Phosphorylation of IκBα in the C-terminal PEST domain by casein kinase II affects intrinsic protein stability

Molecular and Cellular Biology

Volumn 16, Issue 4, 1996, Pages 1401-1409

  Lin, Rongtuan ^a,b   Beauparlant, Pierre ^a,b   Makris, Constantin ^c   Meloche, Sylvain ^c   Hiscott, John ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TUMOR NECROSIS FACTOR; DNA BINDING PROTEIN; HYBRID PROTEIN; I KAPPA B; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; ONCOPROTEIN; PROTEIN SERINE THREONINE KINASE; RELB PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELB;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME PHOSPHORYLATION; GENE ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERMINAL REPEAT; PHOSPHORYLATION; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN STABILITY; REGULATOR GENE; BINDING SITE; DRUG ANTAGONISM; ENZYME STABILITY; GENE DELETION; GENETICS; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY;

BASE SEQUENCE; BINDING SITES; CASEIN KINASE II; DNA-BINDING PROTEINS; ENZYME STABILITY; HUMANS; I-KAPPA B PROTEINS; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; SEQUENCE HOMOLOGY; TRANSCRIPTION FACTOR RELB; TRANSCRIPTION FACTORS;

EID: 0029670085     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.4.1401     Document Type: Article

References (72)

