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Archives of Toxicology

, Volume 87, Issue 7, pp 1157–1180 | Cite as

Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis

  • Krishnendu Sinha
  • Joydeep Das
  • Pabitra Bikash Pal
  • Parames C. Sil
Review Article

Abstract

Oxidative stress basically defines a condition in which prooxidant–antioxidant balance in the cell is disturbed; cellular biomolecules undergo severe oxidative damage, ultimately compromising cells viability. In recent years, a number of studies have shown that oxidative stress could cause cellular apoptosis via both the mitochondria-dependent and mitochondria-independent pathways. Since these pathways are directly related to the survival or death of various cell types in normal as well as pathophysiological situations, a clear picture of these pathways for various active molecules in their biological functions would help designing novel therapeutic strategy. This review highlights the basic mechanisms of ROS production and their sites of formation; detail mechanism of both mitochondria-dependent and mitochondria-independent pathways of apoptosis as well as their regulation by ROS. Emphasis has been given on the redox-sensitive ASK1 signalosome and its downstream JNK pathway. This review also describes the involvement of oxidative stress under various environmental toxin- and drug-induced organ pathophysiology and diabetes-mediated apoptosis. We believe that this review would provide useful information about the most recent progress in understanding the mechanism of oxidative stress–mediated regulation of apoptotic pathways. It will also help to figure out the complex cross-talks between these pathways and their modulations by oxidative stress. The literature will also shed a light on the blind alleys of this field to be explored. Finally, readers would know about the ROS-regulated and apoptosis-mediated organ pathophysiology which might help to find their probable remedies in future.

Keywords

Oxidative stress Apoptosis Mitochondria-dependent pathway Mitochondria-independent pathway ASK1-JNK signaling Pathophysiology 

Notes

Acknowledgments

Krishnendu Sinha acknowledges the Indian Council of Medical Research (ICMR) for providing financial assistance in the form of a fellowship.

References

  1. Aikens J, Dix TA (1991) Perhydroxyl radical (HOO·) Initiated lipid-peroxidation-The role of fatty-acid hydroperoxides. J Biol Chem 266:15091–15098PubMedGoogle Scholar
  2. Ambrosio G, Zweierj JL, Duilio C, Kuppusamy P et al (1993) Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem 268:18532–18541PubMedGoogle Scholar
  3. Ames BN, Gold LS, Willett WC (1995) The causes and prevention of cancer. Proc Natl Acad Sci USA 92:5258–5265PubMedCrossRefGoogle Scholar
  4. Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 70:200–214PubMedGoogle Scholar
  5. Andrus PK, Fleck TJ, Gurney ME, Hall ED (1998) Protein oxidative damage in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neuro chem 71:2041–2048CrossRefGoogle Scholar
  6. Antinozzi PA, Ishihara H, Newgard CB, Wollheim CB (2002) Mitochondrial metabolism sets the maximal limit of fuel-stimulated insulin secretion in a model pancreatic beta cell: a survey of four fuel secretagogues. J Biol Chem 277:11746–11755PubMedCrossRefGoogle Scholar
  7. Aoki H, Kang PM, Hampe J, Yoshimura K, Noma T, Matsuzaki M et al (2002) Direct activation of mitochondrial apoptosis machinery by c-Jun N-terminal kinase in adult cardiac myocytes. J Biol Chem 277:10244–10250PubMedCrossRefGoogle Scholar
  8. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281:1305–1308PubMedCrossRefGoogle Scholar
  9. Barnhart BC, Alappat EC, Peter ME (2003) The CD95 type I/type II model. Semin Immunol 15:185–193PubMedCrossRefGoogle Scholar
  10. Barone MC, Desouza LA, Freeman RS (2008) Pin1 promotes cell death in NGF-dependent neurons through a mechanism requiring c-Jun activity. J Neurochem 106:734–745PubMedCrossRefGoogle Scholar
  11. Baynes JW, Thorpe SR (1999) Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48:1–9PubMedCrossRefGoogle Scholar
  12. Behl C (1999) Alzheimer’s disease and oxidative stress implications for novel therapeutic approaches. Prog Neurobiol 57:301–323PubMedCrossRefGoogle Scholar
  13. Behrens A, Sibilia M, Wagner EF (1999) Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 21:326–329PubMedCrossRefGoogle Scholar
  14. Bhattacharjee R, Sil PC (2007) Protein isolate from the herb, Phyllanthus niruri L. (Euphorbiaceae), plays hepatoprotective role against carbon tetrachloride induced liver damage via its antioxidant properties. Food Chem Toxicol 45:817–826PubMedCrossRefGoogle Scholar
  15. Bhattacharya S, Manna P, Gachhui R, Sil PC (2011) Article title: D-saccharic acid-1,4-lactone ameliorates alloxan-induced Diabetes mellitus and oxidative stress in rats through inhibiting pancreatic beta-cells from apoptosis via mitochondrial dependent pathway. Toxicol Appl Pharmacol 257:272–283PubMedCrossRefGoogle Scholar
  16. Bhattacharya S, Manna P, Gachhui R, Sil PC (2013a) D-saccharic acid 1,4-lactone protects diabetic rat kidney by ameliorating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via NF-κB and PKC signaling. Toxicol Appl Pharmacol 267:16–29PubMedCrossRefGoogle Scholar
  17. Bhattacharya S, Gachhui R, Sil PC (2013b) The prophylactic role of d-saccharic acid-1,4-lactone against hyperglycemia-induced hepatic apoptosis via inhibition of both extrinsic and intrinsic pathways in diabetic rats. Food Funct 4:283–296PubMedCrossRefGoogle Scholar
  18. Bhattacharyya S, Ghosh J, Sil PC (2012) Iron induces hepatocytes death via MAPK activation and mitochondria-dependent apoptotic pathway: beneficial role of glycine. Free Radic Res 46:1296–1307PubMedCrossRefGoogle Scholar
  19. Bilinski T, Litwinska J, Blaszczynski M, Bajus A (1989) Superoxide dismutase deficiency and the toxicity of the products of auto-oxidation of polyunsaturated fatty acids in yeast. Biochem Biophys Acta 1001:102–106PubMedCrossRefGoogle Scholar
  20. Boatright KM, Salvesen GS (2003) Mechanisms of caspase activation. Curr Opin Cell Biol 15:725–731PubMedCrossRefGoogle Scholar
  21. Borges F, Fernandes E, Roleira F (2002) Progress towards the discovery of xanthine oxidase inhibitors. Curr Med Chem 9:195–217PubMedCrossRefGoogle Scholar
  22. Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, Parker N (2004) Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med 37:755–767PubMedCrossRefGoogle Scholar
  23. Bustamante J, Nutt L, Orrenius S, Gogvadze V (2005) Arsenic stimulates release of cytochrome c from isolated mitochondria via induction of mitochondrial permeability transition. Toxicol Appl Pharmacol 207:110–116PubMedCrossRefGoogle Scholar
