Redox regulation of NF-kappa B activation

Free Radical Biology and Medicine

Volumn 22, Issue 6, 1997, Pages 1115-1126

  Flohé, Leopold ^a,d   Brigelius Flohé, Regina ^b   Saliou, Claude ^c   Traber, Maret G ^a   Packer, Lester ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^c Institute de Chimie de'Rennes   (France)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Antioxidants; Glutathione peroxidases; H2O2; I B; Lipid hydroperoxides; NF B; Protein kinases; Protein phosphatases; Rel proteins; Selenium; Thioredoxin

Indexed keywords

ANTIOXIDANT; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID HYDROPEROXIDE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN INHIBITOR; PROTEIN KINASE; SELENIUM; THIOREDOXIN;

ARTICLE; DEPHOSPHORYLATION; HUMAN; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CYTOSOL; HUMANS; HYDROGEN PEROXIDE; NF-KAPPA B; OXIDATION-REDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0031044832     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(96)00501-1     Document Type: Article

References (117)

1. Sen R., Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell. 46:1986;705-716.
2. Baeuerle P. A., Henkel T. Function and activation of NF- κB in the immune system. Annu. Rev. Immunol. 12:1994;141-179.
3. Baldwin A. S. The NF- κB and IκB proteins: New discoveries and insights. Annu. Rev. Immunol. 14:1996;649-681.
4. Schmidt A. M., Hori O., Chen J. X., Li J. F., Crandall J., Zhang J., Cao R., Yan S. D., Brett J., Stern D. Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J. Clin. Invest. 96:1995;1395-1403.
5. Rosenberg Z. F., Fauci A. S. Immunopathogenic mechanisms of HIV infection: Cytokine induction of HIV expression. Immunol. Today. 11:1990;176-180.
6. Wu B. Y., Woffendin C., Duckett C. S., Ohno T., Nabel G. J. Regulation of human retroviral latency by the NF-kappa B/I kappa B family: Inhibition of human immunodeficiency virus replication by I kappa B through a Rev-dependent mechanism. Proc. Natl. Acad. Sci. USA. 92:1995;1480-1484.
7. Higgins K. A., Perez J. R., Coleman T. A., Dorshkind K., McComas W. A., Sarmiento U. M., Rosen C. A., Narayanan R. Antisense inhibition of the p65 subunit of NF-kappa B blocks tumorigenicity and causes tumor regression. Proc. Natl. Acad. Sci. USA. 90:1993;9901-9905.
8. Kitajima I., Shinohara T., Bilakovics J., Brown D., Xu X., Nerenberg M. Ablation of transplanted HTLV-I Tax-transformed tumors in mice by antisense inhibition of NF-kappa B. Science. 258:1993;1792-1795.
9. Beauparlant P., Kwan I., Bitar R., Chou P., Koromilas A., Sonenberg N., Hiscott J. Disruption of I kappa B alpha regulation by antisense RNA expression leads to malignant transformation. Oncogene. 9:1994;3189-3197.
10. St. Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 68:1992;201-219.
11. Lenardo M., Siebenlist U. Bcl-3-mediated nuclear regulation of the NF-kappa B trans-activating factor. Immunol. Today. 15:1994;145-147.
12. Inoue J., Kerr L. D., Kakizuka A., Verma I. M. I kappa B gamma, a 70 kd protein identical to the C-terminal half of p110 NF-kappa B: A new member of the I kappa B family. Cell. 68:1992;1109-1120.
13. Beg A. A., Sha W. C., Bronson R. T., Baltimore D. Constitutive NF-kappa B activation, enhanced granulopoiesis, and neonatal lethality in I kappa B alpha-deficient mice. Genes Dev. 9:1995;2736-2746.
14. Rice N. R., Ernst M. K. In vivo control of NF-kappa B activation by I kappa B alpha. EMBO J. 12:1993;4685-4695.
15. Chiao P. J., Miyamoto S., Verma I. M. Autoregulation of I kappa B alpha activity. Proc. Natl. Acad. Sci. USA. 91:1994;28-32.
16. Schmitz M. L., Baeuerle P. A. The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B. EMBO J. 10:1991;3805-3817.
17. Perez P., Lira S. A., Bravo R. Overexpression of RelA in transgenic mouse thymocytes: Specific increase in levels of the inhibitor protein I kappa B alpha. Mol. Cell. Biol. 15:1995;3523-3530.
