'Apoptotic' biochemical cascades in synaptic compartments: Roles in adaptive plasticity and neurodegenerative disorders

Journal of Neuroscience Research

Volumn 58, Issue 1, 1999, Pages 152-166

  Mattson, Mark P ^a,b   Duan, Wenzhen ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer's disease; Caspase; Dendritic spines; Glutamate; Mitochondrial transmembrane potential; Oxidative stress; Staurosporine; Synaptosomes

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BASIC FIBROBLAST GROWTH FACTOR; CALCIUM; CASPASE; CYTOKINE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; NEUROTROPHIC FACTOR; STAUROSPORINE; TUMOR NECROSIS FACTOR ALPHA;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; CHROMATIN CONDENSATION; DENDRITIC SPINE; ENZYME ACTIVATION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NERVE CELL PLASTICITY; NERVE DEGENERATION; OXIDATIVE STRESS; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; SYNAPTOSOME;

ANIMALS; APOPTOSIS; BRAIN; HUMANS; MODELS, NEUROLOGICAL; NEURODEGENERATIVE DISEASES; NEURONAL PLASTICITY; NEURONS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 0033215252     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19991001)58:1<152::AID-JNR15>3.0.CO;2-V     Document Type: Article

References (124)

1. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P. 1995. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
2. Bailey CH, Chen M. 1991. Morphological aspects of synaptic plasticity in Aplysia. An anatomical substrate for long-term memory. Ann NY Acad Sci 627:181-196.
3. Barger SW, Mattson MP. 1996. Induction of neuroprotective κB-dependent transcription by secreted forms of the Alzheimer's β-amyloid precursor. Mol Brain Res 40:116-126.
4. 2+ accumulation. Proc Natl Acad Sci USA 92:9328-9332.
5. Barnes NY, Li L, Yoshikawa K, Schwartz LM, Oppenheim RW, Milligan CE. 1998. Increased production of amyloid precursor protein provides a substrate for caspase-3 in dying motoneurons. J Neurosci 18:5869-5880.
6. Beal MF. 1998. Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta 1366:211-223.
7. Begley JG, Duan W, Duff K, Mattson MP. 1999. Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice. J Neurochem 72: 1030-1039.
8. Blanc EM, Keller JN, Fernandez S, Mattson MP. 1998. 4-Hydroxynonenal, a lipid peroxidation product, inhibits glutamate transport in asttocytes. Glia 22:149-160.
9. Bredesen DE. 1995. Neural apoptosis. Ann Neurol 38:839-851.
10. Bruce AJ, Boling W, Kindy MS, Peschon J, Kraemer PJ, Carpenter MK, Holtsberg FW, Mattson MP. 1996. Altered neuronal and microglial responses to brain injury in mice lacking TNF receptors. Nature Med 2:788-794.
11. Bruce-Keller AJ, Begley JG, Fu W, Butterfield DA, Bredesen DE, Hutchins JB, Hensley K, Mattson MP. 1997. Bcl-2 protects isolated plasma and mitochondrial membranes against lipid peroxidation induced by hydrogen peroxide and amyloid β-peptide. J Neurochem 70:31-39.
12. Brune B, von Knethen A, Sandau KB. 1998. Nitric oxide and its role in apoptosis. Eur J Pharmacol 351:261-272.
13. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P. 1998. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94:727-737.
14. Chan SL, Griffin WST, Mattson MP. 1999a. Evidence for caspasemediated cleavage of AMPA receptor subunits in neuronal apoptosis and in Alzheimer's disease. J Neurosci Res. (in press).
15. Chan SL, Tammariello SP, Estus S, Mattson MP. 1999b. Involvement of Par-4 in trophic factor withdrawal-induced apoptosis of hippocampal neurons: actions prior to mitochondrial dysfunction and caspase activation. J Neurochem (in press).
16. Cheng B, Mattson MP. 1991. NGF and bFGF protect rat and human central neurons against hypoglycemic damage by stabilizing calcium homeostasis. Neuron 7:1031-1041.
