DNA-dependent protein kinase phosphorylation of IκBα and IκBβ regulates NF-κB DNA binding properties

Molecular and Cellular Biology

Volumn 18, Issue 7, 1998, Pages 4221-4234

  Liu, Li ^a   Kwak, Youn Tae ^a   Bex, Françoise ^a   García Martínez, León F ^a   Li, Xiao Hua ^a   Meek, Katheryn ^b   Lane, William S ^c   Gaynor, Richard B ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HORSE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; SCID MOUSE; TRANSCRIPTION REGULATION;

ANIMALIA; EQUUS CABALLUS; MURINAE;

EID: 0031860923     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.7.4221     Document Type: Article

References (85)

1. Alkalay, I., A. Yaron, A. Hatzubai, A. Orian, A. Ciechanover, and Y. Ben-Neriah. 1995. Stimulation-dependent I kappa B alpha phosphorylation marks the NF-kappa B inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 92:10599-10603.
2. Arenzana-Seisdedos, F., J. Thompson, M. S. Rodriguez, F. Bachelerie, D. Thomas, and R. T. Hay. 1995. Inducible nuclear expression of newly synthesized IκBα negatively regulates DNA-binding and transcriptional activities of NF-κB. Mol. Cell. Biol. 15:2689-2696.
3. Arenzana-Seisdedos, F., P. Turpin, M. Rodriguez, D. Thomas, R. T. Hay, J.-L. Virelizier, and C. Dargemont. 1997. Nuclear localization of IκBα promotes active transport of NF-κB from the nucleus to the cytoplasm. J. Cell Sci. 110:369-378.
4. Baeuerle, P. A., and D. Baltimore. 1988. IκB: a specific inhibitor of the NF-κB transcription factor. Science 242:540-546.
5. Baeuerle, P. A., and D. Baltimore. 1988. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-kappa B transcription factor. Cell 53:211-217.
6. Baeuerle, P. A., and D. Baltimore. 1989. A 65-kD subunit of active NF-kappaB is required for inhibition of NF-kappaB by I kappaB. Genes Dev. 3: 1689-1698.
7. Baeuerle, P. A., and D. Baltimore. 1996. NF-κB: ten years after. Cell 87:13-20.
8. Ballard, D. W., E. P. Dixon, N. J. Peffer, H. Bogerd, S. Doerre, B. Stein, and W. C. Greene. 1992. The 65-kDa subunit of human NF-κB functions as a potent transcriptional activator and a target for v-Rel-mediated repression. Proc. Natl. Acad. Sci. USA 89:1875-1879.
9. Bannister, A. J., T. M. Gottlieb, T. Kouzarides, and S. P. Jackson. 1993. c-Jun is phosphorylated by the DNA-dependent protein kinase in vitro; definition of the minimal kinase recognition motif. Nucleic Acids Res. 21: 1289-1295.
10. Barroga, C. F., J. K. Stevenson, E. M. Schwarz, and I. M. Verma. 1995. Constitutive phosphorylation of IκBα by casein kinase II. Proc. Natl. Acad. Sci. USA 92:7637-7641.
11. Beauparlant, P., R. Lin, and J. Hiscott. 1996. The role of the C-terminal domain of IκBα in protein degradation and stabilization. J. Biol. Chem. 271: 10690-10696.
12. Beg, A. A., T. S. Finco, P. V. Nantermet, and A. S. J. Baldwin. 1993. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBα: a mechanism for NF-κB activation. Mol. Cell. Biol. 13:3301-3310.
13. Beg, A. A., S. M. Ruben, R. I. Scheinman, S. Haskill, C. A. Rosen, and A. S. Baldwin, Jr. 1992. IκB interacts with the nuclear localization sequences of the subunits of NF-κB: a mechanism for cytoplasmic retention. Genes Dev. 6:1899-1913.
14. Biederman, K. A., J. Sun, A. J. Giacia, L. M. Tosto, and J. M. Brown. 1991. scid mutation in mice confers hypersensitivity to ionizing radiation and a deficiency in DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 88:1394-1397.