1. Baeuerle, P. A., and D. Baltimore. 1988. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-κB transcription factor Cell 53:211-217.
2. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu Rev. Immunol 12:141-179.
3. 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.
4. Beauparlant, P., I. Kwan, R. Bitar, P. Chou, A. E. Koromilas, N. Sonenberg, and J. Hiscott. 1994. Disruption of IκBα regulation by antisense RNA expression leads to malignant transformation. Oncogene 9:3189-3197.
5. Beauparlant, P., R. Lin, and J. Hiscott. The role of the C-terminal PEST domain of IκBα in protein degradation and stabilization.
6. Beg, A. A., and A. S. Baldwin, Jr. 1993. The IκB proteins, multifunctional regulators of Rel/NF-κB transcription factors. Genes Dev. 7:2064-2070.
7. Beg, A. A., T. S. Finco, P. V. Nantermet, and A. S. Baldwin, Jr. 1993 Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBα. a mechanism for NF-κB activation. Mol. Cell. Biol. 13:33111-3310
8. 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.
9. Bours, V., P. R. Burd, K. Brown, J. Villalobos, S. Park, R.-P. Ryseck, R. Bravo, K. Kelly, and U. Siebenlist. 1992. A novel mitogen-inducible gene product related to p50/p105-NF-κB participates in transactivation through a κB site. Mol. Cell Biol. 12:685-695
10. Bours, V., J. Villalobos, P. R. Burd, K. Kelly, and U. Siebenlist. 1990. Cloning of a mitogen-inducible gene encoding a κB DNA-binding protein with homology to the rel oncogene and to cell-cycle motifs. Nature (London) 348:76-80.
11. 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.
12. Brown, K., S. Gerstberger, L. Carlson, G. Franzoso, and V. Siebenlist. 1995. Control of IκBα proteolysis by site-specific, signal-induced phosphorylation. Science 267:1485-1488
13. Brown, K., S. Park, T. Kanno, G. Franzoso, and U. Siebenlist. 1993. Mutual regulation of the transcriptional activator NF-κB and its inhibitor, IκB-α. Proc Natl. Acad. Sci. USA 90:2532-2536
14. Brownell, D., N. Mittereder, and N. R. Rice. 1989 A human rel protooncogene cDNA can containing an Alu fragment as a potential coding exon. Oncogene 4:935-942
15. Chen, Z., J. Hagler, V. J. Palombella, F. Melandri, D. Scherer, U. Ballard, and T. Maniatis. 1995 Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
16. Cooper, J. A., B. M. Sefton, and T. Hunter. 1983. Detection and quantification of phosphotyrosine in proteins. Methods Enzymol. 99:387-402.
17. Cordle, S. R., R. Donald, M. A. Read, and J. Hawiger. 1993. Lipopolysaccharide induces phosphoryiation of MAD-3 and activation of c-rel and related NF-κB proteins in human THP-1 cells. J. Biol. Chem. 268:11803-11810.
18. 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.
19. Duckett, C. S., N. D. Perkins, T. F. Kowalik, R. M. Schmid, E.-S. Huang, A. S. Baldwin, Jr., and G. J. Nabel. 1993. Dimenzation of NF-KB2 with RelA(p65) regulates DNA binding, transcriptional activation, and inhibition by an IκB-α (MAD3). Mol. Cell. Biol 13:1315-1322.
20. Filhol, O., J. Baudier, C. Delphin, P. Loue-Mackenbach, E. M. Chambaz, and C. Cochet. 1992. Casein kinase II and tumor suppressor protein p53 associate in a molecular complex that is negatively regulated upon p53 phosphorylation. J. Biol. Chem. 267:20577-20583.
21. Finco, T. S., and A. S. Baldwin, Jr. 1993. κB site-dependent induction of gene expression by diverse inducers of nuclear factor κB requires Raf-1 J Biol. Chem. 268:17676-17679.
22. Garoufalis, E., I. Kwan, R. Lin, A. Mustafa, N. Pepin, A. Roulston, J. Lacoste, and J. Hiscott. 1994. Viral induction of the human interferon beta promoter: modulation of transcription by NF-κB/rel proteins and interferon regulatory factors. J. Virol. 68:4707-4715.
23. Ghosh, S., and D. Baltimore. 1990. Activation in vitro of NF-κB by phosphorylation of its inhibitor IκB. Nature (London) 344:678-682.
24. Ghosh, S., A. M. Gifford, L. R. Riviere, P. Tempst, G. P. Nolan, and D. Baltimore. 1990. Cloning of the p50 DNA binding subunit of NF-κB: homology to rel and dorsal. Cell 62:1019-1029.
25. Gilmore, T. D. 1991. Malignant transformation by mutant Rel proteins. Trends Genet. 7:318-322.
