NF-kappaB signaling pathway and free radical impact

• Autorzy: Siomek A.
• Języki publikacji: EN

Abstrakty

EN

 The activation of NF-κB transcription factor is critical for a wide range of processes such as immunity, inflammation, cell development, growth and survival. It is activated by a variety of stimuli including cytokines, ionizing radiation and oxidative stress. Redox modulations of NF-κB pathway have been widely demonstrated. Studies carried out during last years have advanced our knowledge about possible connections between NF-κB pathway and the impact of free radicals. This review is an endeavor to gather recent results focused on this issue, although an important question, whether oxidative stress plays a physiological role in NF-κB activation, seems to be still unanswered.

Słowa kluczowe

EN

free radical; nuclear-factor kappa B signalling; reactive oxygen species; nitrogen oxygen species; transcription factor; immunity; inflammation; cell development; cell growth; survival; oxidative stress; redox; physiological role

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2012
• Tom: 59
• Numer: 3
• Opis fizyczny: p.323-331,fig.,ref.

Twórcy

autor

Siomek A.

• Nicolaus Copernicus University, Department of Clinical Biochemistry, Collegium Medicum in Bydgoszcz, Bydgoszcz, Poland

Bibliografia

• Ando K, Hirao S, Kabe Y, Ogura Y, Sato I, Yamaguchi Y, Wada T, Handa H (2008) A new APE1/Ref-1-dependent pathway leading to reduction of NF-κB and AP-1, and activation of their DNA-binding activity. Nucleic Acids Res 36: 4327-4336. 
• Barkett M, Gilmore TD (1999) Control of apoptosis by Rel/NF-κB transcription factors. Oncogene 18: 6910-24. 
• Basak S, Hoffmann A (2008) Crosstalk via the NF-κB signaling system. Cytokine Growth Factor Rev 19: 187-197. 
• Bonizzi G, Karin M (2004) The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288. 
• Brzoska K, Sochanowicz B, Siomek A, Olinski R, Kruszewski M (2011) Alterations in the expression of genes related to NF-κB signaling in liver and kidney of CuZnSOD-deficient mice. Mol Cell Biochem 353: 151-157. 
• Bubici C, Papa S, Pham CG, Zazzeroni F, Franzoso G (2004) NF-κB and JNK: an intricate affair. Cell Cycle 3: 1524-1529. 
• Byun MS, Jeon KI, Choi JW, Shim JY, Jue DM (2002) Dual effect of oxidative stress on NF-κB activation in HeLa cells. Exp Mol Med 34: 332-339. 
• Calao M, Burny A, Quivy V, Dekoninck A, Van L C (2008) A pervasive role of histone acetyltransferases and deacetylases in an NF-κB-signaling code. Trends Biochem. Sci 33: 339-349. 
• Chen L F, Greene WC (2003) Regulation of distinct biological activities of the NF-κB transcription factor complex by acetylation. J Mol Med (Berl) 81: 549-557. 
• Cross JV, Templeton D J (2004a) Oxidative stress inhibits MEKK1 by site-specific glutathionylation in the ATP-binding domain. Biochem J 381: 675-683. 
• Cross JV, Templeton D J (2004b) Thiol oxidation of cell signaling proteins: Controlling an apoptotic equilibrium. J Cell Biochem 93: 104-111. 
• Cummins E P, Berra E, Comerford KM, Ginouves A, Fitzgerald KT, Seeballuck F, Godson C, Nielsen J E, Moynagh P, Pouyssegur J, Taylor CT (2006) Prolyl hydroxylase-1 negatively regulates IκB kinase-β giving insight into hypoxia-induced NFκB activity. Proc Natl Acad Sci USA 103: 18154-18159. 
• Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252. 
• Dejardin E (2006) The alternative NF-κB pathway from biochemistry to biology: pitfalls and promises for future drug development. Biochem Pharmacol 72: 1161-1179. 
• Deng WG, Zhu Y, Wu K K (2003) Up-regulation of p300 binding and p50 acetylation in Tumor Necrosis Factor-α-induced cyclooxygenase-2 promoter activation. J Biol Chem 278: 4770-4777. 
• DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M (1997) A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388: 548-554. 