17. Cheng B, Christakos S, Mattson MP. 1994. Tumor necrosis factors protect neurons against excitotoxic/metabolic insults and promote maintenance of calcium homeostasis. Neuron 12:139-153.
18. Cheng EH, Kirsch DG, Clem RJ, Ravi R, Kastan MB, Bedi A, Ueno K, Hardwick JM. 1997. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278:1966-1968.
19. Choi DW. 1994. Calcium and excitotoxic neuronal injury. Ann NY Acad Sci 747:162-171.
20. Cryns VL, Bergeron L, Zhu H, Li H, Yuan J. 1996. Specific cleavage of alpha-fodrin during Fas-and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1 beta-converting enzyme/Ced-3 protease distinct from the poly(ADP-ribose) polymerase protease. J Biol Chem 271:31277-31282.
21. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. 1997a. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
22. Datta R, Kojima H, Yoshida K, Kufe D. 1997b. Caspase-3-mediated cleavage of protein kinase C theta in induction of apoptosis. J Biol Chem 272:20317-20320.
23. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM Jr, Snider WD, Korsmeyer SJ. 1996. BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
24. Deshmukh M, Johnson EM. 1997. Programmed cell death in neurons: focus on the pathway of nerve growth factor deprivation-induced death of sympathetic neurons. Mol Pharmacol 51:897-906.
25. Dodel RC, Du Y, Bales KR, Ling Z, Carvey PM, Paul SM. 1999. Caspase-3-like proteases and 6-hydroxydopamine induced neuronal cell death. Mol Brain Res 64:141-148.
26. Duan W, Mattson MP. 1999. Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson's disease. J Neurosci Res 57:195-206.
27. Duan W, Gash DM, Rangnekar V, Mattson MP. 1999a. Participation of Par-4 in degeneration of dopaminergic neurons in primate and rodent models of Parkinson's disease. Ann Neurol (in press).
28. Duan W, Rangnekar V, Mattson MP. 1999b. Par-4 production in synaptic compartments following apoptotic and excitotoxic insults: evidence for a pivotal role in mitochondrial dysfunction and neuronal degeneration. J Neurochem 72:2312-2322.
29. Finch EA, Augustine GJ. 1998. Local calcium signaling by inositol1,4,5-triphosphate in Purkinje cell dendrites. Nature 396:753-756.
30. Fulda S, Scaffidi C, Susin SA, Krammer PH, Kroemer G, Peter ME, Debatin KM. 1998. Activation of mitochondria and release of mitochondrial apoptogenic factors by betulinic acid. J Biol Chem 273:33942-33948.
31. Furukawa K, Mattson MP. 1998. The transcription factor NF-κB mediates increases in calcium currents and decreases in NMDA and AMPA/kainate-induced currents in response to TNFα in hippocampal neurons. J Neurochem 70:1876-1886.
32. i?. Exp Neurol 133:153-163.
33. + channels and suppression of neuronal activity by secreted β-amyloid precursor protein. Nature 379:74-78.
34. Furukawa K, Sopher BL, Rydel RE, Begley JG, Martin GM, Mattson MP. 1996b. Increased activity-regulating and neuroprotective efficacy of α-secretase-derived secreted APP is conferred by a C-terminal heparin-binding domain. J Neurochem 67:1882-1896.
35. Furukawa K, Estus S, Fu W, Mattson MP. 1997a. Neuroprotective action of cycloheximide involves induction of Bcl-2 and antioxidant pathways. J Cell Biol 136:1137-1150.
36. Furukawa K, Fu W, Witke W, Kwiatkowski DJ, Mattson MP. 1997b. The actin-severing protein gelsolin modulates calcium channel and NMDA receptor activities and vulnerability to excitotoxicity in hippocampal neurons. J Neurosci 17:8178-8186.
37. Greenlund LJ, Deckwerth TL, Johnson EM. 1995. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 14:303-315.
38. Gross A, Jockel J, Wei MC, Korsmeyer SJ. 1998. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 17:3878-3885.
39. Guo ZH, Mattson MP. 1999. Neurotrophic factors protect cortical synaptic termials against amyloid-and oxidative stress-induced impairment of glucose transport, glutamate transport and mitochondrial function. Cereb Cortex (in press).
