Tl(I) and Tl(III) activate both mitochondrial and extrinsic pathways of apoptosis in rat pheochromocytoma (PC12) cells

Toxicology and Applied Pharmacology

Volumn 236, Issue 1, 2009, Pages 59-70

  Hanzel, Cecilia Eliana ^a   Verstraeten, Sandra Viviana ^a  

^a Instituto de Quimica y Fisicoquimica Biologicas Buenos Aires   (Argentina)

Author keywords

Apoptosis; Apoptosis inducing factor; Caspase; Cytochrome c; Thallium; Toxicology

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE 8; CASPASE 9; CASPASE DEPENDENT DEOXYRIBONUCLEASE; CYTOCHROME C; DEOXYRIBONUCLEASE; ENDONUCLEASE G; FAS ANTIGEN; PHOSPHATIDYLSERINE; PROTEIN BAX; THALLIC CATION; THALLIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL LEVEL; CELL STRAIN; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME INDUCTION; ENZYME KINETICS; ENZYME RELEASE; MITOCHONDRIAL DAMAGE; NONHUMAN; OLIGOMERIZATION; PHEOCHROMOCYTOMA CELL; RAT;

ADRENAL GLAND NEOPLASMS; ANIMALS; ANTIGENS, CD95; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CASPASE 8; CASPASE 9; CELL SURVIVAL; CYTOCHROMES C; DEOXYRIBONUCLEASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDODEOXYRIBONUCLEASES; MITOCHONDRIA; NECROSIS; PC12 CELLS; PHEOCHROMOCYTOMA; PHOSPHATIDYLSERINES; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; THALLIUM; TIME FACTORS;

RATTUS;

EID: 61849102373     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.12.029     Document Type: Article

References (47)

