Neuroprotective action of cycloheximide involves induction of Bcl-2 and antioxidant pathways

Journal of Cell Biology

Volumn 136, Issue 5, 1997, Pages 1137-1149

  Furukawa, Katsutoshi ^a   Estus, Steven ^a   Fu, Weiming ^a   Mark, Robert J ^a   Mattson, Mark P ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; ANTIOXIDANT; ANTISENSE OLIGODEOXYNUCLEOTIDE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLOHEXIMIDE; FERROUS SULFATE; GENE PRODUCT; GLUTAMIC ACID; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; NEUROTROPHIC FACTOR; PROTEIN;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; FETUS; GENE; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMYLOID BETA-PROTEIN; ANIMALS; ANTIOXIDANTS; CATALASE; CELLS, CULTURED; CYCLOHEXIMIDE; FERROUS COMPOUNDS; GENE EXPRESSION REGULATION; GENES, BCL-2; GLUTAMIC ACID; HIPPOCAMPUS; NERVE TISSUE PROTEINS; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN SYNTHESIS INHIBITORS; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RNA, HETEROGENEOUS NUCLEAR; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

ANIMALIA;

EID: 0030899235     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.136.5.1137     Document Type: Article

References (86)

1. Aden, U., E. Bona, H. Hagberg, and B.B. Fredholm. 1994. Changes in c-fos mRNA in the neonatal rat brain following hypoxic ischemia. Neurosci. Lett. 180:91-95.
2. Allsopp, T.E., S. Kiselev, S. Wyatt, and A.M. Davies. 1995. Role of Bcl-2 in the brain-derived neurotrophic factor survival response. Eur. J. Neurosci. 7: 1266-1272.
3. Ankarcrona, M., J.M. Dypbukt, E. Bonfoco, B. Zhivotovsky, S. Orrenius, S.A. Lipton, and P. Nicotera. 1995. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 15:961-973.
4. Beal, M.F. 1995. Aging, energy, and oxidative stress in neurodegenerative diseases. Ann. Neurol. 38:357-366.
5. Behl, C. J. Davis, R. Lesley, and D. Schubert. 1994, Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77:817-827.
6. Behrens, M.I., J. Koh, L.M. Canzoniero, S.L. Sensi, C.A. Csernansky, and D.W. Choi. 1995. 3-Nitropropionic acid induces apoptosis in cultured striatal and conical neurons. Neuroreport. 6:545-548.
7. Bondy, S.C., and C.P. LeBel. 1993. The relationship between excitotoxicity and oxidative stress in the central nervous system. Free Radical Biol. Med. 14: 633-642.
8. Bredesen, D.E. 1995. Neural apoptosis. Ann. Neurol. 38:839-851.
9. Butterfield, D.A., K. Hensley, M. Harris, M.P. Mattson, and J. Carney. 1994. β-Amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer's disease. Biochem. Biophyx. Res. Commun. 200:710-715.
10. Carter, D.A. 1993. Up-regulation of β1-adrenoceptor messenger ribonucleic acid in the rat pineal gland: nocturnally, through a beta-adrenoceptor-linked mechanism, and in vitro, through a novel posttranscriptional mechanism activated by specific protein synthesis inhibitors. Endocrinology. 133:2263-2268.
11. Chen, J., S.H. Graham, P.H. Chan, J. Lan, R.L. Zhou, and R.P. Simon. 1995. bcl-2 is expressed in neurons that survive focal ischemia in the rat. Neuroreport. 6:394-398.
12. Cheng, B., and M.P. Mattson. 1991. NGF and bFGF protect rat and human central neurons against hypoglycemic damage by stabilizing calcium homeostasis. Neuron. 7:1031-1041.
13. Cheng, B., and M.P. Mattson. 1994. NT-3 and BDNF protect hippocampal, septal. and cortical neurons against metabolic compromise. Brain Res. 640:56-67.
14. Cheng, B., S. Christakos, and M. P. Mattson. 1994. Tumor necrosis factors protect neurons against excitotoxic/metabolic insults and promote maintenance of calcium homeostasis. Neuron. 12:139-153.
15. Choi, D.W. 1987. Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7: 369-379.
16. Collazo, D., H. Takahashi, and R.D.G, McKay. 1992. Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron. 9:643-656.
17. Cotman, C.W., and A.J. Anderson. 1995. A potential role for apoptosis in neurodegeneration and Alzheimer's disease. Mol. Neurobiol. 10:19-45.
18. Deckwerth, T.L., and E.M. Johnson, Jr. 1993. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J. Cell Biol. 123:1207-1222.