  24. Cabiscol E, Piulats E, Echave P, Herrero E, Ros J (2000) Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J Biol Chem 35:27393–27398Google Scholar
  25. Casalino E, Sblano C, Landriscina C (1997) Enzyme activity alteration by cadmium administration to rats: the possibility of iron involvement in lipid peroxidation. Arch Biochem Biophys 346:171–179Google Scholar
  26. Ceriello A (2000) Oxidative stress and glycemic regulation. Metabolism 49:27–29PubMedCrossRefGoogle Scholar
  27. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605PubMedGoogle Scholar
  28. Chang L, Kamata H, Solinas G, Luo J-L, Maeda S, Venuprasad K, Liu Y-C, Karin M (2006) The E3 ubiquitin ligase itch couples JNK activation to TNFα-induced cell death by inducing c-FLIPL turnover. Cell 124:3601–3613Google Scholar
  29. Chang L, Karin M (2001) Mammalian MAP kinase signaling cascades. Nature 410:37–40PubMedCrossRefGoogle Scholar
  30. Chang HY, Nishitoh H, Yang X, Ichijo H, Baltimore D (1998) Activation of apoptosis signal-regulating kinase 1 (ASK1) by the adapter protein Daxx. Science 281:1860–1863PubMedCrossRefGoogle Scholar
  31. Chatterjee M, Sil PC (2006) Hepatoprotective effect of aqueous extract of Phyllanthus niruri on nimesulide-induced oxidative stress in vivo. Indian J Biochem Biophys 43:299–305PubMedGoogle Scholar
  32. Chatterjee M, Sil PC (2007) Protective role of Phyllanthus niruri against nimesulide induced hepatic damage. Indian J Clin Biochem 22:109–116PubMedCrossRefGoogle Scholar
  33. Chatterjee M, Sarkar K, Sil PC (2006) Herbal (Phyllanthus niruri) protein isolate protects liver from nimesulide induced oxidative stress. Pathophysiology 13:95–102PubMedCrossRefGoogle Scholar
  34. Chauhan D, Li G, Hideshima T, Podar K, Mitsiades C, Mitsiades N et al (2003) JNK-dependent release of mitochondrial protein, Smac, during apoptosis in multiple myeloma (MM) cells. J Biol Chem 278:17593–17596PubMedCrossRefGoogle Scholar
  35. Chen YR, Wang X, Templeton D, Davis RJ, Tan TH (1996) The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and γ radiation. Duration of JNK activation may determine cell death and proliferation. J Biol Chem 271:31929–31936PubMedCrossRefGoogle Scholar
  36. Circu ML, Aw TY (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48:749–762PubMedCrossRefGoogle Scholar
  37. Circu ML, Moyer MP, Harrison L, Aw TY (2009) Contribution of glutathione status to oxidant-induced mitochondrial DNA damage in colonic epithelial cells. Free Radic Biol Med 47:1190–1198PubMedCrossRefGoogle Scholar
  38. Circu ML et al (2012) Glutathione and modulation of cell apoptosis. Biochim Biophys Acta 1823:1767–1777PubMedCrossRefGoogle Scholar
  39. Ciuchi E, Odetti P, Prando R (1996) Relationship between glutathione and sorbitol concentrations in erythrocytes from diabetic patients. Metabolism 45:611–613PubMedCrossRefGoogle Scholar
  40. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656PubMedCrossRefGoogle Scholar
  41. D’Emilio A, Biagiotti L, Burattini S et al (2010) Morphological and biochemical patterns in skeletal muscle apoptosis. Histol Histopathol 25:21–32PubMedGoogle Scholar
  42. Das J, Sil PC (2012) Taurine ameliorates alloxan-induced diabetic renal injury, oxidative stress related signaling pathways and apoptosis in rats. Amino Acids 43:1509–1523PubMedCrossRefGoogle Scholar
  43. Das J, Ghosh J, Manna P, Sil PC (2008) Taurine provides antioxidant defense against NaF-induced cytotoxicity in murine hepatocytes. Pathophysiology 15:181–190PubMedCrossRefGoogle Scholar
  44. Das J, Ghosh J, Manna P, Sinha M, Sil PC (2009a) Arsenic-induced oxidative cerebral disorders: protection by taurine. Drug Chem Toxicol 32:93–102PubMedCrossRefGoogle Scholar
  45. Das J, Ghosh J, Manna P, Sinha M, Sil PC (2009b) Taurine protects rat testes against NaAsO2-induced oxidative stress and apoptosis via mitochondrial dependent and independent pathways. Toxicol Lett 187:201–210PubMedCrossRefGoogle Scholar
  46. Das J, Ghosh J, Manna P, Sil PC (2010a) Taurine protects acetaminophen-induced oxidative damage in mice kidney through APAP urinary excretion and CYP2E1 inactivation. Toxicology 269:24–34PubMedCrossRefGoogle Scholar
  47. Das J, Ghosh J, Manna P, Sil PC (2010b) Protective role of taurine against arsenic-induced mitochondria-dependent hepatic apoptosis via the inhibition of PKCδ-JNK pathway. PLoS ONE 5:e12602PubMedCrossRefGoogle Scholar
  48. Das J, Ghosh J, Manna P, Sil PC (2010c) Acetaminophen induced acute liver failure via oxidative stress and JNK activation: protective role of taurine by the suppression of cytochrome P450 2E1. Free Radic Res 44:340–355PubMedCrossRefGoogle Scholar
  49. Das J, Ghosh J, Manna P, Sil PC (2011) Taurine suppresses doxorubicin-triggered oxidative stress and cardiac apoptosis in rat via up-regulation of PI3-K/Akt and inhibition of p53, p38-JNK. Biochem Pharmacol 81:891–909PubMedCrossRefGoogle Scholar
  50. Das J, Ghosh J, Manna P, Sil PC (2012a) Taurine protects rat testes against doxorubicin-induced oxidative stress as well as p53, Fas and caspase 12-mediated apoptosis. Amino Acids 42:1839–1855PubMedCrossRefGoogle Scholar
  51. Das J, Ghosh J, Roy A, Sil PC (2012b) Mangiferin exerts hepatoprotective activity against D-galactosamine induced acute toxicity and oxidative/nitrosative stress via Nrf2-NFκB pathways. Toxicol Appl Pharmacol 260:35–47PubMedCrossRefGoogle Scholar
  52. Das J, Roy A, Sil PC (2012c) Mechanism of the protective action of taurine in toxin and drug induced organ pathophysiology and diabetic complications: a review. Food Funct 3:1251–1264PubMedCrossRefGoogle Scholar
  53. Das J, Vasan V, Sil PC (2012d) Taurine exerts hypoglycemic effect in alloxan-induced diabetic rats, improves insulin-mediated glucose transport signaling pathway in heart and ameliorates cardiac oxidative stress and apoptosis. Toxicol Appl Pharmacol 258:296–308PubMedCrossRefGoogle Scholar
  54. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239–252PubMedCrossRefGoogle Scholar
  55. De Grey AD (2002) HO2·: the forgotten radical. DNA Cell Biol 21:251–257PubMedCrossRefGoogle Scholar
  56. Deng Y, Ren X, Yang L, Lin Y, Wu XA (2003) JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 115:61–70PubMedCrossRefGoogle Scholar
  57. Dhanasekaran DN, Johnson GL (2007) MAPKs: function, regulation, role in cancer and therapeutic targeting. Oncogene 26:3097–3099PubMedCrossRefGoogle Scholar
  58. Dhanasekaran N, Reddy EP (1998) Signaling by dual specificity kinases. Oncogene 17:1447–1755PubMedCrossRefGoogle Scholar
  59. Dhanasekaran DN, Reddy EP (2008) JNK signaling in apoptosis. Oncogene 27:6245–6251Google Scholar
  60. Donovan N, Becker EB, Konishi Y, Bonni A (2002) JNK phosphorylation and activation of BAD couples the stress-activated signaling pathway to the cell death machinery. J Biol Chem 277:40944–40949PubMedCrossRefGoogle Scholar
