Mediating of caspase-independent apoptosis by cadmium through the mitochondria-ROS pathway in MRC-5 fibroblasts

Journal of Cellular Biochemistry

Volumn 91, Issue 2, 2004, Pages 384-397

  Shih, Chwen Ming ^a   Ko, Wun Chang ^b   Wu, Jui Sheng ^a   Wei, Yau Huei ^c   Wang, Leng Fang ^a   Chang, E E ^a   Lo, Tsui Yun ^a   Cheng, Huey Hwa ^a   Chen, Chien Tsu ^a  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

AIF; Cadmium; Caspase; ETC; Mitochondria; MPTP; ROS

Indexed keywords

ACETYLCYSTEINE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CADMIUM; DICHLORODIHYDROFLUORESCEIN DIACETATE; HYDROGEN PEROXIDE; MANNITOL; OLIGOMYCIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; TIRON; ANTIOXIDANT; APOPTOSIS INDUCING FACTOR; BENZYLOXYCARBONYLVALYL ALANYL ASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLVALYL-ALANYL-ASPARTYL FLUOROMETHYL KETONE; CASPASE; FLAVOPROTEIN; MEMBRANE PROTEIN; PDCD8 PROTEIN, HUMAN; PEPTIDE CHLOROMETHYL KETONE;

APOPTOSIS; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL; RESPIRATORY CHAIN; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECT; ELECTRON TRANSPORT; LUNG; METABOLISM; PHYSIOLOGY;

AMINO ACID CHLOROMETHYL KETONES; ANTIOXIDANTS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CADMIUM; CASPASES; CELL SURVIVAL; CELLS, CULTURED; ELECTRON TRANSPORT; FIBROBLASTS; FLAVOPROTEINS; HUMANS; HYDROGEN PEROXIDE; LUNG; MEMBRANE PROTEINS; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 5144220858     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.10761     Document Type: Article

References (59)

