Redox regulation of NF-κB activation: Distinct redox regulation between the cytoplasm and the nucleus

Antioxidants and Redox Signaling

Volumn 7, Issue 3-4, 2005, Pages 395-403

  Kabe, Yasuaki ^a   Ando, Kozue ^a   Hirao, Satoshi ^a   Yoshida, Makoto ^a   Handa, Hiroshi ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ACETYLCYSTEINE; ANTINEOPLASTIC AGENT; ANTIOXIDANT; CYTOKINE; E 3330; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PYRROLIDINE DITHIOCARBAMATE; QUINONE DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDOX EFFECTOR FACTOR 1; THIOREDOXIN; UNCLASSIFIED DRUG; WORTMANNIN;

CELL NUCLEUS; CELL STIMULATION; CYTOPLASM; DNA BINDING; GENE EXPRESSION; GENE TRANSLOCATION; HUMAN; IMMUNE RESPONSE; INFLAMMATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REDUCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL NUCLEUS; CYTOPLASM; NF-KAPPA B; OXIDATION-REDUCTION; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 14044277556     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2005.7.395     Document Type: Review

References (100)

1. Abo A, Pick E, Hall A, Totty N, Teahan CG, and Segal AW. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 353: 668-670, 1991.
2. Abu-Amer Y, Ross FP, McHugh KP, Livolsi A, Peyron JF, and Teitelbaum SL. Tumor necrosis factor-alpha activation of nuclear transcription factor-kappaB in marrow macrophages is mediated by c-Src tyrosine phosphorylation of Ikappa Balpha. J Biol Chem 273: 29417-29423, 1998.
3. Arias J, Alberts AS, Brindle P, Claret FX, Smeal T, Karin M, Feramisco J, and Montminy M. Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370: 226-229, 1994.
4. Baeuerle PA and Baltimore D. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-kappa B transcription factor. Cell 53: 211-217, 1988.
5. Baeuerle PA and Henkel T. Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12: 141-179, 1994.
6. Baud V and Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 11: 372-377, 2001.
7. Baud V, Liu ZG, Bennett B, Suzuki N, Xia Y, and Karin M. Signaling by proinflammatory cytokines: oligomerization of TRAF2 and TRAF6 is sufficient for JNK and IKK activation and target gene induction via an amino-terminal effector domain. Genes Dev 13: 1297-1308, 1999.
8. Beg AA, Sha WC, Bronson RT, Ghosh S, and Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 376: 167-170, 1995.
9. Beraud C, Henzel WJ, and Baeuerle PA. Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NF-kappaB activation. Proc Natl Acad Sci U S A 96: 429-434, 1999.
10. Blank V, Kourilsky P, and Israel A. Cytoplasmic retention, DNA binding and processing of the NF-kappa B p50 precursor are controlled by a small region in its C-terminus. EMBO J 10: 4159-4167, 1991.
11. Bonizzi G, Piette J, Schoonbroodt S, Greimers R, Havard L, Merville MP, and Bours V. Reactive oxygen intermediate-dependent NF-kappaB activation by interleukin-1beta requires 5-lipoxygenase or NADPH oxidase activity. Mol Cell Biol 19: 1950-1960, 1999.
12. Chandel NS, Schumacker PT, and Arch RH. Reactive oxygen species are downstream products of TRAF-mediated signal transduction. J Biol Chem 276: 42728-42736, 2001.
13. Coso OA, Chiariello M, Yu JC, Teramoto H, Crespo P, Xu N, Miki T, and Gutkind JS. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/ SAPK signaling pathway. Cell 81: 1137-1146, 1995.
14. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252, 2000.
15. de Martin R, Vanhove B, Cheng Q, Hofer E, Csizmadia V, Winkler H, and Bach FH. Cytokine-inducible expression in endothelial cells of an I kappa B alpha-like gene is regulated by NF kappa B. EMBO J 12: 2773-2779, 1993.
16. Derijard B, Raingeaud J, Barrett T, Wu IH, Han J, Ulevitch RJ, and Davis RJ. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267: 682-685, 1995.
17. Devary Y, Rosette C, DiDonato JA, and Karin M. NF-kappa B activation by ultraviolet light not dependent on a nuclear signal. Science 261: 1442-1445, 1993.