  61. Dorion S, Lambert H, Landry J (2002) Activation of the p38 signaling pathway by heat shock involves the dissociation of glutathione S-transferase Mu from Ask1. J Biol Chem 277:30792–30797PubMedCrossRefGoogle Scholar
  62. Du XL (2000) Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci USA 97:12222–12226PubMedCrossRefGoogle Scholar
  63. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516Google Scholar
  64. Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal induced oxidative damage. Curr Top Med Chem 1:529-539Google Scholar
  65. Essers MA, Weijzen S, Vries-Smits AM, Saarloos I, de Ruiter ND, Bos JL, Burgering BM (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 23:4802–4812PubMedCrossRefGoogle Scholar
  66. Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2002) Oxidative stress and stress-activated signalling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23:599–622PubMedCrossRefGoogle Scholar
  67. Evtodienko YV, Teplova VV, Azarashvily TS, Kudin A et al (1999) The Ca2+ threshold for the mitochondrial permeability transition and the content of proteins related to Bcl-2 in rat liver and Zajdela hepatoma mitochondria. Mol Cell Biochem 194:251–256PubMedCrossRefGoogle Scholar
  68. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148:2207–2216PubMedGoogle Scholar
  69. Fan M, Chambers TC (2001) Role of mitogen-activated protein kinases in the response of tumor cells to chemotherapy. Drug Resist Updat 4:253–267PubMedCrossRefGoogle Scholar
  70. Farrugia G, Balzan R (2012) Oxidative stress and programmed cell death in yeast. Front Oncol 2:64PubMedCrossRefGoogle Scholar
  71. Finkel T (2003) Oxidant signals and oxidative stress. Curr Opin Cell Biol 15:247–254PubMedCrossRefGoogle Scholar
  72. Fuchs SY, Adler V, Pincus MR, Ronai Z (1998) MEKK1/JNK signaling stabilizes and activates p53. Proc Natl Acad Sci USA 95:10541–10546PubMedCrossRefGoogle Scholar
  73. Fujino G, Noguchi T, Takeda K, Ichijo H (2006) Thioredoxin and protein kinases in redox signaling. Semin Cancer Biol 16:427–435PubMedCrossRefGoogle Scholar
  74. Fujino G, Noguchi T, Matsuzawa A, Yamauchi S, Saitoh M, Takeda K et al (2007) Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol Cell Biol 27:8152–8163PubMedCrossRefGoogle Scholar
  75. Fukuyo Y, Kitamura T, Inoue M, Horikoshi NT, Higashikubo R, Hunt CR et al (2009) Phosphorylation-dependent Lys63-linked polyubiquitination of Daxx is essential for sustained TNF-{alpha}-induced ASK1 activation. Cancer Res 69:7512–7517PubMedCrossRefGoogle Scholar
  76. Gabai VL, Yaglom JA, Volloch V et al (2000) Hsp72-mediated suppression of c-Jun N-terminal kinase is implicated in development of tolerance to caspase-independent cell death. Mol Cell Biol 20:6826–6836PubMedCrossRefGoogle Scholar
  77. Ghosh A, Sil PC (2007) Anti-oxidative effect of a protein from Cajanus indicus L against acetaminophen-induced hepato-nephro toxicity. J Biochem Mol Biol 40:1039–1049PubMedCrossRefGoogle Scholar
  78. Ghosh A, Sil PC (2008) A protein from Cajanus indicus Spreng protects liver and kidney against mercuric chloride-induced oxidative stress. Biol Pharm Bull 31:1651–1658PubMedCrossRefGoogle Scholar
  79. Ghosh A, Sil PC (2009) Protection of acetaminophen induced mitochondrial dysfunctions and hepatic necrosis via Akt-NF-κB pathway: Role of a novel plant protein. Chem Biol Interact 177:96–106PubMedCrossRefGoogle Scholar
  80. Ghosh J, Das J, Manna P, Sil PC (2009) Taurine prevents arsenic-induced cardiac oxidative stress and apoptotic damage: role of NF-kappaB, p38 and JNK MAPK pathway. Toxicol Appl Pharmacol 240:73–87PubMedCrossRefGoogle Scholar
  81. Ghosh J, Das J, Manna P, Sil PC (2010a) Acetaminophen induced renal injury via oxidative stress and TNF-alpha production: therapeutic potential of arjunolic acid. Toxicology 268:8–18PubMedCrossRefGoogle Scholar
  82. Ghosh J, Das J, Manna P, Sil PC (2010b) Hepatotoxicity of di-(2-ethylhexyl)phthalate is attributed to calcium aggravation, ROS-mediated mitochondrial depolarization, and ERK/NF-κB pathway activation. Free Radic Biol Med 49:1779–1791PubMedCrossRefGoogle Scholar
  83. Ghosh J, Das J, Manna P, Sil PC (2010c) Protective effect of the fruits of Terminalia arjuna against cadmium-induced oxidant stress and hepatic cell injury via MAPK activation and mitochondria dependent pathway. Food Chem 123:1062–1075CrossRefGoogle Scholar
  84. Ghosh J, Das J, Manna P, Sil PC (2010d) Arjunolic acid, a triterpenoid saponin, prevents acetaminophen (APAP)-induced liver and hepatocyte injury via the inhibition of APAP bioactivation and JNK-mediated mitochondrial protection. Free Radic Biol Med 48:535–553PubMedCrossRefGoogle Scholar
  85. Ghosh J, Das J, Manna P, Sil PC (2011a) The protective role of arjunolic acid against doxorubicin induced intracellular ROS dependent JNK-p38 and p53 mediated cardiac apoptosis. Biomaterials 32:4857–4866PubMedCrossRefGoogle Scholar
  86. Ghosh M, Manna P, Sil PC (2011b) Protective role of a coumarin derived schiff base scaffold against TBHP induced oxidative impairment and cell death via MAPKs, NF-κB and mitochondria dependent pathways. Free Radic Res 45:620–637PubMedCrossRefGoogle Scholar
  87. Ghosh M, Das J, Sil PC (2012) D(+) galactosamine induced oxidative and nitrosative stress-mediated renal damage in rats via NF-κB and inducible nitric oxide synthase (iNOS) pathways is ameliorated by a polyphenol xanthone, mangiferin. Free Radic Res 46:116–132PubMedCrossRefGoogle Scholar
  88. Gille G, Sigler K (1995) Oxidative stress and living cells. Folia Microbiol (Praha) 40:131–152CrossRefGoogle Scholar
  89. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M et al (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122:221–233PubMedCrossRefGoogle Scholar
  90. Goldman EH, Chen L, Fu H (2004) Activation of apoptosis signal-regulating kinase 1 by reactive oxygen species through dephosphorylation at serine 967 and 14–3-3 dissociation. J Biol Chem 279:10442–10449PubMedCrossRefGoogle Scholar
  91. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626–629PubMedCrossRefGoogle Scholar
  92. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312PubMedCrossRefGoogle Scholar
  93. Gross A, McDonnell JM, Korsmeyer SJ (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13:1899–1911PubMedCrossRefGoogle Scholar
  94. Guo M, Hay BA (1999) Cell proliferation and apoptosis. Curr Opin Cell Biol 11(6):745–752PubMedCrossRefGoogle Scholar
  95. Guo YL, Baysal K, Kang B, Yang LJ, Williamson JR (1998) Correlation between sustained c-Jun N-terminal protein kinase activation and apoptosis induced by tumor necrosis factor-α in rat mesangial cells. J Biol Chem 273:4027–4034PubMedCrossRefGoogle Scholar
