Cadmium induces apoptosis in human embryonic kidney (HEK) 293 cells by caspase-dependent and -independent pathways acting on mitochondria

Toxicology in Vitro

Volumn 21, Issue 3, 2007, Pages 343-354

  Mao, Wei Ping ^a   Ye, Ji Lin ^a   Guan, Zheng Bing ^a   Zhao, Jie Ming ^a   Zhang, Chao ^a   Zhang, Na Na ^a   Jiang, Ping ^a   Tian, Ting ^a  

^a NANJING NORMAL UNIVERSITY   (China)

Author keywords

m; AIF; Apoptosis; Bcl 2; Caspase 3; Cd; Cyt c; HEK 293 cells; Mitochondria; ROS

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; APOPTOSIS INDUCING FACTOR; CADMIUM; CADMIUM CHLORIDE; CASPASE 3; CYTOCHROME C; DNA FRAGMENT; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; CELL DEATH; CELL STRAIN HEK293; CELL STRUCTURE; CYTOPLASM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NEPHROTOXICITY; NUCLEOSOME; PROTEIN EXPRESSION; PROTEIN SECRETION; TIME;

APOPTOSIS; APOPTOSIS INDUCING FACTOR; CADMIUM CHLORIDE; CASPASE 3; CELL LINE; CELL PROLIFERATION; CYTOCHROMES C; DNA FRAGMENTATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; FORMAZANS; HUMANS; KIDNEY; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS C-BCL-2; TETRAZOLIUM SALTS;

EID: 33947430971     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2006.09.004     Document Type: Article

References (48)

