Crosstalk of reactive oxygen species and NF-κB signaling

Cell Research - Tập 21 Số 1 - Trang 103-115 - 2011
M. Morgan1, Zheng-gang Liu2
1Cell and Cancer Biology Branch, Center for Cancer Research, National Cancer Institute, NIH, 37 Convent Drive, RM1130, Bethesda, MD 20892, USA.
2Cell and Cancer Biology Branch, Center for Cancer Research, National Cancer Institute, Bethesda

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Hayden MS, Ghosh S . Shared principles in NF-kappaB signaling. Cell 2008; 132:344–362.

Vallabhapurapu S, Karin M . Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 2009; 27:693–733.

Hatada EN, Nieters A, Wulczyn FG, et al. The ankyrin repeat domains of the NF-kappa B precursor p105 and the protooncogene bcl-3 act as specific inhibitors of NF-kappa B DNA binding. Proc Natl Sci USA 1992; 89:2489–2493.

Bonizzi G, Karin M . The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25:280–288.

Beinke S, Ley SC . Functions of NF-kappaB1 and NF-kappaB2 in immune cell biology. Biochem J 2004; 382(Pt 2):393–409.

Senftleben U, Cao Y, Xiao G, et al. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 2001; 293:1495–1499.

Xiao G, Harhaj EW, Sun SC . NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell 2001; 7:401–409.

Dejardin E, Droin NM, Delhase M, et al. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 2002; 17:525–535.

Liao G, Zhang M, Harhaj EW, Sun SC . Regulation of the NF-kappaB-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J Biol Chem 2004; 279:26243–26250.

Zarnegar BJ, Wang Y, Mahoney DJ, et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 2008; 9:1371–1378.

Vallabhapurapu S, Matsuzawa A, Zhang W, et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 2008; 9:1364–1370.

Xiao G, Fong A, Sun SC . Induction of p100 processing by NF-kappaB-inducing kinase involves docking IkappaB kinase alpha (IKKalpha) to p100 and IKKalpha-mediated phosphorylation. J Biol Chem 2004; 279:30099–30105.

Rhee SG, Yang KS, Kang SW, Woo HA, Chang TS . Controlled elimination of intracellular H(2)O(2): regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid Redox Signal 2005; 7:619–626.

Holmgren A . Antioxidant function of thioredoxin and glutaredoxin systems. Antioxid Redox Signal 2000; 2:811–820.

Sies H . Oxidative stress: oxidants and antioxidants. Exp Physiol 1997; 82:291–295.

Saitoh M, Nishitoh H, Fujii M, et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998; 17:2596–2606.

Liu H, Nishitoh H, Ichijo H, Kyriakis JM . 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 2000; 20:2198–2208.

Noguchi T, Takeda K, Matsuzawa A et al. 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 2005; 280:37033–37040.

Liu Y, Min W . Thioredoxin promotes ASK1 ubiquitination and degradation to inhibit ASK1-mediated apoptosis in a redox activity-independent manner. Circ Res 2002; 90:1259–1266.

Li X, Luo Y, Yu L, et al. SENP1 mediates TNF-induced desumoylation and cytoplasmic translocation of HIPK1 to enhance ASK1-dependent apoptosis. Cell Death Differ 2008; 15:739–750.

Lambeth JD . NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 2004; 4:181–189.

Brown DI, Griendling KK . Nox proteins in signal transduction. Free Radic Biol Med 2009; 47:1239–1253.

Quinn MT, Ammons MC, Deleo FR . The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction. Clin Sci (Lond) 2006; 111:1–20.

Ushio-Fukai M . Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal 2009; 11:1289–1299.

Saito Y, Nishio K, Ogawa Y, et al. Turning point in apoptosis/necrosis induced by hydrogen peroxide. Free Radic Res 2006; 40:619–630.

Takeda M, Shirato I, Kobayashi M, Endou H . Hydrogen peroxide induces necrosis, apoptosis, oncosis and apoptotic oncosis of mouse terminal proximal straight tubule cells. Nephron 1999; 81:234–238.