  96. Hagenbuchner J, Kuznetsov A, Hermann M, Hausott B, Obexer P, Ausserlechner MJ (2012) FOXO3-induced reactive oxygen species are regulated by BCL2L11 (Bim) and SESN3. J Cell Sci 125:1191–1203PubMedCrossRefGoogle Scholar
  97. Halliwell B, Cross CE (1994) Oxygen-derived species: their relation to human disease and environmental stress. Environ Health Perspect 10:5–12Google Scholar
  98. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, OxfordGoogle Scholar
  99. Hattori K, Naguro I, Runchel C, Ichijo H (2009) The roles of ASK family proteins in stress responses and diseases. Cell Commun Signal 7:9. doi: 10.1186/1478-811X-7-9 PubMedCrossRefGoogle Scholar
  100. Hirsch EC (1993) Does oxidative stress participates in nerve cell death in Parkinson’s disease? Eur Neurol 33:52–59PubMedCrossRefGoogle Scholar
  101. Hirsch T, Marchetti P, Susin SA, Dallaporta B, Zamzami N, Marzo I, Geuskens M, Kroemer G (1997) The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15:1573–1581PubMedCrossRefGoogle Scholar
  102. Hitoshi Y, Lorens J, Kitada SI, Fisher J, LaBarge M, Ring HZ, Francke U, Reed JC, Kinoshita S, Nolan GP (1998) Toso, a cell surface, specific regulator of Fas-induced apoptosis in T cells. Immunity 8:461–471PubMedCrossRefGoogle Scholar
  103. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE (2009) Cell death. N Engl J Med 361:1570–1583PubMedCrossRefGoogle Scholar
  104. Hsu H, Xiong J, Goeddel DV (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81:495–504PubMedCrossRefGoogle Scholar
  105. Huang X, Masselli A, Frisch SM, Hunton IC, Jiang Y, Wang JY (2007) Blockade of tumor necrosis factor-induced Bid cleavage by caspase-resistant Rb. J Biol Chem 282:29401–29413PubMedCrossRefGoogle Scholar
  106. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T et al (1997) Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90–94PubMedCrossRefGoogle Scholar
  107. Jiang Y, Woronicz JD, Liu W, Goeddel DV (1999) Prevention of constitutive TNF receptor 1 signaling by silencer of death domains. Science 283:543–546PubMedCrossRefGoogle Scholar
  108. Johnson GL, Nakamura K (2007) The c-jun kinase/stress-activated pathway: regulation, function and role in human disease. Biochim Biophys Acta 1773:1341–1348PubMedCrossRefGoogle Scholar
  109. Jones EV, Dickman MJ, Whitmarsh AJ (2007) Regulation of p73- mediated apoptosis by c-Jun N-terminal kinase. Biochem J 405:617–623PubMedCrossRefGoogle Scholar
  110. Kagan VE, Tyurin VA, Jiang J, Tyurina YY et al (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1:223–232PubMedCrossRefGoogle Scholar
  111. Kam PCA, Ferch NI (2000) Apoptosis: mechanisms and clinical implications. Anaesthesia 55:1081–1093PubMedCrossRefGoogle Scholar
  112. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M (2005) Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120:649–661PubMedCrossRefGoogle Scholar
  113. Karin M, Lin A (2002) NF-κB at the crossroads of life and death. Nat Immunol 3:221–227PubMedCrossRefGoogle Scholar
  114. Kaufmann SH, Earnshaw WC (2000) Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256:42–49PubMedCrossRefGoogle Scholar
  115. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257PubMedCrossRefGoogle Scholar
  116. Kharbanda S, Saxena S, Yoshida K, Pandey P, Kaneki M, Wang Q et al (2000) Translocation of SAPK/JNK to mitochondria and interaction with Bcl-x(L) in response to DNA damage. J Biol Chem 275:322–327PubMedCrossRefGoogle Scholar
  117. Khawaja NR, Carrè M, Kovacic H, Estève MA, Braguer D (2008) Patupilone-induced apoptosis is mediated by mitochondrial reactive oxygen species through bim relocalization to mitochondria. Mol Pharmacol 74:1072–1083PubMedCrossRefGoogle Scholar
  118. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14:5579–5588PubMedGoogle Scholar
  119. Kolomeichuk SN, Terrano DT, Lyle CS, Sabapathy K, Chambers TC (2008) Distinct signaling pathways of microtubule inhibitors–vinblastine and Taxol induce JNK-dependent cell death but through AP-1-dependent and AP-1-independent mechanisms, respectively. FEBS J 275:1889–1899PubMedCrossRefGoogle Scholar
  120. Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15–18PubMedCrossRefGoogle Scholar
  121. Kothakota S, Azuma T, Reinhard C, Klippel A, Tang J, Chu K, McGarry TJ, Kirschner MW, Koths K, Kwiatkowski DJ, Williams LT (1997) Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278:294–298PubMedCrossRefGoogle Scholar
  122. Kovacic P, Pozos RS, Somanathan R, Shangari N, O’Brien PJ (2005) Mechanism of mitochondrial uncouplers, inhibitors, and toxins: focus on electron transfer, free radicals, and structure–activity relationships. Curr Med Chem 12:2601–2623PubMedCrossRefGoogle Scholar
  123. Laethem A, Van K, Nys S, Van Kelst S, Claerhout H, Ichijo JR, Vandenheede M, Garmyn P (2006) Agostinis, Apoptosis signal regulating kinase-1 connects reactive oxygen species to p38 MAPK induced mitochondrial apoptosis in UVB-irradiated human keratinocytes. Free Radic Biol Med 41:1361–1371PubMedCrossRefGoogle Scholar
  124. Lambert AJ, Brand MD (2004) Superoxide production by NADH: ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochem J 382:511–517PubMedCrossRefGoogle Scholar
  125. LeBlanc HN, Ashkenazi A (2003) Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ 10:66–75PubMedCrossRefGoogle Scholar
  126. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EBE, DiBacco S, de la Iglesia N, Gygi S, Blackwell TK et al (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125:987–1001PubMedCrossRefGoogle Scholar
  127. Lei K, Davis RJ (2003) NK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 100:2432–2437PubMedCrossRefGoogle Scholar
  128. Lei K, Nimnual A, Zong WX, Kennedy NJ, Flavell RA, Thompson CB et al (2002) The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase. Mol Cell Biol 22:4929–4942PubMedCrossRefGoogle Scholar
  129. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183–192PubMedCrossRefGoogle Scholar
  130. Lin Y, Devin A, Rodriguez Y, Liu ZG (1999) Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev 13:2514–2526PubMedCrossRefGoogle Scholar
  131. Liochev SI, Fridovich I (1999) The relative importance of HO* and ONOO in mediating the toxicity of O*. Free Radic Biol Med 26:777–778PubMedCrossRefGoogle Scholar
  132. Liu X, Zou H, Slaughter C, Wang X (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175–184PubMedCrossRefGoogle Scholar
  133. Liu H, Nishitoh H, Ichijo H, Kyriakis JM (2000) Activation of apoptosis signal-regulating kinase 1 (ASK1) by tumor necrosis factor receptor-associated factor 2 requires prior dissociation of the ASK1 inhibitor thioredoxin. Mol Cell Biol 20:2198–2208PubMedCrossRefGoogle Scholar
  134. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780–787PubMedCrossRefGoogle Scholar
