IκBγ inhibits DNA binding of NF-κB p50 homodimers by interacting with residues that contact DNA

Molecular and Cellular Biology

Volumn 16, Issue 11, 1996, Pages 6477-6485

  Bell, Stefan ^a,b   Matthews, James R ^a   Jaffray, Ellis ^a   Hay, Ronald T ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELLULAR DISTRIBUTION; CRYSTAL STRUCTURE; DNA BINDING; DNA FOOTPRINTING; DNA PROTEIN COMPLEX; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION;

EID: 0029851622     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.11.6477     Document Type: Article

References (72)

1. 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 activity of NF-κB. Mol. Cell. Biol. 15:2689-2696.
2. Atassi, M. Z., and A. F. S. A. Habeeb. 1972. Reactions of proteins with citraconic anhydride. Methods Enzymol. 25:546-553.
3. Bacon, D. J., and D. J. Anderson. 1988. A fast algorithm for rendering space-filling molecule pictures. J. Mol. Graphics 6:218-220.
4. 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.
5. Baeuerle, P. A., and D. Baltimore. 1988. IκB: a specific inhibitor of the NF-κB transcription factor. Science 242:540-546.
6. Baeuerle, P. A., and D. Baltimore. 1989. A 65 kD subunit of active NF-κB is required for inhibition of NF-κB by IκB. Genes Dev. 3:1689-1698.
7. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:141-179.
8. 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. 13:3301-3310.
9. 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 localisation sequences of the subunits of NF-κB: a mechanism for cytoplasmic retention. Genes Dev. 6:1899-1913.
10. Blank, V., P. Kourilsky, and A. Israel. 1991. Cytoplasmic retention, DNA binding and processing of the NF-κB p50 precursor are controlled by a small region in its C-terminus. EMBO J. 10:4159-4167.
11. 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.
12. Breeden, L., and K. Nasmyth. 1987. Similarity between cell-cycle genes of budding yeast and fission yeast and the notch gene of Drosophila. Nature (London) 329:651-654.
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. Chen, Z. J., J. Hagler, V. J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995. Signal-induced site specific phosphorylation targets IκB-α to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
15. Chiao, P. J., S. Miyamoto, and I. M. Verma. 1994. Autoregulation of IκB-α activity. Proc. Natl. Acad. Sci. USA 91:28-32.
16. Clark, L., and R. T. Hay. 1989. Sequence requirement for specific interaction of an enhancer binding protein (EBP1) with DNA. Nucleic Acids Res. 17:499-515.
17. Clark, L., J. Nicholson, and R. T. Hay. 1989. Enhancer binding protein (EBP1) makes base and backbone contacts over one complete turn of the DNA double helix. J. Mol. Biol. 206:615-626.
18. Cordle, S. R., R. Donald, M. A. Read, and J. Hawiger. 1993. Lipopolysaccharide induces phosphorylation of MAD3 and activation of c-rel and related NF-κB proteins in human monocytic THP-1 cells. J. Biol. Chem. 268: 11803-11810.
19. de Martin, R., B. Vanhove, Q. Cheng, E. Hofer, V. Csizmadia, H. Winkler, and F. H. Bach. 1993. Cytokine inducible expression in endothelial cells of an IκB-α-like gene is regulated by NF-κB. EMBO J. 12:2773-2779.
20. Ernst, M. K., L. L. Dunn, and N. R. Rice. 1995. The PEST-like sequence of IκBα is responsible for inhibition of DNA binding but not for cytoplasmic retention of c-Rel or RelA homodimers. Mol. Cell. Biol. 15:872-882.
21. Ghosh, G., G. van Duyne, S. Ghosh, and P. B. Sigler. 1995. Structure of NF-κB p50 homodimer bound to a κB site. Nature (London) 373:303-310.
22. 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.
23. Gilmore, T. D., and P. J. Morin. 1993. The IκB proteins: members of a multifunctional family. Trends Genet. 9:427-433.