18. Beg A. A., Sha W. C., Bronson R. T., Ghosh S., Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature. 376:1995;167-170.
19. Franzoso G., Bours V., Azarenko V., Park S., Tomita-Yamaguchi M., Kanno T., Brown K., Siebenlist U. The oncoprotein Bcl-3 can facilitate NF- κB -mediated transactivation by removing inhibiting p50 homodimers from select κB sites. EMBO J. 12:1993;3893-3901.
20. Brigelius-Flohé R., Bilgin B., Eickemeier S., Hipskind R., Singh M., Szamel M., Resch K. The NF- κB heterodimer/homodimer balance and IL-1-stimulated IL-2 production in murine T lymphocytes. BioFactors. 5:1996.
21. Grimm S., Baeuerle P. A. The inducible transcription factor NF- κB : Structure-function relationship of its protein subunits. Biochem. J. 290:1993;297-308.
22. Sha W. C., Liou H. C., Tuomanen E. I., Baltimore D. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell. 80:1995;321-330.
23. Weih F., Carrasco D., Durham S. K., Barton D. S., Rizzo C. A., Ryseck R. P., Lira S. A., Bravo R. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-kappa B/Rel family. Cell. 80:1995;331-340.
24. Burkly L., Hession C., Ogata L., Reilly C., Marconi L., Olson D., Tizard R., Cate R., Lo D. Expression of relB is required for the development of thymic medulla and dendritic cells. Nature. 373:1995;531-536.
25. Kontgen F., Grumont R., Strasser A., Metcalf D., Li R., Tarlinton D., Gerondakis S. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9:1995;1965-1977.
26. Moore N. C., Girdlestone J., Anderson G., Owen J. J., Jenkinson E. J. Stimulation of thymocytes before and after positive selection results in the induction of different NF-kappa B/Rel protein complexes. J. Immunol. 155:1995;4653-4660.
27. Chen Z., Hagler J., Palombella V. J., Melandri F., Scherer D., Ballard D., Maniatis T. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9:1995;1586-1597.
28. Verma I. M., Stevenson J. K., Schwarz E. M., Van Antwerp D., Miyamoto S. Rel/NF-kappa B/I kappa B family: Intimate tales of association and dissociation. Genes Dev. 9:1995;2723-2735.
29. Didonato J., Mercurio F., Rosette C., Wu-Li J., Suyang H., Ghosh S., Karin M. Mapping of the inducible I-kappa-B phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol. 16:1996;1295-1304.
30. Israel A. A role for phosphorylation and degradation in the control of NF-kappa B activity. Trends Genet. 11:1995;203-205.
31. Chen Z. J., Parent L., Maniatis T. Site-specific phosphorylation of IκBα by a novel ubiquitination-dependent protein kinase activity. Cell. 84:1996;853-862.
32. Barroga C. F., Stevenson J. K., Schwarz E. M., Verma I. M. Constitutive phosphorylation of I kappa B alpha by casein kinase II. Proc. Natl. Acad. Sci. USA. 92:1995;7637-7641.
33. Kuno K., Ishikawa Y., Ernst M., Ogata M., Rice N., Mukaida N., Matsushima K. Identification of an I kappa B alpha-associated protein kinase in a human monocytic cell line and determination of its phosphorylation sites on I kappa B alpha. J. Biol. Chem. 270:1995;27914-27919.
34. Whiteside S. T., Ernst M. K., LeBail O., Laurent-Winter C., Rice N., Israel N. N- and C-terminal sequences control degradation of MAD3/l kappa B alpha in response to inducers of NF-kappa B activity. Mol. Cell Biol. 15:1995;5339-5345.
35. Roff M., Thompson J., Rodriguez M. S., Jacque J. M., Baleux F., Arenzana-Seisdedos F., Hay R. T. Role of I-Kappa-B-Alpha ubiquitination in signal-induced activation of NF-Kappa-B in vivo. J. Biol. Chem. 271:1996;7844-7850.
36. Palombella V., Rando O., Goldberg A., Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF- κB . Cell. 78:1994;773-785.
