Removal of serum from primary cultures of cerebellar granule neurons induces oxidative stress and DNA fragmentation: Protection with antioxidants and glutamate receptor antagonists

Journal of Neuroscience Research

Volumn 43, Issue 4, 1996, Pages 465-475

  Atabay, C ^a   Cagnoli, C M ^a   Kharlamov, E ^a   Ikonomovic, M D ^a   Manev, H ^a,b  

^a ALLEGHENY SINGER RESEARCH INSTITUTE   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

antioxidant; apoptosis; free radicals; glutamate; programmed cell death

Indexed keywords

DACTINOMYCIN; DIZOCILPINE; DNA FRAGMENT; DNA NUCLEOTIDYLEXOTRANSFERASE; FREE RADICAL;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL DEATH; CELL VIABILITY; DEPOLARIZATION; ENZYME ACTIVITY; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELLS, CULTURED; CEREBELLUM; CULTURE MEDIA, SERUM-FREE; DNA DAMAGE; EXCITATORY AMINO ACID ANTAGONISTS; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0029940901     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19960215)43:4<465::AID-JNR7>3.0.CO;2-D     Document Type: Article

References (49)

1. Balazs R, Hack N, Jorgensen OS (1990): Selective stimulation of excitatory amino acid receptor subtypes and the survival of cerebellar granule cells in culture: effect of kainic acid. Neuroscience 1:251-258.
2. Behl C, Davis IB, Klier FG, Schubert D (1994): Amyloid β peptide induces necrosis rather than apoptosis. Brain Res 645:253-264.
3. Bolanos JP, Peuchen SJR, Land JM, Clark JB (1994): Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J Neurochemistry 63:910-916.
4. Bondy SC, Lee DK (1993): Oxidative stress induced by glutamate receptor agonists. Brain Res 610:229-233.
5. Cagnoli CM, Atabay C, Kharlamova E, Manev H (1995): Melatonin protects neurons from singlet oxygen-induced apoptosis. J Pineal Res 18:222-226.
6. Chopp M, Li Y, Zhang ZG (1992): P53 expression in brain after middle cerebral artery occlusion in the rat. Biochem Biophys Res Commun 182:1201-1207.
7. Copani A, Bruno VMG, Barresi V, Battaglia G, Condorelli DF, Nicoletti F (1995): Activation of metabotropic glutamate receptors prevents neuronal apoptosis in culture. J Neurochem 64:101-108.
8. Cowan WM, Fawcett JW, O'Leary DDM, Stanfield BB (1984): Regressive events in neurogenesis. Science 225:1258-1265.
9. Coyle JT, Puttfarcken P (1993): Oxidative stress, glutamate, and neurodegenerative disorders. Science 262:689-695.
10. Deckwerth TL, Johnson Jr EM (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.
11. D'Mello SR, Galli C, Ciotti T, Calissano P (1993): Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 90:10989-10993.
12. D'Mello SR, Anelli R, Calissano P (1994): Lithium induces apoptosis in immature cerebellar granule cells but promotes survival of mature neurons. Exp Cell Res 211:332-338.
13. Driscoll BF, Deibler GE, Law MJ, Crane AM (1993): Damage to neurons in culture following medium change: role of glutamine and extracellular generation of glutamate. J Neurochem 61:1795-1800.
14. 2+ and the potentiation by serum albumin. Brain Res 560:282-290.
15. Favaron M, Manev H, Alho H, Bertolino M, Ferret B, Guidotri A, Costa E (1988): Gangliosides prevent glutamate and kainate neurotoxicity in primary cultures of neonatal rat cerebellum and cortex. Proc Natl Acad Sci USA 85:7351-7355.
16. Favaron M, Manev RM, Rimland JM, Candeo P, Beccaro M, Manev H (1993): NMDA-stimulated expression of BDNF mRNA in cultured cerebellar granule neurons. Neuroreport 4:1171-1174.
17. Goodman Y, Mattson MP (1994): Secreted forms of β-amyloid precursor protein protect hippocampal neurons against β-peptide-induced oxidative injury. Exp Neurol 128:1-12.
18. Grunewald RA (1993): Ascorbic acid in the brain. Brain Res Rev 18:123-133.
19. Hall ED, Braughler JM (1986): Role of lipid peroxidation in posttraumatic spinal cord degeneration: a review. Cent Nerv Sys Trauma 3:281-294.
20. Hisanaga K, Sagar S, Sharp FR (1992): Ascorbate neurotoxicity in cortical cell culture. Ann Neurol 31:562-565.
21. Hollmann M, Heinemann S (1994): Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
22. Huet O, Petit JM, Ratinaud MH, Julien R (1992): NADH-dependent dehydrogenase activity estimation of flow cytometric analysis of 3-(4,5-dimethiazolyl-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. Cytometry 13:532-539.