Teramoto S, Tomita T, Matsui H, et al. Hydrogen peroxide-induced apoptosis and necrosis in human lung fibroblasts: protective roles of glutathione. Jpn J Pharmacol 1999; 79:33–40.

Perkins ND, Gilmore TD . Good cop, bad cop: the different faces of NF-kappaB. Cell Death Differ 2006; 13:759–772.

Reuther-Madrid JY, Kashatus D, Chen S, et al. The p65/RelA subunit of NF-kappaB suppresses the sustained, antiapoptotic activity of Jun kinase induced by tumor necrosis factor. Mol Cell Biol 2002; 22:8175–8183.

Tang F, Tang G, Xiang J, et al. The absence of NF-kappaB-mediated inhibition of c-Jun N-terminal kinase activation contributes to tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol 2002; 22:8571–8579.

Morgan MJ, Kim YS, Liu ZG . TNFalpha and reactive oxygen species in necrotic cell death. Cell Res 2008; 18:343–349.

Morgan MJ, Liu ZG . Reactive oxygen species in TNFalpha-induced signaling and cell death. Mol Cells 2010; 30:1–12.

Wullaert A, Heyninck K, Beyaert R . Mechanisms of crosstalk between TNF-induced NF-kappaB and JNK activation in hepatocytes. Biochem Pharmacol 2006; 72:1090–1101.

Nakano H, Nakajima A, Sakon-Komazawa S, et al. Reactive oxygen species mediate crosstalk between NF-kappaB and JNK. Cell Death Differ 2006; 13:730–737.

Papa S, Bubici C, Zazzeroni F, et al. The NF-kappaB-mediated control of the JNK cascade in the antagonism of programmed cell death in health and disease. Cell Death Differ 2006; 13:712–729.

Morgan MJ, Kim YS, Liu Z . Lipid rafts and oxidative stress-induced cell death. Antioxid Redox Signal 2007; 9:1471–1483.

Jones PL, Ping D, Boss JM . Tumor necrosis factor alpha and interleukin-1beta regulate the murine manganese superoxide dismutase gene through a complex intronic enhancer involving C/EBP-beta and NF-kappaB. Mol Cell Biol 1997; 17:6970–6981.

Djavaheri-Mergny M, Javelaud D, Wietzerbin J, Besancon F . NF-kappaB activation prevents apoptotic oxidative stress via an increase of both thioredoxin and MnSOD levels in TNFalpha-treated Ewing sarcoma cells. FEBS Lett 2004; 578:111–115.

Kairisalo M, Korhonen L, Blomgren K, Lindholm D . X-linked inhibitor of apoptosis protein increases mitochondrial antioxidants through NF-kappaB activation. Biochem Biophys Res Commun 2007; 364:138–144.

Das KC, Lewis-Molock Y, White CW . Activation of NF-kappa B and elevation of MnSOD gene expression by thiol reducing agents in lung adenocarcinoma (A549) cells. Am J Physiol 1995; 269(5 Pt 1):L588–L602.

Li Y, Huang TT, Carlson EJ, et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 1995; 11:376–381.

Macmillan-Crow LA, Cruthirds DL . Invited review: manganese superoxide dismutase in disease. Free Radic Res 2001; 34:325–336.

Huang P, Feng L, Oldham EA, Keating MJ, Plunkett W . Superoxide dismutase as a target for the selective killing of cancer cells. Nature 2000; 407:390–395.

Rojo AI, Salinas M, Martin D, Perona R, Cuadrado A . Regulation of Cu/Zn-superoxide dismutase expression via the phosphatidylinositol 3 kinase/Akt pathway and nuclear factor-kappaB. J Neurosci 2004; 24:7324–7334.

Elchuri S, Oberley TD, Qi W, et al. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 2005; 24:367–380.

Pham CG, Bubici C, Zazzeroni F, et al. Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell 2004; 119:529–542.

