Different sources of reactive oxygen species contribute to low potassium-induced apoptosis in cerebellar granule cells

International Journal of Molecular Medicine

Volumn 21, Issue 6, 2008, Pages 737-745

  Bobba, Antonella ^a   Atlante, Anna ^a   Petragallo, Vito A ^a   Marra, Ersilia ^a  

^a CNR   (Italy)

Author keywords

Apoptosis; Cerebellar granule cells; Inhibitors; Reactie oxygen species; ROS generating enzymes

Indexed keywords

3 [3 TERT BUTYLTHIO 1 (4 CHLOROBENZYL) 5 ISOPROPYL 2 INDOLYL] 2,2 DIMETHYLPROPIONIC ACID; ALLOPURINOL; ARACHIDONIC ACID; ARACHIDONYL TRIFLUOROMETHYL KETONE; BAICALEIN; CYTOCHROME P450; DIPHENYLIODONIUM SALT; ENZYME INHIBITOR; ESCULETIN; HYDROXYUREA; INDOMETACIN; LIPOXYGENASE; LIPOXYGENASE INHIBITOR; METYRAPONE; PD 146176; PHOSPHOLIPASE; POTASSIUM; PROSTAGLANDIN SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RIBONUCLEOTIDE REDUCTASE; UNCLASSIFIED DRUG; XANTHINE OXIDASE; PROSTAGLANDIN SYNTHASE INHIBITOR; SUPEROXIDE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; GRANULE CELL; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; NERVE CELL; WISTAR RAT;

ANIMALS; APOPTOSIS; ARACHIDONIC ACID; CELLS, CULTURED; CEREBELLUM; CYCLOOXYGENASE INHIBITORS; CYTOCHROME P-450 ENZYME SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; LIPOXYGENASE; LIPOXYGENASE INHIBITORS; MODELS, BIOLOGICAL; NADPH OXIDASE; NEURONS; PHOSPHOLIPASES; POTASSIUM; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RIBONUCLEOTIDE REDUCTASES; SUPEROXIDES; XANTHINE OXIDASE;

EID: 47649105754     PISSN: 11073756     EISSN: None     Source Type: Journal    
DOI: 10.3892/ijmm.21.6.737     Document Type: Article

References (59)

