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

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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.

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References

  • Aikens J, Dix TA (1991) Perhydroxyl radical (HOO·) Initiated lipid-peroxidation-The role of fatty-acid hydroperoxides. J Biol Chem 266:15091–15098

    PubMed  CAS  Google Scholar 

  • 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 268:18532–18541

    PubMed  CAS  Google Scholar 

  • Ames BN, Gold LS, Willett WC (1995) The causes and prevention of cancer. Proc Natl Acad Sci USA 92:5258–5265

    Article  PubMed  CAS  Google Scholar 

  • Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 70:200–214

    PubMed  CAS  Google Scholar 

  • 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 71:2041–2048

    Article  CAS  Google Scholar 

  • 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 277:11746–11755

    Article  PubMed  CAS  Google Scholar 

  • 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 277:10244–10250

    Article  PubMed  CAS  Google Scholar 

  • Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281:1305–1308

    Article  PubMed  CAS  Google Scholar 

  • Barnhart BC, Alappat EC, Peter ME (2003) The CD95 type I/type II model. Semin Immunol 15:185–193

    Article  PubMed  CAS  Google Scholar 

  • Barone MC, Desouza LA, Freeman RS (2008) Pin1 promotes cell death in NGF-dependent neurons through a mechanism requiring c-Jun activity. J Neurochem 106:734–745

    Article  PubMed  CAS  Google Scholar 

  • Baynes JW, Thorpe SR (1999) Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48:1–9

    Article  PubMed  CAS  Google Scholar 

  • Behl C (1999) Alzheimer’s disease and oxidative stress implications for novel therapeutic approaches. Prog Neurobiol 57:301–323

    Article  PubMed  CAS  Google Scholar 

  • Behrens A, Sibilia M, Wagner EF (1999) Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 21:326–329

    Article  PubMed  CAS  Google Scholar 

  • 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 45:817–826

    Article  PubMed  CAS  Google Scholar 

  • 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 257:272–283

    Article  PubMed  CAS  Google Scholar 

  • 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 267:16–29

    Article  PubMed  CAS  Google Scholar 

  • 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 4:283–296

    Article  PubMed  CAS  Google Scholar 

  • 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 46:1296–1307

    Article  PubMed  CAS  Google Scholar 

  • 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 1001:102–106

    Article  PubMed  CAS  Google Scholar 

  • Boatright KM, Salvesen GS (2003) Mechanisms of caspase activation. Curr Opin Cell Biol 15:725–731

    Article  PubMed  CAS  Google Scholar 

  • Borges F, Fernandes E, Roleira F (2002) Progress towards the discovery of xanthine oxidase inhibitors. Curr Med Chem 9:195–217

    Article  PubMed  CAS  Google Scholar 

  • 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 37:755–767

    Article  PubMed  CAS  Google Scholar 

  • 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 207:110–116

    Article  PubMed  CAS  Google Scholar 

  • Cabiscol E, Piulats E, Echave P, Herrero E, Ros J (2000) Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J Biol Chem 35:27393–27398

    Google Scholar 

  • 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 346:171–179

    Google Scholar 

  • Ceriello A (2000) Oxidative stress and glycemic regulation. Metabolism 49:27–29

    Article  PubMed  CAS  Google Scholar 

  • Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605

    PubMed  CAS  Google Scholar 

  • 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 124:3601–3613

    Google Scholar 

  • Chang L, Karin M (2001) Mammalian MAP kinase signaling cascades. Nature 410:37–40

    Article  PubMed  CAS  Google Scholar 

  • 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 281:1860–1863

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee M, Sil PC (2006) Hepatoprotective effect of aqueous extract of Phyllanthus niruri on nimesulide-induced oxidative stress in vivo. Indian J Biochem Biophys 43:299–305

    PubMed  CAS  Google Scholar 

  • Chatterjee M, Sil PC (2007) Protective role of Phyllanthus niruri against nimesulide induced hepatic damage. Indian J Clin Biochem 22:109–116

    Article  PubMed  Google Scholar 

  • Chatterjee M, Sarkar K, Sil PC (2006) Herbal (Phyllanthus niruri) protein isolate protects liver from nimesulide induced oxidative stress. Pathophysiology 13:95–102