Torti FM, Torti SV . Regulation of ferritin genes and protein. Blood 2002; 99:3505–3516.

Zhou LZ, Johnson AP, Rando TA . NF kappa B and AP-1 mediate transcriptional responses to oxidative stress in skeletal muscle cells. Free Radic Biol Med 2001; 31:1405–1416.

Schreiber J, Jenner RG, Murray HL, et al. Coordinated binding of NF-kappaB family members in the response of human cells to lipopolysaccharide. Proc Natl Acad Sci USA 2006; 103:5899–5904.

Matsui M, Oshima M, Oshima H, et al. Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev Biol 1996; 178:179–185.

Tanaka T, Hosoi F, Yamaguchi-Iwai Y, et al. Thioredoxin-2 (TRX-2) is an essential gene regulating mitochondria-dependent apoptosis. EMBOJ 2002; 21:1695–1703.

Nonn L, Williams RR, Erickson RP, Powis G . The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol Cell Biol 2003; 23:916–922.

Xia C, Hu J, Ketterer B, Taylor JB . The organization of the human GSTP1-1 gene promoter and its response to retinoic acid and cellular redox status. Biochem J 1996; 313(Pt 1):155–161.

Dourado DF, Fernandes PA, Ramos MJ . Mammalian cytosolic glutathione transferases. Curr Protein Pept Sci 2008; 9:325–337.

Salinas AE, Wong MG . Glutathione S-transferases--a review. Curr Med Chem 1999; 6:279–309.

Dang DT, Chen F, Kohli M, et al. Glutathione S-transferase pi1 promotes tumorigenicity in HCT116 human colon cancer cells. Cancer Res 2005; 65:9485–9494.

Hinata K, Gervin AM, Jennifer Zhang Y, Khavari PA . Divergent gene regulation and growth effects by NF-kappa B in epithelial and mesenchymal cells of human skin. Oncogene 2003; 22:1955–1964.

Howells C, West AK, Chung RS . Neuronal growth-inhibitory factor (metallothionein-3): evaluation of the biological function of growth-inhibitory factor in the injured and neurodegenerative brain. FEBS J 2010; 277:2931–2939.

Kumari MV, Hiramatsu M, Ebadi M . Free radical scavenging actions of metallothionein isoforms I and II. Free Radic Res 1998; 29:93–101.

Yao KS, Hageboutros A, Ford P, O'Dwyer PJ . Involvement of activator protein-1 and nuclear factor-kappaB transcription factors in the control of the DT-diaphorase expression induced by mitomycin C treatment. Mol Pharmacol 1997; 51:422–430.

Dinkova-Kostova AT, Talalay P . NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys 2010; 501:116–123.

Ahn KS, Sethi G, Jain AK, Jaiswal AK, Aggarwal BB . Genetic deletion of NAD(P)H:quinone oxidoreductase 1 abrogates activation of nuclear factor-kappaB, IkappaBalpha kinase, c-Jun N-terminal kinase, Akt, p38, and p44/42 mitogen-activated protein kinases and potentiates apoptosis. J Biol Chem 2006; 281:19798–19808.

Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG . Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci USA 1994; 91:5987–5991.

Wu G, Marin-Garcia J, Rogers TB, Lakatta EG, Long X . Phosphorylation and hypoxia-induced heme oxygenase-1 gene expression in cardiomyocytes. J Card Fail 2004; 10:519–526.

Lin CC, Chiang LL, Lin CH, et al. Transforming growth factor-beta1 stimulates heme oxygenase-1 expression via the PI3K/Akt and NF-kappaB pathways in human lung epithelial cells. Eur J Pharmacol 2007; 560:101–109.

Prawan A, Kundu JK, Surh YJ . Molecular basis of heme oxygenase-1 induction: implications for chemoprevention and chemoprotection. Antioxid Redox Signal 2005; 7:1688–1703.