1. Achanzar WE, Achanzar KB, Lewis JG, Webber MM, Waalkes MP. 2000. Cadmium induces c-myc, p53, and c-jun expression in normal human prostate epithelial cells as a prelude to apoptosis. Toxicol Appl Pharmacol 164:291-300.
2. Arnoult D, Tatischeff I, Estaquier J, Girard M, Sureau F, Tissier JP, Grodet A, Dellinger M, Traincard F, Kahn A, Ameisen JC, Petit PX. 2001. On the evolutionary conservation of the cell death pathway: Mitochondrial release of an apoptosis-inducing factor during Dictyostelium discoideum cell death. Mol Biol Cell 12:3016-3030.
3. Aruoma OI, Halliwell B, Hoey BM, Butler J. 1989. The antioxidant action of N-acetylcysteine: Its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic Biol Med 6:593-597.
4. Biagioli M, Watjen W, Beyersmann D, Zoncu R, Cappellini C, Ragghianti M, Cremisi F, Bucci S. 2001. Cadmium-induced apoptosis in murine fibroblast is suppressed by Bcl-2. Arch Toxicol 75:313-320.
5. Borner C. Monney L. 1999. Apoptosis without caspases: An inefficient molecular guillotine? Cell Death Differ 6:497-507.
6. Braun JS, Novak R, Murray PJ, Eischen CM, Susin SA, Kroemer G, Halle A, Weber JR, Tuomanen EI, Cleveland JL. 2001. Apoptosis-inducing factor mediates microglial and neuronal apoptosis caused by pneumococcus. J Infect Dis 184:1300-1309.
7. Buchet K, Godinot C. 1998. Functional F1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted rho degrees cells. J Biol Chem 273:22983-22989.
8. Cande C, Cohen I, Daugas E, Ravagnan L, Larochette N, Zamzami N, Kroemer G. 2002. Apoptosis-inducing factor (AIF): A novel caspase-independent death effector released from mitochondria. Biochimie 84:215-222.
9. Carmody RJ, Cotter TG. 2000. Oxidative stress induces caspase-independent retinal apoptosis in vitro. Cell Death Differ 7:282-291.
10. Castedo M, Ferri K, Roumier T, Motivier D, Zamzami N, Kroemer G. 2002. Quantitation of mitochondrial alterations associated with apoptosis. J Immunol Methods 265:39-47.
11. Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C. 1993. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′- tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 197:40-45.
12. Creagh EM, Carmody RJ, Cotter TG. 2000. Heat shock protein 70 inhibits caspase-dependent and -independent apoptosis in Jurkat T cells. Exp Cell Res 257:58-66.
13. Davison AG, Fayers PM, Taylor AJ, Venables KM, Darbyshire J, Pickering CA, Chettle DR, Franklin D, Guthrie CJ, Scott MC. 1988. Cadmium fume inhalation and emphysema. Lancet 1:663-667.
14. Degli EM. 1998. Inhibitors of NADH-ubiquinone reductase: An overview. Biochim Biophys Acta 1364:222-235.
15. Dumont C, Durrbach A, Bidere N, Rouleau M, Kroemer G, Bernard G, Hirsch F, Charpentier B, Susin SA, Senik A. 2000. Caspase-independent commitment phase to apoptosis in activated blood T lymphocyte: Reversibility at low apoptotic insult. Blood 96:1030-1038.
16. Fadeel B, Orrenius S, Zhivotovsky B. 1999. Apoptosis in human disease: A new skin for the old ceremony? Biochem Biophys Res Commun 266:699-717.
17. Goyer RA, Cherian MG. 1995. Renal effects of metals. In: Goyer RA, Klaassen CD, Waalkes MP, editors. Metal toxicology. San Diego: Academic Press, pp 389-412.
18. Hail N, Jr., Youssef EM, Lotan R. 2001. Evidence supporting a role for mitochondrial respiration in apoptosis induction by the synthetic retinoid CD437. Cancer Res 61:6698-6702.
19. Harstad EB, Klaassen CD. 2002. Tumor necrosis factor-α-null mice are not resistant to cadmium chloride-induced hepatotoxicity. Toxicol Appl Pharmacol 179:155-162.
20. Hart BA, Lee CH, Shukla GS, Shukla A, Osier M, Eneman JD, Chiu JF. 1999. Characterization of cadmium-induced apoptosis in rat lung epithelial cells: Evidence for the participation of oxidant stress. Toxicology 133:43-58.
21. Ink B, Zornig M, Baum B, Hjibagheri N, James C, Chittenden T, Evan G. 1997. Human Bak induces cell death in Schizosaccharomyces pombe with morphological changes similar to those with apoptosis in mammalian cells. Mol Cell Biol 17:2468-2474.
22. 1 cells. J Pharmacol Exp Ther 290:923-928.
23. Jackson GR, Salecker I, Dong X, Yao X, Arnheim N, Faber PW, MacDonald ME, Zipursky SL. 1998. Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 21:633-642.
24. Jacobs JP, Jones CM, Baille JP. 1970. Characteristics of a human diploid cell designated MRC-5. Nature 227:168-170.
25. Jones BE, Lo C-R, Liu H, Srinivasan A, Streetz K, Valentino KL, Czaja MJ. 2000. Hepatocytes sensitized to tumor necrosis factor-alpha cytotoxicity undergo apoptosis through caspase-dependent and caspase-independent pathways. J Biol Chem 275:705-712.
26. Kim MS, Kim BJ, Woo HN, Kim KW, Kim KB, Kim IK, Jung YK. 2000. Cadmium induces caspase-mediated cell death: Suppression by Bcl-2. Toxicology 145:27-37.
27. Kohler C, Orrenius S, Zhivotovsky B. 2002. Evaluation of caspase activity in apoptotic cells. J Immunol Methods 265:97-110.
28. Kondoh M, Araragi S, Sato K, Higashimoto M, Takiguchi M, Sato M. 2002. Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170:111-117.