    Article  PubMed  Google Scholar 

  • 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 278:17593–17596

    Article  PubMed  CAS  Google Scholar 

  • 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 271:31929–31936

    Article  PubMed  CAS  Google Scholar 

  • Circu ML, Aw TY (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48:749–762

    Article  PubMed  CAS  Google Scholar 

  • 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 47:1190–1198

    Article  PubMed  CAS  Google Scholar 

  • Circu ML et al (2012) Glutathione and modulation of cell apoptosis. Biochim Biophys Acta 1823:1767–1777

    Article  PubMed  CAS  Google Scholar 

  • Ciuchi E, Odetti P, Prando R (1996) Relationship between glutathione and sorbitol concentrations in erythrocytes from diabetic patients. Metabolism 45:611–613

    Article  PubMed  CAS  Google Scholar 

  • Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656

    Article  PubMed  CAS  Google Scholar 

  • D’Emilio A, Biagiotti L, Burattini S et al (2010) Morphological and biochemical patterns in skeletal muscle apoptosis. Histol Histopathol 25:21–32

    PubMed  Google Scholar 

  • Das J, Sil PC (2012) Taurine ameliorates alloxan-induced diabetic renal injury, oxidative stress related signaling pathways and apoptosis in rats. Amino Acids 43:1509–1523

    Article  PubMed  CAS  Google Scholar 

  • Das J, Ghosh J, Manna P, Sil PC (2008) Taurine provides antioxidant defense against NaF-induced cytotoxicity in murine hepatocytes. Pathophysiology 15:181–190

    Article  PubMed  CAS  Google Scholar 

  • Das J, Ghosh J, Manna P, Sinha M, Sil PC (2009a) Arsenic-induced oxidative cerebral disorders: protection by taurine. Drug Chem Toxicol 32:93–102

    Article  PubMed  CAS  Google Scholar 

  • 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 187:201–210

    Article  PubMed  CAS  Google Scholar 

  • 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 269:24–34

    Article  PubMed  CAS  Google Scholar 

  • 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:e12602

    Article  PubMed  CAS  Google Scholar 

  • 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 44:340–355

    Article  PubMed  CAS  Google Scholar 

  • 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 81:891–909

    Article  PubMed  CAS  Google Scholar 

  • 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 42:1839–1855

    Article  PubMed  CAS  Google Scholar 

  • 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 260:35–47

    Article  PubMed  CAS  Google Scholar 

  • 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 3:1251–1264

    Article  PubMed  CAS  Google Scholar 

  • 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 258:296–308

    Article  PubMed  CAS  Google Scholar 

  • Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239–252

    Article  PubMed  CAS  Google Scholar 

  • De Grey AD (2002) HO2·: the forgotten radical. DNA Cell Biol 21:251–257

    Article  PubMed  Google Scholar 

  • Deng Y, Ren X, Yang L, Lin Y, Wu XA (2003) JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 115:61–70

    Article  PubMed  CAS  Google Scholar 

  • Dhanasekaran DN, Johnson GL (2007) MAPKs: function, regulation, role in cancer and therapeutic targeting. Oncogene 26:3097–3099

    Article  PubMed  CAS  Google Scholar 

  • Dhanasekaran N, Reddy EP (1998) Signaling by dual specificity kinases. Oncogene 17:1447–1755

    Article  PubMed  CAS  Google Scholar 

  • Dhanasekaran DN, Reddy EP (2008) JNK signaling in apoptosis. Oncogene 27:6245–6251

    Google Scholar 

  • 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 277:40944–40949

    Article  PubMed  CAS  Google Scholar 

  • 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 277:30792–30797

    Article  PubMed  CAS  Google Scholar 

  • 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 97:12222–12226

    Article  PubMed  CAS  Google Scholar 

  • Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516

    Google Scholar 

  • 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 1:529-539

    Google Scholar 

  • 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 23:4802–4812

    Article  PubMed  CAS  Google Scholar 

  • 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 23:599–622

    Article  PubMed  CAS  Google Scholar 

  • 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 194:251–256

    Article  PubMed  CAS  Google Scholar 

  • 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 148:2207–2216

    PubMed  CAS  Google Scholar 

  • Fan M, Chambers TC (2001) Role of mitogen-activated protein kinases in the response of tumor cells to chemotherapy. Drug Resist Updat 4:253–267