37. Naumann M., Scheidereit C. Activation of NF-kappa B in vivo is regulated by multiple phosphorylations. EMBO J. 13:1994;4597-4607.
38. MacKichan M. L., Logeat F., Israel A. Phosphorylation of p105 PEST sequences via a redox-insensitive pathway upregulates processing to p50 NF-kappa-B. J. Biol. Chem. 271:1996;6084-6091.
39. Reddy S. A., Chaturvedi M. M., Darnay B. G., Chan H., Higuchi M., Aggarwal B. B. Reconstitution of nuclear factor kappa B activation induced by tumor necrosis factor requires membrane-associated components. Comparison with pathway activated by ceramide. J. Biol. Chem. 269:1994;25369-25372.
40. Iwasaki T., Uehara Y., Graves L., Rachie N., Bomsztyk K. Herbimycin A blocks IL-1-induced NF-kappa B DNA-binding activity in lymphoid cell lines. FEBS Lett. 298:1992;240-244.
41. Mahon T. M., O'Neill L. A. 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. 270:1995;28557-28564.
42. 2-induced T cell signal transduction. J. Biol. Chem. 269:1994;20718-20726.
43. Anderson M. T., Staal F. J. T., Gitler C., Herzenberg L. A., Herzenberg L. A. Separation of oxidant-initiated and redox-regulated steps in the NF- κB signal transduction pathway. Proc. Natl. Acad. Sci. USA. 91:1994;11527-11531.
44. Hayashi T., Sekine T., Okamoto T. Identification of a new serine kinase that activates NF kappa B by direct phosphorylation. J. Biol. Chem. 268:1993;26790-26795.
45. Menon S. D., Guy G. R., Tan Y. H. Involvement of a putative protein-tyrosine phosphatase and I kappa B-alpha serine phosphorylation in nuclear factor kappa B activation by tumor necrosis factor. J. Biol. Chem. 270:1995;18881-18887.
46. Sun S. C., Maggirwar S. B., Harhaj E. Activation of NF-kappa B by phosphatase inhibitors involves the phosphorylation of I kappa B alpha at phosphatase 2A-sensitive sites. J. Biol. Chem. 270:1995;18347-18351.
47. Frantz B., Nordby E. C., Bren G., Steffan N., Paya C. V., Kincaid R. L., Tocci M. J., O'Keefe S. J., O'Neill E. A. Calcineurin acts in synergy with PMA to inactivate I kappa B/MAD3, an inhibitor of NF-kappa B. EMBO J. 13:1994;861-870.
48. Singh S., Aggarwal B. B. Protein-tyrosine phosphatase inhibitors block tumor necrosis factor-dependent activation of the nuclear transcription factor NF-kappa B. J. Biol. Chem. 270:1995;10631-10639.
49. Schulze-Osthoff K., Beyaert R., Vandevoorde V., Haegeman G., Fiers W. Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inductive effects of TNF. EMBO J. 12:1993;3095-3104.
50. Hayashi T., Ueno Y., Okamoto T. Oxidoreductive regulation of nuclear factor kappa B. Involvement of a cellular reducing catalyst thioredoxin. J. Biol. Chem. 268:1993;11380-11388.
51. Schreck R., Rieber P., Baeuerle P. A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 10:1991;2247-2258.
52. Schmidt K. N., Traenckner E. B., Meier B., Baeuerle P. A. Induction of oxidative stress by okadaic acid is required for activation of transcription factor NF-kappa B. J. Biol. Chem. 270:1995;27136-27142.
53. Schulze-Osthoff K., Bakker A. C., Vanhaesebroeck B., Beyaert R., Jacob W. A., Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J. Biol. Chem. 267:1992;5317-5323.
54. Hennet T., Richter C., Peterhans E. Tumour necrosis factor-alpha induces superoxide anion generation in mitochondria of L929 cells. Biochem. J. 289:1993;587-592.
55. Richter C., Gogvadze V., Laffranchi R., Schlapbach R., Schweizer M., Suter M., Walter P., Yaffee M. Oxidants in mitochondria: From physiology to diseases. Biochim. Biophys. Acta. 127:1995;67-74.
56. Hsu H., Xiong J., Goeddel D. V. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell. 81:1995;495-504.
57. Higuchi M., Singh S., Chan H., Aggarwal B. B. Protease inhibitors differentially regulate tumor necrosis factor-induced apoptosis, nuclear factor-kappa B activation, cytotoxicity, and differentiation. Blood. 86:1995;2248-2256.
