36, 77-87.
102. Maiese K., Boniece I., DeMeo D. and Wagner J. A. (1993b) Peptide growth factors protect against ischemia in culture by preventing nitric oxide toxicity. J. Neurosci. 13, 3034-3040.
103. Mansour-Robaey S., Clarke D. B., Wang Y.-C., Bray, G. M. and Aguayo, A. J. (1994) Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomised retinal ganglion cells. Proc. Natl. Acad. Sci. USA 91, 1632-1636.
104. Martin D. P.,Schmidt R. E., Distefano P. S., Lowry O. H., Carter J. G. and Johnson E. M. (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106, 829-844.
105. Mattson M. P., Cheng B. and Smith-Swintosky V. L. (1993) Neurotrophic factor-mediated protection from excitotoxicity and disturbances in calcium and free-radical metabolism. Semin. Neurosci. 5, 295-307.
106. Mattson M. P., Rychlik B., Chu C. and Christakos S. (1991) Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28K in cultured hippocampal neurons. Neuron 6, 41-51.
107. Meredith J. E., Fazeli B. and Schwartz M. A. (1993) The extracellular matrix as a cell survival factor. Mol. Biol. Cell 4, 953-961.
108. Mey J. and Thanos S. (1993) Intravitreal injections of neurotrophic factors support the survival of axotomised retinal ganglion cells in adult rats in vivo. Brain Res. 620, 304-317.
109. Michel P. P., Vyas S., Anglade P., Ruberg M. and Agid Y. (1994) Morphological and molecular characterisation of the response of differentiated PC12 cells to calcium stress. Eur. J. Neurosci. 6, 577-586.
110. Miller R. J. (1991) The control of neuronal Ca2+ homeostasis. Prog. Neurobiol. 37, 255-285.
111. Mitchell I. J., Lawson S., Moser B., Laidlaw S. M., Cooper A. J., Walkinshaw G. and Waters C. M. (1994) Glutamate-induced apoptosis results in a loss of striatal neurons in the parkinsonian rat. Neurosci. 63, 1-5.
112. Nagafuji T., Matsui T., Koide T. and Asano T. (1992) Blockade of nitric oxide formation by N-omega-nitro-L-arginine mitigates ischemic brain edema and subsequent cerebral infarction in rats. Neurosci. Lett. 147, 159-162.
113. Nichol K. A., Everett A. W., Schulz M. and Bennett M. R. (1994) Retinal ganglion cell survival in vitro maintained by a chondroitin sulfate proteoglycan from the superior colliculus carrying the HNK-1 epitope. J. Neurosci. Res. 37, 623-632.
114. Nikodijevic B. and Guroff G. (1992) Nerve growth factor-stimulated calcium uptake into PC12 cells: uniqueness of the channel and evidence for phophorylation. J. Neurosci. Res. 31, 591-599.
115. Nomura Y. and Kitomura Y. (1993) Inducible nitric oxide synthase in glial cells. Neurosci. Res. 18, 103-107.
116. Nowicki J. P., Duval D., Poignet H. and Scatton B. (1992) Nitric oxode mediates neuronal death after focal ischemia in the mouse. Eur. J. Pharmac. 204, 339-340.
117. Nozaki K., Finkelstein S. P. and Beal M. F. (1993) Delayed administration of basic fibroblast growth factor protects against N-methyl-D-asparate neurotoxicity in neonatal rats. Eur. J. Pharmac. 232, 295-297.
118. O'Malley D. M. (1994) Calcium permeability of the neuronal nuclear envelope: evaluation using confocal volumes and intracellular perfusion. J. Neurosci. 14, 5741-5758.
119. Oohira A., Matsui F., Matsuda M., Takida Y. and Kuboki Y. (1989) Occurrence of three distinct molecular species of chondroitin sulfate proteoglycan in the developing rat brain. J. Biol. Chem. 263, 10240-10246.
120. Oppenheim R. W. (1991) Cell death during development of the nervous system. Ann. Rev. Neurosci. 14, 453-501.
121. Oppenheim R. W., Prevette D., Tytell M. and Homma S. (1990) Naturally occuring 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.
122. Owens G. P., Hahn W. E. and Cohen J. J. (1991) Identification of mRNAs associated with programmed cell death in immature thymocytes. Mol Cell. Biol. 11, 4177-4188.
123. Parducz A., Toldi J., Joo F., Siklos L. and Wolff J. R. (1987) Transient increase of calcium in pre- and postsynaptic organelles of rat superior cervical ganglion after tetanizing stimulation. Neuroscience 23, 1057-1061.
124. Penfold P. L. and Provis J. M. (1986) Cell death in the development of the human retina: phagocytosis of pyknotic and apoptotic bodies by retinal cells. Graefe's Arch. Clin. Exp. Ophtalmol. 224, 549-553.