    Article  PubMed  CAS  Google Scholar 

  • Farrugia G, Balzan R (2012) Oxidative stress and programmed cell death in yeast. Front Oncol 2:64

    Article  PubMed  Google Scholar 

  • Finkel T (2003) Oxidant signals and oxidative stress. Curr Opin Cell Biol 15:247–254

    Article  PubMed  CAS  Google Scholar 

  • Fuchs SY, Adler V, Pincus MR, Ronai Z (1998) MEKK1/JNK signaling stabilizes and activates p53. Proc Natl Acad Sci USA 95:10541–10546

    Article  PubMed  CAS  Google Scholar 

  • Fujino G, Noguchi T, Takeda K, Ichijo H (2006) Thioredoxin and protein kinases in redox signaling. Semin Cancer Biol 16:427–435

    Article  PubMed  CAS  Google Scholar 

  • 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 27:8152–8163

    Article  PubMed  CAS  Google Scholar 

  • 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 69:7512–7517

    Article  PubMed  CAS  Google Scholar 

  • 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 20:6826–6836

    Article  PubMed  CAS  Google Scholar 

  • 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 40:1039–1049

    Article  PubMed  CAS  Google Scholar 

  • Ghosh A, Sil PC (2008) A protein from Cajanus indicus Spreng protects liver and kidney against mercuric chloride-induced oxidative stress. Biol Pharm Bull 31:1651–1658

    Article  PubMed  CAS  Google Scholar 

  • 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 177:96–106

    Article  PubMed  CAS  Google Scholar 

  • 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 240:73–87

    Article  PubMed  CAS  Google Scholar 

  • 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 268:8–18

    Article  PubMed  CAS  Google Scholar 

  • 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 49:1779–1791

    Article  PubMed  CAS  Google Scholar 

  • 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 123:1062–1075

    Article  CAS  Google Scholar 

  • 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 48:535–553

    Article  PubMed  CAS  Google Scholar 

  • 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 32:4857–4866

    Article  PubMed  CAS  Google Scholar 

  • 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 45:620–637

    Article  PubMed  CAS  Google Scholar 

  • 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 46:116–132

    Article  PubMed  CAS  Google Scholar 

  • Gille G, Sigler K (1995) Oxidative stress and living cells. Folia Microbiol (Praha) 40:131–152

    Article  CAS  Google Scholar 

  • 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 122:221–233

    Article  PubMed  CAS  Google Scholar 

  • 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 279:10442–10449

    Article  PubMed  CAS  Google Scholar 

  • Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626–629

    Article  PubMed  CAS  Google Scholar 

  • Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312

    Article  PubMed  CAS  Google Scholar 

  • Gross A, McDonnell JM, Korsmeyer SJ (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13:1899–1911

    Article  PubMed  CAS  Google Scholar 

  • Guo M, Hay BA (1999) Cell proliferation and apoptosis. Curr Opin Cell Biol 11(6):745–752

    Article  PubMed  CAS  Google Scholar 

  • 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 273:4027–4034

    Article  PubMed  CAS  Google Scholar 

  • 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 125:1191–1203

    Article  PubMed  CAS  Google Scholar 

  • Halliwell B, Cross CE (1994) Oxygen-derived species: their relation to human disease and environmental stress. Environ Health Perspect 10:5–12

    Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, Oxford

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hirsch EC (1993) Does oxidative stress participates in nerve cell death in Parkinson’s disease? Eur Neurol 33:52–59

    Article  PubMed  Google Scholar 

  • 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 15:1573–1581

    Article  PubMed  CAS  Google Scholar 

  • 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 8:461–471

    Article  PubMed  CAS  Google Scholar 

  • Hotchkiss RS, Strasser A, McDunn JE, Swanson PE (2009) Cell death. N Engl J Med 361:1570–1583