  135. Liu FT, Newland AC, Jia L (2003) Bax conformational change is a crucial step for PUMA-mediated apoptosis in human leukemia. Biochem Biophys Res Commun 310:956–962PubMedCrossRefGoogle Scholar
  136. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501PubMedCrossRefGoogle Scholar
  137. Los M, Wesselborg S, Schulze-Osthoff K (1999) The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10:629–639PubMedCrossRefGoogle Scholar
  138. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481–490PubMedCrossRefGoogle Scholar
  139. Madesh M, Antonsson B, Srinivasula SM, Alnemri ES, Hajnóczky G (2002) Rapid kinetics of tBid-induced cytochrome c and Smac/DIABLO release and mitochondrial depolarization. J Biol Chem 277:5651–5659PubMedCrossRefGoogle Scholar
  140. Manna P, Sil PC (2012a) Arjunolic acid: beneficial role in type 1 diabetes and its associated organ pathophysiology. Free Radic Res 46:815–830PubMedCrossRefGoogle Scholar
  141. Manna P, Sil PC (2012b) Impaired redox signaling and mitochondrial uncoupling contributes vascular inflammation and cardiac dysfunction in type 1 diabetes: protective role of arjunolic acid. Biochimie 94:786–797PubMedCrossRefGoogle Scholar
  142. Manna SK, Zhang HJ, Yan T, Oberley LW, Aggarwal BB (1998) Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappaB and activated protein-1. J Biol Chem 273:13245–13254PubMedCrossRefGoogle Scholar
  143. Manna P, Sinha M, Sil PC (2007a) Protection of arsenic-induced hepatic disorder by arjunolic Acid. Basic Clin Pharmacol Toxicol 101:333–338PubMedCrossRefGoogle Scholar
  144. Manna P, Sinha M, Pal P, Sil PC (2007b) Arjunolic acid, a triterpenoid saponin, ameliorates arsenic-induced cyto-toxicity in hepatocytes. Chem Biol Interact 170:187–200PubMedCrossRefGoogle Scholar
  145. Manna P, Sinha M, Sil PC (2008a) Arsenic induced oxidative myocardial injury: protective role of arjunolic acid. Arch Toxicol 82:137–149PubMedCrossRefGoogle Scholar
  146. Manna P, Sinha M, Sil PC (2008b) Taurine triggers a chemoprevention against cadmium induced testicular oxidative injury. Reprod Toxicol 26:282–291PubMedCrossRefGoogle Scholar
  147. Manna P, Sinha M, Sil PC (2008c) Amelioration of cadmium-induced cardiac impairment by taurine. Chem Biol Interact 174:88–97PubMedCrossRefGoogle Scholar
  148. Manna P, Sinha M, Sil PC (2008d) Protection of arsenic-induced testicular oxidative stress by arjunolic acid. Redox Rep 13:67–77PubMedCrossRefGoogle Scholar
  149. Manna P, Sinha M, Sil PC (2009a) Prophylactic role of arjunolic acid in response to streptozotocin mediated diabetic renal injury: activation of polyol pathway and oxidative stress responsive signaling cascades. Chem Biol Interact 181:297–308PubMedCrossRefGoogle Scholar
  150. Manna P, Sinha M, Sil PC (2009b) Protective role of arjunolic acid in response to streptozotocin-induced type-I diabetes via the mitochondrial dependent and independent pathways. Toxicology 257:53–63PubMedCrossRefGoogle Scholar
  151. Manna P, Sinha M, Sil PC (2009c) Taurine plays a beneficial role against cadmium-induced oxidative renal dysfunction. Amino Acids 36:417–428PubMedCrossRefGoogle Scholar
  152. Manna P, Das J, Ghosh J, Sil PC (2010a) Contribution of type 1 diabetes to rat liver dysfunction and cellular damage via activation of NOS, PARP, IκBα/NF-κB, MAPKs, and mitochondria-dependent prophylactic role of arjunolic acid. Free Radic Biol Med 48:1465–1484PubMedCrossRefGoogle Scholar
  153. Manna P, Ghosh J, Das J, Sil PC (2010b) Streptozotocin induced activation of oxidative stress responsive splenic cell signaling pathways: protective role of arjunolic acid. Toxicol Appl Pharmacol 244:114–129PubMedCrossRefGoogle Scholar
  154. Manna P, Ghosh M, Ghosh J, Das J, Sil PC (2012) Contribution of nano-copper particles to in vivo liver dysfunction and cellular damage: role of IκBα/NF-κB, MAPKs and mitochondrial signal. Nanotoxicology 6:1–21PubMedCrossRefGoogle Scholar
  155. Marani M, Tenev T, Hancock D, Downward J, Lemoine NR (2002) Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol Cell Biol 22:3577–3589Google Scholar
  156. Masutani H, Yodoi J (2002) Thioredoxin. Overview. Methods Enzymol 347:279–286PubMedCrossRefGoogle Scholar
  157. Matés JM, Segura JA, Alonso FJ, Marquez J (2010) Roles of dioxins and heavy metals in cancer and neurological diseases using ROS-mediated mechanisms. Free Radic Biol Med 49:1328–1341PubMedCrossRefGoogle Scholar
  158. Matés JA, Segura FJ, Alonso JM, Javier M (2012) Oxidative stress in apoptosis and cancer: an update. Arch Toxicol. doi: 10.1007/s00204-012-0906-3 PubMedGoogle Scholar
  159. Matsukawa J, Matsuzawa A, Takeda K, Ichijo H (2004) The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 136:261–265PubMedCrossRefGoogle Scholar
  160. Matsuura H, Nishitoh H, Takeda K, Matsuzawa A, Amagasa T, Ito M, Yoshioka K, Ichijo H (2002) Phosphorylation-dependent scaffolding role of JSAP1/JIP3 in the ASK1–JNK signaling pathway: a new mode of regulation of the MAP kinase cascade. J Biol Chem 277:40703–40709PubMedCrossRefGoogle Scholar
  161. Matsuzawa A, Ichijo H (2001) Molecular mechanisms of the decision between life and death: regulation of apoptosis by apoptosis signal-regulating kinase 1. J Biochem 130:1–8PubMedCrossRefGoogle Scholar
  162. Matsuzawa A, Ichijo H (2008) Redox control of cell fate by MAP kinase: physiological roles of ASK1–MAP kinase pathway in stress signaling. Biochim Biophys Acta 1708:1325–1336CrossRefGoogle Scholar
  163. Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114:181–190PubMedCrossRefGoogle Scholar
  164. Migliaccio E, Giorgio M, Pelicci PG (2006) Apoptosis and aging: role of p66Shc redox protein. Antioxid Redox Signal 8:600–608PubMedCrossRefGoogle Scholar
  165. Miller DM, Buettner GR, Aust SD (1990) Transition metals as catalysts of “autoxidation” reactions. Free Radic Biol Med 8:95–108PubMedCrossRefGoogle Scholar
  166. Min W, Lin Y, Tang S, Yu L, Zhang H, Wan T, Luhn T, Fu H, Chen H (2008) AIP1 recruits phosphatase PP2A to ASK1 in tumor necrosis factor-induced ASK1-JNK activation. Circ Res 102:840–848PubMedCrossRefGoogle Scholar
  167. Moreira ME, Barcinski MA (2004) Apoptotic cell and phagocyte interplay: recognition and consequences in different cell systems. An Acad Bras Cienc 76:93–115PubMedCrossRefGoogle Scholar
  168. Morita K, Saitoh M, Tobiume K, Matsuura H, Enomoto S, Nishitoh H, Ichijo H (2001) Negative feedback regulation of ASK1 by protein phosphatase 5 (PP5) in response to oxidative stress. EMBO J 20:6028–6036PubMedCrossRefGoogle Scholar
  169. Mullarkey CJ, Edelstein D, Brownlee M (1990) Free radical generation by early glycation products: a mechanism for accelerated atherogenesis in diabetes. Biochem Biophys Res Commun 173:932–939PubMedCrossRefGoogle Scholar