Lei XG, Cheng WH, McClung JP . Metabolic regulation and function of glutathione peroxidase-1. Annu Rev Nutr 2007; 27:41–61.

Sies H, Sharov VS, Klotz LO, Briviba K . Glutathione peroxidase protects against peroxynitrite-mediated oxidations. A new function for selenoproteins as peroxynitrite reductase. J Biol Chem 1997; 272:27812–27817.

Ciaccio PJ, Walsh ES, Tew KD . Promoter analysis of a human dihydrodiol dehydrogenase. Biochem Biophys Res Commun 1996; 228:524–529.

Penning TM, Ohnishi ST, Ohnishi T, Harvey RG . Generation of reactive oxygen species during the enzymatic oxidation of polycyclic aromatic hydrocarbon trans-dihydrodiols catalyzed by dihydrodiol dehydrogenase. Chem Res Toxicol 1996; 9:84–92.

Chen J, Adikari M, Pallai R, Parekh HK, Simpkins H . Dihydrodiol dehydrogenases regulate the generation of reactive oxygen species and the development of cisplatin resistance in human ovarian carcinoma cells. Cancer Chemother Pharmacol 2008; 61:979–987.

Anrather J, Racchumi G, Iadecola C . NF-kappaB regulates phagocytic NADPH oxidase by inducing the expression of gp91phox. J Biol Chem 2006; 281:5657–5667.

Xu P, Huecksteadt TP, Hoidal JR . Molecular cloning and characterization of the human xanthine dehydrogenase gene (XDH). Genomics 1996; 34:173–180.

Hille R, Nishino T . Flavoprotein structure and mechanism. 4. Xanthine oxidase and xanthine dehydrogenase. FASEB J 1995; 9:995–1003.

Maia L, Vala A, Mira L . NADH oxidase activity of rat liver xanthine dehydrogenase and xanthine oxidase-contribution for damage mechanisms. Free Radic Res 2005; 39:979–986.

Kolyada AY, Savikovsky N, Madias NE . Transcriptional regulation of the human iNOS gene in vascular-smooth-muscle cells and macrophages: evidence for tissue specificity. Biochem Biophys Res Commun 1996; 220:600–605.

Hughes JE, Srinivasan S, Lynch KR, et al. Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ Res 2008; 102:950–958.

Guo Z, Shao L, Du Q, Park KS, Geller DA . Identification of a classic cytokine-induced enhancer upstream in the human iNOS promoter. FASEB J 2007; 21:535–542.

Morris KR, Lutz RD, Choi HS, et al. Role of the NF-kappaB signaling pathway and kappaB cis-regulatory elements on the IRF-1 and iNOS promoter regions in mycobacterial lipoarabinomannan induction of nitric oxide. Infect Immun 2003; 71:1442–1452.

Nakata S, Tsutsui M, Shimokawa H et al. Statin treatment upregulates vascular neuronal nitric oxide synthase through Akt/NF-kappaB pathway. Arterioscler Thromb Vasc Biol 2007; 27:92–98.

Li Y, Zhao Y, Li G, et al. Regulation of neuronal nitric oxide synthase exon 1f gene expression by nuclear factor-kappaB acetylation in human neuroblastoma cells. J Neurochem 2007; 101:1194–1204.

Ahmad R, Rasheed Z, Ahsan H . Biochemical and cellular toxicology of peroxynitrite: implications in cell death and autoimmune phenomenon. Immunopharmacol Immunotoxicol 2009; 31:388–396.

Liaudet L, Vassalli G, Pacher P . Role of peroxynitrite in the redox regulation of cell signal transduction pathways. Front Biosci 2009; 14:4809–4814.

Deng WG, Zhu Y, Wu KK . Up-regulation of p300 binding and p50 acetylation in tumor necrosis factor-alpha-induced cyclooxygenase-2 promoter activation. J Biol Chem 2003; 278:4770–4777.