    Article  PubMed  CAS  Google Scholar 

  • Hsu H, Xiong J, Goeddel DV (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81:495–504

    Article  PubMed  CAS  Google Scholar 

  • 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 282:29401–29413

    Article  PubMed  CAS  Google Scholar 

  • 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 275:90–94

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Woronicz JD, Liu W, Goeddel DV (1999) Prevention of constitutive TNF receptor 1 signaling by silencer of death domains. Science 283:543–546

    Article  PubMed  CAS  Google Scholar 

  • Johnson GL, Nakamura K (2007) The c-jun kinase/stress-activated pathway: regulation, function and role in human disease. Biochim Biophys Acta 1773:1341–1348

    Article  PubMed  CAS  Google Scholar 

  • Jones EV, Dickman MJ, Whitmarsh AJ (2007) Regulation of p73- mediated apoptosis by c-Jun N-terminal kinase. Biochem J 405:617–623

    Article  PubMed  CAS  Google Scholar 

  • 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 1:223–232

    Article  PubMed  CAS  Google Scholar 

  • Kam PCA, Ferch NI (2000) Apoptosis: mechanisms and clinical implications. Anaesthesia 55:1081–1093

    Article  PubMed  CAS  Google Scholar 

  • 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 120:649–661

    Article  PubMed  CAS  Google Scholar 

  • Karin M, Lin A (2002) NF-κB at the crossroads of life and death. Nat Immunol 3:221–227

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann SH, Earnshaw WC (2000) Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256:42–49

    Article  PubMed  CAS  Google Scholar 

  • Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257

    Article  PubMed  CAS  Google Scholar 

  • 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 275:322–327

    Article  PubMed  CAS  Google Scholar 

  • 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 74:1072–1083

    Article  PubMed  CAS  Google Scholar 

  • 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 14:5579–5588

    PubMed  CAS  Google Scholar 

  • 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 275:1889–1899

    Article  PubMed  CAS  Google Scholar 

  • Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15–18

    Article  PubMed  CAS  Google Scholar 

  • 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 278:294–298

    Article  PubMed  CAS  Google Scholar 

  • 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 12:2601–2623

    Article  PubMed  CAS  Google Scholar 

  • 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 41:1361–1371

    Article  PubMed  CAS  Google Scholar 

  • 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 382:511–517

    Article  PubMed  CAS  Google Scholar 

  • LeBlanc HN, Ashkenazi A (2003) Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ 10:66–75

    Article  PubMed  CAS  Google Scholar 

  • 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 125:987–1001

    Article  PubMed  CAS  Google Scholar 

  • Lei K, Davis RJ (2003) NK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 100:2432–2437

    Article  PubMed  CAS  Google Scholar 

  • 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 22:4929–4942

    Article  PubMed  CAS  Google Scholar 

  • 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 2:183–192

    Article  PubMed  CAS  Google Scholar 

  • 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 13:2514–2526

    Article  PubMed  CAS  Google Scholar 

  • Liochev SI, Fridovich I (1999) The relative importance of HO* and ONOO in mediating the toxicity of O*. Free Radic Biol Med 26:777–778

    Article  PubMed  CAS  Google Scholar 

  • 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 89:175–184

    Article  PubMed  CAS  Google Scholar 

  • 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 20:2198–2208

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780–787

    Article  PubMed  CAS  Google Scholar 

  • 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 310:956–962

    Article  PubMed  CAS  Google Scholar 

  • Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501

    Article  PubMed  CAS  Google Scholar 

  • Los M, Wesselborg S, Schulze-Osthoff K (1999) The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10:629–639

    Article  PubMed  CAS  Google Scholar 

  • 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 94:481–490

    Article  PubMed  CAS  Google Scholar 

  • 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 277:5651–5659

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sil PC (2012a) Arjunolic acid: beneficial role in type 1 diabetes and its associated organ pathophysiology. Free Radic Res 46:815–830

    Article  PubMed  CAS  Google Scholar 

  • 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 94:786–797

    Article  PubMed  CAS  Google Scholar 

  • 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 273:13245–13254

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sinha M, Sil PC (2007a) Protection of arsenic-induced hepatic disorder by arjunolic Acid. Basic Clin Pharmacol Toxicol 101:333–338