  170. Muller FL, Liu Y, Van Remmen H (2004) Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 279:49064–49073PubMedCrossRefGoogle Scholar
  171. Nagai H, Noguchi T, Takeda K, Ichijo H (2007) Pathophysiological roles of ASK1-MAP kinase signaling pathways. J Biochem Mol Biol 40:1–6PubMedCrossRefGoogle Scholar
  172. Nagai H, Noguchi T, Homma K, Katagiri K, Takeda K, Matsuzawa A, Ichijo H (2009) Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Mol Cell 36:805–818PubMedCrossRefGoogle Scholar
  173. Nagata S (1999) Fas ligand-induced apoptosis. Annu Rev Genet 33:29–55PubMedCrossRefGoogle Scholar
  174. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98–103PubMedCrossRefGoogle Scholar
  175. Nakamura T, Kazuichi S (2008) Forkhead transcription factor FOXO subfamily is essential for reactive oxygen species-induced apoptosis. Mol Cell Endocrinol 281:47–55PubMedCrossRefGoogle Scholar
  176. Nishikawa T, Edelstein D, Du XL, Yamagishi S et al (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787–790PubMedCrossRefGoogle Scholar
  177. Nishitoh H, Saitoh M, Mochida Y, Takeda K, Nakano H, Rothe M et al (1998) ASK1 is essential for JNK/SAPK activation by TRAF2. Mol Cell 2:389–395PubMedCrossRefGoogle Scholar
  178. Noguchi T, Takeda K, Matsuzawa A, Saegusa K, Nakano H, Gohda J, Inoue J, Ichijo H (2005) Recruitment of tumor necrosis factor receptor associated factor family proteins to apoptosis signal-regulating kinase 1 signalosome is essential for oxidative stress induced cell death. J Biol Chem 280:37033–37040Google Scholar
  179. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, Tanaka N (2000) Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288:1053–1058PubMedCrossRefGoogle Scholar
  180. Oleinik NV, Krupenko NI, Krupenko SA (2007) Cooperation between JNK1 and JNK2 in activation of p53 apoptotic pathway. Oncogene 26:7222–7230PubMedCrossRefGoogle Scholar
  181. Orr WC, Sohal RS (1994) Extension of life-span by over expression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263:1128–1130PubMedCrossRefGoogle Scholar
  182. Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183PubMedCrossRefGoogle Scholar
  183. Orrenius S, Nicotera P, Zhivotovsky B (2011) Cell death mechanisms and their implications in toxicology. Toxicol Sci 119:3–19PubMedCrossRefGoogle Scholar
  184. Ott M, Robertson JD, Gogvadze V, Zhivotovsky B, Orrenius S (2002) Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA 99:1259–1263PubMedCrossRefGoogle Scholar
  185. Pal S, Sil PC (2012) A 43 kD protein from the leaves of the herb Cajanus indicus L. modulates doxorubicin induced nephrotoxicity via MAPKs and both mitochondria dependent and independent pathways. Biochimie 94:1356–1367PubMedCrossRefGoogle Scholar
  186. Pal S, Pal PB, Das J, Sil PC (2011) Involvement of both intrinsic and extrinsic pathways in hepatoprotection of arjunolic acid against cadmium induced acute damage in vitro. Toxicology 283:129–139PubMedCrossRefGoogle Scholar
  187. Pal PB, Pal S, Das J, Sil PC (2012) Modulation of mercury-induced mitochondria-dependent apoptosis by glycine in hepatocytes. Amino Acids 42:1669–1683PubMedCrossRefGoogle Scholar
  188. Pal PB, Sinha K, Sil PC (2013) Mangiferin, a natural xanthone, protects murine liver in Pb(II) induced hepatic damage and cell death via MAP kinase, NF-κB and mitochondria dependent pathways. PLoS ONE. doi:  10.1371/journal.pone.0056894
  189. Park HS, Cho SG, Kim CK, Hwang HS et al (2002) Heat shock protein hsp72 is a negative regulator of apoptosis signal-regulating kinase 1. Mol Cell Biol 22:7721–7730PubMedCrossRefGoogle Scholar
  190. Pastor N, Weinstein H, Jamison E, Brenowitz M (2000) A detailed interpretation of OH radical footprints in a TBP DNA complex reveals the role of dynamics in the mechanism of sequence specific binding. J Mol Biol 304:55–68PubMedCrossRefGoogle Scholar
  191. Pastorino JG, Chen ST, Tafani M, Snyder JW, Farber JL (1998) The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J Biol Chem 273:7770–7775PubMedCrossRefGoogle Scholar
  192. Perier C, Tieu K, Guegan C, Caspersen C, Jackson-Lewis V et al (2005) Complex I deficiency primes Bax-dependent neuronal apoptosis through mitochondrial oxidative damage. Proc Natl Acad Sci USA 102:19126–19131PubMedCrossRefGoogle Scholar
  193. Pierce GB, Parchment RE, Lewellyn AL (1991) Hydrogen peroxide as a mediator of programmed cell death in the blastocyst. Differentiation 46:181–186PubMedCrossRefGoogle Scholar
  194. Puthalakath H, Strasser A (2002) Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ 9:505–512PubMedCrossRefGoogle Scholar
  195. Puthalakath H, Huang DC, O’Reilly LA, King SM, Strasser A (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 3:287–296PubMedCrossRefGoogle Scholar
  196. Rachek LI, Yuzefovych LV, Ledoux SP, Julie NL, Wilson GL (2009) Troglitazone, but not rosiglitazone, damages mitochondrial DNA and induces mitochondrial dysfunction and cell death in human hepatocytes. Toxicol Appl Pharmacol 240:348–354PubMedCrossRefGoogle Scholar
  197. Raman M, Chen W, Cobb MH (2007) Differential regulation and properties of MAPKs. Oncogene 26:3100–3112PubMedCrossRefGoogle Scholar
  198. Rashid K, Bhattacharya S, Sil PC (2012) Protective role of D-saccharic acid-1,4-lactone in alloxan induced oxidative stress in the spleen tissue of diabetic rats is mediated by suppressing mitochondria dependent apoptotic pathway. Free Radic Res 46:240–252PubMedCrossRefGoogle Scholar
  199. Rashid K, Das J, Sil PC (2013) Taurine ameliorate alloxan induced oxidative stress and intrinsic apoptotic pathway in the hepatic tissue of diabetic rats. Food Chem Toxicol 51:317–329PubMedCrossRefGoogle Scholar
  200. Rasola A, Bernardi P (2007) The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12:815–833Google Scholar
  201. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990PubMedCrossRefGoogle Scholar
  202. Rhee SG (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312:1882–1883PubMedCrossRefGoogle Scholar
  203. Ricci C, Pastukh V, Leonard J, Turrens J, Wilson G, Schaffer D, Schaffer SW (2008) Mitochondrial DNA damage triggers mitochondrial-superoxide generation and apoptosis. Am J Physiol Cell Physiol 294:C413–C422PubMedCrossRefGoogle Scholar
  204. Ristow M, Zarse K (2010) How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 45:410–418PubMedCrossRefGoogle Scholar
  205. Rostovtseva TK, TanW Colombini M (2005) On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 37:129–142PubMedCrossRefGoogle Scholar
  206. Roulston A, Reinhard C, Amiri P, Williams LT (1998) Early activation of c-Jun N-terminal kinase and p38 kinase regulate cell survival in response to tumor necrosis factor α. J Biol Chem 273:10232–10239PubMedCrossRefGoogle Scholar