• DiDonato JA, Mercurio F, Karin M (1995) Phosphorylation of IκBα precedes but is not sufficient for its dissociation from NF-κB. Mol Cell Biol 15: 1302-1311. 
• Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95. 
• Dudek EJ, Shang F, Taylor A (2001) H2O2-mediated oxidative stress activates NF-κB in lens epithelial cells. Free Radic Biol Med 31: 651-658. 
• Elchuri S, Oberley TD, Qi W, Eisenstein R S, Jackson RL, Van RH, Epstein CJ, Huang TT (2005) CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24: 367-380. 
• Fridovich I (1997) Superoxide anion radical (O2•- ), superoxide dismutases, and related matters. J Biol Chem 272: 18515-18517. 
• Gallagher D, Gutierrez H, Gavalda N, O'Keeffe G, Hay R, Davies AM (2007) Nuclear factor-κB activation via tyrosine phosphorylation of inhibitor κB-α is crucial for ciliary neurotrophic factor-promoted neurite growth from developing neurons. J Neurosci 27: 9664-9669. 
• Ghosh S, Karin M, (2002) Missing pieces in the NF-κB puzzle. Cell 109 (Suppl): S81-S96. 
• Gloire G, Legrand-Poels S, Piette J (2006) NF-κB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol 72: 1493-1505. 
• Gloire G, Piette J (2009) Redox regulation of nuclear post-translational modifications during NF-κB activation. Antioxid Redox Signal 11: 2209-2222. 
• Hayakawa M, Miyashita H, Sakamoto I, Kitagawa M, Tanaka H, Yasuda H, Karin M, Kikugawa K (2003) Evidence that reactive oxygen species do not mediate NF-κB activation. EMBO J 22: 3356-3366. 
• Herscovitch M, Comb W, Ennis T, Coleman K, Yong S, Armstead B, Kalaitzidis D, Chandani S, Gilmore TD (2008) Intermolecular disulfide bond formation in the NEMO dimer requires Cys54 and Cys347. Biochem Biophys Res Commun 367: 103-108. 
• Hoffmann A, Baltimore D (2006) Circuitry of nuclear factor κB signaling. Immunol Rev 210: 171-186. 
• Huang TT, Raineri I, Eggerding F, Epstein CJ (2002) Transgenic and mutant mice for oxygen free radical studies. Methods Enzymol 349: 191-213. 
• Imbert V, Rupec RA, Livolsi A, Pahl HL, Traenckner E B, Mueller-Dieckmann C, Farahifar D, Rossi B, Auberger P, Baeuerle PA, Peyron JF (1996) Tyrosine phosphorylation of IκB-α activates NF-κB without proteolytic degradation of IκB-α. Cell 86: 787-798. 
• Jamaluddin M, Wang S, Boldogh I, Tian B, Brasier AR (2007) TNF-α-induced NF-κB/RelA Ser(276) phosphorylation and enhanceosome formation is mediated by an ROS-dependent PKAc pathway. Cell Signal 19: 1419-1433. 
• Johnson F, Giulivi C (2005) Superoxide dismutases and their impact upon human health. Mol Aspects Med 26: 340-352. 
• Kabe Y, Ando K, Hirao S, Yoshida M, Handa H (2005) Redox regulation of NF-κB activation: distinct redox regulation between the cytoplasm and the nucleus. Antioxid Redox Signal 7: 395-403. 
• Kamata H, Manabe T, Oka S, Kamata K, Hirata H (2002) Hydrogen peroxide activates IκB kinases through phosphorylation of serine residues in the activation loops. FEBS Lett 519: 231-237. 
• Kasof GM, Lu JJ, Liu D, Speer B, Mongan KN, Gomes B C, Lorenzi MV (2001) Tumor necrosis factor-α induces the expression of DR6, a member of the TNF receptor family, through activation of NF-κB. Oncogene 20: 7965-7975. 
• Kelleher ZT, Matsumoto A, Stamler JS, Marshall HE (2007) NOS2 regulation of NF-κB by S-nitrosylation of p65. J Biol Chem 282: 30667-30672. 
• Korn SH, Wouters EF, Vos N, Janssen-Heininger YM (2001) Cytokine-induced activation of nuclear factor-κB is inhibited by hydrogen peroxide through oxidative inactivation of IκB kinase. J Biol Chem 276: 35693-35700. 
• Kucharczak J, Simmons MJ, Fan Y, Gélinas C (2003) To be, or not to be: NF-κB is the answer - role of Rel/NF-κB in the regulation of apoptosis. Oncogene 22: 8961-82.  
• Lee F S, Hagler J, Chen ZJ, Maniatis T (1997) Activation of the IκBα kinase complex by MEKK1, a kinase of the JNK pathway. Cell 88: 213-222. 