15. Blunt, T., N. J. Finnie, G. E. Taccioli, G. C. M. Smith, J. Demengeot, T. M. Gottlieb, R. Mizuta, A. J. Varghese, F. W. Alt, P. A. Jeggo, and S. P. Jackson. 1995. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80:813-823.
16. Brockman, J. A., D. C. Scherer, T. A. McKinsey, S. M. Hall, X. Qi, W. Y. Lee, and D. W. Ballard. 1995. Coupling of a signal response domain in IκBα to multiple pathways for NF-κB activation. Mol. Cell. Biol. 15:2809-2818.
17. Brown, K., S. Gerstberger, L. Carlson, G. Fransozo, and U. Siebenlist. 1995. Control of IκBα proteolysis by site-specific, signal-induced phosphorylation. Science 267:1485-1488.
18. Brush, G. S., C. W. Anderson, and T. J. Kelly. 1994. The DNA-activated protein kinase is required for the phosphorylation of replication protein A during simian virus 40 DNA replication. Proc. Natl. Acad. Sci. USA 91: 12520-12524.
19. Carter, T., I. Vancurova, I. Sun, W. Lou, and S. DeLeon. 1990. A DNA-activated protein kinase from HeLa cell nuclei. Mol. Cell. Biol. 10:6460-6471.
20. Chan, D. W., and S. P. Lees-Miller. 1996. The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J. Biol. Chem. 271:8936-8941.
21. Chen, J., T. Willingham, L. R. Margraf, N. Schreiber-Agus, R. A. DePhinho, and P. D. Nisen. 1995. Effects of the MYC oncogene antagonist, MAD, on proliferation, cell cycling and the malignant phenotype of human brain tumour cells. Nat. Med. 1:638-643.
22. Chen, Y.-R., S. P. Lees-Miller, P. Tegtmeyer, and C. W. Anderson. 1991. The human DNA-activated protein kinase phosphorylates simian virus 40 T antigen at amino-and carboxy-terminal sites. J. Virol. 65:5131-5140.
23. Chen, Z., J. Hagler, V. J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
24. Chen, Z. J., L. Parent, and T. Maniatis. 1996. Site-specific phosphorylation of IκBα by a novel ubiquitination-dependent protein kinase activity. Cell 84: 853-862.
25. Chu, Z.-L., T. A. McKinsey, L. Liu, X. Qi, and D. W. Ballard. 1996. Basal phosphorylation of the PEST domain in IκBβ regulates its functional interaction with the c-rel proto-oncogene product. Mol. Cell Biol. 16:5974-5984.
26. Cimprich, K. A., T. B. Shin, C. T. Keith, and S. L. Schreiber. 1996. cDNA cloning and gene mapping of a candidate human cell cycle checkpoint protein. Proc. Natl. Acad. Sci. USA 93:2850-2855.
27. DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388:548-554.
28. DiDonato, J. A., F. Mercurio, and M. Karin. 1995. Phosphorylation of IκBα precedes but is not sufficient for its dissociation from NF-κB. Mol. Cell Biol. 15:1302-1311.
29. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
30. Dvir, A., L. Y. Stein, B. L. Calore, and W. S. Dynan. 1993. Purification and characterization of a template-associated protein kinase that phosphorylates RNA polymerase II. J. Biol. Chem. 268:10440-10447.
31. Eng, J. K., A. L. McCormick, and J. R. Yates. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5:976-989.
32. Finco, T. S., A. A. Beg, and A. S. J. Baldwin. 1994. Inducible phosphorylation of IκBα is not sufficient for its dissociation from NF-κB and is inhibited by protease inhibitors. Proc. Natl. Acad. Sci. USA 91:11884-11888.
33. Fiscella, M., S. J. Ullrich, N. Zambrano, M. T. Shields, D. Lin, S. P. Lees-Miller, C. W. Anderson, W. E. Mercer, and E. Appella. 1993. Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression. Oncogene 8:1519-1528.