  207. Roy A, Manna P, Sil PC (2009) Prophylactic role of taurine on arsenic mediated oxidative renal dysfunction via MAPKs/NF-kappaB and mitochondria dependent pathways. Free Radic Res 43:995–1007PubMedCrossRefGoogle Scholar
  208. Rudel T, Bokoch GM (1997) Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276:1571–1574PubMedCrossRefGoogle Scholar
  209. Saeki K, Kobayashi N, Inazawa Y, Zhang H, Nishitoh H, Ichijo H, Saeki K, Isemura M, You A (2002) Oxidation-triggered c-Jun N-terminal kinase (JNK) and p38 mitogen-activated protein (MAP) kinase pathways for apoptosis in human leukaemic cells stimulated by epigallocatechin-3-gallate (EGCG): a distinct pathway from those of chemically induced and receptor-mediated apoptosis. Biochem J 368:705–720PubMedCrossRefGoogle Scholar
  210. Saelens X, Festjens N, Vande Walle L, van Gurp M, van Loo G, Vandenabeele P (2004) Toxic proteins released from mitochondria in cell death. Oncogene 23:2861–2874PubMedCrossRefGoogle Scholar
  211. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17:2596–2606PubMedCrossRefGoogle Scholar
  212. Sarkar MK, Sil PC (2010) Prevention of tertiary butyl hydroperoxide induced oxidative impairment and cell death by a novel antioxidant protein molecule isolated from the herb, Phyllanthus niruri. Toxicol In Vitro 24:1711–1719PubMedCrossRefGoogle Scholar
  213. Sarkar A, Das J, Manna P, Sil PC (2011) Nano-copper induces oxidative stress and apoptosis in kidney via both extrinsic and intrinsic pathways. Toxicology 290:208–217PubMedCrossRefGoogle Scholar
  214. Schneider-Brachert W, Tchikov V, Neumeyer J, Jakob M et al (2004) Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 21:415–428PubMedCrossRefGoogle Scholar
  215. Schroeter H, Boyd CS, Ahmed R, Spencer JP, Duncan RF, Rice-Evans C et al (2003) c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis. Biochem J 372:359–369PubMedCrossRefGoogle Scholar
  216. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA et al (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2:55–67PubMedCrossRefGoogle Scholar
  217. Shiizaki S, Isao N, Hidenori I (2012) Activation mechanisms of ASK1 in response to various stresses and its significance in intracellular signaling. Adv Biol Regul. doi:  10.1016/j.jbior.2012.09.006
  218. Shim JH, Xiao C, Paschal AE, Bailey ST, Rao P, Hayden MS, Lee KY, Bussey C, Steckel M, Tanaka N, Yamada G, Akira S, Matsumoto K, Ghosh S (2005) TAK1, but not TAB 1 or TAB 2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 19:2668–2681PubMedCrossRefGoogle Scholar
  219. Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483–487PubMedCrossRefGoogle Scholar
  220. Sies H (1991) Oxidative stress: from basic research to clinical application. Am J Med 91:31S–38SPubMedCrossRefGoogle Scholar
  221. Singh BK, Tripathi M, Chaudhari BP, Pandey PK, Kakkar P (2012) Natural terpenes prevent mitochondrial dysfunction, oxidative stress and release of apoptotic proteins during nimesulide-hepatotoxicity in rats. PLoS ONE 7:e34200PubMedCrossRefGoogle Scholar
  222. Sinha M, Manna P, Sil PC (2007a) Taurine, a conditionally essential amino acid, ameliorates arsenic-induced cytotoxicity in murine hepatocytes. Toxicol In Vitro 21:1419–1428PubMedCrossRefGoogle Scholar
  223. Sinha M, Manna P, Sil PC (2007b) Attenuation of cadmium chloride induced cytotoxicity in murine hepatocytes by a protein isolated from the leaves of the herb Cajanus indicus L. Arch Toxicol 81:397–406PubMedCrossRefGoogle Scholar
  224. Sinha M, Manna P, Sil PC (2008a) Taurine protects antioxidant defense system in the erythrocytes of cadmium treated mice. BMB Rep 41:657–663PubMedCrossRefGoogle Scholar
  225. Sinha M, Manna P, Sil PC (2008b) Terminalia arjuna protects mice hearts against sodium fluoride-induced oxidative stress. J Med Food 11:733–740PubMedCrossRefGoogle Scholar
  226. Sinha M, Manna P, Sil PC (2008c) Cadmium induced neurological disorders: prophylactic role of taurine. J Appl Toxicol 28:974–986PubMedGoogle Scholar
  227. Sinha M, Manna P, Sil PC (2008d) Arjunolic acid attenuates arsenic-induced nephrotoxicity. Pathophysiology 15:147–156PubMedCrossRefGoogle Scholar
  228. Sinha M, Manna P, Sil PC (2008e) Protective effect of arjunolic acid against arsenic-induced oxidative stress in mouse brain. J Biochem Mol Toxicol 22:15–26PubMedCrossRefGoogle Scholar
  229. Sinha M, Manna P, Sil PC (2009) Induction of necrosis in cadmium-induced hepatic oxidative stress and its prevention by the prophylactic properties of taurine. J Trace Elem Med Biol 23:300–313PubMedCrossRefGoogle Scholar
  230. Soga M, Matsuzawa A, Ichijo H (2012) Oxidative stress-induced diseases via the ASK1 Signaling pathway. Int J Cell Biol 2012:439587PubMedGoogle Scholar
  231. Song JJ, Lee YJ (2003) Differential role of glutaredoxin and thioredoxin in metabolic oxidative stress-induced activation of apoptosis signal-regulating kinase 1. Biochem J 373:845–853PubMedCrossRefGoogle Scholar
  232. Song JJ, Rhee JG, Suntharalingam M, Walsh SA, Spitz DR, Lee YJ (2002) Role of glutaredoxin in metabolic oxidative stress. Glutaredoxin as a sensor of oxidative stress mediated by H2O2. J Biol Chem 277:46566–46575PubMedCrossRefGoogle Scholar
  233. Srivastava RK, Mi QS, Hardwick JM, Longo DL (1999) Deletion of the loop region of Bcl-2 completely blocks paclitaxel-induced apoptosis. Proc Natl Acad Sci USA 96:3775–3780PubMedCrossRefGoogle Scholar
  234. Stehlik C, de Martin R, Kumabashiri I, Schmid JA, Binder BR, Lipp J (1998) Nuclear factor (NF)-κB–regulated X-chromosome–linked iap Gene expression protects endothelial cells from tumor necrosis Factor α–induced apoptosis. JEM 188:211–216Google Scholar
  235. Strasser A, O’Connor L, Dixit VM (2000) Apoptosis signaling. Annu Rev Biochem 69:217–245PubMedCrossRefGoogle Scholar
  236. Sunayama J, Tsuruta F, Masuyama N, Gotoh Y (2005) JNK antagonizes Akt-mediated survival signals by phosphorylating 14–3-3. J Cell Biol 170:295–304PubMedCrossRefGoogle Scholar
  237. Supale S, Li N, Brun T, Maechler P (2012) Mitochondrial dysfunction in pancreatic β cells. Trends Endocrinol Metab 23(9):477–487PubMedCrossRefGoogle Scholar
  238. Takeda K, Matsuzawa A, Nishitoh H, Ichijo H (2003) Roles of MAPKKK ASK1 in stress-induced cell death. Cell Struct Funct 28:23–29PubMedCrossRefGoogle Scholar
  239. Takeda K, Shimozono R, Noguchi T, Umeda T, Morimoto Y, Naguro I, Tobiume K, Saitoh M, Matsuzawa A, Ichijo H (2007) Apoptosis signal-regulating kinase (ASK) 2 functions as amitogen-activated protein kinase kinase kinase in a heteromeric complex with ASK1. J Biol Chem 282:7522–7531PubMedCrossRefGoogle Scholar
  240. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T, Ichijo H (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2:222–228PubMedCrossRefGoogle Scholar