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sinha M, Pal P, Sil PC (2007b) Arjunolic acid, a triterpenoid saponin, ameliorates arsenic-induced cyto-toxicity in hepatocytes. Chem Biol Interact 170:187–200

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sinha M, Sil PC (2008a) Arsenic induced oxidative myocardial injury: protective role of arjunolic acid. Arch Toxicol 82:137–149

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sinha M, Sil PC (2008b) Taurine triggers a chemoprevention against cadmium induced testicular oxidative injury. Reprod Toxicol 26:282–291

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sinha M, Sil PC (2008c) Amelioration of cadmium-induced cardiac impairment by taurine. Chem Biol Interact 174:88–97

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sinha M, Sil PC (2008d) Protection of arsenic-induced testicular oxidative stress by arjunolic acid. Redox Rep 13:67–77

    Article  PubMed  CAS  Google Scholar 

  • 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 181:297–308

    Article  PubMed  CAS  Google Scholar 

  • 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 257:53–63

    Article  PubMed  CAS  Google Scholar 

  • Manna P, Sinha M, Sil PC (2009c) Taurine plays a beneficial role against cadmium-induced oxidative renal dysfunction. Amino Acids 36:417–428

    Article  PubMed  CAS  Google Scholar 

  • 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 48:1465–1484

    Article  PubMed  CAS  Google Scholar 

  • 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 244:114–129

    Article  PubMed  CAS  Google Scholar 

  • 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 6:1–21

    Article  PubMed  CAS  Google Scholar 

  • 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 22:3577–3589

    Google Scholar 

  • Masutani H, Yodoi J (2002) Thioredoxin. Overview. Methods Enzymol 347:279–286

    Article  PubMed  CAS  Google Scholar 

  • 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 49:1328–1341

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Matsukawa J, Matsuzawa A, Takeda K, Ichijo H (2004) The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 136:261–265

    Article  PubMed  CAS  Google Scholar 

  • 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 277:40703–40709

    Article  PubMed  CAS  Google Scholar 

  • 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 130:1–8

    Article  PubMed  CAS  Google Scholar 

  • 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 1708:1325–1336

    Article  CAS  Google Scholar 

  • Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114:181–190

    Article  PubMed  CAS  Google Scholar 

  • Migliaccio E, Giorgio M, Pelicci PG (2006) Apoptosis and aging: role of p66Shc redox protein. Antioxid Redox Signal 8:600–608

    Article  PubMed  CAS  Google Scholar 

  • Miller DM, Buettner GR, Aust SD (1990) Transition metals as catalysts of “autoxidation” reactions. Free Radic Biol Med 8:95–108

    Article  PubMed  CAS  Google Scholar 

  • 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 102:840–848

    Article  PubMed  CAS  Google Scholar 

  • Moreira ME, Barcinski MA (2004) Apoptotic cell and phagocyte interplay: recognition and consequences in different cell systems. An Acad Bras Cienc 76:93–115

    Article  PubMed  CAS  Google Scholar 

  • 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 20:6028–6036

    Article  PubMed  CAS  Google Scholar 

  • 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 173:932–939

    Article  PubMed  CAS  Google Scholar 

  • Muller FL, Liu Y, Van Remmen H (2004) Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 279:49064–49073

    Article  PubMed  CAS  Google Scholar 

  • Nagai H, Noguchi T, Takeda K, Ichijo H (2007) Pathophysiological roles of ASK1-MAP kinase signaling pathways. J Biochem Mol Biol 40:1–6

    Article  PubMed  CAS  Google Scholar 

  • 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 36:805–818

    Article  PubMed  CAS  Google Scholar 

  • Nagata S (1999) Fas ligand-induced apoptosis. Annu Rev Genet 33:29–55

    Article  PubMed  CAS  Google Scholar 

  • 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 403:98–103

    Article  PubMed  CAS  Google Scholar 

  • Nakamura T, Kazuichi S (2008) Forkhead transcription factor FOXO subfamily is essential for reactive oxygen species-induced apoptosis. Mol Cell Endocrinol 281:47–55