18. Ema M, Hirota K, Mimura J, Abe H, Yodoi J, Sogawa K, Poellinger L, and Fujii-Kuriyama Y. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J 18: 1905-1914, 1999.
19. Fan CM and Maniatis T. Generation of p50 subunit of NF-kappa B by processing of p105 through an ATP-dependent pathway. Nature 354: 395-398, 1991.
20. Fan C, Li Q, Ross D, and 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 278: 2072-2080, 2003.
21. Fritz G, Grosch S, Tomicic M, and Kaina B. APE/Ref-1 and the mammalian response to genotoxic stress. Toxicology 193: 67-78, 2003.
22. Hayakawa M, Miyashita H, Sakamoto I, Kitagawa M, Tanaka H, Yasuda H, Karin M, and Kikugawa K. Evidence that reactive oxygen species do not mediate NF-kappaB activation. EMBO J 22: 3356-3366, 2003.
23. Hiramoto M, Shimizu N, Sugimoto K, Tang J, Kawakami Y, Ito M, Aizawa S, Tanaka H, Makino I, and Handa H. Nuclear targeted suppression of NF-kappa B activity by the novel quinone derivative E3330. J Immunol 160: 810-819, 1998.
24. Hirota K, Matsui M, Iwata S, Nishiyama A, Mori K, and Yodoi J. AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci U S A 94: 3633-3638, 1997.
25. Hirota K, Murata M, Sachi Y, Nakamura H, Takeuchi J, Mori K, and Yodoi J. 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 274: 27891-27897, 1999.
26. Hirota K, Matsui M, Murata M, Takashima Y, Cheng FS, Itoh T, Fukuda K, and Yodoi J. Nucleoredoxin, glutaredoxin, and thioredoxin differentially regulate NF-kappaB, AP-1, and CREB activation in HEK293 cells. Biochem Biophys Res Commun 274: 177-182, 2000.
27. Howe CJ, LaHair MM, Maxwell JA, Lee JT, Robinson PJ, Rodriguez-Mora O, McCubrey JA, and Franklin RA. Participation of the calcium/calmodulin-dependent kinases in hydrogen peroxide-induced Ikappa B phosphorylation in human T lymphocytes. J Biol Chem 277: 30469-30476, 2002.
28. Hu Y, Jin X, and Snow ET. Effect of arsenic on transcription factor AP-1 and NF-kappaB DNA binding activity and related gene expression. Toxicol Lett 133: 33-45, 2002.
29. Huxford T, Huang DB, Malek S, and Ghosh G. The crystal structure of the IkappaBalpha/NF-kappaB complex reveals mechanisms of NF-kappaB inactivation. Cell 95: 759-770, 1998.
30. Imbert V, Peyron JF, Farahi Far D, Mari B, Auberger P, and Rossi B. Induction of tyrosine phosphorylation and T-cell activation by vanadate peroxide, an inhibitor of protein tyrosine phosphatases. Biochem J 297 (Pt 1): 163-173, 1994.
31. Imbert V, Rupec RA, Livolsi A, Pahl HL, Traenckner EB, Mueller-Dieckmann C, Farahifar D, Rossi B, Auberger P, Baeuerle PA, and Peyron JF. Tyrosine phosphorylation of I kappa B-alpha activates NF-kappa B without proteolytic degradation of I kappa B-alpha. Cell 86: 787-798, 1996.
32. Jacobs MD and Harrison SC. Structure of an IkappaBalpha/NF-kappaB complex. Cell 95: 749-758, 1998.
33. Janssen-Heininger YM, Poynter ME, and Baeuerle PA. Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radic Biol Med 28: 1317-1327, 2000.
34. Jayaraman L, Murthy KG, Zhu C, Curran T, Xanthoudakis S, and Prives C. Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes Dev 11: 558-570, 1997.
35. Johnson GL and Vaillancourt RR. Sequential protein kinase reactions controlling cell growth and differentiation. Cutr Opin Cell Biol 6: 230-238, 1994.
36. Kamata H, Manabe T, Oka S, Kamata K, and Hirata H. Hydrogen peroxide activates IkappaB kinases through phosphorylation of serine residues in the activation loops. FEBS Lett 519: 231-237, 2002.
