Brain-derived neurotrophic factor prevents superoxide anion-induced death of PC12h cells stably expressing TrkB receptor via modulation of reactive oxygen species

Neuroscience Research

Volumn 35, Issue 1, 1999, Pages 9-17

  Yamagata, Tomoko ^a   Satoh, Takumi ^a,b   Ishikawa, Yasuyuki ^a   Nakatani, Atsushi ^a   Yamada, Masashi ^a   Ikeuchi, Toshihiko ^a   Hatanaka, Hiroshi ^a  

^a BIOMOL ENG RESEARCH INSTITUTE   (Japan)

^b OSAKA BIOSCIENCE INSTITUTE   (Japan)

Author keywords

Apoptosis; Neurotrophin; NGF; Oxygen radical; Superoxide

Indexed keywords

BRAIN DERIVED GROWTH FACTOR; SUPEROXIDE; 2.5S NERVE GROWTH FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FLUORESCENT DYE; NERVE GROWTH FACTOR; NEUROPROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; XANTHINE; XANTHINE OXIDASE;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CELL STRAIN; CELL SURVIVAL; NEUROPROTECTION; NONHUMAN; OXIDATION REDUCTION REACTION; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; RAT; ANIMAL; CELL DEATH; DRUG EFFECT; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; KINETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DEATH; CELL SURVIVAL; FLUORESCENT DYES; KINETICS; MICROSCOPY, FLUORESCENCE; NERVE GROWTH FACTORS; NEUROPROTECTIVE AGENTS; PC12 CELLS; RATS; REACTIVE OXYGEN SPECIES; RECEPTOR, TRKB; RECOMBINANT PROTEINS; SUPEROXIDES; TRANSFECTION; XANTHINE; XANTHINE OXIDASE;

EID: 0032589586     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-0102(99)00062-0     Document Type: Article

References (53)