40. Guo Q, Furukawa K, Sopher BL, Pham DG, Robinson N, Martin GM, Mattson MP. 1996, Alzheimer's PS-1 mutation perturbs calcium homeostasis and sensitizes PC12 cells to death induced by amyloid β-peptide. NeuroReport 8:379-383.
41. Guo Q, Sopher BL, Pham DG, Furukawa K, Robinson N, Martin GM, Mattson MP. 1997. Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid β-peptide: involvement of calcium and oxyradicals. J Neurosci 17:4212-4222.
42. Guo Q, Fu W, Xie J, Luo H, Sells SF, Geddes JW, Bondada V, Rangnekar V, Mattson MP. 1998a. Par-4 is a novel mediator of neuronal degeneration associated with the pathogenesis of Alzheimer's disease. Nature Med 4:957-962.
43. Guo Q, Robinson N, Mattson MP. 1998b. Secreted APPα counteracts the pro-apoptotic action of mutant presenilin-1 by activation of NF-κB and stabilization of calcium homeostasis. J Biol Chem 273:12341-12351.
44. Guo Q, Fu W, Sopher BL, Miller MW, Ware CB, Martin GM, Mattson MP. 1999a. Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knockin mice. Nature Med 5:101-107.
45. Guo Q, Sebastian L, Sopher BL, Miller MW, Ware CB, Martin GM, Mattson MP. 19996. Increased vulnerability of hippocampal neurons from presenilin-1 mutant knock-in mice to amyloid β-peptide toxicity: central roles of superoxide production and caspase activation. J Neurochem 72:1019-1029.
46. Hockenbery D, Oltvai ZN, Yin XM, Milliman CL, Korsraeyer SH. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-251.
47. Ishida A, Furukawa K, Keller JN, Mattson MP. 1997. Secreted form of β-amyloid precursor protein shifts the frequency dependence for induction of LTD, and enhances LTP in hippocampal slices. NeuroReport 8:2133-2137.
48. Jenner P, Olanow CW. 1998. Understanding cell death in Parkinson's disease. Ann Neurol 44:S72-S84.
49. Jessell TM, Kandel ER. 1993. Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Neuron 10:1-31.
50. Johnson EM Jr, Deckwerth TL. 1993. Molecular mechanisms of developmental neuronal death. Annu Rev Neurosci 16:31-46.
51. Johnson MD, Xiang H, London S, Kinoshita Y, Knudson M, Mayberg M, Korsmeyer SJ, Morrison RS. 1998. Evidence for involvement of Bax and p53, but not caspases, in radiation-induced cell death of cultured postnatal hippocampal neurons. J Neurosci Res 54:721-733.
52. Jones TA, Klintsova AY, Kilman VL, Sirevaag AM, Greenough WT. 1997. Induction of multiple synapses by experience in the visual cortex of adult rats. Neurobiol Learn Mem 68:13-20.
53. Kayalar C, Ord T, Testa MP, Zhong LT, Bredesen DE. 1996. Cleavage of actin by interleukin 1 β-converting enzyme to reverse DNase I inhibition. Proc Natl Acad Sci USA 93:2234-2238.
54. Kelckar A, Thompson CV. 1998. Bcl-2 family proteins: the role of the BH3 domain in apoptosis. Trends Cell Biol 8:324-330.
55. Keller JN, Pang Z, Geddes JW, Begley JG, Germeyer A, Waeg G, Mattson MP. 1997. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J Neurochem 69:273-284.
56. Keller JN, Guo Q, Holtsberg FW, Bruce-Keller AJ, Mattson MP. 1998a. Increased sensitivity to mitochondrial toxin-induced apoptosis in neural cells expressing mutant presenilin-1 is linked to perturbed calcium homeostasis and enhanced oxyradical production. J Neurosci 18:4439-4450.