37. Knaus UG, Heyworth PG, Evans T, Curnutte JT, and Bokoch GM. Regulation of phagocyte oxygen radical production by the GTP-binding protein Rac 2. Science 254: 1512-1515, 1991.
38. Koong AC, Chen EY, and Giaccia AJ. Hypoxia causes the activation of nuclear factor kappa B through the phosphorylation of I kappa B alpha on tyrosine residues. Cancer Res 54: 1425-1430, 1994.
39. Krejsa CM, Nadler SG, Esselstyn JM, Kavanagh TJ, Ledbetter JA, and Schieven GL. Role of oxidative stress in the action of vanadium phosphotyrosine phosphatase inhibitors. Redox independent activation of NF-kappaB. J Biol Chem 272: 11541-11549, 1997.
40. Kumar S, Bharti A, Mishra NC, Raina D, Kharbanda S, Saxena S, and Kufe D. Targeting of the c-Abl tyrosine kinase to mitochondria in the necrotic cell death response to oxidative stress. J Biol Chem 276: 17281-17285, 2001.
41. Le Bail O, Schmidt-Ullrich R, and Israel A. Promoter analysis of the gene encoding the I kappa B-alpha/MAD3 inhibitor of NF-kappa B: positive regulation by members of the rel/NF-kappa B family. EMBO J 12: 5043-5049, 1993.
42. Lee FS, Hagler J, Chen ZJ, and Maniatis T. Activation of the IkappaB alpha kinase complex by MEKK1, a kinase of the JNK pathway. Cell 88: 213-222, 1997.
43. Lee FS, Peters RT, Dang LC, and Maniatis T. MEKK1 activates both IkappaB kinase alpha and IkappaB kinase beta. Proc Natl Acad Sci U S A 95: 9319-9324, 1998.
44. Lin A. Activation of the JNK signaling pathway: breaking the brake on apoptosis. Bioessays 25: 17-24, 2003.
45. Lin A, Minden A, Martinetto H, Claret FX, Lange-Carter C, Mercurio F, Johnson GL, and Karin M. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268: 286-290, 1995.
46. Livolsi A, Busuttil V, Imbert V, Abraham RT, and Peyron JF. Tyrosine phosphorylation-dependent activation of NF-kappa B. Requirement for p56 LCK and ZAP-70 protein tyrosine kinases. Eur J Biochem 268: 1508-1515, 2001.
47. 2-terminal kinases. J Biol Chem 271: 15703-15707, 1996.
48. Mahabeleshwar GH and Kundu GC. Tyrosine kinase p561ck regulates cell motility and nuclear factor kappaB-mediated secretion of urokinase type plasminogen activator through tyrosine phosphorylation of IkappaBalpha following hypoxia/reoxygenation. J Biol Chem 278: 52598-52612, 2003.
49. Mahon TM and O'Neill LA. Studies into the effect of the tyrosine kinase inhibitor herbimycin A on NF-kappa B activation in T lymphocytes. Evidence for covalent modification of the p50 subunit. J Biol Chem 270: 28557-28564, 1995.
50. Malinin NL, Boldin MP, Kovalenko AV, and Wallach D. MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1. Nature 385: 540-544, 1997.
51. Manna SK, Sah NK, and Aggarwal BB. Protein tyrosine kinase p561ck is required for ceramide-induced but not tumor necrosis factor-induced activation of NF-kappa B, AP-1, JNK, and apoptosis. J Biol Chem 275: 13297-13306, 2000.
52. Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, and Hay RT. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 20: 3821-3830, 1992.
53. Matthews JR, Botting CH, Panico M, Morris HR, and Hay RT. Inhibition of NF-kappaB DNA binding by nitric oxide. Nucleic Acids Res 24: 2236-2242, 1996.
54. Meyer CF, Wang X, Chang C, Templeton D, and Tan TH. Interaction between c-Rel and the mitogen-activated protein kinase kinase kinase I signaling cascade in mediating kappaB enhancer activation. J Biol Chem 271: 8971-8976, 1996.
55. 2 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 12: 2005-2015, 1993.
56. Minden A, Lin A, Claret FX, Abo A, and Karin M. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81: 1147-1157, 1995.