    Article  PubMed  CAS  Google Scholar 

  • Nishikawa T, Edelstein D, Du XL, Yamagishi S et al (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787–790

    Article  PubMed  CAS  Google Scholar 

  • 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 2:389–395

    Article  PubMed  CAS  Google Scholar 

  • 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 280:37033–37040

    Google Scholar 

  • 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 288:1053–1058

    Article  PubMed  CAS  Google Scholar 

  • Oleinik NV, Krupenko NI, Krupenko SA (2007) Cooperation between JNK1 and JNK2 in activation of p53 apoptotic pathway. Oncogene 26:7222–7230

    Article  PubMed  CAS  Google Scholar 

  • Orr WC, Sohal RS (1994) Extension of life-span by over expression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263:1128–1130

    Article  PubMed  CAS  Google Scholar 

  • Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183

    Article  PubMed  CAS  Google Scholar 

  • Orrenius S, Nicotera P, Zhivotovsky B (2011) Cell death mechanisms and their implications in toxicology. Toxicol Sci 119:3–19

    Article  PubMed  CAS  Google Scholar 

  • 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 99:1259–1263

    Article  PubMed  CAS  Google Scholar 

  • 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 94:1356–1367

    Article  PubMed  CAS  Google Scholar 

  • 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 283:129–139

    Article  PubMed  CAS  Google Scholar 

  • Pal PB, Pal S, Das J, Sil PC (2012) Modulation of mercury-induced mitochondria-dependent apoptosis by glycine in hepatocytes. Amino Acids 42:1669–1683

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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 22:7721–7730

    Article  PubMed  CAS  Google Scholar 

  • 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 304:55–68

    Article  PubMed  CAS  Google Scholar 

  • 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 273:7770–7775

    Article  PubMed  CAS  Google Scholar 

  • 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 102:19126–19131

    Article  PubMed  CAS  Google Scholar 

  • Pierce GB, Parchment RE, Lewellyn AL (1991) Hydrogen peroxide as a mediator of programmed cell death in the blastocyst. Differentiation 46:181–186

    Article  PubMed  CAS  Google Scholar 

  • 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 9:505–512

    Article  PubMed  CAS  Google Scholar 

  • 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 3:287–296

    Article  PubMed  CAS  Google Scholar 

  • 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 240:348–354

    Article  PubMed  CAS  Google Scholar 

  • Raman M, Chen W, Cobb MH (2007) Differential regulation and properties of MAPKs. Oncogene 26:3100–3112

    Article  PubMed  CAS  Google Scholar 

  • 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 46:240–252

    Article  PubMed  CAS  Google Scholar 

  • 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 51:317–329

    Article  PubMed  CAS  Google Scholar 

  • Rasola A, Bernardi P (2007) The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12:815–833

    Google Scholar 

  • Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990

    Article  PubMed  CAS  Google Scholar 

  • Rhee SG (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312:1882–1883

    Article  PubMed  Google Scholar 

  • 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–C422

    Article  PubMed  CAS  Google Scholar 

  • Ristow M, Zarse K (2010) How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 45:410–418

    Article  PubMed  CAS  Google Scholar 

  • Rostovtseva TK, TanW Colombini M (2005) On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 37:129–142

    Article  PubMed  CAS  Google Scholar 

  • 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 273:10232–10239

    Article  PubMed  CAS  Google Scholar 

  • 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 43:995–1007

    Article  PubMed  CAS  Google Scholar 

  • Rudel T, Bokoch GM (1997) Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276:1571–1574

    Article  PubMed  CAS  Google Scholar 

  • 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 368:705–720

    Article  PubMed  CAS  Google Scholar 

  • 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 23:2861–2874

    Article  PubMed  CAS  Google Scholar 

  • 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 17:2596–2606

    Article  PubMed  CAS  Google Scholar 

  • 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 24:1711–1719

    Article  PubMed  CAS  Google Scholar 

  • 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 290:208–217

    Article  PubMed  CAS  Google Scholar 

  • 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 21:415–428

    Article  PubMed  CAS  Google Scholar 

  • 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 372:359–369

    Article  PubMed  CAS  Google Scholar 

  • 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 2:55–67

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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 19:2668–2681