57. Keller JN, Kindy MS, Holtsberg FW, St Clair DK, Yen HC, Germeyer A, Steiner SM, Bruce-Keller AJ, Hutchins JB, Mattson MP. 1998b. Mitochondrial MnSOD prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation and mitochondrial dysfunction. J Neurosci 18:687-697.
58. Kim TW, Pettingell WH, Jung YK, Kovacs DM, Tanzi RE. 1997. Alternative cleavage of Alzheimer-associated presenilins during apoptosis by a caspase-3 family protease. Science 277:373-376.
59. Koh JY, Wie MB, Gwag BJ, Sensi SL, Canzoniero LM, Demaro J, Csemansky C, Choi DW. 1995. Staurosporine-induced neuronal apoptosis. Exp Neurol 135:153-159.
60. Korsching S. 1993. The neurotrophic factor concept: a reexamination. J Neurosci 13:2739-2748.
61. Kroemer G, Zamzami N, Susin SA. 1997. Mitochondrial control of apoptosis. Jmmunol Today 18:44-51.
62. Kruman I, Bruce-Keller AJ, Bredesen DE, Waeg G, Mattson MP. 1997. Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J Neurosci 17:5089-5100.
63. Kruman I, Quo Q, Mattson MP. 1998. Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC 12 cells. J Neurosci Res 51:293-308.
64. Kruman I, Pang Z, Geddes JW, Mattson MP. 1999. Pivotal role of mitochondrial calcium uptake in neural cell apoptosis and necrosis. J Neurochem 72:529-540.
65. Linnik MD, Zobrist RH, Hatfield MD. 1993. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2008.
66. Loo DT, Copani A, Pike CJ, Whittemore ER, Walencewicz AJ, Cotman CW. 1993. Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc Natl Acad Sci USA 90:7951-7955.
67. Lowenstein DH, Chan P, Miles M. 1991. The stress protein response in cultured neurons: characterization and evidence for a protective role in excitotoxicity. Neuron 7:1053-1060.
68. MacManus JP, Buchan AM, Hill IE, Rasquinha I, Preston E. 1993. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett 164:89-92.
69. 2+ homeostasis and cell death. J Neurosci 15:6239-6249.
70. +-ATPase activity in hippocampal neurons. Brain Res 756:205-214.
71. Mark RJ, Pang Z, Geddes JW, Uchida K, Mattson MP. 1997b. Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J Neurosci 17:1046-1054.
72. Markus EJ, Petit TL. 1989. Synaptic structural plasticity: role of synaptic shape. Synapse 3:1-11.
73. Martin SJ, O'Brian GA, Nishioka WK, McGahon AJ, Saido T, Green DR. 1995. Proteolysis of fodrin (nonerythroid spectrin) during apoptosis. J Biol Chem 270:6425-6428.
74. Mashima T, Naito M, Noguchi K, Miller DK, Nicholson DW, Tsuruo T. 1997. Actin cleavage by CPP-32/apopain during the development of apoptosis. Oncogene 14:1007-1012.
75. Mattson MP. 1988. Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Res 472:179-212.
76. Mattson MP. 1989. Cellular signaling mechanisms common to the development and degeneration of neuroarchitecture. A review. Mech Ageing Dev 50:103-157.
77. Mattson MP. 1994. Secreted forms of β-amyloid precursor protein modulate dendrite outgrowth and calcium responses to glutamate in cultured embryonic hippocampal neurons. J Neurobiol 25:439-450.
78. Mattson MP. 1996. Calcium and free radicals: mediators of neurotrophic factor-and excitatory transmitter-regulated developmental plasticity and cell death. Perspect Dev Neurobiol 3:79-91.
79. Mattson MP. 1997. Cellular actions of β-amyloid precursor protein, and its soluble and fibrillogenic peptide derivatives. Physiol Rev 77:1081-1132.
80. Mattson MP. 1998. Free radicals, calcium, and the synaptic plasticity-cell death continuum: emerging roles of the transcription factor NF-κB. Int Rev Neurobiol 42:103-168.
81. Mattson MP, Furukawa K. 1996. Programmed cell life: anti-apoptotic signaling and therapeutic strategies for neurodegenerative disorders. Rest Neurol Neurosci 9:191-205.