57. Muzio M, Ni J, Feng P, and Dixit VM. IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278: 1612-1615, 1997.
58. Nagakawa J, Hishinuma I, Hirota K, Miyamoto K, Yamanaka T, Yamatsu I, and Katayama K. Protective effects of E3330, a novel quinone derivative, on galactosamine/ tumor necrosis factor-alpha-induced hepatitis in mice. Eur J Pharmacol 229: 63-67, 1992.
59. Nakamura K, Hori T, Sato N, Sugie K, Kawakami T, and Yodoi J. Redox regulation of a src family protein tyrosine kinase p561ck in T cells. Oncogene 8: 3133-3139, 1993.
60. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, and Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398: 252-256, 1999.
61. Nishi T, Shimizu N, Hiramoto M, Sato I, Yamaguchi Y, Hasegawa M, Aizawa S, Tanaka H, Kataoka K, Watanabe H, and Handa H. Spatial redox regulation of a critical cysteine residue of NF-kappa B in vivo. J Biol Chem 277: 44548-44556, 2002.
62. Nishitoh H, Saitoh M, Mochida Y, Takeda K, Nakano H, Rothe M, Miyazono K, and Ichijo H. ASK1 is essential for JNK/SAPK activation by TRAF2. Mol Cell 2: 389-395, 1998.
63. Oka S, Kamata H, Kamata K, Yagisawa H, and Hirata H. N-Acetylcysteine suppresses TNF-induced NF-kappaB activation through inhibition of IkappaB kinases. FEBS Lett 472: 196-202, 2000.
64. O'Neill LA, Bird TA, Gearing AJ, and Saklatvala J. Interleukin-1 signal transduction. Increased GTP binding and hydrolysis in membranes of a murine thymoma line (EL4). J Biol Chem 265: 3146-3152, 1990.
65. Perkins ND. The Rel/NF-kappa B family: friend and foe. Trends Biochem Sci 25: 434-440, 2000.
66. Pomerantz JL and Baltimore D. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 18: 6694-6704, 1999.
67. Pulverer BJ, Kyriakis JM, Avruch J, Nikolakaki E, and Woodgett JR. Phosphorylation of c-jun mediated by MAP kinases. Nature 353: 670-674, 1991.
68. Rayet B and Gelinas C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene 18: 6938-6947, 1999.
69. Regnier CH, Song HY, Gao X, Goeddel DV, Cao Z, and Rothe M. Identification and characterization of an IkappaB kinase. Cell 90: 373-383, 1997.
70. Rice NR, MacKichan ML, and Israel A. The precursor of NF-kappa B p50 has I kappa B-like functions. Cell 71: 243-253, 1992.
71. Rogers RJ, Monnier JM, and Nick HS. Tumor necrosis factor-alpha selectively induces MnSOD expression via mitochondria-to-nucleus signaling, whereas interleukin-1beta utilizes an alternative pathway. J Biol Chem 276: 20419-20427, 2001.
72. Rothe M, Wong SC, Henzel WJ, and Goeddel DV. A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell 78: 681-692, 1994.
73. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazon o K, and Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17: 2596-2606, 1998.
74. Sanchez I, Hughes RT, Mayer BJ, Yee K, Woodgett JR, Avruch J, Kyriakis JM, and Zon LI. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature 372: 794-798, 1994.
75. Sanlioglu S, Williams CM, Samavati L, Butler NS, Wang G, McCray PB Jr, Ritchie TC, Hunninghake GW, Zandi E, and Engelhardt JF. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem 276: 30188-30198, 2001.
76. Schenk H, Klein M, Erdbrugger W, Droge W, and Schulze-Osthoff K. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1. Proc Natl Acad Sci U S A 91: 1672-1676, 1994.
77. Schieven GL, Kirihara JM, Myers DE, Ledbetter JA, and Uckun FM. Reactive oxygen intermediates activate NF-kappa B in a tyrosine kinase-dependent mechanism and in combination with vanadate activate the p561ck and p59fyn tyrosine kinases in human lymphocytes. Blood 82: 1212-1220, 1993.
78. Sen R and Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46: 705-716, 1986.
79. Shimizu N, Sugimoto K, Tang J, Nishi T, Sato I, Hiramoto M, Aizawa S, Hatakeyama M, Ohba R, Hatori H, Yoshikawa T, Suzuki F, Oomori A, Tanaka H, Kawaguchi H, Watanabe H, and Handa H. High-performance affinity beads for identifying drug receptors. Nat Biotechnol 18: 877-881, 2000.