  241. Tobiume K, Saitoh M, Ichijo H (2002) Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer. J Cell Physiol 191:95–104PubMedCrossRefGoogle Scholar
  242. Tormo D, Checinska A, Alonso-Curbelo D et al (2009) Targeted activation of innate immunity for therapeutic induction of autophagy and apoptosis in melanoma cells. Cancer Cell 16:103–114PubMedCrossRefGoogle Scholar
  243. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A et al (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288:870–874PubMedCrossRefGoogle Scholar
  244. Tretter L, Adam-Vizi V (2004) Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J Neurosci 24:7771–7778PubMedCrossRefGoogle Scholar
  245. Tsai WB, Chung YM, Takahashi Y, Xu Z, Hu MC (2008) Functional interaction between FOXO3a and ATM regulates DNA damage response. Nat Cell Biol 10:460–467PubMedCrossRefGoogle Scholar
  246. Tsuruta F, Sunayama J, Mori Y, Hattori S, Shimizu S, Tsujimoto Y et al (2004) JNK promotes Bax translocation to mitochondria through phosphorylation of 14–3-3 proteins. EMBO J 23:1889–1899PubMedCrossRefGoogle Scholar
  247. Turjanski AG, Vaque JP, Gutkind JS (2007) MAP kinases and the control of nuclear events. Oncogene 26:3240–3253PubMedCrossRefGoogle Scholar
  248. Turrens JF, Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191:421–427PubMedGoogle Scholar
  249. Turrens JF, Alexandre A, Lehninger AL (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237:408–414PubMedCrossRefGoogle Scholar
  250. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266:37–56PubMedCrossRefGoogle Scholar
  251. Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208PubMedCrossRefGoogle Scholar
  252. Valko M, Leibfritz D, Moncola J, Cronin Mark TD, Mazura M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84PubMedCrossRefGoogle Scholar
  253. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43–53PubMedCrossRefGoogle Scholar
  254. Vorbach C, Harrison R, Capecchi MR (2003) Xanthine oxidoreductase is central to the evolution and function of the innate immune system. Trends Immunol 24:512–517Google Scholar
  255. Wallace DC (1999) Mitochondrial diseases in man and mouse. Science 283:1482–1488PubMedCrossRefGoogle Scholar
  256. Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15:2922–2933PubMedGoogle Scholar
  257. Wang XS, Diener K, Tan TH, Yao Z (1998) MAPKKK6, a novel mitogen-activated protein kinase kinase kinase, that associates with MAPKKK5. Biochem Biophys Res Commun 253:33–37PubMedCrossRefGoogle Scholar
  258. Wang XT, Pei DS, Xu J, Guan QH et al (2007) Opposing effects of Bad phosphorylation at two distinct sites by Akt1 and JNK1/2 on ischemic brain injury. Cell Signal 19:1844–1856PubMedCrossRefGoogle Scholar
  259. Wang L, Azad N, Kongkaneramit L, Chen F, Lu Y, Jiang BH, Rojanasakul Y (2008) The Fas death signaling pathway connecting reactive oxygen species generation and FLICE inhibitory protein down-regulation. J Immunol 180:3072–3080PubMedGoogle Scholar
  260. Watanabe N, Kuriyama H, Sone H, Neda H, Yamauchi N, Maeda M, Niitsu Y (1988) Continuous internalization of tumor necrosis factor receptors in a human myosarcoma cell line. J Biol Chem 263:10262–10266PubMedGoogle Scholar
  261. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A et al (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14:2060–2071PubMedGoogle Scholar
  262. Wold LE, Ceylan-Isik AF, Ren J (2005) Oxidative stress and stress signaling: menace of diabetic cardiomyopathy. Acta Pharmacol Sin 26:908–917PubMedCrossRefGoogle Scholar
  263. Wolff SP, Dean RT (1987) Glucose autoxidation and protein modification. The potential role of “autoxidative glycosylation” in diabetes. Biochem J 245: 243–250PubMedGoogle Scholar
  264. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555–556PubMedCrossRefGoogle Scholar
  265. Wyllie AH (2010) “Where, O death, is thy sting?” A brief review of apoptosis biology. Mol Neurobiol 42:4–9PubMedCrossRefGoogle Scholar
  266. Xu YC, Wu RF, Gu Y, Yang YS, Yang MC, Nwariaku FE, Terada LS (2002) Involvement of TRAF4 in oxidative activation of c-Jun N-terminal kinase. J Biol Chem 277:28051–28057PubMedCrossRefGoogle Scholar
  267. Yakes FM, VanHouten B (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA 94:516–519CrossRefGoogle Scholar
  268. Yamamoto K, Ichijo H, Korsmeyer SJ (1999) BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol Cell Biol 19:8469–8478PubMedGoogle Scholar
  269. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80:285–291PubMedCrossRefGoogle Scholar
  270. Yim S, Malhotra A, Veves A (2007) Antioxidants and CVD in diabetes: where do we stand now? Curr Diab Rep 7:8–13PubMedCrossRefGoogle Scholar
  271. Zeiss CJ (2003) The apoptosis-necrosis continuum: insights from genetically altered mice. Vet Pathol 40:481–495PubMedCrossRefGoogle Scholar
  272. Zhang L, Chen J, Fu H (1999) Suppression of apoptosis signal-regulating kinase 1- induced cell death by 14–3-3 proteins. Proc Natl Acad Sci USA 96:8511–8515PubMedCrossRefGoogle Scholar
  273. Zhang H, Zhang R, Luo Y, D’Alessio A, Pober JS, Min W (2004) AIP1/DAB2IP, a novel member of the Ras–GAP family, transduces TRAF2-induced ASK1–JNK activation. J Biol Chem 279:44955–44965PubMedCrossRefGoogle Scholar
  274. Zhang AY, Yi F, Zhang G, Gulbins E, Li PL (2006a) Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells. Hypertension 47:74–80PubMedCrossRefGoogle Scholar
  275. Zhang M, Kho AL, Anilkumar N, Chibber R, Pagano PJ, Shah AM, Cave AC (2006b) Glycated proteins stimulate reactive oxygen species production in cardiacmyocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 113:1235–1243PubMedCrossRefGoogle Scholar
  276. Zhang AY, Yi F, Jin S, Xia M, Chen QZ, Gulbins E, Li PL (2007) Acid sphingomyelinase and its redox amplification in formation of lipid raft redox signaling platforms in endothelial cells. Antioxid Redox Signal 9:817–828PubMedCrossRefGoogle Scholar
  277. Zhou J, Shao Z, Kerkela R, Ichijo H et al (2009) Serine 58 of 14–3-3zeta is a molecular switch regulating ASK1 and oxidant stress-induced cell death. Mol Cell Biol 29:4167–4176PubMedCrossRefGoogle Scholar
  278. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C (1999) The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev 13:382–387PubMedCrossRefGoogle Scholar
  279. Zwacka RM, Dudus L, Epperly MW et al (1998) Redox gene therapy protects human IB-3 lung epithelial cells against ionizing radiation-induced apoptosis. Hum Gene Ther 9:1381–1386PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Krishnendu Sinha
    • 1
  • Joydeep Das
    • 1
  • Pabitra Bikash Pal
    • 1
  • Parames C. Sil
    • 1
  1. 1.Division of Molecular MedicineBose InstituteCalcuttaIndia

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