34. Ganchi, P., S.-C. Sun, W. C. Greene, and D. W. Ballard. 1992. IκB/MAD-3 masks the nuclear localization signal of NF-κB p65 and requires the transactivation domain to inhibit NF-κB p65 DNA binding. Mol. Biol. Cell. 3: 1339-1352.
35. Giffin, W., H. Torrance, D. J. Rodda, G. G. Prefontaine, L. Pope, and R. J. G. Hache. 1996. Sequence-specific DNA binding by Ku autoantigen and its effects on transcription. Nature 380:265-268.
36. Gomez-Foix, A., W. Coats, S. Baque, T. Alam, R. Gerard, and C. Newgard. 1992. Adenovirus-mediated transfer of the muscle glycogen phosphorylase gene into hepatocytes confers altered regulation of glycogen metabolism. J. Biol. Chem. 267:25129-25134.
37. Gottlieb, T. M., and S. P. Jackson. 1993. The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72: 131-142.
38. Graham, F., and L. Preved. 1991. Manipulation of adenovirus vectors, p. 109-128. In E. Murray (ed.), Methods in molecular biology. Humana Press, Inc., Jersey City, N.J.
39. Harrington, J., C.-L. Hsieh, J. Gerton, G. Bosma, and M. R. Lieber. 1992. Analysis of the defect in DNA end joining in the murine scid mutation. Mol. Cell. Biol. 12:4758-4768.
40. Hartley, K. O., D. Gell, G. C. M. Smith, H. Zhang, N. Divecha, M. A. Connelly, A. Admon, S. P. Lees-Miller, C. W. Anderson, and S. P. Jackson. 1995. DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82: 849-856.
41. Haskill, S., A. A. Beg, S. M. Tompkins, J. S. Morris, A. D. Yurochko, A. Sampson-Johannes, K. Mondal, P. Ralph, and A. S. Baldwin. 1991. Characterization of an immediate-early gene induced in adherent monocytes that encodes a kappa B-like activity. Cell 65:1281-1289.
42. Hellman, U., C. Wernstedt, J. Gonez, and C. H. Heldin. 1995. Improvement of an in gel digestion procedure for the micro-preparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224:451-4155.
43. Henkel, T., T. Machleidt, I. Alkalay, M. Kronke, N. Y. Ben, and P. A. Baeuerle. 1993. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature 365:182-185.
44. Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin. 1993. Identification of an oncoprotein and UV-responsive protein kinase that binds and potentiates c-Jun activation domain. Genes Dev. 7:2135-2148.
45. Imbert, V., R. A. Rupec, A. Livolsi, H. L. Pahl, E. B.-M. Traenckner, C. Mueller-Dieckmann, D. Farahifar, B. Rossi, P. Auberger, P. A. Baeuerle, and J.-F. Peyron. 1996. Tyrosine phosphorylation of IκB-α activates NF-κB without proteolytic degradation of IκB-α. Cell 86:787-798.
46. Jackson, S. P., J. J. MacDonald, S. Lees-Miller, and R. Tjian. 1990. GC box binding induces phosphorylation of SP1 by a DNA dependent protein kinase. Cell 63:155-165.
47. Jung, M., A. Kondratyev, S. A. Lee, A. Dimtchev, and A. Dritschillo. 1997. ATM gene product phosphorylates I kappa B-alpha. Cancer Res. 57:24-27.
48. Jung, M., Y. Zhang, S. Lee, and A. Dritschilo. 1995. Correction of radiation sensitivity in ataxia-telangiectasia cells by a truncated IκBα. Science 268: 1619-1621.
49. Kirchgessner, C. U., C. K. Patil, J. W. Evans, C. A. Cuomo, L. M. Fried, T. Carter, M. A. Oettinger, and J. M. Brown. 1995. DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267:1178-1183.
50. Lane, W. S., A. Galat, M. W. Harding, and S. L. Schreiber. 1991. Complete amino acid sequence of the FK506 and rapamycin binding protein, FKBP, isolated from calf thymus. J. Protein Chem. 10:151-160.
51. Lee, F. S., J. Hagler, Z. J. Chen, and T. Maniatis. 1997. Activation of the IκBα kinase complex by MEKK1, a kinase of the JNK pathway. Cell 88:213-222.
