Trimethyltin-induced apoptosis is associated with upregulation of inducible nitric oxide synthase and Bax in a hippocampal cell line

Toxicology and Applied Pharmacology

Volumn 216, Issue 1, 2006, Pages 34-43

  Zhang, L ^a   Li, L ^a   Prabhakaran, K ^a   Borowitz, J L ^a   Isom, G E ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Apoptosis; Hippocampus; Nitric oxide synthase; Oxidative stress; Trimethyltin

Indexed keywords

CASPASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROTEIN BAX; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TRIMETHYLTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CELL DEATH; CELL IMMORTALIZATION; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DEATH; ENZYME ACTIVATION; HIPPOCAMPUS; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; UPREGULATION;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL LINE; CYCLIC N-OXIDES; CYCLOSPORINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; HIPPOCAMPUS; MEMBRANE POTENTIALS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITROGEN OXIDES; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDES; REACTIVE OXYGEN SPECIES; TRIMETHYLTIN COMPOUNDS; UP-REGULATION;

EID: 33748744939     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2006.05.004     Document Type: Article

References (53)

1. Acquaviva R., Campisi A., Murabito P., Raciti G., Avola R., Mangiameli S., Musumeci I., Barcellona M.L., Vanella A., and Li Volti G. Propofol attenuates peroxynitrite-mediated DNA damage and apoptosis in cultured astrocytes: an alternative protective mechanism. Anesthesiology 101 (2004) 1363-1371
2. Bagetta G., Piccirilli S., Del Duca C., Morrone L.A., Rombola L., Nappi G., De Alba J., Knowles R.G., and Corasaniti M.T. Inducible nitric oxide synthase is involved in the mechanisms of cocaine enhanced neuronal apoptosis induced by HIV-1 gp120 in the neocortex of rat. Neurosci. Lett. 356 (2004) 183-186
3. Bonini M.G., Rota C., Tomasi A., and Mason R.P. The oxidation of 2′,7′-dichlorofluorescin to reactive oxygen species: a self-fulfilling prophesy?. Free Radical Biol. Med. 40 (2006) 968-975
4. Brand M.D., Buckingham J.A., Esteves T.C., Green K., Lambert A.J., Miwa S., Murphy M.P., Pakay J.L., Talbot D.A., and Echtay K.S. Mitochondrial superoxide and aging: uncoupling-protein activity and superoxide production. Biochem. Soc. Symp. 71 (2004) 203-213
5. Brown G.C., and Borutaite V. Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim. Biophys. Acta 1658 (2004) 44-49
6. Cardounel A., Regelson W., and Kalimi M. Dehydroepiandrosterone protects hippocampal neurons against neurotoxin-induced cell death: mechanism of action. Proc. Soc. Exp. Biol. Med. 222 (1999) 145-149
7. Chabrier P.E., Demerle-Pallardy C., and Auguet M. Nitric oxide synthases: targets for therapeutic strategies in neurological diseases. Cell. Mol. Life Sci. 55 (1999) 1029-1035
8. Chen J., Wersinger C., and Sidhu A. Chronic stimulation of D1 dopamine receptors in human SK-N-MC neuroblastoma cells induces nitric-oxide synthase activation and cytotoxicity. J. Biol. Chem. 278 (2003) 28089-28100
9. Cookson M.R., Slamon N.D., and Pentreath V.W. Glutathione modifies the toxicity of triethyltin and trimethyltin in C6 glioma cells. Arch. Toxicol. 72 (1998) 197-202
10. Eskes C., Juillerat-Jeanneret L., Leuba G., Honegger P., and Monnet-Tschudi F. Involvement of microglia-neuron interactions in the tumor necrosis factor-α release, microglial activation, and neurodegeneration induced by trimethyltin. J. Neurosci. Res. 71 (2003) 583-590
11. Fechter L.D., and Liu Y. Elevation of intracellular calcium levels in spiral ganglion cells by trimethyltin. Hear. Res. 91 (1995) 101-109
12. Feldman R.G., White R.F., and Eriator I.I. Trimethyltin encephalopathy. Arch. Neurol 50 (1993) 1320-1324