125. Peunova N. and Enikolopov G. (1995) Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375, 68-73.
126. Politis M. J. and Miller J. E. (1985) Induction of CNS regeneration by localised exogenous tropic factor and systemic mitotic inhibitor administration. J. Neuropathol. Exp. Neurol. 44, 354.
127. Pollard H., Charriautmarlangue C., Cantagrel S. Represa A., Robain O., Moreau J. and Benari Y. (1994) Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience 63, 7-18.
128. Prehn J. H., Backhauss C. and Krieglstein J. (1993a) Transforming growth factor-beta 1 prevents glutamate neurotoxicity in rat neocortical cultures and protects mouse neocortex from ischemic injury in vivo. J. Cereb. Blood Flow Met. 13, 521-525.
129. Prehn J. H., Peruche B., Unsicker K. and Krieglstein J. (1993b) Isoform-specific effects of transforming growth factors-beta on degeneration of primary neuronal cultures induced by cytotoxic hypoxia or glutamate. J. Neurochem. 60, 1665-1672.
130. Rabacchi S. A., Ensini M., Bonfanti L., Gravina A. and Maffei L. (1994) Nerve growth factor reduces apoptosis of axotomised retinal ganglion cells in the neonatal rat. Neurosci. 63, 969-973.
131. Radomski M. W., Palmer R. M. and Moncada S. (1990) Glucocorticoids inhibit the expression of an inducible, but not the constitutive, nitric oxide synthase in vascular endothelial cells. Proc. Nat. Acad. Sci. USA 87, 10043-10047.
132. ++ -endonuclease and poly(ADP-ribose) polymerase inhibitors in mice. J. Pharmac. Exp. Ther. 263, 387-394.
133. Richardson P. M., Issa V. M. K. and Schemie S. (1982) Regeneration and retrograde degeneration of axons in the rat optic nerve. J. Neurocytol. 11, 949-966.
134. 2+: their relationship to apoptosis and oncogenesis. FEBS Lett. 325, 104-107.
135. Robert-Lewis J. M., Marcy V. R., Zhao Y., Vaught J. L., Siman R. and Lewis M. E. (1993) Aurintricarboxylic acid protects hippocampal neurons from NMDA- and ischaemia-induced toxicity in vivo. J. Neurochem. 61, 378-381.
136. Robert-Lewis J. M., Savage M. J., Marcy V. R., Pinsker L. R. and Siman R. (1994) Immunolocalisation of calpain I-mediated spectrin degradation to vulnerable neurons in ischemic gerbil brain. J. Neurosci. 14, 3934-3944.
137. Rogers L. M. and Dani J. A (1995) Comparison of quantitative calcium flux through NMDA, ATP, and ACh receptor channels. Biophys. J. 68, 501-506.
138. Ruoslahti E. (1988) Structure and biology of proteoglycans. Ann. Rev. Biol. 4, 229-255.
139. Samples S. D. and Dubinsky J. M. (1993) Aurintricarboxylic acid protects hippocampal neurons from glutamate excitotoxicity in vitro. J. Neurochem. 61, 382-385.
140. Sanchez-Armass S. and Blaustein M. P. (1987) Role of sodium-calcium exchange in regulation of intracellular calcium in nerve terminals. Am. J. Physiol. 252, 595-603.
141. 2+ homeostasis in rat sympathetic ganglion cells. Eur. J. Neuroci. 6, 9-17.
142. Sarafian T. A. and Bredesen D. E. (1994) Is apoptosis mediated by reactive oxygen species? Free Radical Res. 21, 1-8.
143. + exchange and its inhibition in cardiac ischaemia and reperfusion. Basic Res. Cardiol. 88, 443-455.
144. Schreiber S. S., Tocco G., Najam I., Thompson R. F. and Baudry M. (1993) Cycloheximide prevents kainate-induced neuronal death and C-Fos expression in adult rat brain. J. Mol. Neurosci. 4, 149-159.
145. Schulz M., Raju T., Ralston G and Bennett M. R. (1990) A retinal ganglion cell neurotrophic factor purified from the superior colliculus. J. Neurochem. 55, 832-834.
146. Schulze-Osthoff K., Walczak H., Droge W. and Krammer P. H. (1994) Cell nucleus and DNA fragmentation are not required for apoptosis. J. Cell Biol. 127, 15-20.
147. Schumacher J. M., Short M. P., Hyman B. T., Breakefield X. O. and Isacson O. (1991) Intracerebral implantation of nerve growth factor-producing fibroblasts protects striatum against neurotoxic levels of excitatory amino acids. Neuroscience 45, 561-570.
148. Schweichel J. U. and Merker H. J. (1973) The morphology of various types of cell death in prenatal tissues. Teratology 7, 253-266.