19. Downen, M., L. Mudd, J.D. Roback, H.C. Palfrey, and B.H. Wainer. 1993. Early nerve growth factor-induced events in developing rat septal neurons. Dev. Brain Res. 74:1-13.
20. Dragunow, M., E. Beilharz, E. Sirimanne, P. Lawlor, C. Williams, R. Bravo, and P. Gluckman. 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.
21. Dreyer, E.B., D. Zhang, and S.A. Lipton. 1995. Transcriptional or translational inhibition blocks low dose NMDA-mediated cell death. Neuroreport. 6:942-944.
22. Dugan, L.L., S.L. Sensi, L.M.T. Canzoniero, S.D. Handran, S.M. Rothman, T.-S. Lin, M.P. Goldberg, and D.W. Choi. 1995. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15:6377-6388.
23. Edwards, D.R., and L.C. Mahadevan. 1992. Protein synthesis inhibitors differentially superinduce c-fos and c-jun by three distinct mechanisms: lack of evidence for labile repressors. EMBO (Eur. Mol. Biol. Organ.) J. 11:2415-2424.
24. Estus, S., W.J, Zaks, R. S. Freeman, M. Gruda, R. Bravo, and E.M. Johnson, Jr. 1994. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127: 1717-1727.
25. Estus, S., C. van Rooyen, M.P. Mattson, E.F. Brigham, and R.E. Rydel. 1995. Comparison of altered gene expression during neuronal death induced by NGF withdrawl, amyloid β-protein treatment, or glucose deprivation. Soc. Neurosci. Abstr. 21:1721.
26. Fukunaga-Johnson, N., J.J. Ryan, M. Wicha, G. Nunez, and M.F. Clarke. 1995. Bcl-2 protects murine erythroleukemia cells from p53-dependent and -independent radiation-induced cell death. Carcinogenesis. 16:1761-1767.
27. Ghosh, A., D.D. Ginty, H. Bading, and M.E. Greenberg. 1994. Calcium regulation of gene expression in neuronal cells. J. Neurobiol. 25:294-303.
28. Goldstone, S.D., J.C Fragonas, T.M. Jeitner, and N.H. Hunt, 1995. Transcription factors as targets for oxidative signalling during lymphocyte activation. Biochim. Biophys. Acta. 1263:114-122.
29. Goodman, Y., and M.P. Mattson. 1994. Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peptide-induced oxidative injury. Exp. Neurol. 128:1-12.
30. Goto, K., A. Ishige, K. Sekiguchi, S. Iizuka, A. Sugimoto, and M. Yuzurihara. 1990. Effects of cycloheximide on delayed neuronal death in rat hippocampus. Brain Res. 534:299-302.
31. Greenberg, M.E., and E.B. Ziff. 1984. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature (Lond.). 311:433-438.
32. Greenlund, L.J.S., T.L. Deckwerth, and E.M. Johnson, Jr. 1995a. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron. 14:303-315.
33. Greenlund, L. J., S.J. Korsmeyer, and E.M. Johnson, Jr. 1995b. Role of BCL-2 in the survival and function of developing and mature sympathetic neurons. Neuron. 15:649-661.
34. Griffith, O.W., and A. Meister. 1979. Potent and specific inhibition of glutalhione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem. 254:7558-7560.
35. Hockenbery, D., G. Nunez, C. Milliman, R.D. Schreiber, and S.J. Korsmeyer. 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature (Lond.). 348:334-336.
36. Hockenbery, D., Z.N. Oltvai, X.M. Yin, C.L. Milliman, and S.H. Korsmeyer. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis Cell. 75:241-251.
37. Jackson, G.R., K. Werrbach-Perez, Z. Pan, D. Sampath, and J.R. Perez-poio. 1994. Neurotrophin regulation of energy homeostasis in the central nervous system. Dev. Neurosci. 16:285-290.
38. Kane, D.J., T.A. Sarafian, R. Anton, H. Hahn, E.B. Gralla, J.S. Valentine, T. Ord, and D.E. Bredesen. 1993. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science (Wash. DC). 262:1274-1277.
39. Kane, D.J., T. Ord, R. Anton, and D.E. Bredesen. 1995. Expression of bcl-2 inhibits necrotic neural cell death. J. Neurosci. Res. 40:269-275.
40. Keller, J.N., R.J. Mark, A.J. Bruce, E.M. Blanc, J.D. Rothstein, K. Uchida, and M.P. Mattson. 1997. 4-hydroxynonenal, an aldehydic product of membrane lipid peroxidation, impairs glutamate transport and mitochondrial function in synaptosomes. Neurosci. In press.
41. Keith, F.J., D.A. Bradbury, Y.M. Zhu, and N.H. Russell. 1995. Inhibition of bcl-2 with antisense oligonudeotides induces apoptosis and increases the sensitivity of AML blasts to Ara-C. Leukemia. 9:131-138.