26. Gilmore, T. D., and P. J. Morin. 1993 The IκB proteins: member of a multifunctional family. Trends Genet. 9:427-433.
27. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
28. Grimm, S., and P. Baeuerle. 1993. The inducible transcription factor NF-κB: structure-function relationship of its protein subunits. Biochem. J. 290:297-308.
29. 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, Jr. 1991. Characterization of an immediate-early gene induced in adherent monocytes that encodes IκB-like activity. Cell 65:1281-1289.
30. Hathaway, G. M., T. H. Lubben, and J. A. Traugh. 1980. Inhibition of casein kinase II by heparin. J. Biol. Chem. 255:8038-8041.
31. Hayashi, T., T. Sekine, and T. Okamoto. 1993 Identification of a new serine kinase that activates NF-κB by direct phosphorylation J. Biol Chem. 268: 26790-26795.
32. Herrmann, C. P., S. Kraiss, and M. Montenarh. 1991. Association of casein kinase II with immunopurified p53. Oncogene 6:877-884.
33. Hibi, M., A. Lin, M. Minden, and M. Karin. 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7:2135-2148.
34. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
35. Jaffray, E., K. M. Wood, and R. T. Hay. 1995. Domain organization of IκBα and sites of interaction with NF-κB p65. Mol. Cell. Biol. 15:2166-2172
36. Jelinek, T., and M. J. Weber. 1993. Optimization of the resolution of phosphoamino acids by one-dimensional thin-layer electrophoresis. BioTechniques 15:629-630.
37. Jin, Y. J., and S. J. Burakoff. 1993. The 25-kDa FK506-binding protein is localized in the nucleus and associates with casein kinase II and nucleolin. Proc. Natl. Acad. Sci USA 90:7769-7773.
38. 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.
39. Kamps, M. D. 1991. Determination of phosphoamino acid composition by acid hydrolysis of protein blotted to immobilon Methods Enzymol. 201:21-27.
40. Kerr, L. D., C. S. Duckett, P. Wamsley, Q. Zhang, P. Chiao, G. J. Nabel, T. W. McKeithan, P. A. Baeuerle, and I. M. Verma. 1992. The protooncogene BCL-3 encodes an IκB protein. Genes Dev. 6:2352-2363.
41. Kerr, L. D., J. I. Inoue, N. Davis, E. Link, P. A. Baeuerle, H. R. Bose, Jr., and I. M. Verma. 1991 The rel-associated pp40 protein prevents DNA binding of Rel and NF-κB. relationship with IκBα and regulation by phosphorylation. Genes Dev. 5:1464-1476.
42. Kieran, M., V. Blank, F. Logeat, J. Vandekerckhove, F. Lottspeich, O. Le Bail, M. B. Urban, P. Kourilsky, P. A. Baeuerle, and A. Israel. 1990. The DNA-binding subunit of NF-κB is identical to factor KBF1 and homologous to the rel oncogene product. Cell 62:1007-1018.
43. Krek, W., G. Maridor, and E. A. Nigg. 1992. Casein kinase II is a predominantly nuclear enzyme. J. Cell Biol. 116:43-55
44. Kumar, A., J. Haque, J. Lacoste, J. Hiscott, and B. R. G. Williams. 1994. Double-stranded RNA-dependent protein kinase activates transcription factor NF-κB by phosphorylating IκB Proc Natl. Acad. Sci USA 91:6288-6292.
45. Kunsch, C., S. M. Ruben, and C. A. Rosen. 1992 Selection of optimal κB/Rel DNA binding motifs: interaction of both subunits of NF-κB with DNA is required for transcnptional activation. Mol. Cell. Biol. 12:4412-4421.
46. Le Bail, O., R. Schmidt-Ullrich, and A. Israel. 1993 Promoter analysis of the gene encoding the IκBα/MAD-3 inhibitor of NF-κB: positive regulation by members of the rel/NF-κB family. EMBO J. 12:5043-5049.
47. Lin, A., J. Frost, T. Deng, T. Smeal, N. al-Alawi, U. Kikkawa, T. Hunter, D. Brenner, and M. Karin. 1992. Casein kinase II is a negative regulator of c-Jun DNA binding and AP-1 activity. Cell 70:777-789.
48. Lin, R. Unpublished data.
49. Lin, R., D. Gewert, and J. Hiscott. 1995. Differential transcriptional activation in vitro by NF-κB/Rel proteins. J. Biol. Chem. 270:3123-3131.
50. Liou, H. C., and D. Baltimore. 1993. Regulation of the NF-κB/rel transcription factor and IκB inhibitor system. Curr. Opin. Cell Biol. 5:477-487.
51. Meisner, H., and M. P. Czech. 1991. Phosphorylation of transcriptional factors and cell-cycle-dependent proteins by casein kinase II Curr. Opin. Cell Biol. 3:474-483.