1. Abiru Y., Nishio C., Hatanaka H. The survival of striatal cholinergic neurons cultured from postnatal 2-week-old rats is promoted by neurotrophins. Dev. Brain Res. 91:1996;260-267.
2. Aoshima H., Satoh T., Sakai N., Yamada M., Enokido Y., Ikeuchi T., Hatanaka H. Generation of free radicals during lipid hydroperoxide-triggered apoptosis in PC12h cells. Biochem. Biophys. Acta. 1345:1996;35-42.
3. Barbacid M. The trk family neurotrophin receptors. J. Neurobiol. 25:1994;1386-1403.
4. Behl C., Davis J.B., Lesley R., Schubert D. Hydrogen peroxide mediates amyloid b protein toxicity. Cell. 77:1994;817-827.
5. Biondkas V.P., Jordan J., Lee C.C., Miller R.J. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neueosci. 16:1996;1324-1336.
6. Bocchini V., Angeletti P.U. The nerve growth factor: purification as a 30,000-molecular weight protein. Proc. Natl. Acad. Sci. USA. 64:1969;787-794.
7. Dudek H., Datta S.R., Franke T.F., Birnbaum M.J., Yao R., Cooper G.M., Segal R.A., Kaplan D.R., Greenberg M.E. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science. 275:1997;661-665.
8. Dugan L.L., Sensi S.L., Canzoniero L.M., Handran S.D., Rothman S.M., Lin T.S., Goldberg M.P., Choi D.W. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15:1995;6377-6388.
9. Enokido Y., Hatanaka H. High oxygen atmosphere for neuronal cell culture with nerve growth factor. II. Survival and growth of clonal rat pheochromocytoma PC12 cells. Brain Res. 536:1990;23-29.
10. Enokido Y., Hatanaka H. Apoptotic cell death occurs in hippocampal neurons cultured in a high oxygen atmosphere. Neuroscience. 57:1993;965-972.
11. Fagen A.M., Garber M., Barbacid M., Silos-Santiago I., Holzman D.M. A role for trkA during maturation of striatal and basal forebrain cholinergic neurons in vivo. J. Neurosci. 15:1997;7644-7654.
12. Greenlund L.J.S., Deckworth T.L., Johnson E.M. Jr Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron. 14:1995;303-315.
13. Gunasekar P.G., Kanthasamy A.G., Borowitz J.L., Isom G.E. Monitoring intracellular nitric oxide formation by dichlorofluoescein in neuronal cells. J. Neurosci. Methods. 61:1995;15-21.
14. Hatanaka H. Nerve growth factor-mediated differentiation of nerve cell line cultured in a hormone-supplemented serum-free medium. Dev. Brain Res. 222:1981;225-233.
15. Henderson L.M., Chappell J.B. Dihydrorhodamine 123: a fluorescent probe for superoxide generation? Eur. J. Biochem. 217:1993;973-980.
16. Hockberger P.E., Ahmed M.S., Skimina T.A., Lee C., Hung W.Y., Siddique T. Imaging of hydrogen peroxide generation in cultured cells using dichlorofluorescein derivatives. Asakura T., Farkas D.L., Lief R.C., Priezzhev A.V., Tromberg B. Optical Diagnostics of Living Cells and Biofluids. SPIE Proceeding Series. 2678:1996;129-140 SPIE, Bellingham, Washington, DC.
17. Ishikawa, Y., Satoh, T., Enokido, Y., Nishio, C., Ikeuchi, T., Hatanaka, H., 1999. Generation of reactive oxygen species, release of L-glutamate and activation of caspases are required for oxygen-induced apoptosis of embryonic hippocampal neurons in culture. Brain Res. (in press).
18. Jacobson M.D., Raff M.C. Programmed cell death and Bcl-2 protection in very low oxygen. Nature. 374:1995;814-816.
19. Johonson E.M., Gorin P.G. Dorsal root ganglion neurons are stroyed by exposure in utero to maternal antibody to nerve growth factor. Science. 210:1980;916-918.
20. Kirschner P.B., Jenkins B.G., Schulz J.B., Finkelstein S.P., Matthews R.T., Rosen B.R., Beal M.F. NGF, BDNF and NT-5, but not NT-3 protect against MPP+ toxicity and oxidative stress in neonatal animals. Brain Res. 713:1996;178-185.
21. Klein R., Martin-Zanca D., Barbacid M., Parada L.F. Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development. 109:1990;845-850.
22. Koh J.Y., Gwag B.J., Lobner D., Choi D.W. Potentiated necrosis of cultured cortical neurons by neurotrophins. Science. 268:1995;573-575.
23. Koliatsos V.E., Clatterbuck R.E., Winslow J.W., Cayouette M.H., Price D.L. Evidence that brain-derived neurotrophic factor is a trophic factor for motor neuron in vivo. Neuron. 10:1993;359-367.
24. Kubo T., Nonomura T., Enokido Y., Hatanaka H. Brain-derived neurotrophic factor (BDNF) can prevent apoptosis of rat cerebellar granule neurons in culture. Dev. Brain Res. 85:1994;249-258.
25. Kubo T., Enokido Y., Yamada M., Oka T., Uchiyama Y., Hatanaka H. Oxygen-induced apoptosis in PC12 cells with special reference to the role of Bcl-2. Brain Res. 733:1996;175-183.
26. Lindholm D., Dechant G., Heisenberg C.P., Thoenen H. Brain-derived neurotrophic factor for cultured rat cerebellar granule neurons and protect them against glutamate-induced neurotoxicity. Eur. J. Neurosci. 5:1993;1455-1464.