42. Kitada, S., S. Takayama, K. De Riel, S. Tanaka, and J.C. Reed. 1994. Reversal of chemoresistance of lymphoma cells by antisensc-mediated reduction of bcl-2 gene expression. Antisense Res. Dev. 4:71-79.
43. Koketsu, N., D.J. Berlove, M.A. Moskowitz, N.W. Kowall, G.G. Caday, and S.P. Finklestein. 1994. Pretreatment with intraventricular basic fibroblast growth factor decreases infarct size following focal cerebral ischemia in rats, Ann. Neurol. 35-451-457.
44. Lafon-Cazal, M., S. Pietri, M. Culcasi, and J. Bockaert. 1993. NMDA-dependent Superoxide production and neurotoxicity. Nature (Lond.). 364:535-537.
45. Lawrence, M.S., D.Y. Ho, G.H. Sun, G.K. Steinberg, and R.M. Sapolsky. 1996. Overexpression of Bcl-2 with herpes simplex virus vectors protects CNS neurons against neurological insults in vitro and in vivo. J. Neurosci. 16:486-496.
46. Lindvall, O., Z. Kokaia, J. Bengzon, E. Elmer, and M. Kokaia, 1994. Neurotrophins and brain insults. Trends Neurosci. 17:490-496.
47. Linnik, M.D., R.H. Zobrist, and M.D. Hatfield. 1993. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke. 24: 2002-2008.
48. Linnik, M.D., P. Zahos, M.D. Geschwind, and H.J. Federoff. 1995. Expression of bcl-2 from a defective herpes simplex virus-1 vector limits neuronal death in focal cerebral ischemia. Stroke. 26:1670-1674.
49. Loo, D.T., A. Copani, C.J. Pike, E.R. Whittemore, A.J. Walencewicz, and C.W. Cotman. 1993. Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA. 90:7951-7955.
50. MacManus, J.P., A.M. Buchan, I.E. Hill, I. Rasquinha, and E. Preston. 1993. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci. Lett. 164:89-92.
51. 2+ homeostasis and cell death. J. Neurosci. 15:6239-6249.
52. Mark, R.J., E.M. Blanc, and M.P. Mattson. 1996. Amyloid β-peptide and oxidative cell injury in Alzheimer's disease. Mol. Neurobiol. 12:211-224.
53. Mark, R.J., M.A. Lovell, W.R. Markesbery, K. Uchida, and M.P. Mattson. 1997a. A role for 4-hydroxynonenal in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68:255-264.
54. Mark, R.J., Z. Pang, J.W. Geddes, and M.P. Mattson. 1997b. Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17:1046-1054.
55. Marsh, H.N., W.K. Scholz, F. Lamballe, R. Klein, V. Nanduri, M. Barbacid, and H.C. Palfrey. 1993. Signal transduction events mediated by the BDNF receptor gp 145trkB in primary hippocampal pyramidal cell culture. J. Neurosci. 13:4281-4292.
56. Martin, D.P., R.E. Schmidt, P.S. DiStefano, O.H. Lowry, J.G. Carter, and E.M. Johnson, Jr. 1988. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106: 829-844.
57. Martin, D.P., A. Ito, K. Horigome, P.A. Lampe, and E.M. Johnson, Jr. 1992. Biochemical characterization of programmed cell death in NGF-deprived sympathetic neurons. J. Neurobiol. 23:1205-1220.
58. Martinou, J.C., M. Dubois-Dauphin, J.K. Staple, I. Rodriguez, H. Frankowiki. M. Missotten, P. Albertini, D. Talabot, S. Catsicas, and C. Pietra. 1994. Overexpression of Bcl-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron. 13:1017-1030.
59. Mattson, M.P., and S.W. Barger. 1995. Programmed cell life: neuroprotective signal transduction and ischemic brain injury. In Cerebrovascular Diseases: Nineteenth Princeton Stroke Conference, M.A. Moskowitz and L.R. Caplan. editors. Butterworth, Stoneham, MA. 271-290.
60. Mattson, M.P., M. Murrain, P.B. Guthrie, and S.B. Kater. 1989. Fibroblast growth factor and glutamate: opposing actions in the generation and degeneration of hippocampal neuroarchitecture. J. Neurosci. 9:3728-3740.
61. Mattson, M.P., S.W. Barger, B. Cheng, I. Lieberburg, V.L. Smith-Swintosky, and R.E. Rydel. 1993a. β-Amyloid precursor protein metabolites and loss of neuronal calcium homeostasis in Alzheimer's disease. Trends Neurosci. 16: 409-415.
62. Mattson, M.P., B. Cheng, and V.L. Smith-Swintosky. 1993b. Growth factor-mediated protection from excitotoxicity and disturbances in calcium and free radical metabolism. Semin. Neurosci. 5:295-307.
63. Mattson, M.P., K. Kumar, B. Cheng, H. Wang, and E.K. Michaelis. 1993c. 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.