52. Lee, S. E., R. A. Mitchell, A. Cheng, and E. A. Hendrickson. 1997. Evidence for DNA-PK-dependent and -independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle. Mol. Cell. Biol. 17:1425-1433.
53. Lees-Miller, S. P. 1996. The DNA-dependent protein kinase, DNA-PK: 10 years and no ends in sight. Biochem. Cell Biol. 74:503-512.
54. Lees-Miller, S. P., Y.-R. Chen, and C. W. Anderson. 1990. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell. Biol. 10: 6472-6481.
55. Lees-Miller, S. P., R. Godbout, D. W. Chan, M. Weinfeld, R. S. Day, G. M. Barron, and J. Allalunis-Turner. 1995. Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science 267: 1183-1185.
56. Lees-Miller, S. P., K. Sakaguchi, S. J. Ullrich, E. Appella, and C. W. Anderson. 1992. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12:5041-5049.
57. Lin, R., P. Beauparlant, C. Makris, S. Meloche, and J. Hiscott. 1996. Phosphorylation of IκBα in the C-terminal PEST domain by casein kinase II affects intrinsic protein stability. Mol. Cell. Biol. 16:1401-1409.
58. Lin, Y.-C., K. Brown, and U. Siebenlist. 1995. Activation of NF-κB requires proteolysis of the inhibitor IκB-α: signal-induced phosphorylation of IκB-α alone does not release active NF-κB. Proc. Natl. Acad. Sci. USA 92:552-556.
59. Liu, S.-H., J.-T. Ma, A. Y. Yueh, S. P. Lees-Miller, C. W. Anderson, and S.-Y. Ng. 1993. The carboxyl-terminal transactivation domain of human serum response factor contains DNA-activated protein kinase phosphorylation sites. J. Biol. Chem. 268:21147-21154.
60. Luque, I., and C. Gelinas. 1998. Distinct domains of IκBα regulate c-Rel in the cytoplasm and in the nucleus. Mol. Cell. Biol. 18:1213-1224.
61. McElhinny, J. A., S. A. Trushin, G. D. Bren, N. Chester, and C. V. Paya. 1996. Casein kinase II phosphorylates IκBα at S-283, S-289, S-293, and T-291 and is required for its degradation. Mol. Cell. Biol. 16:899-906.
62. McKinsey, T. A., J. A. Brockman, D. C. Scherer, S. W. Al-Murrani, P. L. Green, and D. W. Ballard. 1996. Inactivation of IκBβ by the Tax protein of human T-cell leukemia virus type 1: a potential mechanism for constitutive induction of NF-κB. Mol. Cell. Biol. 16:2083-2090.
63. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, and M. Mann. 1997. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation. Science 278:860-866.
64. Peterson, S. R., A. Dvir, C. W. Anderson, and W. S. Dynan. 1992. DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapetide repeats. Genes Dev. 6:426-438.
65. Regnier, C. H., H. Y. Song, X. Gao, D. V. Goeddel, Z. Cao, and M. Rothe. 1997. Identification and characterization of an IκB kinase. Cell 90:373-383.
66. Rodriguez, M. S., I. Michalopoulos, F. Arenzana-Seisdedos, and R. T. Hay. 1995. Inducible degradation of IκBα in vitro and in vivo requires the acidic C-terminal domain of the protein. Mol. Cell. Biol. 15:2413-2419.
67. Ruben, S. M., R. Narayanan, J. F. Klement, C.-H. Chen, and C. A. Rosen. 1992. Functional characterization of the NF-κB p65 transcriptional activator and an alternatively spliced derivative. Mol. Cell. Biol. 12:444-454.
68. Savitsky, K., A. Bar-Shira, S. Gilad, G. Rotman, Y. Ziv, L. Vanagaite, D. A. Tagle, S. Smith, T. Uziel, S. Sfez, M. Ashkenazi, I. Pecker, M. Frydman, R. Harnik, S. R. Patanjali, A. Simmons, G. A. Clines, A. Sartiel, R. A. Gatti, L. Chessa, O. Sanal, M. F. Lavin, N. G. J. Jaspers, A. M. R. Taylor, C. F. Arlett, T. Miki, S. Wesissman, M. Lovett, F. S. Collins, and Y. A. Shiloh. 1995. A single ataxia-telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749-1753.