1. Adayev T., Estephan R., Meserole S., Mazza B., Yurkow E.J., and Banerjee P. Externalization of phosphatidylserine may not be an early signal of apoptosis in neuronal cells, but only the phosphatidylserine-displaying apoptotic cells are phagocytosed by microglia. J Neurochem. 71 (1998) 1854-1864
2. ATSDR. Thallium. ATSDR (Agency for Toxic Substances and Disease Registry). Prepared by Clement International Corp., under contract 205-88-0608, Atlanta, GA (1999)
3. Balasubramanian K., Mirnikjoo B., and Schroit A.J. Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis. J. Biol. Chem. 282 (2007) 18357-18364
4. Bauer M.K., Vogt M., Los M., Siegel J., Wesselborg S., and Schulze-Osthoff K. Role of reactive oxygen intermediates in activation-induced CD95 (APO-1/Fas) ligand expression. J. Biol. Chem. 273 (1998) 8048-8055
5. Biswas D., Banerjee M., Sen G., Das J.K., Banerjee A., Sau T.J., Pandit S., Giri A.K., and Biswas T. Mechanism of erythrocyte death in human population exposed to arsenic through drinking water. Toxicol. Appl. Pharmacol. 230 (2008) 57-66
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
7. Bragadin M., Toninello A., Bindoli A., Rigobello M.P., and Canton M. Thallium induces apoptosis in Jurkat cells. Ann. N.Y. Acad. Sci. 1010 (2003) 283-291
8. Bunzl K., Trautmannsheimer M., Schramel P., and Reifenhäuser W. Availability of arsenic, copper, lead, thallium, and zinc to various vegetables grown in slag-contaminated soils. J. Environ. Qual. 30 (2001) 934-939
9. Chen T.K., Luo G., and Ewing A.G. Amperometric monitoring of stimulated catecholamine release from rat pheochromocytoma (PC12) cells at the zeptomole level. Anal. Chem. 66 (1994) 3031-3035
10. Chia C.F., Chen S.C., Chen C.S., Shih C.M., Lee H.M., and Wu C.H. Thallium acetate induces C6 glioma cell apoptosis. Ann. N.Y. Acad. Sci. 1042 (2005) 523-530
11. Distelhorst C.W., and McCormick T.S. Bcl-2 acts subsequent to and independent of Ca2+ fluxes to inhibit apoptosis in thapsigargin- and glucocorticoidmtreated mouse lymphoma cells. Cell Calcium 19 (1996) 473-483
12. Douglas K.T., Bunni M.A., and Baindur S.R. Thallium in biochemistry. Int. J. Biochem. 22 (1990) 429-438
13. Eichler T., Ma Q., Kelly C., Mishra J., Parikh S., Ransom R.F., Devarajan P., and Smoyer W.E. Single and combination toxic metal exposures induce apoptosis in cultured murine podocytes exclusively via the extrinsic caspase 8 pathway. Toxicol. Sci. 90 (2006) 392-399
14. Fadok V.A., Voelker D.R., Campbell P.A., Cohen J.J., Bratton D.L., and Henson P.M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148 (1992) 2207-2216
15. Fujita K., Lazarovici P., and Guroff G. Regulation of the differentiation of PC12 pheochromocytoma cells. Environ. Health Perspect. 80 (1989) 127-142
16. Galvan-Arzate S., and Santamaria A. Thallium toxicity. Toxicol. Lett. 99 (1998) 1-13
17. Greene L.A., and Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. U.S.A. 73 (1976) 2424-2428
18. Hanzel C.E., and Verstraeten S.V. Thallium induces hydrogen peroxide generation by impairing mitochondrial function. Toxicology and Applied Pharmacology 216 (2006) 485-492
19. Harris W.R., and Messori L. A comparative study of aluminum(III), gallium(III), indium(III), and thallium(III) binding to human serum transferrin. Coord. Chem. Reviews 228 (2002) 237-262
20. Hassa P.O., and Hottiger M.O. The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci. 13 (2008) 3046-3082
21. Heim M., Wappelhorst O., and Markert B. Thallium in terrestrial environments - occurrence and effects. Ecotoxicology 11 (2002) 369-377
22. Kagan V.E., Borisenko G.G., Tyurina Y.Y., Tyurin V.A., Jiang J., Potapovich A.I., Kini V., Amoscato A.A., and Fujii Y. Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic. Biol. Med. 37 (2004) 1963-1985
23. Kagan V.E., Fabisiak J.P., Shvedova A.A., Tyurina Y.Y., Tyurin V.A., Schor N.F., and Kawai K. Oxidative signaling pathway for externalization of plasma membrane phosphatidylserine during apoptosis. FEBS Lett. 477 (2000) 1-7
24. Kitagawa K., and Niikura Y. Caspase-independent mitotic death (CIMD). Cell Cycle 7 (2008) 1001-1005
25. Korotkov S.M., and Brailovskaya L.V. Tl+ increases the permeability of the inner membranes of rat liver mitochondria for monovalent cations. Dokl. Biochem. Biophys. 378 (2001) 145-149
26. Korotkov S.M., and Lapin A.V. Thallium induces opening of the mitochondrial permeability transition pore in the inner membrane of rat liver mitochondria. Dokl. Biochem. Biophys. 392 (2003) 247-252
27. Laakko T., King L., and Fraker P. Versatility of merocyanine 540 for the flow cytometric detection of apoptosis in human and murine cells. J. Immunol. Methods 261 (2002) 129-139
28. Lim M.L., Lum M.G., Hansen T.M., Roucou X., and Nagley P. On the release of cytochrome c from mitochondria during cell death signaling. J. Biomed. Sci. 9 (2002) 488-506
29. Lin T.S., Nriagu J., and Wang X.Q. Thallium concentration in lake trout from Lake Michigan. Bull. Environ. Contam. Toxicol. 67 (2001) 921-925
30. Liu Q., Hilsenbeck S., and Gazitt Y. Arsenic trioxide-induced apoptosis in myeloma cells: p53-dependent G1 or G2/M cell cycle arrest, activation of caspase-8 or caspase-9, and synergy with APO2/TRAIL. Blood 101 (2003) 4078-4087
31. Lorenzo H.K., and Susin S.A. Mitochondrial effectors in caspase-independent cell death. FEBS Lett. 557 (2004) 14-20
32. Martin G., Sabido O., Durand P., and Levy R. Phosphatidylserine externalization in human sperm induced by calcium ionophore A23187: relationship with apoptosis, membrane scrambling and the acrosome reaction. Hum. Reprod. 20 (2005) 3459-3468
33. Moore D., House I., and Dixon A. Thallium poisoning. B.M.J. 306 (1993) 1527-1529
34. Oh S.H., Lee B.H., and Lim S.C. Cadmium induces apoptotic cell death in WI 38 cells via caspase-dependent Bid cleavage and calpain-mediated mitochondrial Bax cleavage by Bcl-2-independent pathway. Biochem. Pharmacol. 68 (2004) 1845-1855
35. Parrish J.Z., and Xue D. Functional genomic analysis of apoptotic DNA degradation in C. elegans. Mol. Cell 11 (2003) 987-996
36. Peter A.L., and Viraraghavan T. Thallium: a review of public health and environmental concerns. Environ. Int. 31 (2005) 493-501
37. Pflueger E., Mueller E.A., and Anderer F.A. Preservation of cytotoxic function during multi-cycle immunomagnetic cell separations of human NK cells using a new type of magnetic bead. J. Immunol. Methods 129 (1990) 165-173
38. Provinciali M., Donnini A., Argentati K., Di Stasio G., Bartozzi B., and Bernardini G. Reactive oxygen species modulate Zn(2+)-induced apoptosis in cancer cells. Free Radic. Biol. Med. 32 (2002) 431-445
39. Puga Molina L.C., and Verstraeten S.V. Thallium(III)-mediated changes in membrane physical properties and lipid oxidation affect cardiolipin-cytochrome c interactions. Biochim. Biophys. Acta 1778 (2008) 2157-2164
40. Repetto G., Del Peso A., and Repetto M. Human thallium toxicity. In: Nriagu J. (Ed). Thallium in the Environment. Advances in Environmental Science and Technology (1998) 167-199 Wiley USA
41. Schaub G. Thallium (1996), World Health Organization, Geneva
42. Susin S.A., Daugas E., Ravagnan L., Samejima K., Zamzami N., Loeffler M., Costantini P., Ferri K.F., Irinopoulou T., Prevost M.C., Brothers G., Mak T.W., Penninger J., Earnshaw W.C., and Kroemer G. Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192 (2000) 571-580
43. Vahsen N., Cande C., Briere J.J., Benit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., Feraud O., Debili N., Wissing S., Engelhardt S., Madeo F., Piacentini M., Penninger J.M., Schagger H., Rustin P., and Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J. 23 (2004) 4679-4689
44. van Wijk S.J., and Hageman G.J. Poly(ADP-ribose) polymerase-1 mediated caspase-independent cell death after ischemia/reperfusion. Free Radic. Biol. Med. 39 (2005) 81-90
45. Villaverde M.S., Hanzel C.E., and Verstraeten S.V. In vitro interactions of thallium with components of the glutathione-dependent antioxidant defence system. Free Radic. Res. 38 (2004) 977-984
46. Wu M., Xu L.G., Li X., Zhai Z., and Shu H.B. AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J. Biol. Chem. 277 (2002) 25617-25623
47. Zierold K. Heavy metal cytotoxicity studied by electron probe X-ray microanalysis of cultured rat hepatocytes. Toxicol In Vitro 14 (2000) 557-563