64. Mattson, M.P., Y. Zhang, and S. Bose. 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.
65. i and neurotoxicity, and increase antioxidant enzyme activities in hippocampal neurons. J. Neurochem. 65:1740-1751.
66. Mesner, P.W., C.L. Epting, J.L. Hegarty, and S.H. Green. 1995. A timetable of events during programmed cell death induced by trophic factor withdrawal from neuronal PC12 cells. J. Nerosci. 15:7357-7366.
67. Naveilhan, P., I. Neveu, F. Jehan, C. Baudet, D. Wion, and P. Brachet. 1994. Reactive oxygen species influence nerve growth factor synthesis in primary rat asirocytes. J. Neurochem. 62:2178-2186.
68. Oguchi, S., A. Weisz, and H. Esumi. 1994. Enhancement of inducible-type NO synthase gene transcription by protein synthesis inhibitors. Activation of an intracellular signal transduction pathway by low concentrations of cycloheximide. FEBS Lett. 338:326-330.
69. Pittman, R.N., S. Wang, A.J. DiBenedetto, and J.C. Mills. 1993. A system for characterizing cellular and molecular events in programmed neuronal cell death. J. Neurosci. 13:3669-3680.
70. Pollard, H., S. Cantagrel, C. Charriaut-Marlangue, J. Moreau, and Y. Ben-Ari. 1994. Apoptosis-associated DNA fragmentation in epileptic brain damage. Neuroreport. 5:1053-1055.
71. Portera-Calliau, C., J.C. Hedreen, D.L. Price, and V.E. Koliatsos, 1995, Evjdencc for apoptotic cell death in Hunungton disease and excitoloxic animal models. J. Neurosci. 15:3775-3787.
72. Ratan, R.R., T.H. Murphy, and J.M. Baraban. 1994a. Oxidative stress induces apoptosis in embryonic cortical neurons. J. Neurochem. 62:376-379.
73. Ratan, R.R., T.H. Murphy, and J.M. Baraban. 1994b. Macromolecuiar synthesis inhibitors prevent oxidative stress-induced apoptosis in embryonic cortical neurons by shunting cysteine from protein synthesis to glutathione, J. Neurosci. 14:4385-4392.
74. Schwanz, L.M., and B.A. Osborne. 1993. Programmed cell death, apoptosis and killer genes. Immunol. Today. 14:582-590.
75. Seger, R., and E.G. Krebs. 1995. The MAPK signaling cascade. FASEB (Fed. Am. Soc. Eur. Biol.) 1, 9:726-735.
76. Serghini, R., P. Froissard, B. Sola, and D. Duval. 1994. Cycloheximide and actinomycin D block the toxic effect of glutamic acid on PC12 cells. Neuroreport. 6:29-32.
77. Spina, M.B., S.P. Squinto, J. Miller, R.M. Lindsay, and C. Hyman. 1992. Brain-derived neurotrophic factor protects dopamine neurons against 6-hydroxydopamine and N-methyl-4-phenylpyridinium ion toxicity: involvement of glutathione system. J. Neurochem. 59:99-106.
78. Steller, H. 1995. Mechanisms and genes of cellular suicide. Science (Wash. DC). 267:1445-1449.
79. Subramaniam, M., L.J, Schmidt, C.E. Crutchfield III, and M.J. Getz. 1989. Negative regulation of serum-responsive enhancer elements. Nature (Lond.). 340:64-66.
80. Svendsen, C.N., J.N. Kew, K. Staley, and M.V. Sofroniew. 1994. Death of developing septal cholinergic neurons following NGF withdrawal in vitro: protection by protein synthesis inhibition. J. Neurosci. 14:75-87.
81. Takashima, A., K. Noguchi, K. Sato, T. Hoshino, and K. Imahori. 1993. Tau protein kinase I is essential for amyloid β-protein-induccd neurotoxicity. Proc. Natl. Acad. Sci. USA. 90:7789-7793.
82. Tortosa, A., R. Rivera, and I. Ferrer. 1994. Dose-related effects of cycloheximide on delayed neuronal death in the gerbil hippocampus after bilateral transitory forebrain ischemia. J. Neurol. Sci 121:10-17.
83. Wyllie, A.M., J.F. Kerr, and A.R. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306.
84. Yankner, B.A. 1996. Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron. 16:921-932.
85. Zhang, Y., T. Tatsuno, J. Carney, and M.P. Mattson. 1993. Basic FGF, NGF, and IGFs protect hippocampal neurons against iron-induced degeneration. J. Cereb. Btood Flow Metab. 13:378-388.
86. Zinck, R., M.A. Cahill, M. Kracht, C. Sachsenmaier, R.A. Hipskind, and A. Nordheim. 1995. Protein synthesis inhibitors reveal differential regulation of mitogen-activated protein kinase and stress-activated protein kinase pathways that converge on Elk-1, Mol. Cell. Biol 15:4930-4938.