24. Grilli, M., J. J.-S. Chiu, and M. J. Lenardo. 1993. NF-κB and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143: 1-62.
25. Gross, E. 1967. The cyanogen bromide reaction. Methods Enzymol. 11:238-255.
26. Hanai, R., and J. C. Wang. 1994. Protein footprinting by the combined use of reversible and irreversible lysine modifications. Proc. Natl. Acad. Sci. USA 91:11904-11908.
27. Hanke, T., P. Szawlowski, and R. E. Randall. 1992. Construction of solid matrix-antibody complexes containing simian immunodeficiency virus p27 using tag-specific monoclonal antibody and tag-linked antigen. J. Gen. Virol. 73:653-660.
28. 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. Characterisation of an immediate-early gene induced in adherent monocytes that encodes IκB like activity. Cell 65:1281-1289.
29. Hatada, E. N., M. Naumann, and C. Scheidereit. 1993. Common structural constituents confer IκB activity to NF-κB p105 and IκB/MAD-3. EMBO J. 12:2781-2788.
30. Hay, R. T., and J. Nicholson. 1993. DNA binding alters the protease susceptibility of the p50 subunit of NF-κB. Nucleic Acids Res. 21:4592-4598.
31. Henkel, T., T. Machleidt, I. Alkalay, M. Kroenke, Y. Ben-Neriah, and P. A. Baeuerle. 1993. Rapid proteolysis of IκB-α is necessary for activation of transcription factor NF-κB. Nature (London) 365:182-185.
32. Inoue, J.-I., L. D. Kerr, D. Rashid, N. Davis, H. R. Bose, Jr., and I. M. Verma. 1992. Direct association of pp40/IκB-β with rel/NF-κB transcription factors: role of ankyrin repeats in the inhibition of DNA binding activity. Proc. Natl. Acad. Sci. USA 89:4333-4337.
33. Ip, Y. T., M. Reach, Y. Engstrom, L. Kadalayil, H. Cai, S. Gonzalez-Crespo, K. Tatei, and M. Levine. 1993. Dif, a dorsal-related gene that mediates an immune response in Drosophita. Cell 75:753-763.
34. 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.
35. Juillerat, M., G. R. Parr, and H. Taniuchi. 1980. A biologically active, three fragment complex of horse heart cytochrome. J. Biol. Chem. 255:845-853.
36. Kieran, M., V. Blank, F. Logeat, J. Vandekerckhove, F. Lottspeich, O. LeBail, 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.
37. Kumar, S., and C. Gelinas. 1993. IκB α-mediated inhibition of v-Rel DNA binding requires direct interaction with the RXXRXRXXC Rel/κB DNA-binding motif. Proc. Natl. Acad. Sci. USA 90:8962-8966.
38. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
39. LeBail, O., R. Schmidt-Ullrich, and A. Israel. 1993. Promoter analysis of the gene encoding the IκB-α/MAD-3 inhibitor of NF-κB: positive regulation by members of the rel/NF-κB family. EMBO J. 12:5043-5049.
40. Lehming, N., S. McGuire, J. M. Brickman, and M. Ptashne. 1995. Interactions of a Rel protein with its inhibitor. Proc. Natl. Acad. Sci. USA 92:10242-10246.
41. Lindsay, D. G., and S. Shall. 1971. Acetylation of the free amino groups of insulin. Biochem. J. 121:737-745.
42. Lindsley, J. E., and J. C. Wang. 1991. Proteolysis patterns of epitopically labelled yeast DNA topoisomerase II suggests an allosteric transition in the enzyme induced by ATP binding. Proc. Natl. Acad. Sci. USA 88:10485-10489.
43. 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.
44. Liou, H.-C., G. P. Nolan, S. Ghosh, T. Fujita, and D. Baltimore. 1992. The NF-κB p50 precursor, p105, contains an internal IκB-like inhibitor that preferentially inhibits p50. EMBO J. 11:3003-3009.
45. Lopez de Saro, F. J., A. Y. M. Woody, and D. Helmann. 1995. Structural analysis of the Bacillus subtilis δ factor: a protein polyanion which displaces RNA from RNA polymerase. J. Mol. Biol. 252:184-202.
46. Lux, S. E., M. K. John, and V. Bennett. 1990. Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature (London) 344:36-42.