58. Hsu H., Shu H. B., Pan M. G., Goeddel D. V. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell. 84:1996;299-308.
59. Loschen G., Azzi A., Richter C. H., Flohé L. Superoxide radicals of precursors of mitochondrial hydrogen peroxide. FEBS Lett. 42:1974;68-72.
60. Israel N., Gougerot-Pocidalo M. A., Aillet F., Virelizier J. L. Redox status of cells influences constitutive or induced NF-kappa B translocation and HIV long terminal repeat activity in human T and monocytic cell lines. J. Immunol. 149:1992;3386-3393.
61. Brennan P., O'Neill L. Effects of oxidants and antioxidants on nuclear factor kappa B activation in three different cell lines: Evidence against a universal hypothesis involving oxygen radicals. Biochim. Biophys. Acta. 1260:1995;167-175.
62. Suzuki Y. J., Mizuno M., Packer L. Signal transduction for NF- κB activation: Proposed location of antioxidant-inhibitable step. J. Immunol. 153:1994;5008-5015.
63. Suzuki Y. J., Mizuno M., Packer L. Transient overexpression of catalase does not inhibit TNF- or PMA-induced NF-kappa B activation. Biochem. Biophys. Res. Commun. 210:1995;537-541.
64. Meyer M., Pahl H. L., Baeuerle P. A. Regulation of the transcription factors NF-kappa B and AP-1 by redox changes. Chem. Biol. Interact. 91:1994;91-100.
65. Kinscherf R., Fischbach T., Mihm S., Roth S., Hohenhaus-Sievert E., Weiss C., Edler L., Bartsch P., Dröge W. Effect of glutathione depletion and oral N-acetyl-cysteine treatment on CD4+ and CD8+ cells. FASEB J. 8:1994;448-451.
66. Dröge W., Schulze-Osthoff K., Mihm S., Galter D., Schenk H., Eck H. P., Roth S., Gmünder H. Functions of glutathione and glutathione disulfide in immunology and immunopathology. FASEB J. 8:1994;1131-1138.
67. Han D., Tritschler H. J., Packer L. α -Lipoic acid increases intracellular glutathione in a human T-lymphocyte Jurkat cell line. Biochem. Biophys. Res. Commun. 207:1995;258-264.
68. Ursini F., Maiorino M., Brigelius-Flohé R., Aumann K. D., Roveri A., Schomburg D., Flohé L. Diversity of glutathione peroxidases. Methods Enzymol. 252:1995;38-53.
69. Flohé L. The selenoprotein glutathione peroxidase. Dolphin D., Poulson R., Avramovic O. Glutathione: Chemical, biochemical and medical aspects. 1989;643-731 John Wiley & Sons, New York.
70. Warso M. A., Lands W. E. Presence of lipid hydroperoxide in human plasma. J. Clin. Invest. 75:1985;667-671.
71. Haurand M., Flohé L. Kinetic studies on arachidonate 5-lipoxygenase from rat basophilic leukemia cells. Biol. Chem. Hoppe Seyler. 369:1988;133-142.
72. Weitzel F., Wendel A. Selenoenzymes regulate the activity of leukocyte 5-lipoxygenase via the peroxide tone. J. Biol. Chem. 268:1993;6288-6292.
73. Schnurr K., Belkner J., Ursini F., Schewe T., Kühn H. The selenoenzyme phospholipid hydroperoxide glutathione peroxidase controls the activity of the 15-lipoxygenase with complex substrates and preserves the specificity of the oxygenation products. J. Biol. Chem. 271:1996;4653-4658.
74. Galter D., Mihm S., Dröge W. Distinct effects of glutathione disulphide on the nuclear transcription factor kappa B and the activator protein-1. Eur. J. Biochem. 221:1994;639-648.
75. Sappey C., Legrand-Poels S., Best-Belpomme M., Favier A., Rentier B., Piette J. Stimulation of glutathione peroxidase activity decreases HIV type activation after oxidative stress. AIDS Res. Hum. Retroviruses. 10:1994;1451-1461.