82. Mattson MP, Guo Q. 1999. The presenilins. Neuroscientist 5:112-124.
83. Mattson MP, Lindvall O. 1997. Neurotrophic factor and cytokine signaling in the aging brain. In: Mattson MP, Geddes JW, editors. The aging brain. Volume 2, Advances in cell aging and gerontology. p 299-345.
84. Mattson MP, Murrain M, Guthrie PB, Kater SB. 1989. Fibroblast growth factor and glutamate: opposing roles in the generation and degeneration of hippocampal neuroarchitecture. J Neurosci 9:3728-3740.
85. Mattson MP, Barger SW, Cheng B, Lieberburg I, Smith-Swintosky VL, Rydel RE. 1993a. β-Amyloid precursor protein metabolites and loss of neuronal calcium homeostasis in Alzheimer's disease. Trends Neurosci 16:409-415.
86. Mattson MP, Kumar K, Cheng B, Wang H, Michaelis EK. 1993b. Basic FGF regulates the expression of a functional 71 kDa NMDA receptor protein that mediates calcium influx and neurotoxicity in cultured hippocampal neurons. J Neurosci 13:4575-4588.
87. Mattson MR, Tomaselli K, Rydel RE. 1993c. Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res 621:35-49.
88. Mattson MP, Zhang Y, Bose S. 1993d. Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp Neurol 121:1-13.
89. 2+], and neurotoxicity, and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 65:1740-1751.
90. Mattson MP, Goodman Y, Luo H, Fu W, Furukawa K. 1997. Activation of NF-κB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of Mn-SOD and suppression of peroxynitrite production and protein tyrosine nitration. J Neurosci Res 49:681-697.
91. Mattson MP, Keller JN, Begley JG. 1998a. Evidence for synaptic apoptosis. Exp Neurol 153:35-48.
92. Mattson MP, Partin J, Begley JG. 1998b. Amyloid β-peptide induces apoptosis-related events in synapses and dendrites. Brain Res 807:167-176.
93. Mattson MP, Guo ZH, Geiger JD. 1999. Secreted form of amyloid precursor protein enhances basal glucose and glutamate transport, and protects against oxidative impairment of glucose and glutamate transport in synaptosomes by a cyclic GMP-mediated mechanism. J Neurochem. Forthcoming.
94. McGinnis KM, Whitton MM, Gnegy ME, Wang KK. 1998. Calcium/ calmodulin-dependent protein kinase IV is cleaved by caspase-3 and calpain in SH-SY5Y human neuroblastoma cells undergoing apoptosis. J Biol Chem 273:19993-20000.
95. Miller DK. 1997. The role of the caspase family of cysteine proteases in apoptosis. Semin Immunol 9:35-49.
96. Moore S, Thanos S. 1996. The concept of microglia in relation to central nervous system disease and regeneration. Prog Neurobiol 48:441-460.
97. Neame SJ, Rubin LL, Philpott KL. 1998. Blocking cytochrome c activity within intact neurons inhibits apoptosis. J Cell Biol 142:1583-1593.
98. Nicotera P, Ankarcrona M, Bonfoco E, Orrenius S, Lipton SA. 1997. Neuronal necrosis and apoptosis: two distinct events induced by exposure to glutamate or oxidative stress. Adv Neurol 72:95-101.
99. Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, Kominami E, Uchiyama Y. 1995. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 15:1001-1011.
100. Nitsch R, Farber AS, Growdon HJ, Wurtman JR. 1993. Release of amyloid β-protein precursor derivatives by electrical depolarization of rat hippocampal slices. Proc Natl Acad Sci USA 90:5191-5193.
101. Nunez G, Benedict MA, Hu Y, Inohara N. 1998, Caspases: the proteases of the apoptotic pathway. Oncogene 17:3237-3245.
102. Oppenheim RW. 1991. Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
103. Pang Z, Geddes JW. 1997. Mechanisms of cell death induced by the mitochondrial toxin 3-nitropropionic acid: acute excitotoxic necrosis and delayed apoptosis. J Neurosci 17:3064-3073.