1. Schulz JB, Weller M and 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: 4696-4706, 1996.
2. Atlante A, Gagliardi S, Marra E and Calissano P: Neuronal apoptosis in rats is accompanied by rapid impairment of cellular respiration and is prevented by scavengers of reactive oxygen species. Neurosci Lett 245: 127-300, 1998.
3. Valencia A and Moran J: Role of oxidative stress in the apoptotic cell death of cultured cerebellar granule neurons. J Neurosci Res 64: 284-297, 2001.
4. Martin-Romero FJ, Garcia-Martin E and Gutierrez-Merino C: Inhibition of oxidative stress produced by plasma membrane NADH oxidase delays low-potassium-induced apoptosis of cerebellar granule cells. J Neurochem 82: 705-715, 2002.
5. Atlante A, Bobba A, Calissano P, Passarella S and Marra E: The apoptosis/ necrosis transition in cerebellar granule cells depends on the mutual relationship of the antioxidant and the proteolytic systems which regulate ROS production and cytochrome c release en rout to death. J Neurochem 84: 960-971, 2003.
6. Surette ME, Fonteh AN, Bernatchez C and Chilton FH: Pertubations in the control of cellular arachidonic acid levels block cell growth and induce apoptosis of HL60 cells. Carcinogenesis 5: 757-763, 1999.
7. Brash AR: Arachidonic acid as a bioactive molecule. J Clin Invest 107: 1339-1345, 2001.
8. Maccarrone M, Melino G and Finazzi Agrò A: Lipoxygenases and their involvement in programmed cell death. Cell Death Diff 8: 776-784, 2001.
9. Strauss KI and Marini AM: Cyclooxygenase-2 inhibition protects cultured cerebellar granule neurons from glutamate-mediated cell death. J Neurotrauma 19: 627-638, 2002.
10. Boldyrev AA, Carpenter DO, Huentelman MJ, Peters CM and Johnson P: Sources of reactive oxygen species production in excitotoxin-stimulated cerebellar granule cells. Biochem Biophys Res Commun 256: 320-324, 1999.
11. Cross AR and Jones OT: Enzymatic mechanisms of superoxide production. Biochim Biophys Acta 1057: 281-298, 1991.
12. Shiba D and Shimamoto N: Attenuation of endogenous oxidative stress-induced cell death by cytochrome P450 inhibitors in primary cultures of rat hepatocytes. Free Radic Biol Med 27: 1019-1026, 1999.
13. Ferrara R, Zanovello A, Bortolato S, White IN and Manno M: Bioactivation and cytotoxicity of 1,1-dichloro-2,2,2-trifluorethane (HCFC-123) in isolated rat hepatocytes. Pharmacol Toxicol 88: 192-197, 2001.
14. Atlante A, Calissano P, Bobba A, Giannattasio S, Marra E and Passarella S: Glutamate neurotoxicity, oxidative stress and mitochondria. (Review). FEBS Lett 497: 1-5, 2001.
15. Rosenberger G, Fuhrmann G, Grusch M, et al: The ribonucleotide reductase inhibitor trimidox induces c-myc and apoptosis of human ovarian carcinoma cells. Life Sci 67: 3131-3142, 2000.
16. Lee YS, Kang YS, Lee SH and Kim JA: Role of NAD(P)H oxidase in the tamoxifen-induced generation of reactive oxygen species and apoptosis in HepG2 human hepatoblastoma cells. Cell Death Differ 7: 925-932, 2000.
17. Suzukawa K, Miura K, Mitsushita J, Resau J, Hirose K, Crystal R and Kamata T: Nerve growth factor-induced neuronal differentaition requires Rac1-regulated reactive oxygen species. J Biol Chem 275: 13175-13178, 2000.
18. Tammariello SP, Quinn MT and Estus S: NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. J Neurosci 20: RC53, 2000.
19. Samhan-Arias AK, Martin-Romero FJ and Gutierrez-Merino C: Kaempferol blocks oxidative stress in cerebellar granule cells and reveals a key role for reactive oxygen species production at the plasma membrane in the commitment to apoptosis. Free Radic Biol Med 37: 48-61, 2004.
20. Lenaz G: The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology (Review). IUBMB Life 52:159-164, 2001.
21. Jekabsons MB and Nicholls DG: Bioenergetic analysis of cerebellar granule neurons undergoing apoptosis by potassium/serum deprivation. Cell Death Differ 13: 1595-1610, 2006.
22. Cai J and Jones DP: Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273: 11401-11404, 1998.
23. Bobba A, Canu N, Atlante A, Petragallo V, Calissano P and Marra E: Proteasome inhibitors prevent cytochrome c release during apoptosis but not in excitotoxic death of cerebellar granule neurons. FEBS Lett 515: 8-12, 2002.
24. Atlante A, De Bari L, Bobba A, Marra E, Calissano P and Passarella S: Cytochrome c, released form cerebellar granule cells undergoing apoptosis or excitotoxic death, can generate protonmotive force and drive ATP synthesis in isolated mitochondria. J Neurochem 86: 591-604, 2003.
25. Atlante A, Calissano P, Bobba A, Azzariti A, Marra E and Passarella S: Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J Biol Chem 275: 37159-37166, 2000.
26. Bobba A, Atlante A, Giannattasio S, Sgaramella G, Calissano P and Marra E: Early release and subsequent caspase-mediated degradation of cytochrome c in apoptotic cerebellar granule cells. FEBS Lett 457: 126-130, 1999.
27. Levi G, Aloisi F, Ciotti MT and Gallo V: Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures. Brain Res 290: 77-86, 1984.
28. D'Mello SR, Galli C, Ciotti T and Calissano P: Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-Re growth factor I and cAMP. Proc Natl Acad Sci USA 90: 10989-10993, 1993.
29. Volontè C, Ciotti T and Battistini L: Development of a method for measuring cell number: application to CNS primary neuronal cultures. Cytometry 17: 274-276, 1994.
30. Stefanis L, Park DS, Friedman WJ and Greene LA: Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J Neurosci 19: 6235-6247, 1999.