    Article  PubMed  CAS  Google Scholar 

  • Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483–487

    Article  PubMed  CAS  Google Scholar 

  • Sies H (1991) Oxidative stress: from basic research to clinical application. Am J Med 91:31S–38S

    Article  PubMed  CAS  Google Scholar 

  • 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:e34200

    Article  PubMed  CAS  Google Scholar 

  • Sinha M, Manna P, Sil PC (2007a) Taurine, a conditionally essential amino acid, ameliorates arsenic-induced cytotoxicity in murine hepatocytes. Toxicol In Vitro 21:1419–1428

    Article  PubMed  CAS  Google Scholar 

  • 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 81:397–406

    Article  PubMed  CAS  Google Scholar 

  • Sinha M, Manna P, Sil PC (2008a) Taurine protects antioxidant defense system in the erythrocytes of cadmium treated mice. BMB Rep 41:657–663

    Article  PubMed  CAS  Google Scholar 

  • Sinha M, Manna P, Sil PC (2008b) Terminalia arjuna protects mice hearts against sodium fluoride-induced oxidative stress. J Med Food 11:733–740

    Article  PubMed  CAS  Google Scholar 

  • Sinha M, Manna P, Sil PC (2008c) Cadmium induced neurological disorders: prophylactic role of taurine. J Appl Toxicol 28:974–986

    PubMed  CAS  Google Scholar 

  • Sinha M, Manna P, Sil PC (2008d) Arjunolic acid attenuates arsenic-induced nephrotoxicity. Pathophysiology 15:147–156

    Article  PubMed  CAS  Google Scholar 

  • Sinha M, Manna P, Sil PC (2008e) Protective effect of arjunolic acid against arsenic-induced oxidative stress in mouse brain. J Biochem Mol Toxicol 22:15–26

    Article  PubMed  CAS  Google Scholar 

  • 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 23:300–313

    Article  PubMed  CAS  Google Scholar 

  • Soga M, Matsuzawa A, Ichijo H (2012) Oxidative stress-induced diseases via the ASK1 Signaling pathway. Int J Cell Biol 2012:439587

    PubMed  Google Scholar 

  • 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 373:845–853

    Article  PubMed  CAS  Google Scholar 

  • 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 277:46566–46575

    Article  PubMed  CAS  Google Scholar 

  • 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 96:3775–3780

    Article  PubMed  CAS  Google Scholar 

  • 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 188:211–216

    Google Scholar 

  • Strasser A, O’Connor L, Dixit VM (2000) Apoptosis signaling. Annu Rev Biochem 69:217–245

    Article  PubMed  CAS  Google Scholar 

  • Sunayama J, Tsuruta F, Masuyama N, Gotoh Y (2005) JNK antagonizes Akt-mediated survival signals by phosphorylating 14–3-3. J Cell Biol 170:295–304

    Article  PubMed  CAS  Google Scholar 

  • Supale S, Li N, Brun T, Maechler P (2012) Mitochondrial dysfunction in pancreatic β cells. Trends Endocrinol Metab 23(9):477–487

    Article  PubMed  CAS  Google Scholar 

  • Takeda K, Matsuzawa A, Nishitoh H, Ichijo H (2003) Roles of MAPKKK ASK1 in stress-induced cell death. Cell Struct Funct 28:23–29

    Article  PubMed  CAS  Google Scholar 

  • 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 282:7522–7531

    Article  PubMed  CAS  Google Scholar 

  • 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 2:222–228

    Article  PubMed  CAS  Google Scholar 

  • 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 191:95–104

    Article  PubMed  CAS  Google Scholar 

  • 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 16:103–114

    Article  PubMed  CAS  Google Scholar 

  • 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 288:870–874

    Article  PubMed  CAS  Google Scholar 

  • Tretter L, Adam-Vizi V (2004) Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J Neurosci 24:7771–7778