76. Makropoulos V., Bruening T., Schulze-Osthoff K. Selenium-mediated inhibition of transcription factor NF-kappa-B and HIV-1 LTR promoter activity. Arch. Toxicol. 70:1996;277-283.
77. Kretz-Remy C., Mehlen P., Mirault M.-E., Arrigo A.-P. Inhibition of I-kappa-B-alpha phosphorylation and degradation and subsequent NF-kappa-B activation by glutathione peroxidase overexpression. J. Cell Biol. 133:1996;1083-1093.
78. Brigelius-Flohé R., Lotzer K., Maurer S., Schultz M., Leist M. Utilization of selenium from different chemical entities for selenoprotein biosynthesis by mammalian cell lines. Biofactors. 5:1996;125-131.
79. Flohé L., Wingender E., Brigelius-Flohé R. The regulation of glutathione peroxidases. Forman H., Cadenas E. Oxidative stress and signal transduction. 1996;Chapman and Hall, London.
80. Schenk H., Klein M., Erdbrugger W., Dröge W., 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. USA. 91:1994;1672-1676.
81. Chae H. Z., Robison K., Poole L. B., Church G., Storz G., Rhee S. G. Cloning and sequencing of thiol-specific antioxidant from mammalian brain: Alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc. Natl. Acad. Sci. USA. 91:1994;7017-7021.
82. Tamura T., Stadtman T. C. A new selenoprotein from human lung adenocarcinoma cells: Purification, properties, and thioredoxin reductase activity. Proc. Natl. Acad. Sci. USA. 93:1996;1006-1011.
83. Suzuki Y. J., Packer L. Inhibition of NF- κB activation by vitamin E derivatives. Biochem. Biophys. Res. Commun. 193:1993;277-283.
84. Burton G. W., Traber M. G. Vitamin E: Antioxidant activity, biokinetics and bioavailability. Annu. Rev. Nutr. 10:1990;357-382.
85. Maiorino M., Coassin M., Roveri A., Ursini F. Microsomal lipid peroxidation: Effect of vitamin E and its functional interaction with phospholipid hydroperoxide glutathione peroxidase. Lipids. 24:1989;721-726.
86. O'Donnell V., Spycher S., Azzi A. Involvement of oxidants and oxidant-generating enzyme(s) in tumour-necrosis-factor-alpha-mediated apoptosis: Role for lipoxygenase pathway but not mitochondrial respiratory chain. Biochem. J. 310:1995;133-141.
87. Kopp E., Ghosh S. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science. 265:1994;956-959.
88. Scheinman R. I., Cogswell P. C., Lofquist A. K., Baldwin A. S. J. Role of transcriptional activation of I kappa B alpha in mediation of immunosuppression by glucocorticoids. Science. 270:1995;283-286.
89. Auphan N., DiDonato J. A., Rosette C., Helmberg A., Karin M. Immunosuppression by glucocorticoids: Inhibition of NF-kappa B activity through induction of I kappa B synthesis. Science. 270:1995;286-290.
90. Kazmi S. M., Plante R. K., Visconti V., Taylor G. R., Zhou L., Lau C. Y. Suppression of NF kappa B activation and NF kappa B-dependent gene expression by tepoxalin, a dual inhibitor of cyclooxygenase and 5-lipoxygenase. J. Cell. Biochem. 57:1995;299-310.
91. Los M., Schenk H., Hexel K., Baeuerle P. A., Dröge W., Schulze-Osthoff K. IL-2 gene expression and NFκB activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J. 14:1995;3731-3740.
92. Frankenberger M., Pforte A., Sternsdorf T. H., Passlick B., Baeuerle P. A., Ziegler-Heitbrock H. W. L. Constitutive nuclear NF- κB in cells of the monocyte lineage. Biochem. J. 304:1994;87-94.
93. Siebenlist U., Franzoso G., Brown K. Structure, regulation and function of NF-kappa B. Annu. Rev. Cell Biol. 10:1994;405-455.
94. Mathias S., Dressler K. A., Kolesnick R. N. Characterization of a ceramide-activated protein kinase: Stimulation by tumor necrosis factor alpha. Proc. Natl. Acad. Sci. USA. 88:1991;10009-10013.
95. Mathias S., Younes S., Kan C.-C., Orlow, I., Joseph C., Kolesnick R. N. Activation of the sphingomyelin signaling pathway in intact EL-4 cells and in a cell-free system by IL-1- β Science. 259:1993;519-522.