104. Parent A, Linden DJ, Sisodia SS, Borchelt DR. 1999. Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1. Neurobiol Dis 6:56-62.
105. Pasinelli P, Borchelt DR, Houseweart MK, Cleveland DW, Brown RH Jr. 1998. Caspase-1 is activated in neural cells and tissue with amyotrophic lateral sclerosis-associated mutations in copper-zinc superoxide dismutase. Proc Natl Acad Sci USA 95:15763-15768.
106. Pettmann B, Henderson CE. 1998. Neuronal cell death. Neuron 20:633-647.
107. Portera-Cailliau C, Hedren JC, Price DL, Koliatsos VE. 1995. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J Neurosci 15:3775-3787.
108. Purves D, Snider WD, Voyvodic JT. 1988. Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature 336:123-128.
109. Richter C. 1993. Pro-oxidants and mitochondrial calcium: thier relationship to apoptosis and oncogenesis. FEBS Lett 325:104-107.
110. Schreck R, Baeuerle PA. 1994. Assessing oxygen radicals as mediators in activation of inducible eukaryotic transcription factor NF-κB. Methods Enzymol 234:151-163.
111. Sells SF, Han SS, Muthukkumar S, Maddiwar N, Johnstone R, Boghaert E, Gillis D, Liu G, Nair P, Monning S, Collini P, Mattson MP, Sukatme VP, Zimmer S, Wood DP, McRoberts JW, Shi Y, Rangnekar V. 1997. Expression and function of the leucine zipper protein Par-4 in apoptosis. Mol Cell Biol 17:3823-3832.
112. Soderling TR, Tan SE, McGlade-McCulloh E, Yamamoto H, Fukunaga K. 1994. Excitatory interactions between glutamate receptors and protein kinases. J Neurobiol 25:304-311.
113. Stefanis L, Troy CM, Qi H, Shelanski ML, Greene LA. 1998. Caspase-2 (Nedd-2) processing and death of trophic factor-deprived PC12 cells and sympathetic neurons occur independently of caspase-3 (CPP32)-like activity. J Neurosci 18:9204-9215.
114. Su JH, Anderson AJ, Cummings B, Cotman CW. 1994. Immunocytochemical evidence for apoptosis in Alzheimer's disease. NeuroReport 5:2529-2533.
115. Takechi H, Eilers J, Konnerth A. 1998. A new class of synaptic response involving calcium release in dendritic spines. Nature 396:757-760.
116. Tenneti L, D'Emilia DM, Troy CM, Lipton SA. 1998. Role of caspases in N-methyl-D-aspartate-induced apoptosis in cerebrocortical neurons. J Neurochem 71:946-959.
117. van Engeland M, Nieland LJ, Ramaekers FC, Schutte B, Reutelingsperger CP. 1998. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31:1-9.
118. Vekrellis K, McCarthy MJ, Watson A, Whitfield J, Rubin LI, Ham J. 1997. Bax promotes neuronal cell death and is downregulated during the development of the nervous system. Development 124:1239-1249.
119. Wang KK, Posmantur R, Nath R, McGinnis K, Whitton M, Talanian RV, Glantz SB, Morrow JS. 1998. Simultaneous degradation of alphall-and betall-spectrin by caspase 3 (CPP32) in apoptotic cells. J Biol Chem 273:22490-22497.
120. Wyllie AH, Kerr JFR, Currie AR. 1990. Cell death: the significance of apoptosis. Int Rev Cytol 68:251-306.
121. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS. 1998. Bax involvement in p53-mediated neuronal cell death. J Neurosci 18:1363-1373.
122. Yu ZF, Mattson MP. 1999. Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J Neurosci Res 57:830-839.
123. Yu ZF, Luo H, Fu W, Mattson MP. 1999. The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: suppression of oxidative stress and stabilization of calcium homeostasis. Exp Neurol 155:302-314.
124. Zorumski CF, Izumi Y. 1993. Nitric oxide and hippocampal synaptic plasticity. Biochem Pharmacol 46:777-785.