149. Sen S. (1992) Programmed cell death: concept, mechanism and control. Biol. Rev. Cambridge Phil. Soc. 67, 287-319.
150. Shaposhnikova V. V., Dobrovinskaya O. R., Eidus L. K. H. and Korystov Y. N. (1994) Dependence of thymocyte apoptosis on protein kinase C and phospholipase A2. FEBS Lett. 348, 317-319.
151. Sheardown M. J., Nielsen E. O., Hansen A. J., Jacobsen P. and Honore T. (1990) 2, 3-Dihydroxy-6-nitro-7-sulfamoly-benzo(F) quinoxaline: a neuroprotectant for cerebral ischaemia. Science 247, 571-574.
152. 2+ accumulation and early DNA fragmentation with cell death. Toxicol. Appl. Pharmac. 111, 242-254.
153. 2+-endonucleases, DNA repair and glutathione depletion inhibitors on DNA fragmentation and cell death. Toxicol. Appl. Pharmacol. 112, 32-40.
154. Shigeno T., Yamasaki Y., Kato G., Kusaka K., Mima T., Takakura K., Graham D. I. and Furukawa S. (1990) Reduction of delayed neuronal death by inhibition of protein synthesis. Neurosci. Lett. 120, 117-119.
155. Siesjo B. K., Agardh C. D. and Bengtsson F. (1989) Free radicals and brain damage. Cerebrovasc. Brain Metab. Rev. 1, 165-211.
156. Sievers J., Hausmann B. and Berry M. (1987) Fibroblast growth factor promotes the survival of adult rat ganglion cells after transection of the optic nerve. Neurosci. Lett. 76, 157-162.
157. Simmons M. L. and Murphy S. (1992) Induction of nitric oxide synthase in glial cells. J. Neurochem. 59, 897-905.
158. Simon R. P., Griffiths T., Evans M. D., Swan J. H. and Meldrum B. S. (1984a) Calcium overload in selectively vulnerable neurons of the hippocampus during and after ischaemia: an electron microscopy study in the rat. J. Cereb. Blood Flow Metab. 4, 350-361.
159. Simon R. P., Swan J. H., Griffiths T. and Meldrum B. S. (1984b) Blockade of N-methyl-D-aspartate receptors may protect against ischaemic damage in the brain. Science 226, 850-852.
160. Snow D. M., Atkinson P. B., Hassinger T. D., Letourneau P. C. and Kater S. B. (1994) Chondroitin sulfate proteoglycan elevates cytoplasmic calcium in DRG neurons. Dev. Biol. 166, 87-100.
161. Snow D. M., Lemmon V., Carrino D. A., Caplan A. I. and Silver J. (1990) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 109, 111-130.
162. Snow D. M., Watanabe M., Letourneau P. C. and Silver J. (1991) A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development 113, 1473-1485.
163. Snyder S. H. (1992) Nitric oxide: first in a new class of neurotransmitters. Science 257, 494-496.
164. Squier M. K., Miller A. C., Malkinson A. M. and Cohen I. J. (1994) Calpain activation in apoptosis. J. Cell Physiol. 159, 229-137.
165. Stamler J. S., Singel D. J. and Loscalzo J. (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258, 1898-1902.
166. Stehno-Bittel L., Luckhoff A. and Clapham D. E. (1995) Calcium-release from the nucleus by InsP3 receptor channels. Neuron. 14, 163-167.
167. Steindler D. A., O'Brien T. F., Laywell E., Harrington K., Faissner A. (1990) and Schachner M., Boundaries during normal and abnormal brain development in vivo and in vitro studies of glia and glycoconjugates. Exp. Neural. 109, 35-56.
168. Stevenson J. A. (1985) Growth of optic tract axons in nerve grafts in hamsters. Exp. Neurol. 87, 446-457.
169. Steuhr D. J. and Marietta M. A. (1985) Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc. Nat. Acad. Sci. USA 82, 7738-7742.
170. + conductance in rat optic nerve axons. Proc. Natl. Acad. Sci. USA 90, 6976-6980.
171. Takahashi K., Lam T. T., Edward D. P., Buchi E. R. and Tso M. O. (1992) Protective effects of flunarizine on ischaemic injury in the rat retina. Arch. Ophtalmol. 110, 862-870.
172. Tamura Y., Sato Y., Akaike A. and Shiomi H. (1992) Mechanisms of cholecystokinin-induced protection of cultured neurons agains N-methyl-D-aspartate receptor-mediated glutamate neurotoxicity. Brain Res. 592, 317-325.
173. Tanaka S. and Koike T. (1995) Up-regulation of L-type calcium channels associated with the development of elevated potassium-mediated survival of superior cervical ganglion cells in vitro. Develop. Biol. 168, 166-178.