Inoue H, Tanabe T . Transcriptional role of the nuclear factor kappa B site in the induction by lipopolysaccharide and suppression by dexamethasone of cyclooxygenase-2 in U937 cells. Biochem Biophys Res Commun 1998; 244:143–148.

Marnett LJ, Rowlinson SW, Goodwin DC, Kalgutkar AS, Lanzo CA . Arachidonic acid oxygenation by COX-1 and COX-2. Mechanisms of catalysis and inhibition. J Biol Chem 1999; 274:22903–22906.

Arakawa T, Nakamura M, Yoshimoto T, Yamamoto S . The transcriptional regulation of human arachidonate 12-lipoxygenase gene by NF kappa B/Rel. FEBS Lett 1995; 363:105–110.

Chopra A, Ferreira-Alves DL, Sirois P, Thirion JP . Cloning of the guinea pig 5-lipoxygenase gene and nucleotide sequence of its promoter. Biochem Biophys Res Commun 1992; 185:489–495.

Schweiger D, Furstenberger G, Krieg P . Inducible expression of 15-lipoxygenase-2 and 8-lipoxygenase inhibits cell growth via common signaling pathways. J Lipid Res 2007; 48:553–564.

Uchida K . 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 2003; 42:318–343.

Kim C, Kim JY, Kim JH . Cytosolic phospholipase A(2), lipoxygenase metabolites, and reactive oxygen species. BMB Rep 2008; 41:555–559.

Gillette JR, Brodie BB, La Du BN . The oxidation of drugs by liver microsomes: on the role of TPNH and oxygen. J Pharmacol Exp Ther 1957; 119:532–540.

Thurman RG, Ley HG, Scholz R . Hepatic microsomal ethanol oxidation. Hydrogen peroxide formation and the role of catalase. Eur J Biochem 1972; 25:420–430.

Nordblom GD, Coon MJ . Hydrogen peroxide formation and stoichiometry of hydroxylation reactions catalyzed by highly purified liver microsomal cytochrome P-450. Arch Biochem Biophys 1977; 180:343–347.

Imaoka S, Osada M, Minamiyama Y, et al. Role of phenobarbital-inducible cytochrome P450s as a source of active oxygen species in DNA-oxidation. Cancer Lett 2004; 203:117–125.

Abdel-Razzak Z, Garlatti M, Aggerbeck M, Barouki R . Determination of interleukin-4-responsive region in the human cytochrome P450 2E1 gene promoter. Biochem Pharmacol 2004; 68:1371–1381.

Morgan ET, Li-Masters T, Cheng PY . Mechanisms of cytochrome P450 regulation by inflammatory mediators. Toxicology 2002; 181–182:207–210.

Dulos J, Kaptein A, Kavelaars A, Heijnen C, Boots A . Tumour necrosis factor-alpha stimulates dehydroepiandrosterone metabolism in human fibroblast-like synoviocytes: a role for nuclear factor-kappaB and activator protein-1 in the regulation of expression of cytochrome p450 enzyme 7b. Arthritis Res Ther 2005; 7:R1271–R1280.

Caro AA, Cederbaum AI . Oxidative stress, toxicology, and pharmacology of CYP2E1. Annu Rev Pharmacol Toxicol 2004; 44:27–42.

Cederbaum AI, Wu D, Mari M, Bai J . CYP2E1-dependent toxicity and oxidative stress in HepG2 cells. Free Radic Biol Med 2001; 31:1539–1543.

Nieto N, Friedman SL, Cederbaum AI . Cytochrome P450 2E1-derived reactive oxygen species mediate paracrine stimulation of collagen I protein synthesis by hepatic stellate cells. J Biol Chem 2002; 277:9853–9864.

Kabe Y, Ando K, Hirao S, Yoshida M, Handa H . Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus. Antioxid Redox Signal 2005; 7:395–403.

Meyer M, Schreck R, Baeuerle PA . H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 1993; 12:2005–2015.

Hirota K, Matsui M, Iwata S, et al. AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci USA 1997; 94:3633–3638.