47. Matthews, J. R., and R. T. Hay. 1995. Regulation of the DNA binding activity of NF-κB. Int. J. Biochem. Cell Biol. 9:865-879.
48. Matthews, J. R., W. Kaszubska, G. Turcatti, T. N. C. Wells, and R. T. Hay. 1993. The role of cysteine 62 in DNA recognition by the p50 subunit of NF-κB. Nucleic Acids Res. 21:1727-1734.
49. Matthews, J. R., J. Nicholson, E. Jaffray, S. M. Kelly, N. D. Price, and R. T. Hay. 1995. Conformational changes induced by DNA binding of NF-κB. Nucleic Acids Res. 23:3393-3402.
50. Matthews, J. R., N. Wakasugi, J.-L. Virelizier, J, Yodoi, and R. T. Hay. 1992. Thioredoxin regulates the DNA binding activity of NF-κB by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res. 20:3821-3830.
51. Matthews, J. R., E. A. Watson, S. L. Buckley, and R. T. Hay. 1993. Interaction of the C-terminal region of p105 with the nuclear localisation signal of p50 is required for inhibition of NF-κB DNA binding activity. Nucleic Acids Res. 21:4516-4523.
52. Mellitis, K. H., R. T. Hay, and S. Goodbourn. 1993. Proteolytic degradation of MAD-3 (IκB α) and enhanced processing of the NF-κB precursor p105 are obligatory steps in the activation of NF-κB. Nucleic Acids Res. 21:5059-5066.
53. Merrit, E. A., and M. E. P. Murphy. 1994. Raster3D version-2.0. A program for photorealistic molecular graphics. Acta Crystallogr. Sect. D 50:869-873.
54. Müller, C. W., F. A. Rey, M. Sodeoka, G. L. Verdine, and S. C. Harrison. 1995. Structure of the NF-κB p50 homodimer bound to DNA. Nature (London) 373:311-317.
55. 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 associated chromosomal translocation involves candidate oncogene lyt-10, homologous to NF-κB p50. Cell 67:1075-1087.
56. 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.
57. Palombella, V. J., O. J. Rando, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-κBI precursor protein and the activation of NF-κB. Cell 78:773-785.
58. Rice, N. R., and M. K. Ernst. 1993. In vivo control of NF-κB activation by IκB-α. EMBO J. 12:4685-4695.
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-terminal 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. 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.
62. Schägger, H., and G. Jagov. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
63. Schmid, R. M., N. D. Perkins, C. S. Duckett, P. C. Andrews, and G. J. Nabel. 1991. Cloning of a NF-κB subunit which stimulates HIV transcription in synergy with p65. Nature (London) 352:733-736.
64. Schmitz, M. L., and P. A. Baeuerle. 1991. The p65 subunit is responsible for the strong transcription activating potential of NF-κB. EMBO J. 10:3805-3817.
65. Sen, R., and D. Baltimore. 1986. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46:705-716.
66. Siebenlist, U., G. Franzoso, and K. Brown. 1994. Structure, regulation and function of NF-κB. Annu. Rev. Cell Biol. 10:405-455.
67. Steward, R. 1987. Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science 238:692-694.
68. Sun, S.-C., P. A. Ganchi, D. W. Ballard, and W. C. Greene. 1993. NF-κB controls expression of inhibitor IκB-α: evidence for an inducible autoregulatory pathway. Science 259:1912-1915.
69. Thanos, D., and T. Maniatis. 1995. NF-κB: a lesson in family values. Cell 80:529-532.
70. Thompson, J. E., R. J. Phillips, H. Erdjument-Bromage, P. Tempst, and S. Ghosh. 1995. IκB-B regulates the persistent response in a biphasic activation of NF-κB. Cell 80:573-582.
71. Wilhelmsen, K. C., K. Eggleton, and H. M. Temin. 1984. Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel. J. Virol. 52:172-182.
72. Zabel, U., and P. A. Baeuerle. 1990. Purified human IκB can rapidly dissociate the complex of the NF-κB transcription factor with its cognate DNA. Cell 61:255-265.