69. Scherer, D. C., J. A. Brockman, Z. Chen, T. Maniatis, and D. W. Ballard. 1995. Signal-induced degradation of IκBα requires site-specific ubiquitination. Proc. Natl. Acad. Sci. USA 92:11259-11263.
70. Schmitz, M. L., and Baenerle, P. A. 1991. The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B. EMBO J. 10: 3805-3817.
71. Schouten, G. J., A. C. O. Vertegaal, S. T. Whiteside, A. Israel, M. Toebes, J. C. Dorsman, A. van der Eb, and A. Zantema. 1997. IκBα is a target for the mitogen-activated 90 kDa ribosomal S6 kinase. EMBO J. 16:3133-3144.
72. Sipley, J. D., J. C. Menninger, K. O. Hartley, D. C. Ward, and S. P. Jackson. 1995. Gene for the catalytic subunit of the human DNA-activated protein kinase maps to the site of the XRCC7 gene on chromosome 8. Proc. Natl. Acad. Sci. USA 92:7515-7519.
73. Sun, S.-C., P. Ganchi, D. W. Ballard, and W. C. Greene. 1993. NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science 259:1912-1915.
74. Suwa, A., M. Hirakata, Y. Takeda, S. A. Jesch, T. Mimori, and J. A. Hardin. 1994. DNA-dependent protein kinase (Ku protein-p350 complex) assembles on double-stranded DNA. Proc. Natl. Acad. Sci. USA 91:6904-6908.
75. Thanos, D., and T. Maniatis. 1995. NF-κB: a lesson in family values. Cell 80: 529-532.
76. Thompson, J. E., R. J. Phillips, H. Erdjument-Bromage, P. Tempst, and S. Ghosh. 1995. IκBβ regulates the persistent response in a biphasic activation of NF-κB. Cell 80:573-582.
77. Traenckner, E. B. M., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human IκBα on serines 32 and 36 controls IκBα proteolysis and NF-κB activation in response to diverse stimuli. EMBO J. 14:2876-2883.
78. Tran, K., M. Merika, and D. Thanos. 1997. Distinct functional properties of IκBα and IκBβ. Mol. Cell. Biol. 17:5386-5399.
79. Verma, I. M., J. K. Stevenson, E. M. Schwartz, D. Van Antwerp, and S. Miyamoto. 1995. Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev. 9:2723-2735.
80. Whiteside, S. T., J. Epinat, N. R. Rice, and A. Israel. 1997. I kappa B epsilon, a novel member of the IκB family, controls RelA and cRel NF-κB activity. EMBO J. 16:1413-1426.
81. Whiteside, S. T., M. K. Ernst, O. LeBail, C. Laurent-Winter, N. Rice, and A. Israel. 1995. N-and C-terminal sequences control degradation of MAD3/ IκBα in response to inducers of NF-κB activity. Mol. Cell. Biol. 15:5339-5345.
82. Wiler, R., R. Leber, B. B. Moore, L. F. VanDyke, L. E. Perryman, and K. Meek. 1995. Equine severe combined immunodeficiency: a defect in V(D)J recombination and DNA-dependent protein kinase activity. Proc. Natl. Acad. Sci. USA 92:11485-11489.
83. Woronicz, J. D., X. Gao, Z. Cao, M. Rothe, and D. V. Goeddel. 1997. IκB kinase-β: NF-κB activation and complex formation with IκB kinase-α and NIK. Science 278:866-869.
84. Zabel, U., and P. A. Baeuerle. 1990. Purified human IκB can rapidly dissociate the complex of the NF-kappa B transcription factor with its cognate DNA. Cell 61:255-265.
85. Zandi, E., D. M. Rothwarf, M. Delhase, M. Hayakawa, and M. Karin. 1997. The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell 91: 243-252.