31. Forman HJ and Fridovich I: Superoxide dismutase: a comparison of rate constants. Arch Biochem Biophys 158: 396-400, 1973.
32. Herrera B, Murillo MM, Alvarez-Barrientos A, Beltran J, Fernandez M and Fabregat I: Source of early reactive oxygen species in the apoptosis induced by transforming growth factor-beta in fetal rat hepatocytes. Free Radic Biol Med 36: 16-26, 2004.
33. Woo C-H, Lee ZW, Kim BC, Ha KS and Kim JH: Involvement of cytosolic phospholipase A2, and the subsequent release of arachidonic acid, in signalling by Rac for the generation of intracellular reactive oxygen species in Rat-2 fibroblasts. Biochem J 348: 525-530, 2000.
34. Taketo MM and Sonoshita M: Phospolipase A2 and apoptosis (Review). Biochim Biophys Acta 1585: 72-76, 2002.
35. Arioka M, Cheon SH, Ikeno Y, Nakashima S and Kitamoto K: A novel neurotrophic role of secretory phospholipases A2 for cerebellar granule neurons. FEBS Lett 579: 2693-2701, 2005.
36. Cummings BS, Mchowat J and Schnellmann RG: Phospholipase A2s in cell injury and death. J Pharmacol Exp Ther 294: 793-799, 2000.
37. Moore SA, Giordano MJ, Kim HY, Salem N Jr and Spector AA: Brain microvessel 12-hydroxyeicosatetraenoic acid is the (S) enantiomer and is lipoxygenase derived. J Neurochem 57: 922-999, 1991.
38. Huang HC, Wang HR and Hsieh LM: Antiproliferative effect of baicalein, a flavonoid from a Chinese herb, on vascular smooth muscle cell. Eur J Pharmacol 251: 91-93, 1994.
39. Sendobry SM, Comicelli JA, Welch K, et al: Attenuation of diet-induced atherosclerosis in rabbits with a highly selective 15-lipoxygenase inhibitor lacking significant antioxidant properties. Br J Pharmacol 120: 1199-1206, 1997.
40. Ford-Hutchinson AW, Gresser M and Young RN: 5-Lipoxygenase (Review). Annu Rev Biochem 63: 383-417, 1994.
41. Phillis JW, Horrocks LA and Farooqui AA: Cyclooxygenases, lipoxygenases, and epoxygenases in CNS: their role and involvement in neurological disorders (Review). Brain Res Rev 52: 201-243, 2006.
42. Stanciu M, Wang Y, Kentor R, et al: Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J Biol Chem 275: 12200-12206, 2000.
43. Li Y, Maher P and Schubert D: A role for 12-lipoxygenase in nerve cell death caused by glutathione depletion. Neuron 19: 453-463, 1997.
44. Khanna S, Roy S, Ryu H, Bahadduri P, Swaan PW, Ratan RR and Sen CK: Molecular basis of vitamin E action: tocotrienol modulates 12-lipoxygenase, a key mediator of glutamate-induced neurodegeneration. J Biol Chem 278: 43508-43515, 2003.
45. Lebeau A, Terro F, Rostene W and Pelaprat D: Blockade of 12-lipoxygenase expression protects cortical neurons from apoptosis induced by beta-amyloid peptide. Cell Death Differ 11: 875-884, 2004.
46. Manev H, Uz T, Manev R and Zhang Z: Neurogenesis and neuroprotection in the adult brain. A putative role for 5-lipoxygenase? Ann NY Acad Sci 939: 45-51, 2001.
47. Ghosh J and Myers CE: Inhibition of arachidonate 5-lipoxygenase triggers massive apoptosis in human prostate cancer cells. Proc Natl Acad Sci USA 95: 13182-13187, 1998.
48. Maccarrone M, Salucci ML, Melino G, Rosato N and Finazzi-Agro A: The early phase of apoptosis in human neuroblastoma CHP100 cells is characterized by lipoxygenase-dependent ultraweak light emission. Biochem Biophys Res Commun 265: 758-762, 1999.
49. Zangar RC, Davydov DR and Verma S: Mechanisms that regulate production of reactive oxygen species by cytochrome P450 (Review). Toxicol Appl Pharmacol 199: 316-331, 2004.
50. Brezna B, Kweon O, Stingley RL, et al: Molecular characterization of cytochrome P450 genes in the polycyclic aromatic hydrocarbon degrading Mycobacterium vanbaalenii PYR-1 Appl Microbiol Biotechnol 71: 522-532, 2006.
51. Chen YC, Lin-Shiau SY and Lin JK: Involvement of reactive oxygen species and caspase 3 activation in arsenite-induced apoptosis. J Cell Physiol 177: 324-333, 1998.
52. Qin W, Peng Y, Ksiezak-Reding H, et al: Inhibition of cyclooxygenase as potential novel therapeutic strategy in N141I presenilin-2 familial Alzheimer's disease. Mol Psychiatry 11: 172-181, 2006.
53. Hewett SJ, Uliasz TF, Vidwans AS and Hewett JA: Cyclooxygenase-2 contributes to N-methyl-D-aspartate-mediated neuronal cell death in primary cortical cell culture. J Pharmacol Exp Ther 293: 417-425, 2000.
54. Kanno S, Kakuta M, Kitajima Y, et al: Preventive effect of trimidox on oxidative stress in U937 cell line. Biol Pharm Bull 30: 994-998, 2007.
55. O'Donnell VB, Spycher S and Azzi A: Involvement of oxidants and oxidant-generating enzyme(s) in tumour-necrosis-factor-alpha-mediated apoptosis: role for lipoxygenase pathway but not mitochondrial respiratory chain. Biochem J 310: 133-141, 1995.
56. Saito S, Ogawa J and Minamiya Y: Pulmonary reexpansion causes xanthine oxidase-induced apoptosis in rat lung. Am J Physiol Lung Cell Mol Physiol 289: L400-L406, 2005.
57. González-Polo RA, Rodríguez-Martín A, Morán JM, Niso M, Soler G and Fuentes JM: Paraquat-induced apoptotic cell death in cerebellar granule cells. Brain Res 1011: 170-176, 2004.
58. Beetsch JW, Park TS, Dugan LL, Shah AR and Gidday JM: Xanthine oxidase-derived superoxide causes reoxygenation injury of ischemic cerebral endothelial cells. Brain Res 786: 89-95, 1998.
59. Bobba A, Atlante A, Azzariti A, Sgaramella G, Calissano P and Marra E: Mitochondrial impairment induces excitotoxic death in cerebellar granule cells. Int J Mol Med 13: 873-876, 2004.