1. Ahn H.J., Kim Y.S., Kim J.U., Han S.M., Shin J.W., and Yang H.O. Mechanism of taxol-induced apoptosis in human SKOV3 ovarian carcinoma cells. Journal of Cellular Biochemistry 91 (2004) 1043-1052
2. Budd S.L., Tenneti L., Lishnak T., and Lipton S.A. Mitochondrial and extramitochondrial apoptotic signaling pathways in cerebrocortical neurons. Proceedings of the National Academy of Sciences of USA 97 (2000) 6161-6166
3. Budihardjo I., Oliver H., Lutter M., Luo X., and Wang X. Biochemical pathways of caspase activation during apoptosis. Annual Review of Cell and Developmental Biology 15 (1999) 269-290
4. Carmody R.J., and Cotter T.G. Signalling apoptosis: a radical approach. Redox Report 6 (2001) 77-90
5. 2 and Cd-metallothionein on cultured mesangial cells. Toxicology and Applied Pharmacology 116 (1992) 133-141
6. Daugas E., Susin S.A., Zamzami N., Ferri K.F., Irinopoulou T., Laroch-ette N., Prevost M.C., Leber B., Andrews D., Penninger J., and Kroemer G. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB Journal 14 (2000) 729-739
7. Dlamini Z., Mbita Z., and Zungu M. Genealogy, expression and molecular mechanisms in apoptosis. Pharmacology and Therapeutics 101 (2004) 1-15
8. Evan G.I., and Vousden K.H. Proliferation, cell cycle and apoptosis in cancer. Nature 411 (2001) 342-348
9. Gebhart E., and Rossman T.G. In: Merian E. (Ed). Metals and their Compounds in the Environment (1991), VCH Publishers Inc., New York 617-640
10. Gennari A., Cortese E., Boberi M., Casado J., and Prieto P. Sensitive endpoints for evaluating cadmium-induced acute toxicity in LLC-PK1 cells. Toxicology 183 (2003) 211-220
11. Goyer R.A. Toxic and essential metal interactions. Annual Review of Nutrition 17 (1997) 37-50
12. Hamada T., Tanimoto A., and Sasaguri Y. Apoptosis induced by cadmium. Apoptosis 2 (1997) 359-367
13. Harstad E.B., and Klaassen C.D. Tumor necrosis factor-alpha-null mice are not resistant to cadmium chloride-induced hepatotoxicity. Toxicology and Applied Pharmacology 179 (2002) 155-162
14. Herrmann M., Lorenz H.M., Voll R., Grunke M., Woith W., and Kalden J.R. A rapid and simple method for the isolation of apoptotic DNA fragments. Nuclear Acids Research 22 (1994) 5506-5507
15. IARC (International Agency for Research on Cancer), 1993. Cadmium and cadmium compounds. CAS number 7440-43-9. International Agency for Research on Cancer. Monograph. IARC Press, Lyon.
16. Ishido M., Homma S.T., Leung P.S., and Tohyama C. Cadmium-induced DNA fragmentation is inhibitable by zinc in porcine kidney LLC-PK1 cells. Life Sciences 56 (1995) 351-356
17. Ishido M., Ohtsubo R., Adachi T., and Kunimoto M. Attenuation of both apoptotic and necrotic actions of cadmium by Bcl-2. Environmental Health Prospectives 110 (2002) 37-42
18. Izban K.F., Wrone-Smith T., His E.D., Schnitzer B., Quevedo M.E., and Alkan S. Characterization of the interleukin-1beta-converting enzyme/ced-3-family protease, caspase-3/CPP32, in Hodgkin's disease: lack of caspase-3 expression in nodular lymphocyte predominance Hodgkin's disease. American Journal of Pathology 154 (1999) 1439-1447
19. Joza N., Susin S.A., Daugas E., Stanford W.L., Cho S.K., Li C.Y., Sasaki T., Elia A.J., Cheng H.Y., Ravagnan L., Ferri K.F., Zamzami N., Wakeham A., Hakem R., Yoshida H., Kong Y.Y., Mak T.W., Zuniga-PXucker J.C., Kroemer G., and Penninger J.M. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410 (2001) 549-554
20. Kim M.S., Kim B.J., Woo H.N., Kim K.W., Kim K.B., Kim I.K., and Jung Y.K. Cadmium-induced caspase-mediated cell death: suppression by Bcl-2. Toxicology 145 (2000) 27-37
21. Kondoh M., Araragi S., Sato K., Higashimoto M., Takiguchi M., and Sato M. Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170 (2002) 111-117
22. Lemarié A., Lagadic-Gossmann D., Morzadec C., Allain N., Fardel O., and Vernhet L. Cadmium induces caspase-independent apoptosis in liver Hep3B cells: role for calcium in signaling oxidative stress-related impairment of mitochondria and relocation of endonuclease G and apoptosis-inducing factor. Free Radical Biology and Medicine 36 (2004) 1517-1531
23. 2+-calpain and caspase-mitochondria-dependent pathway. Journal of Biological Chemistry 275 (2000) 39702-39709
24. Liu X., Kim C.N., Yang J., Jemmerson R., and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86 (1996) 147-157
25. Mao W.P., Zhao J.M., Shi X.J., Xu F., Zou X.S., Jiang P., Tian T., and Ye J.L. Mitochondrial pathway in cadmium-induced apoptosis in HEK 293 cells. Chinese Journal of Pharmacology and Toxicology 19 (2005) 305-307