• Li N, Karin M (1999) Is NF-κB the sensor of oxidative stress? FASEB J 13: 1137-1143. 
• Lin A (2003) Activation of the JNK signaling pathway: breaking the brake on apoptosis. Bioessays 25: 17-24. 
• Lin A, Karin M (2003) NF-κB in cancer: a marked target. Semin Cancer Biol 13: 107-14. 
• Lin X, Cunningham ET Jr, Mu Y, Geleziunas R, Greene WC (1999) The proto-oncogene Cot kinase participates in CD3/CD28 induction of NF-κB acting through the NF-κB-inducing kinase and IκB kinases. Immunity 10: 271-280. 
• Liu J, Yoshida Y, Yamashita U (2008) DNA-binding activity of NF-κB and phosphorylation of p65 are induced by N-acetylcysteine through phosphatidylinositol (PI) 3-kinase. Mol Immunol 45: 3984-3989. 
• Livolsi A, Busuttil V, Imbert V, Abraham RT, Peyron JF (2001) Tyrosine phosphorylation-dependent activation of NF-κB. Requirement for p56 LCK and ZAP-70 protein tyrosine kinases. Eur J Biochem 268: 1508-1515. 
• Matsuzawa A, Nishitoh H, Tobiume K, Takeda K, Ichijo H (2002) Physiological roles of ASK1-mediated signal transduction in oxidative stress- and endoplasmic reticulum stress-induced apoptosis: advanced findings from ASK1 knockout mice. Antioxid Redox Signal 4: 415-425. 
• Morgan MJ, Liu Z G (2011) Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res 21: 103-115. 
• Nakano H, Nakajima A, Sakon-Komazawa S, Piao JH, Xue X, Okumura K (2006) Reactive oxygen species mediate crosstalk between NF-κB and JNK. Cell Death Differ 13: 730-737. 
• Nemoto S, DiDonato JA, Lin A (1998) Coordinate regulation of IκB kinases by mitogen-activated protein kinase kinase kinase 1 and NF-κB-inducing kinase. Mol Cell Biol 18: 7336-7343. 
• Nemoto S, Finkel T (2002) Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 295: 2450-2452. 
• Nishi T, Shimizu N, Hiramoto M, Sato I, Yamaguchi Y, Hasegawa M, Aizawa S, Tanaka H, Kataoka K, Watanabe H, Handa H (2002) Spatial redox regulation of a critical cysteine residue of NF-κB in vivo. J Biol Chem 277: 44548-44556. 
• Oliveira-Marques V, Marinho HS, Cyrne L, Antunes F (2009) Role of hydrogen peroxide in NF-κB activation: from inducer to modulator. Antioxid Redox Signal 11: 2223-2243.  
• Oliver KM, Garvey JF, Ng CT, Veale DJ, Fearon U, Cummins EP, Taylor CT (2009) Hypoxia activates NF-κB-dependent gene expression through the canonical signaling pathway. Antioxid Redox Signal 11: 2057-2064. 
• Peters RT, Maniatis T (2001) A new family of IKK-related kinases may function as IκB kinase kinases. Biochim Biophys Acta 1471: M57-M62. 
• Qing G, Qu Z, Xiao G (2005) Stabilization of basally translated NF-κB-inducing kinase (NIK) protein functions as a molecular switch of processing of NF-κB2 p100. J Biol Chem 280: 40578-40582. 
• Ravi R, Bedi GC, Engstrom LW, Zeng Q, Mookerjee B, Gelinas C, Fuchs EJ, Bedi A (2001) Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-κB. Nat Cell Biol 3: 409-416. 
• Reynaert NL, van der Vliet A, Guala AS, McGovern T, Hristova M, Pantano C, Heintz NH, Heim J, Ho YS, Matthews DE, Wouters EF, Janssen-Heininger YM (2006) Dynamic redox control of NF-κB through glutaredoxin-regulated S-glutathionylation of inhibitory κB kinase β. Proc Natl Acad Sci USA 103: 13086-13091. 
• Rossi A, Kapahi P, Natoli G, Takahashi T, Chen Y, Karin M, Santoro MG (2000) Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature 403: 103-108. 
• Rothwarf DM, Karin M (1999) The NF-κB activation pathway: a paradigm in information transfer from membrane to nucleus. Sci STKE 1999: RE1. 
• Saito Y, Nishio K, Ogawa Y, Kimata J, Kinumi T, Yoshida Y, Noguchi N, Niki E (2006) Turning point in apoptosis/necrosis induced by hydrogen peroxide. Free Radic Res 40: 619-630. 
• Sakon S, Xue X, Takekawa M, Sasazuki T, Okazaki T, Kojima Y, Piao JH, Yagita H, Okumura K, Doi T, Nakano H (2003) NF-κB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J 22: 3898-3909. 