27. Martinez H.J., Dreyfus C.F., Jonakait G.M., Black I.B. Nerve growth factor promotes cholinergic development in brain striatal culture. Proc. Natl. Acad. Sci. USA. 82:1985;7777-7781.
28. Mobley W.C., Rutkowski J.L., Tennekoon S.J., Buchanan K., Johnston M.V. Choline acetyltransferase in stiratum of neonatal rats increased by nerve growth factor. Science. 229:1985;284-287.
29. Nakatani A., Yamada M., Asada A., Okada M., Ikeuchi T., Hatanaka H. Comparison between survival-promoting effects of brain-derived neurotrophic factor and neurotrophin-3 on PC12h cells stably expressing TrkB receptor. J. Biochem. 123:1998;707-714.
30. Nonomura T., Hatanaka H. Neurotrophic effects of brain-derived neurotrophic factor on basal forebrain cholinergic neurons in culture from postnatal rats. Neurosci. Res. 14:1992;226-233.
31. del-Peso L., Gonzalez G.M., Page C., Herrera R., Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science. 278:1997;687-689.
32. Raten R.R., Murphy T.H., Baraban J.M. Oxidative stress induces apoptosis in embryonic cortical neurons. J. Neurosci. 62:1994;376-379.
33. Reynolds I.J., Hastings T.G. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15:1995;3318-3327.
34. 2 in cultured endothelial cells. Arch. Biochem. Biophys. 302:1993;348-355.
35. Satoh T., Sakai N., Kubo T., Enokido Y., Uchiyama Y., Hatanaka H. Flow cytometric analysis of serum deprivation-induced death of PC12 cells, with special reference to role of bcl-2. Neurosci. Lett. 201:1995;119-122.
36. Satoh T., Sakai N., Enokido Y., Uchiyama Y., Hatanaka H. Free radical-independent protection of PC12 cells from hydrogen peroxide-triggered death by nerve growth factor and bcl-2 gene product. J. Biochem. 120:1996a;540-546.
37. Satoh T., Sakai N., Enokido Y., Uchiyama Y., Hatanaka H. Survival factor-insensitive generation of reactive oxygen species induced by serum deprivation in neuronal cells. Brain Res. 733:1996b;9-14.
38. Satoh T., Enokido Y., Aoshima H., Uchiyama Y., Hatanaka H. Changes in mitochondrial membrane potential during oxidative stress-induced apoptosis in PC12 cells. J. Neurosci. Res. 50:1997;413-420.
39. Satoh T., Numakawa T., Abiru Y., Yamagata T., Enokido Y., Hatanaka H. Production of reactive oxygen species and release of l-glutamate during superoxide anion-induced cell death of cerebellar granule neurons. J. Neurochem. 70:1998a;316-324.
40. Satoh T., Enokido Y., Kubo T., Yamada M., Hatanaka H. Oxygen toxicity induces apoptosis in neuronal cells. Cell. Mol. Neurobiol. 18:1998b;649-666.
41. Satoh T., Yamagata T., Ishikawa Y., Yamada M., Uchiyama Y., Hatanaka H. Regulation of reactive oxygen species by nerve growth factor but not by Bcl-2 as a novel mechanism of protection of PC12 cells from superoxide anion-induced death. J. Biochem. 125:1999;952-959.
42. Schulz J.B., Weller M., Klockgether T. Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J. Neurosci. 16:1996;4696-4706.
43. Segal R., Greenberg M.E. Intracellular signaling pathway activated by neurotrophic factors. Annu. Rev. Neurosci. 19:1996;463-489.
44. Shimizu S., Eguchi Y., Kamiike W., Matsuda H., Tsujimoto Y. Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature. 374:1995;811-813.
45. +-induced apoptosis of cerebellar granule neurons. Dev. Brain Res. 101:1997;197-206.
46. +-induced apoptosis of cerebellar granule neurons via Akt kinase activation. FEBS Lett. 437:1998;221-224.
47. Shimoke K., Yamagishi S., Yamada M., Ikeuchi T., Hatanaka H. Inhibition of phosphatidylinositol 3-kinase activity elevates c-Jun N-terminal kinase activity in apoptosis of cultured cerebellar granule neurons. Dev. Brain Res. 112:1999;245-253.
48. Suda K., Barde Y., Thoenen H. Nerve growth factor in mouse and rat serum: correlation between bioassay and radioimmunoassay determinations. Proc. Natl. Acad. Sci. USA. 75:1978;4042-4046.
49. Troy C.M., Shelanski M.L. Downregluration of Cu/Zn superoxide dismutase causes apoptotic cell death in PC12 neuronal cells. Proc. Natl. Acad. Sci. USA. 91:1996;6384-6387.
50. Troy C.M., Derossi D., Prochiantz A., Greene L.A., Shelanski M.L. Downregluration of Cu/Zn superoxide dismutase leads to cell death via the nitric oxide-peroxynitrite pathway. J. Neurosci. 16:1996;253-261.
51. Vantini G., Schavo N., Dimartino A., Polato P., Triban C., Callegaro L., Toffano G., Leon A. Evidence for a physiological role for nerve growth factor in the central nervous system of neonatal rats. Neuron. 3:1989;267-273.
52. Yao R., Cooper G.M. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science. 267:1995;2003-2006.
53. Yamada M., Ohnishi H., Sano S., Nakatani A., Ikeuchi T., Hatanaka H. Insulin receptor substrate (IRS)-1 and IRS-2 are tyrosine-phosphorylated and associated with phosphatidylinositol 3-kinase in response to brain-derived neurotrophic factor in cultured cerebral cortical neurons. J. Biol. Chem. 272:1997;30334-30339.