13. Figiel I., and Fiedorowicz A. Trimethyltin-evoked neuronal apoptosis and glia response in mixed cultures of rat hippocampal dentate gyrus: a new model for the study of the cell type-specific influence of neurotoxins. Neurotoxicology 23 (2002) 77-86
14. 2+ (i) transients induced by trimethyltin chloride in HeLa cells: types and levels of response. Cell Calcium 37 (2005) 251-258
15. Fosslien E. Mitochondrial medicine-cardiomyopathy caused by defective oxidative phosphorylation. Ann. Clin. Lab. Sci. 33 (2003) 371-395
16. Garvey E.P., Oplinger J.A., Furfine E.S., Kiff R.J., Laszlo F., Whittle B.J., and Knowles R.G. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J. Biol. Chem. 272 (1997) 4959-5963
17. Geloso M.C., Vercelli A., Corvino V., Repici M., Boca M., Haglid K., Zelano G., and Michetti F. Cyclooxygenase-2 and caspase 3 expression in trimethyltin-induced apoptosis in the mouse hippocampus. Exp. Neurol. 175 (2002) 152-160
18. Gunasekar P.G., Li L., Prabhakaran K., Eybl V., Borowitz J.L., and Isom G.E. Mechanisms of the apoptotic and necrotic actions of trimethyltin in cerebellar granule cells. Toxicol. Sci. 64 (2001) 83-89
19. Gunasekar P.G., Mickova V., Kotyzova D., Li L., Borowitz J.L., Vladislav V., and Isom G.E. Role of astrocytes in trimethyltin neurotoxicity. J. Biochem. Mol. Toxicol. 15 (2001) 256-261
20. Gursoy E., Cardounel A., Al-khlaiwi T., Al-drees A., and Kalimi M. Tamoxifen protects clonal mouse hippocampal (HT-22) cells against neurotoxins-induced cell death. Neurochem. Int. 40 (2002) 405-412
21. Huang H.M., Ou H.C., Xu H., Chen H.L., Fowler C., and Gibson G.E. Inhibition of alpha-ketoglutarate dehydrogenase complex promotes cytochrome c release from mitochondria, caspase-3 activation, and necrotic cell death. J. Neurosci. Res. 74 (2003) 309-317
22. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., and Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Nat. Acad. Sci. U. S. A. 84 (1987) 9265-9269
23. Jenkins S.M., and Barone S. The neurotoxicant trimethyltin induced apoptosis via caspase activation, p38 protein kinase, and oxidative stress in PC12 cells. Toxicol. Lett. 147 (2004) 63-72
24. Jones D.C., Gunasekar P.G., Borowitz J.L., and Isom G.E. Dopamine-induced apoptosis is mediated by oxidative stress and is enhanced by cyanide in differentiated PC12 cells. J. Neurochem. 74 (2000) 2296-2304
25. Kane M.D., Yang Y.-C., Gunasekar P.G., and Isom G.E. Trimethyltin stimulates protein kinase C translocation through receptor-mediated phospholipase C activation in PC12 cells. J. Neurochem. 70 (1998) 509-514
26. Kassed C.A., Butler T.L., Patton G.W., Demesquita D.D., Navidomskis M.T., Memet S., Israel A., and Pennypacker K.R. Injury-induced NF-kappaB activation in the hippocampus: implications for neuronal survival. FASEB J. 18 (2004) 723-724
27. Lee S.M., Yune T.Y., Kim S.J., Kim Y.C., Oh Y.J., Markelonis G.J., and Oh T.H. Minocycline inhibits apoptotic cell death via attenuation of TNF-alpha expression following iNOS/NO induction by lipopolysaccharide in neuron/glia co-cultures. J. Neurochem. 91 (2004) 568-578
28. Maher P., and Davis J.B. The role of monoamine metabolism in oxidative glutamate toxicity. J. Neurosci. 16 (1996) 6394-6401
29. Marriott H.M., Ali F., Read R.C., Mitchell T.J., Whyte M.K., and Dockrell D.H. Nitric oxide levels regulate macrophage commitment to apoptosis or necrosis during pneumococcal infection. FASEB J. 18 (2004) 1126-1128
30. Mundy W.R., and Freudenrich T.M. Apoptosis of cerebellar granule cells induced by organotin compounds found in drinking water: involvement of MAP kinases. Neurotoxicology 27 (2006) 71-81
31. Mungrue I.N., Bredt D.S., Stewart D.J., and Husain M. From molecules to mammals: what's NOS got to do with it?. Acta Physiol. Scand. 179 (2003) 123-135