Hirota K, Murata M, Sachi Y, et al. Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J Biol Chem 1999; 274:27891–27897.

Paulsen CE, Carroll KS . Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem Biol 2010; 5:47–62.

Groen A, Lemeer S, van der Wijk T, et al. Differential oxidation of protein-tyrosine phosphatases. J Biol Chem 2005; 280:10298–10304.

Nakashima I, Kato M, Akhand AA, et al. Redox-linked signal transduction pathways for protein tyrosine kinase activation. Antioxid Redox Signal 2002; 4:517–531.

Nakashima I, Takeda K, Kawamoto Y, et al. Redox control of catalytic activities of membrane-associated protein tyrosine kinases. Arch Biochem Biophys 2005; 434:3–10.

Kamata H, Honda S, Maeda S, et al. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005; 120:649–661.

den Hertog J, Groen A, van der Wijk T . Redox regulation of protein-tyrosine phosphatases. Arch Biochem Biophys 2005; 434:11–15.

Toledano MB, Leonard WJ . Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci USA 1991; 88:4328–4332.

Toledano MB, Ghosh D, Trinh F, Leonard WJ . N-terminal DNA-binding domains contribute to differential DNA-binding specificities of NF-kappa B p50 and p65. Mol Cell Biol 1993; 13:852–860.

Matthews JR, Kaszubska W, Turcatti G, Wells TN, Hay RT . Role of cysteine62 in DNA recognition by the P50 subunit of NF-kappa B. Nucleic Acids Res 1993; 21:1727–1734.

Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, Hay RT . Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 1992; 20:3821–3830.

Klatt P, Lamas S . Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 2000; 267:4928–4944.

Pineda-Molina E, Klatt P, Vazquez J, et al. Glutathionylation of the p50 subunit of NF-kappaB: a mechanism for redox-induced inhibition of DNA binding. Biochemistry 2001; 40:14134–14142.

Nishi T, Shimizu N, Hiramoto M, et al. Spatial redox regulation of a critical cysteine residue of NF-kappa B in vivo. J Biol Chem 2002; 277:44548–44556.

Ando K, Hirao S, Kabe Y, et al. A new APE1/Ref-1-dependent pathway leading to reduction of NF-kappaB and AP-1, and activation of their DNA-binding activity. Nucleic Acids Res 2008; 36:4327–4336.

Matthews JR, Botting CH, Panico M, Morris HR, Hay RT . Inhibition of NF-kappaB DNA binding by nitric oxide. Nucleic Acids Res 1996; 24:2236–2242.

Kelleher ZT, Matsumoto A, Stamler JS, Marshall HE . NOS2 regulation of NF-kappaB by S-nitrosylation of p65. J Biol Chem 2007; 282:30667–30672.

Nowak DE, Tian B, Jamaluddin M, et al. RelA Ser276 phosphorylation is required for activation of a subset of NF-kappaB-dependent genes by recruiting cyclin-dependent kinase 9/cyclin T1 complexes. Mol Cell Biol 2008; 28:3623–3638.

Zhong H, May MJ, Jimi E, Ghosh S . The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol Cell 2002; 9:625–636.

Zhong H, Voll RE, Ghosh S . Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1998; 1:661–671.

Gloire G, Piette J . Redox regulation of nuclear post-translational modifications during NF-kappaB activation. Antioxid Redox Signal 2009; 11:2209–2222.

Jamaluddin M, Wang S, Boldogh I, Tian B, Brasier AR . TNF-alpha-induced NF-kappaB/RelA Ser(276) phosphorylation and enhanceosome formation is mediated by an ROS-dependent PKAc pathway. Cellular signalling 2007; 19:1419–1433.

Liu J, Yoshida Y, Yamashita U . DNA-binding activity of NF-kappaB and phosphorylation of p65 are induced by N-acetylcysteine through phosphatidylinositol (PI) 3-kinase. Mol Immunol 2008; 45:3984–3989.