26. Marzo I., Perez-Galan P., Giraldo P., Rubio-felix D., Anel A., and Naval J. Cladribine induces apoptosis in human leukaemia cells by caspase-dependent and -independent pathways acting on mitochondria. Biochemical Journal 359 (2001) 537-546
27. Nordberg G.F. Application of the 'critical effect' and 'critical concentration' concept to human risk assessment for cadmium. IARC Scientific Publications 118 (1992) 3-14
28. Rego A.C., and Oliveira C.R. Mitochondria dysfunction and reactive oxygen species in excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases. Neurochemical Research 28 (2003) 1563-1574
29. Risso-de Faverney C., Devaux A., Lafaurie M., Girard J.P., Bailly B., and Rahmani R. Cadmium induces apoptosis and genotoxicity in rainbow trout hepatocytes through generation of reactive oxygen species. Aquatic Toxicology 53 (2001) 65-76
30. Robertson J.D., and Orrenius S. Molecular mechanisms of apoptosis induced by cytotoxic chemicals. Critical Reviews in Toxicology 30 (2000) 609-627
31. Savolainen H. Cadmium-associated renal disease. Renal Failure 17 (1995) 483-487
32. Shibutani M., Mitsumori K., Niho N., Satoh S., Hiratsuka H., Satoh M., Sumiyoshi M., Nishijima M., Katsuki Y., and Nakagawa. Assessment of renal toxicity by analysis of regeneration of tubular epithelium in rats given low-dose cadmium chloride or cadmium-polluted rice for 22 months. Archives of Toxicology 74 (2000) 571-577
33. Shih C.M., Wu J.S., Ko W.C., Wang L.F., Wei Y.H., Liang H.F., Chen Y.C., and Chen C.T. Mitochondria-mediated caspase-independent apoptosis induced by cadmium in normal human lung cells. Journal of Cellular Biochemistry 89 (2003) 335-347
34. Shih C.M., Ko W.C., Wu J.S., Wei Y.H., Wang L.F., Chang E.E., Lo T.Y., Chen H.H., and Chen C.T. Mediating of caspase-independent apoptosis by cadmium through the mitochondria-ROS pathway in MRC-5 Wbroblasts. Journal of Cellular Biochemistry 91 (2004) 384-397
35. Simon H.U., Haj-Yehia A., and Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5 (2000) 415-418
36. Spector D.L., Goldman R.D., and Leinwand L.A. Cells: A Laboratory Manual (1998), Cold Spring Harbor Laboratory Press, Cold Spring
37. Stinson L.J., Darmon A.J., Dagnino L., and D'Souza S.J. Delayed apoptosis post-cadmium injury in renal proximal tubule epithelial cells. American Journal of Nephrol 23 1 (2003) 27-37
38. Susin S.A., Zamzami N., and Kroemer G. Mitochondria as regulators of apoptosis: doubt no more. Biochimica et biophysica acta 366 (1998) 151-165
39. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., LoeZer M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., and Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397 (1999) 441-446
40. Tan S., Sagara Y., Liu Y., Maher P., and Schubert D. The regulation of reactive oxygen species production during programmed cell death. Journal of Cell Biology 141 (1998) 1423-1432
41. Terui Y., Furukawa Y., Sakoe K., Otha M., and Saito M. Expression of differentiation-related phenotypes and apoptosis are independently regulated during myeloid cell differentiation. Journa of Biochemistry (Tokyo) 117 (1995) 77-84
42. Terui Y., Furukawa Y., Kikuchi J., Iwase S., Hatake K., and Miura Y. Bcl-x is a regulatory factor of apoptosis and differentiation in megakaryocytic lineage cells. Experimental Hematology 26 (1998) 236-244
43. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science 267 (1995) 1456-1462
44. Vander Heiden M.G., Chandel N.S., Williamson E.K., Schumacker P.T., and Thompson C.B. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 91 (1997) 627-637
45. Watanabe M., Henmi K., Ogawa K., and Suzuki T. Cadmium-dependent generation of reactive oxygen species and mitochondrial DNA breaks in photosynthetic and non-photosynthetic strains of Euglena gracilis. Comparative Biochemistry and Physiology C-Toxicology and Pharmacology 134 (2003) 227-234
46. Yu S.W., Wang H., Poitras M.F., Coombs C., Bowers W.J., Federo V H.J., Poirier G.G., Dawson T.M., and Dawson V.L. Mediation of poly (ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297 (2002) 259-263
47. Zhang X., Chen J., Du Graham S.H.L., Kochanek P.M., Draviam R., Guo F., Nathaniel P.D., Szabo C., Watkins S.C., and Clark R.S. Intracellular localisation of apoptosis-inducing factor (AIF) and large scale DNA fragmentation after traumatic brain injury in rats and in neuronal cultures exposed to peroxynitrite. Journal of Neurochemistry 82 (2002) 181-191
48. Zhu H.J., Wang J.S., Guo Q.L., Jiang Y., and Liu G.Q. Reversal of p-glycoprotein mediated multidrug resistance in K562 cell line by a novel synthetic calmodulin inhibitor, E6. Biological and Pharmacology Bulletin 28 (2005) 1974-1978