29. Ledenev AN, Konstantinov AA, Popova E, Ruuge EK. 1986. A simple assay of the superoxide generation rate with tiron as an EPR-visible radical scavenger. Biochem Int 13:391-396.
30. 2+-calpain and caspase-mitochodria-dependent pathways. J Biol Chem 275:39702-39709.
31. Li LY, Luo X, Wang X. 2001. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412:95-99.
32. Loeffler M, Daugas E, Susin SA, Zamzami N, Metivier D, Nieminen AL, Brothers G, Penninger JM, Kroemer G. 2001. Dominant cell death induction by extramitochondrially targeted apoptosis-inducing factor. FASEB J 15:758-767.
33. Magovern GJ, Jr., Bolling SF, Casale AS, Bulkley BH, Gardner TJ. 1984. The mechanism of mannitol in reducing ischemic injury: Hyperosmolarity or hydroxyl scavenger? Circulation 70:191-195.
34. Martel J, Marion M, Denizeau F. 1990. Effect of cadmium on membrane potential in isolated rat hepatocytes. Toxicology 60:161-172.
35. Marzo I, Perez-Galan P, Giraldo P, Rubio-Felix D, Anel A, Naval J. 2001. Cladribine induces apoptosis in human leukaemia cells by caspase-dependent and -independent pathways acting on mitochondria. Biochem J 359:537-546.
36. Mate MJ, Ortiz-Lombardia M, Boitel B, Haouz A, Tello D, Susin SA, Penninger J, Kroemer G, Alzari PM. 2002. The crystal structure of the mouse apoptosis-inducing factor AIF. Nat Struct Biol 9:442-446.
37. Miller LK. 1997. Baculovirus interaction with host apoptotic pathway. J Cell Physiol 173:178-182.
38. Nordberg GF. 1992. Application of the 'critical effect' and 'critical concentration' concept to human risk assessment for cadmium. In: Nordberg GF, Herber RMF, Allesio L, editors. Cadmium in the human environment: Toxicity and carcinogenecity. Lyon: IARC Sci Publ. pp 3-14.
39. Ormerod MG, Collins MK, Rodriguez-Tarduchy G, Robertson D. 1992. Apoptosis in interleukin-3-dependent haemopoietic cells. Quantification by two flow cytometric methods. J Immunol Methods 153:57-65.
40. Pietra G, Mortarini R, Parmiani G, Anichini A. 2001. Phases of apoptosis of melanoma cells, but not of normal melanocytes, differently affect maturation of myeloid dendritic cells. Cancer Res 61:8218-8226.
41. Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jaattela M, Penninger JM, Garrido C, Kroemer G. 2001. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3:839-843.
42. Ravagnan L, Roumier T, Kroemer G. 2002. Mitochondria, the killer organelles and their weapons. J Cell Physiol 192:131-137.
43. Risso-de Faverney C, Devaux A, Lafaurie M, Girard JP, Bailly B, Rahmani R. 2001. Cadmium induces apoptosis and genotoxicity in rainbow trout hepatocytes through generation of reactive oxygen species. Aquat Toxicol 53:65-76.
44. Robertson JD, Orrenius S. 2000. Molecular mechanisms of apoptosis induced by cytotoxic chemicals. Crit Rev Toxicol 30:609-627.
45. Saikumar P, Dong Z, Mikhailov V, Denton M, Weinberg JM, Venkatachalam MA. 1999. Apoptosis: Definition, mechanisms, and relevance to disease. Am J Med 107:489-506.
46. Shen HM, Dong SY, Ong CN. 2001. Critical role of calcium overloading in cadmium-induced apoptosis in mouse thymocytes. Toxicol Appl Pharmacol 171:12-19.
47. Shigenaga MK, Hagen TM, Ames BN. 1994. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci USA 91:10771-10778.
48. Stohs SJ, Bagchi D. 1995. Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321-336.
49. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
50. Susin SA, Daugas E, Ravagnan L, Samejima K, Zamzami N, Loeffler M, Costantini P, Ferri KF, Irinopoulou T, Prevost M-C, Brothers G, Mak TW, Penninger J, Earnshaw WC, Kroemer G. 2000. Two distinct pathways leading to nuclear apoptosis. J Exp Med 192:571-580.
51. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. 2001. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8:613-621.
52. Takeyama N, Miki S, Hirakawa A, Tanaka T. 2002. Role of the mitochondrial permeability transition and cytochrome c release in hydrogen peroxide-induced apoptosis. Exp Cell Res 274:16-24.
53. Van Engeland M, Ramaekers FC, Schutte B, Reutelingsperger CP. 1996. A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 24:131-139.
54. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. 1995. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein-labeled Annexin V. J Immunol Methods 184:39-5.
55. Xanthoudakis S, Nicholson DW. 2000. Heat-shock proteins as death determinants. Nat Cell Biol 2:E163-E165.
56. Xue D, Horvitz HR. 1995. Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377:248-251.
57. Yang CF, Shen HM, Shen Y, Zhuang ZX, Ong CN. 1997. Cadmium-induced oxidative cellular damage in human fetal lung fibroblasts (MRC-5 cells). Environ Health Perspect 105:712-716.
58. Yuan C, Kadiiska M, Achanzar WE, Mason RP, Waalkes MP. 2000. Possible role of caspase-3 inhibition in cadmium-induced blockage of apoptosis. Toxicol Appl Pharmacol 164:321-329.
59. Zamzami N, Kroemer G. 1999. Apoptosis: Condensed matter in cell death. Nature 401:127-128.