Schieven GL, Kirihara JM, Myers DE, Ledbetter JA, Uckun FM . Reactive oxygen intermediates activate NF-kappa B in a tyrosine kinase-dependent mechanism and in combination with vanadate activate the p56lck and p59fyn tyrosine kinases in human lymphocytes. Blood 1993; 82:1212–1220.

Schoonbroodt S, Ferreira V, Best-Belpomme M, et al. Crucial role of the amino-terminal tyrosine residue 42 and the carboxyl-terminal PEST domain of I kappa B alpha in NF-kappa B activation by an oxidative stress. J Immunol 2000; 164:4292–4300.

Takada Y, Mukhopadhyay A, Kundu GC, et al. Hydrogen peroxide activates NF-kappa B through tyrosine phosphorylation of I kappa B alpha and serine phosphorylation of p65: evidence for the involvement of I kappa B alpha kinase and Syk protein-tyrosine kinase. J Biol Chem 2003; 278:24233–24241.

Canty TG Jr, Boyle EM, Jr ., Farr A, et al. Oxidative stress induces NF-kappaB nuclear translocation without degradation of IkappaBalpha. Circulation 1999; 100(19 Suppl):II361–II364.

Fan C, Li Q, Ross D, Engelhardt JF . Tyrosine phosphorylation of I kappa B alpha activates NF kappa B through a redox-regulated and c-Src-dependent mechanism following hypoxia/reoxygenation. J Biol Chem 2003; 278:2072–2080.

Imbert V, Rupec RA, Livolsi A, et al. Tyrosine phosphorylation of I kappa B-alpha activates NF-kappa B without proteolytic degradation of I kappa B-alpha. Cell 1996; 86:787–798.

Lluis JM, Buricchi F, Chiarugi P, Morales A, Fernandez-Checa JC . Dual role of mitochondrial reactive oxygen species in hypoxia signaling: activation of nuclear factor-{kappa}B via c-SRC and oxidant-dependent cell death. Cancer Res 2007; 67:7368–7377.

Koong AC, Chen EY, Giaccia AJ . Hypoxia causes the activation of nuclear factor kappa B through the phosphorylation of I kappa B alpha on tyrosine residues. Cancer Res 1994; 54:1425–1430.

Beraud C, Henzel WJ, Baeuerle PA . Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NF-kappaB activation. Proc Natl Acad Sci USA 1999; 96:429–434.

Fan C, Li Q, Zhang Y, et al. IkappaBalpha and IkappaBbeta possess injury context-specific functions that uniquely influence hepatic NF-kappaB induction and inflammation. J Clin Invest 2004; 113:746–755.

Llacuna L, Mari M, Lluis JM, et al. Reactive oxygen species mediate liver injury through parenchymal nuclear factor-kappaB inactivation in prolonged ischemia/reperfusion. Am J Pathol 2009; 174:1776–1785.

Kil IS, Kim SY, Park JW . Glutathionylation regulates IkappaB. Biochem Biophys Res Commun 2008; 373:169–173.

Wu M, Bian Q, Liu Y, et al. Sustained oxidative stress inhibits NF-kappaB activation partially via inactivating the proteasome. Free Radic Biol Med 2009; 46:62–69.

Panopoulos A, Harraz M, Engelhardt JF, Zandi E . Iron-mediated H2O2 production as a mechanism for cell type-specific inhibition of tumor necrosis factor alpha-induced but not interleukin-1beta-induced IkappaB kinase complex/nuclear factor-kappaB activation. J Biol Chem 2005; 280:2912–2923.

Reynaert NL, van der Vliet A, Guala AS, et al. Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc Natl Sci USA 2006; 103:13086–13091.

Korn SH, Wouters EF, Vos N, Janssen-Heininger YM . Cytokine-induced activation of nuclear factor-kappa B is inhibited by hydrogen peroxide through oxidative inactivation of IkappaB kinase. J Biol Chem 2001; 276:35693–35700.