80. Singh S, Darnay BG, and Aggarwal BB. Site-specific tyrosine phosphorylation of IkappaBalpha negatively regulates its inducible phosphorylation and degradation. J Biol Chem 271: 31049-31054, 1996.
81. Sizemore N, Leung S, and Stark GR. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelA subunit. Mol Cell Biol 19: 4798-4805, 1999.
82. Song HY, Regnier CH, Kirschning CJ, Goeddel DV, and Rothe M. Tumor necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kappaB and c-jun N-terminal kinase (JNK/SAPK) pathways at TNF receptor-associated factor 2. Proc Natl Acad Sci U S A 94: 9792-9796, 1997.
83. Storz P and Toker A. Protein kinase D mediates a stress-induced NF-kappaB activation and survival pathway. EMBO J 22: 109-120, 2003.
84. Storz P, Doppler H, and Toker A. Protein kinase Cdelta selectively regulates protein kinase D-dependent activation of NF-kappaB in oxidative stress signaling. Mol Cell Biol 24: 2614-2626, 2004.
85. Sulciner DJ, Irani K, Yu ZX, Ferrans VJ, Goldschmidt-Clermont P, and Finkel T. rac1 regulates a cytokine-stimulated, redox-dependent pathway necessary for NF-kappaB activation. Mol Cell Biol 16: 7115-7121, 1996.
86. Suyang H, Phillips R, Douglas I, and Ghosh S. Role of unphosphorylated, newly synthesized 1 kappa B beta in persistent activation of NF-kappa B. Mol Cell Biol 16: 5444-5449, 1996.
87. Toledano MB and Leonard WJ. Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci U S A 88: 4328-4332, 1991.
88. Urban MB, Schreck R, and Baeuerle PA. NF-kappa B contacts DNA by a heterodimer of the p50 and p65 subunit. EMBO J 10: 1817-1825, 1991.
89. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, and Verma IM. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274: 787-789, 1996.
90. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, and Miyamoto S. Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation. Genes Dev 9: 2723-2735, 1995.
91. Voncken JW, van Schaick H, Kaartinen V, Deemer K, Coates T, Landing B, Pattengale P, Dorseuil O, Bokoch GM, Groffen J, et al. Increased neutrophil respiratory burst in bcr-null mutants. Cell 80: 719-728, 1995.
92. Walker LJ, Robson CN, Black E, Gillespie D, and Hickson ID. Identification of residues in the human DNA repair enzyme HAP1 (Ref-1) that are essential for redox regulation of Jun DNA binding. Mol Cell Bio 13: 5370-5376, 1993.
93. Wei SJ, Botero A, Hirota K, Bradbury CM, Markovina S, Laszlo A, Spitz DR, Goswami PC, Yodoi J, and Gius D. Thioredoxin nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation. Cancer Res 60: 6688-6695, 2000.
94. Xanthoudakis S and Curran T. Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J 11: 653-665, 1992.
95. Xanthoudakis S, Miao GG, and Curran T. The redox and DNA-repair activities of Ref-1 are encoded by nonoverlapping domains. Proc Natl Acad Sci U S A 91: 23-27, 1994.
96. Xie QW, Kashiwabara Y, and Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem 269: 4705-4708, 1994.
97. Yamaoka S, Courtois G, Bessia C, Whiteside ST, Weil R, Agou F, Kirk HE, Kay RJ, and Israel A. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 93: 1231-1240, 1998.
98. Ye J, Ding M, Zhang X, Rojanasakul Y, Nedospasov S, Vallyathan V, Castranova V, and Shi X. Induction of TNFalpha in macrophages by vanadate is dependent on activation of transcription factor NF-kappaB and free radical reactions. Mol Cell Biochem 198: 193-200, 1999.
99. Yurchak LK, Hardwick JS, Amrein K, Pierno K, and Sefton BM. Stimulation of phosphorylation of Tyr394 by hydrogen peroxide reactivates biologically inactive, non-membrane-bound forms of Lck. J Biol Chem 271: 12549-12554, 1996.
100. Zhong H, SuYang H, Erdjument-Bromage H, Tempst P, and Ghosh S. The transcriptional activity of NF-kappaB is regulated by the IkappaB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89: 413-424, 1997.