174. Tepper C. G. and Studzinski G. P. (1993) Resistance of mitochondrial DNA to degradation characterises the apoptotic but not necrotic mode of human leukemia cell death. J. Cellular Biochem. 52, 352-361.
175. Thayer S. A. and Miller R. J. (1990) Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurones in vitro. J. Physiol. 425, 85-115.
176. Threlkeld A., Adler R. and Hewitt A. T. (1989) Proteoglycan biosynthesis by chick embryo retina glial-like cells. Dev. Biol. 132, 559-568.
177. G-nitro-L-arginine in focal stroke in the 7 day old rat. Eur. J. Pharmac. 218, 197-198.
178. 2+ chelators. J. Cereb. Blood Flow Met. 14, 911-923.
179. Tymiansky M., Charlton M. P., Carlen P. L. and Tator C. H. (1993) Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J. Neurosci. 13, 2085-2104.
180. 2+ chelators reduce early excitotoxic and ischaemic neuronal injury in vitro and in vivo. Neuron 11, 221-235.
181. Uematsu D., Greenberg J. H., Hickey W. F. and Reivich M. (1989) Nimodipine attenuates both increase in cytosolic free calcium and histologic damage following focal cerebral ischaemia and reperfusion in cats. Stroke 20, 1531-1537.
182. Valentino K., Newcomb R., Gadbois T., Singh T., Bowersox S., Bitner S., Justice A., Yamashiro D., Hoffman B. B. and Ciaranello R. (1993) A selective N-type calcium channel antagonist protects against neuronal loss after global cerebral ischaemia. Proc. Natl. Acad. Sci. USA 90, 7894-7897.
183. Valera S., Hussy N., Evans R. J., Adami N., North R. A., Suprenant A. and Buell G. (1994) A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP. Nature 371, 516-519.
184. Vayssiere J. L., Petit P. X., Risler Y. and Mignotte B. (1994) Committment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalised with simian virus 40. Proc Natl. Acad. Sci. USA 91, 11752-11756.
185. Verma A., Hirsch D. J., Hanley M. R., Thastrup O., Christensen S. B. and Snyder S. H. (1990) Inositol trisphosphate and thapsigargin discriminate endoplasmic reticulum stores of calcium in rat brain. Biochem. Biophys. Res. Commun. 172, 811-816.
186. Villegas-Perez M. P., Vidal-Sanz M., Bray G. M. and Aguayo A. J. (1989) Influences of peripheral nerve grafts on the survival and regrowth of axotomised retinal ganglion cells in adult rats. J Neurosci. 8, 265-280.
187. Villegas-Perez M. P., Vidal-Sanz M., Rasminsky M., Bray G. M. and Aguayo A. J. (1993) Rapid and protracted phases of retinal ganglion cell loss following axotomy in the optic nerve of adult rats. J. Neumbiol 24, 23-36.
188. Waters C. M., Moser W., Walkinshaw G. and Mitchell I. J. (1994) Death of neurons in the neonatal rodent and primate globus pallidus occurs by a mechanism of apoptosis. Neuroscience 6, 881-894.
189. Weaver V. M., Lach B., Walker P. R. and Sikorska M. (1993) Role of proteolysis in apoptosis: involvement of serine proteases in internucleosomal DNA fragmentation in immature thymocytes. Biochem. Cell Biol. 71, 488-500.
190. Werth J. L. and Thayer S. A. (1994) Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons. J. Neurosci. 14, 348-356.
191. Wolvetang E. J., Johnson K. L., Krauer K., Ralph S. J. and Linnane A. W. (1994) Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett. 339, 40-44.
192. Wyllie A. H. (1987) Apoptosis: cell death in tissue regulation. J. Pathol. 153, 313-316.
193. Wyllie A. H. (1980) Glucocortocoid-induced thymocyte apoptosis associated with endogenous endonuclease activation. Nature 284, 555-556.
194. Xie Q-W., Cho H. J., Calaycay J., Mumford R. A., Swidereck K. M., Lee T. D., Ding A., Trosco T. and Nathan C. (1992) Cloning and characterisation of inducible nitric oxide synthase from mouse macrophages. Science 256, 225-228.
195. Yamashita A. and Kawana A. (1991) Nerve growth factor-induced intracellular calcium ion release in chick dorsal root ganglion neurons. Neurosci. Lett. 128, 147-149.
196. Zheng L. M., Zychlinsky A., Liu C. C., Ojcius D. M. and Young J. D. (1991) Extracellular ATP as a trigger for apoptosis or programmed cell death. J. Cell Biol. 112, 279-288.
197. 2+ and endonuclease activation in radiation-induced lymphoid cell death. Exp. Cell Res. 207, 163-170.