32. O'Callaghan J.P., and Miller D.B. Neuron-specific phosphoproteins as biochemical indicators of neurotoxicity: effects of acute administration of trimethyltin to the adult rat. J. Pharmacol. Exp. Ther. 231 (1984) 736-743
33. Pahan K., Sheikh F.G., Liu X., Hilger S., McKinney M., and Petro T.M. Induction of nitric-oxide synthase and activation of NF-kappaB by interleukin-12 p40 in microglial cells. J. Biol. Chem. 276 (2001) 7899-7905
34. Paule M.G., Reuhl K., Chen J.J., Ali S.F., and Slikker W. Developmental toxicology of trimethyltin in the rat. Toxicol. Appl. Pharmacol. 84 (1986) 412-417
35. Polster B.M., and Fiskum G. Mitochondrial mechanisms of neural cell apoptosis. J. Neurochem. 90 (2004) 1281-1289
36. Prabhakaran K., Li L., Borowitz J.L., and Isom G.E. Cyanide induces different modes of death in cortical and mesencephalon cells. J. Pharmacol. Exp. Ther. 303 (2002) 510-519
37. Qu B., Li Q.T., Wong K.P., Tan T.M., and Halliwell B. Mechanism of clofibrate hepatotoxicity: mitochondrial damage and oxidative stress in hepatocytes. Free Radical Biol. Med. 31 (2001) 659-669
38. Reali C., Scintu F., Pillai R., Donato R., Michetti F., and Sogos V. S100b counteracts effects of the neurotoxicant trimethyltin on astrocytes and microglia. J. Neurosci. Res. 81 (2005) 677-686
39. Reers M., Smiley S.T., Mottola-Hartshorn C., Chen A., Lin M., and Chen L.B. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 260 (1995) 406-417
40. Rohl C., and Sievers J. Microglia is activated by astrocytes in trimethyltin intoxication. Toxicol. Appl. Pharmacol. 204 (2005) 36-45
41. Scorrano L., and Korsmeyer S.J. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 304 (2003) 437-444
42. Shin E.J., Suh S.K., Lim Y.K., Jhoo W.K., Hjelle O.P., Ottersen O.P., Shin C.Y., Ko K.H., Kim W.K., Kim D.S., Chun W., Ali S., and Kim H.C. Ascorbate attenuates trimethyltin-induced oxidative burden and neuronal degeneration in the rat hippocampus by maintaining glutathione homeostasis. Neuroscience 133 (2005) 715-727
43. Shou Y., Li N., Li L., Borowitz J., and Isom G.E. NFkB-mediated upregulation of Bcl-Xs and BAX contributes to cytochrome c release in cyanide-induced apoptosis. J. Neurochemistry 81 (2002) 842-852
44. Small C.I., Lyles G.A., and Breen K.C. Inducible form of nitric oxide synthase expression in rat cortical neuronal cells in vitro. Neurobiol. Dis. 17 (2004) 70-76
45. Snoeij N.J., Penninks A.H., and Seinen W. Biological activity of organotin compounds-an overview. Environ. Res. 44 (1987) 335-353
46. Tamatani M., Ogawa S., Niitsu Y., and Tohyama M. Involvement of Bcl-2 family and caspase-3-like protease in NO-mediated neuronal apoptosis. J. Neurochem. 71 (1998) 1588-1596
47. Tan S., Wood M., and Maker P. Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J. Neurochem. 71 (1998) 95-105
48. Thorburne S.K., and Juurlink B.H. Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 67 (1996) 1014-1022
49. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (2003) 335-344
50. Viviani G., Corsini E., Galli C.L., and Marinovich M. Glia increase of degeneration of hippocampal neurons through release of tumor necrosis factor-α. Toxicol. Appl. Pharmacol. 150 (1998) 271-276
51. Weitsman G.E., Ravid A., Liberman U.A., and Koren R. Vitamin D enhances caspase-dependent and independent TNF-induced breast cancer cell death: the role of reactive oxygen species. Ann. N. Y. Acad. Sci. 1010 (2003) 437-440
52. Yung H.W., Bal-Price A.K., Brown G.C., and Tolkovsky A.M. Nitric oxide-induced cell death of cerebrocortical murine astrocytes is mediated through p53- and Bax-dependent pathways. J. Neurochem. 89 (2004) 812-821
53. Zawia N.H., and Harry G.J. Trimethyltin-induced c-fos expression: adolescent vs neonatal rat hippocampus. Toxicol. Appl. Pharmacol. 121 (1993) 99-102