• Shishodia S, Aggarwal BB (2004) Nuclear factor-κB: a friend or a foe in cancer? Biochem Pharmacol 68: 1071-1080. 
• Schoonbroodt S, Piette J (2000) Oxidative stress interference with the nuclear factor-κB activation pathways. Biochem Pharmacol 60: 1075-1083. 
• Schreck R, Rieber P, Baeuerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J 10: 2247-2258. 
• Sen R, Baltimore D (1986) Inducibility of κ immunoglobulin enhancer-binding protein NF-κB by a posttranslational mechanism. Cell 47: 921-928. 
• Sheppard KA, Rose DW, Haque ZK, Kurokawa R, McInerney E, Westin S, Thanos D, Rosenfeld MG, Glass CK, Collins T (1999) Transcriptional activation by NF-κB requires multiple coactivators. Mol Cell Biol 19: 6367-6378. 
• Sies H, Cadenas E (1985) Oxidative stress: damage to intact cells and organs. Philos Trans R Soc Lond B Biol Sci 311: 617-631. 
• Siomek A, Brzoska K, Sochanowicz B, Gackowski D, Rozalski R, Foksinski M, Zarakowska E, Szpila A, Guz J, Bartlomiejczyk T, Kalinowski B, Kruszewski M, Olinski R (2010) Cu,Zn-superoxide dismutase deficiency in mice leads to organ-specific increase in oxidatively damaged DNA and NF-κB1 protein activity. Acta Biochim Pol 57: 577-583. 
• Storz P, Doppler H, Toker A (2004) Protein kinase Cdelta selectively regulates protein kinase D-dependent activation of NF-κB in oxidative stress signaling. Mol Cell Biol 24: 2614-2626. 
• Storz P, Doppler H, Toker A (2005) Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol Cell Biol 25: 8520-8530. 
• Storz P, Toker A (2003) Protein kinase D mediates a stress-induced NF-κB activation and survival pathway. EMBO J 22: 109-120. 
• Toledano M B, Leonard WJ (1991) Modulation of transcription factor NF-κB binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci USA 88: 4328-4332. 
• Traenckner EB, Pahl HL, Henkel T, Schmidt KN, Wilk S, Baeuerle PA (1995) Phosphorylation of human IκB-α on serines 32 and 36 controls IκB-α proteolysis and NF-κB activation in response to diverse stimuli. EMBO J 14: 2876-2883. 
• Ventura JJ, Cogswell P, Flavell R A, Baldwin AS Jr, Davis RJ (2004) JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species. Genes Dev 18: 2905-2915. 
• Vermeulen L, De WG, Van DP, Vanden BW, Haegeman G (2003) Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 22: 1313-1324. 
• Volanti C, Matroule JY, Piette J (2002) Involvement of oxidative stress in NF-κB activation in endothelial cells treated by photodynamic therapy. Photochem Photobiol 75: 36-45. 
• Walker LJ, Robson CN, Black E, Gillespie D, Hickson ID (1993) Identification of residues in the human DNA repair enzyme HAP1 (Ref-1) that are essential for redox regulation of Jun DNA binding. Mol Cell Biol 13: 5370-5376. 
• Wang T, Zhang X, Li JJ (2002) The role of NF-κB in the regulation of cell stress responses. Int Immunopharmacol 2: 1509-1520. 
• Wu M, Bian Q, Liu Y, Fernandes AF, Taylor A, Pereira P, Shang F (2009) Sustained oxidative stress inhibits NF-κB activation partially via inactivating the proteasome. Free Radic Biol Med 46: 62-69. 
• Yang SR, Chida AS, Bauter MR, Shafiq N, Seweryniak K, Maggirwar SB, Kilty I, Rahman I (2006) Cigarette smoke induces proinflammatory cytokine release by activation of NF-κB and posttranslational modifications of histone deacetylase in macrophages. Am J Physiol Lung Cell Mol Physiol 291: L46-L57. 
• Zarnegar B, Yamazaki S, He JQ, Cheng G (2008) Control of canonical NF-κB activation through the NIK-IKK complex pathway. Proc Natl Acad Sci USA 105: 3503-3508. 
• Zhong H, Voll RE, Ghosh S (1998) Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1: 661-671. 
• Zhou Q, Mrowietz U, Rostami-Yazdi M (2009) Oxidative stress in the pathogenesis of psoriasis. Free Radic Biol Med 47: 891-905.