    Article  PubMed  CAS  Google Scholar 

  • Tsai WB, Chung YM, Takahashi Y, Xu Z, Hu MC (2008) Functional interaction between FOXO3a and ATM regulates DNA damage response. Nat Cell Biol 10:460–467

    Article  PubMed  CAS  Google Scholar 

  • 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 23:1889–1899

    Article  PubMed  CAS  Google Scholar 

  • Turjanski AG, Vaque JP, Gutkind JS (2007) MAP kinases and the control of nuclear events. Oncogene 26:3240–3253

    Article  PubMed  CAS  Google Scholar 

  • Turrens JF, Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191:421–427

    PubMed  CAS  Google Scholar 

  • Turrens JF, Alexandre A, Lehninger AL (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237:408–414

    Article  PubMed  CAS  Google Scholar 

  • Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266:37–56

    Article  PubMed  CAS  Google Scholar 

  • Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  PubMed  CAS  Google Scholar 

  • 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 39:44–84

    Article  PubMed  CAS  Google Scholar 

  • 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 102:43–53

    Article  PubMed  CAS  Google Scholar 

  • Vorbach C, Harrison R, Capecchi MR (2003) Xanthine oxidoreductase is central to the evolution and function of the innate immune system. Trends Immunol 24:512–517

    Google Scholar 

  • Wallace DC (1999) Mitochondrial diseases in man and mouse. Science 283:1482–1488

    Article  PubMed  CAS  Google Scholar 

  • Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15:2922–2933

    PubMed  CAS  Google Scholar 

  • 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 253:33–37

    Article  PubMed  CAS  Google Scholar 

  • 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 19:1844–1856

    Article  PubMed  CAS  Google Scholar 

  • 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 180:3072–3080

    PubMed  CAS  Google Scholar 

  • 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 263:10262–10266

    PubMed  CAS  Google Scholar 

  • 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 14:2060–2071

    PubMed  CAS  Google Scholar 

  • Wold LE, Ceylan-Isik AF, Ren J (2005) Oxidative stress and stress signaling: menace of diabetic cardiomyopathy. Acta Pharmacol Sin 26:908–917

    Article  PubMed  CAS  Google Scholar 

  • Wolff SP, Dean RT (1987) Glucose autoxidation and protein modification. The potential role of “autoxidative glycosylation” in diabetes. Biochem J 245: 243–250

    PubMed  CAS  Google Scholar 

  • Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555–556

    Article  PubMed  CAS  Google Scholar 

  • Wyllie AH (2010) “Where, O death, is thy sting?” A brief review of apoptosis biology. Mol Neurobiol 42:4–9

    Article  PubMed  CAS  Google Scholar 

  • 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 277:28051–28057

    Article  PubMed  CAS  Google Scholar 

  • 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 94:516–519

    Article  Google Scholar 

  • 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 19:8469–8478

    PubMed  CAS  Google Scholar 

  • 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 80:285–291

    Article  PubMed  CAS  Google Scholar 

  • Yim S, Malhotra A, Veves A (2007) Antioxidants and CVD in diabetes: where do we stand now? Curr Diab Rep 7:8–13

    Article  PubMed  CAS  Google Scholar 

  • Zeiss CJ (2003) The apoptosis-necrosis continuum: insights from genetically altered mice. Vet Pathol 40:481–495

    Article  PubMed  CAS  Google Scholar 

  • 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 96:8511–8515

    Article  PubMed  CAS  Google Scholar 

  • 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 279:44955–44965

    Article  PubMed  CAS  Google Scholar 

  • 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 47:74–80

    Article  PubMed  CAS  Google Scholar 

  • 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 113:1235–1243

    Article  PubMed  CAS  Google Scholar 

  • 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 9:817–828

    Article  PubMed  CAS  Google Scholar 

  • 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 29:4167–4176

    Article  PubMed  CAS  Google Scholar 

  • 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 13:382–387

    Article  PubMed  CAS  Google Scholar 

  • 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 9:1381–1386

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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

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Sinha, K., Das, J., Pal, P.B. et al. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87, 1157–1180 (2013). https://doi.org/10.1007/s00204-013-1034-4

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