23. Kontos HA, Wei EP, Ellis EF, Jenkins LW, Povlishock JT, Rowe GT, Hess ML (1985): Appearance of superoxide anion radical in cerebral extracellular space during increased prostaglandin synthesis in cats. Circ Res 57:142-151.
24. Kure S, Tominaga T, Yoshimoto T, Tada K, Narisawa K (1991): Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem Biophys Res Commun 179:39-45.
25. Li X, Gong J, Feldman E, Seiter K, Traganos F, Darzynkiewicz Z (1994): Apoptotic cell death during treatment of leukemias. Leukemia Lymphoma 13:65-70.
26. Linnik MD, Zobrist RH, Hatfield MD (1993): Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2009.
27. 2+ influx elicited by glutamate: role in neuronal death. Mol Pharmacol 36:106-122.
28. Manev H, Costa E, Wroblewski JT, Guidotti A (1990): Abusive stimulation of excitatory amino acid receptors: a strategy to limit neurotoxicity. FASEB J 4:2789-2797.
29. Manev H, Atabay C, Kharlamov E, Grayson DR, Ikonomovic S, Armstrong DM, Cagnoli CM (1994a): Photochemical oxidative stress in primary cultures of cerebellar granule neurons causes apoptosis: protection with melatonin. Soc Neurosci Abstr 20:452.
30. Manev H, Kharlamov A, Armstrong DM (1994b): Photochemical brain injury in rats triggers DNA fragmentation, p53, and HSP72. Neuroreport 5:2661-2664.
31. Margolis RL, Chuang D-M, Post RM (1994): Programmed cell death: implications for neuropsychiatric disorders. Biol Psychiatry 35:946-956.
32. Meister A (1994): Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269:9397-9400.
33. Milani D, Candeo P, Favaron M, Blackstone CD, Manev H (1993): A subpopulation of cerebellar granule cells in culture expresses a functional metabotropic glutamate receptor: effect of depolarizing growing conditions. Receptors Channels 1:243-250.
34. Mosmann T (1983): Rapid colorimetric assay of cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63.
35. Oyama Y, Furukawa K, Chikahisa L, Hatakeyama Y (1994): Effect of N,N-diethyldithiocarbamate on iomycin-induced increase in oxidation of cellular 2′,7′-dichlorofluorescein in dissociated cerebellar neurons. Brain Res 660:158-161.
36. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD (1993): Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262:695-700.
37. Ratan RR, Murphy TH, Baraban JM (1994a): Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 62:376-379.
38. Ratan RR, Murphy TH, Baraban JM (1994b): Macromolecular synthesis inhibitors prevent oxidative stress-induced apoptosis in embryonic cortical neurons by shunting cysteine from protein synthesis to glutathione. J Neuroscience 14:4385-4392.
39. Schramm M, Eimerl S, Costa E (1990): Serum and depolarizing agents cause acute neurotoxicity in cultured cerebellar granule cells: role of the glutamate receptor responsive to N-methyl-D-aspartate. Proc Natl Acad Sci USA 87:1193-1197.
40. Serghini R, Froissard P, Sola B, Duval D (1994): Cycloheximide and actinomycin D block the toxic effect of glutamic acid on PC12 cells. Neuroreport 6:29-32.
41. 2+ overload indicates early neuronal injury which precedes staining with viability indicators. Brain Res 607:319-323.
42. Vaccarino FM, Alho H, Santi MR, Guidotti A (1987): Coexistence of GABA receptors and GABA-modulin in primary cultures of cerebellar granule cells. J Neurosci 7:65-76.
43. Volonte C, Ciotti MT, Merlo D (1994): LiCl promotes survival of GABAergic neurons from cerebellum and cerebral cortex: LiCl induces survival of GABAergic neurons. Neurosci Lett 172:6-10.
44. Volterra A, Trotti D, Tromba C, Floridi S, Racagni G (1994): Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. J Neurosci 14:2924-2932.
45. Wolvetang EJ, Johnson KL, Krauer K, Ralph SJ, Linnane AW (1994): Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett 339:40-44.
46. Wood KA, Dipasquale B, Youle RJ (1993): In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron 11:621-632.
47. Yan G-M, Ni B, Weller M, Wood KA, Paul SM (1994): Depolarization or glutamate receptor activation blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res 656:43-51.
48. Zhang Y, Marcillat O, Giulivi C, Ernster L, Davies KJA (1990): The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J Biol Chem 265:16330-16336.
49. Zona C, Ragozzino D, Ciotti MT, Mercanti D, Avoli M, Brancati A, Calissano P (1993): Sodium, calcium and late potassium currents are reduced in cerebellar granule cells cultured in the presence of a protein complex conferring resistance to excitatory amino acids. Eur J Neurosci 5:1479-1484.