52. Muller, E., B. Boldyreff, and K. H. Scheidtmann. 1993. Characterization of protein kinase activities associated with p53-Large-T immune complexes from SV40-transformed ret cells. Oncogene 8:2193-2205.
53. Neri, A., C.-C. Chang, L. Lombardi, M. Salina, P. Corradini, A. T. Maiolo, R. S. K. Chaganti, and R. Dalla-Favera. 1991. B cell lymphoma-asiociated chromosomal translocation involves candidate oncogene lyt-10, homologous to NF-κB p50. Cell 67:1075-1087.
54. Nolan, G. P., S. Ghosh, H.-C. Liou, P. Tempst, and D. Baltimore. 1991. DNA binding and IκB inhibition of the cloned p65 subunit of NF-κB, a rel-related polypeptide. Cell 64:961-969.
55. Ostrowski, J., J. E. Sims, C. H. Sibley, M. A. Valentine, S. K. Dower, K. E. Meier, and K. Bomsztyk. 1991. A serine/threonine kinase activity is closely associated with a 65 kDa phosphoprotein specifically recognized by the κB enhancer element. J. Biol. Chem. 266:12722-12733.
56. Padmanabha, R., J. L.-P. Chen-Wu, D. E. Hanna, and C. V. C. Glover. 1990. Isolation, sequencing, and disruption of the yeast CKA2 gene, casein kinase II is essential for viability in Saccharomyces cerevisiae Mol. Cell. Biol. 10: 4089-4099.
57. Pepin, N., A. Roulston, J. Lacoste, R. Lin, and J. Hiscott. 1994. Subcellular redistribution of HTLV-1-Tax protein by NF-κB/Rel transcription factors. Virology 204:706-716.
58. Pinna, L. A. 1990 Casein kinase II: An 'eminence grise' in cellular regulation? Biochim. Biophys. Acta 1054:267-284.
59. 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-termmal domain of the protein. Mol. Cell. Biol. 15:2413-2419.
60. Ruben, S. M., P. J. Dillon, R. Schreck, T. Henkel, C. H. Chen, M. Maher, P. A. Baeuerle, and C. A. Rosen. 1991 Isolation of a rel-related human cDNA that potentially encodes the 65-kD subunit of NF-κB. Science 251:1490-1493
61. Ruben, S. M., J. F. Klement, T. A. Coleman, M. Maher, C.-H. Chen, and C. A. Rosen. 1992. I-Rel: a novel rel-related protein that inhibits NF-κB transcriptional activity. Genes Dev 6:745-760.
62. Ryseck, R.-P., P. Bull, M. Takamiya, V. Bours, U. Siebenlist, P. Dobrzanski, and R. Bravo. 1992. RelB, a new rel family transcription activator that can interact with p50-NF-κB. Mol. Cell. Biol. 12:674-684.
63. Sachdev, S., E. M. Rottjakob, J. A. Diehl, and M. Hannink. 1995. IκBα-mediated inhibition of nuclear transport and DNA-binding by Rel proteins are separable functions: phosphorylation of C-termmal serine residues of IκBα is specifically required for inhibition of DNA-binding. Oncogene 11: 811-823.
64. Schmid, R. M., N. D. Perkins, C. S. Duckett, P. C. Andrews, and G. J. Nabel. 1991. Cloning of an NF-κB subunit which stimulates HIV transcription in synergy with p65. Nature (London) 352:733-736.
65. Seldin, D. C., and P. Leder. 1995. Casein kinase IIα transgene-induced murine lymphoma relation to theileriosis in cattle. Science 267:894-897.
66. Shi, Y., E. D. Brown, and C. T. Walsh. 1994. Expression of recombinant casein kinase II and recombinant heat shock protein 90 in Escherichia coli and characterization of their interactions Proc. Natl. Acad. Sci. USA 91: 2767-2771.
67. Steward, R. 1987. Dorsal, an embryonic polarity gene in Drosophilia, is homologous to the vertebrate proto-oncogene, c-tel. Science 238:692-694.
68. Sun, S., P. A. 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.
69. Sun, S.-C., P. A. Ganchi, C. Béraud, D. W. Ballard, and W. C. Greene. 1994. Autoregulation of the NF-κB transactivator RelA (p65) by multiple cytoplasmic inhibitors containing ankyrin motifs. Proc. Natl. Acad. Sci. USA 91:1346-1350.
70. Traenckner, E. B.-M., S. Wilk, and P. A. Baeuerle. 1994. A proteasome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylated form of IκBα that is still bound to NF-κB EMBO J 13:5433-5441.
71. 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 MAD/IκBα in response to inducers of NF-κB activity. Mol. Cell. Biol. 15:5339-5345.
72. Yu, I. J., D. L. Spector, Y.-S. Bae, and D. R. Marshak. 1991. Immunocytochemical localization of casein kinase II during interphase and mitosis. J. Cell Biol. 114:1217-1232.