Byun MS, Jeon KI, Choi JW, Shim JY, Jue DM . Dual effect of oxidative stress on NF-kappakB activation in HeLa cells. Exp Mol Med 2002; 34:332–339.

Kapahi P, Takahashi T, Natoli G, et al. Inhibition of NF-kappa B activation by arsenite through reaction with a critical cysteine in the activation loop of Ikappa B kinase. J Biol Chem 2000; 275:36062–36066.

Reynaert NL, Ckless K, Korn SH, et al. Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation. Proc Natl Acad Sci USA 2004; 101:8945–8950.

Rossi A, Kapahi P, Natoli G, et al. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase. Nature 2000; 403:103–108.

Herscovitch M, Comb W, Ennis T, et al. Intermolecular disulfide bond formation in the NEMO dimer requires Cys54 and Cys347. Biochem Biophys Res Commun 2008; 367:103–108.

Jaspers I, Zhang W, Fraser A, Samet JM, Reed W . Hydrogen peroxide has opposing effects on IKK activity and IkappaBalpha breakdown in airway epithelial cells. Am J Respir Cell Mol Biol 2001; 24:769–777.

Kamata H, Manabe T, Oka S, Kamata K, Hirata H . Hydrogen peroxide activates IkappaB kinases through phosphorylation of serine residues in the activation loops. FEBS Lett 2002; 519:231–237.

Cross JV, Templeton DJ . Thiol oxidation of cell signaling proteins: Controlling an apoptotic equilibrium. J Cell Biochem 2004; 93:104–111.

Xia Y, Makris C, Su B, et al. MEK kinase 1 is critically required for c-Jun N-terminal kinase activation by proinflammatory stimuli and growth factor-induced cell migration. Proc Natl Acad Sci USA 2000; 97:5243–5248.

Yang J, Lin Y, Guo Z, et al. The essential role of MEKK3 in TNF-induced NF-kappaB activation. Nat Immunol 2001; 2:620–624.

Blonska M, Shambharkar PB, Kobayashi M, et al. TAK1 is recruited to the tumor necrosis factor-alpha (TNF-alpha) receptor 1 complex in a receptor-interacting protein (RIP)-dependent manner and cooperates with MEKK3 leading to NF-kappaB activation. J Biol Chem 2005; 280:43056–43063.

Ryabinina OP, Subbian E, Iordanov MS . D-MEKK1, the Drosophila orthologue of mammalian MEKK4/MTK1, and Hemipterous/D-MKK7 mediate the activation of D-JNK by cadmium and arsenite in Schneider cells. BMC Cell Biol 2006; 7:7.

Liu HH, Xie M, Schneider MD, Chen ZJ . Essential role of TAK1 in thymocyte development and activation. Proc Natl Acad Sci USA 2006; 103:11677–11682.

Shim JH, Xiao C, Paschal AE, et al. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 2005; 19:2668–2681.

Sato S, Sanjo H, Takeda K, et al. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 2005; 6:1087–1095.

Takaesu G, Surabhi RM, Park KJ, et al. TAK1 is critical for IkappaB kinase-mediated activation of the NF-kappaB pathway. J Mol Biol 2003; 326:105–115.

Li Q, Engelhardt JF . Interleukin-1beta induction of NFkappaB is partially regulated by H2O2-mediated activation of NFkappaB-inducing kinase. J Biol Chem 2006; 281:1495–1505.

Madrid LV, Mayo MW, Reuther JY, Baldwin AS Jr . Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38. J Biol Chem 2001; 276:18934–18940.

Dan HC, Cooper MJ, Cogswell PC, et al. Akt-dependent regulation of NF-{kappa}B is controlled by mTOR and Raptor in association with IKK. Genes Dev 2008; 22:1490–1500.

Murata H, Ihara Y, Nakamura H, et al. Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J Biol Chem 2003; 278:50226–50233.

Lee SR, Yang KS, Kwon J, et al. Reversible inactivation of the tumor suppressor PTEN by H2O2. J Biol Chem 2002; 277:20336–20342.