96. Dobrowsky R. T., Hannun Y. A. Ceramide stimulates a cytosolic protein phosphatase. J. Biol. Chem. 267:1992;5048-5051.
97. 2+ in oxidant-induced NFκB activation. FEBS Lett. 385:1996;58-62.
98. Peng H.-B., Libby P., Liao J. K. Induction and stabilization of IκBα by nitric oxide mediates inhibition of NF- κB . J. Biol. Chem. 270:1995;14214-14219.
99. Matthews J. R., Botting C. H., Panico M., Morris H. R., Hay R. T. Inhibition of NF-kappa-B DNA binding by nitric oxide. Nucleic Acids Res. 24:1996;2236-2242.
100. Lander H. M., Sehajpal P., Levine D. M., Novogrodsky A. Activation of human peripheral blood mononuclear cells by nitric oxide-generating compounds. J. Immunol. 150:1993;1509-1516.
101. Hershko A., Heller H., Eytan E., Reiss Y. The protein substrate binding site of the ubiquitin-protein ligase system. J. Biol. Chem. 261:1986;11992-11999.
102. Brown K., Gerstberger S., Carlson L., Franzoso G., Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science. 267:1995;1485-1488.
103. Hunter T. Protein kinases and phosphatases: The yin and yang of protein phosphorylation and signaling. Cell. 80:1995;225-236.
104. 2 and vanadate stimulate protein tyrosine phosphorylation in intact cells. J. Biol. Chem. 265:1990;2896-2902.
105. Bauskin A., Alkalay I., Ben-Neriah Y. Redox regulation of a protein tyrosine kinase in the endoplasmic reticulum. Cell. 66:1991;685-696.
106. Hardwick J. S., Sefton B. M. Activation of the Lck tyrosine protein kinase by hydrogen peroxide requires the phosphorylation of Tyr-394. Proc. Natl. Acad. Sci. USA. 92:1995;4527-4531.
107. 2 for platelet-derived growth factor signal transduction. Science. 270:1995;296-299.
108. Brigelius R. Mixed disulfides: Biological functions and increase in oxidative stress. Sies H. Oxidative stress. 1985;243-272 Academic Press, London.
109. Rokutan K., Johnston R. B. J., Kawai K. Oxidative stress induces S-thiolation of specific proteins in cultured gastric mucosal cells. Am. J. Physiol. 266:1994;G247-G254.
110. Schuppe-Koistinen I., Moldeus P., Bergman T., Cotgreave I. S-Thiolation of human endothelial cell glyceraldehyde-3-phosphate dehydrogenase after hydrogen peroxide treatment. Eur. J. Biochem. 221:1994;1033-1037.
111. Thomas J. A., Chai Y. C., Jung C. H. Protein S-thiolation and dethiolation. Methods Enzymol. 233:1994;385-395.
112. Gitler C., Mogyoros M., Kalef E. Labeling of protein vicinal dithiols: Role of protein-S2 to protein-(SH)2 conversion in metabolic regulation and oxidative stress. Methods Enzymol. 233:1994;403-415.
113. Dröge W., Eck H.-P., Mihm S. HIV-induced cysteine deficiency and T-cell dysfunction a rationale for treatment with N-acetylcysteine. Immunol. Today. 13:1992;211-213.
114. Sandstrom P. A., Tebbey P. W., Van Cleave S., Buttke T. M. Lipid hydroperoxides induce apoptosis in T cells displaying a HIV-associated glutathione peroxidase deficiency. J. Biol. Chem. 269:1994;798-801.
115. Dworkin B. M. Selenium deficiency in HIV infection and the acquired immunodeficiency syndrome (AIDS). Chem. Biol. Interact. 91:1994;181-186.
116. Bours V., Franzoso G., Brown K., Park S., Azarenko V., Tomita-Yamaguchi M., Kelly K., Siebenlist U. Lymphocyte activation and the family of NF- κB transcription factor complexes. Curr. Top. Microbiol. Immunol. 182:1992;411-420.
117. Lu D., Thompson J. D., Gorski G. K., Rice N. R., Mayer M. G., Yunis J. J. Alterations at the rel locus in human lymphoma. Oncogene. 6:1991;1235-1241.