Signal-induced degradation of IκBα: Association with NF-κB and the PEST sequence in IκBα are not required

Molecular and Cellular Biology

Volumn 16, Issue 11, 1996, Pages 6037-6045

  Van Antwerp, Daniel J ^a,b   Verma, Inder M ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSINE; PROTEASOME; SERINE; TRANSCRIPTION FACTOR; UBIQUITIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEGRADATION; HUMAN; HUMAN CELL; PHOSPHORYLATION; PRIORITY JOURNAL;

EID: 0029851617     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.11.6037     Document Type: Article

References (71)

1. Alkalay, I., A. Yaron, A. Hatzubai, S. Jung, A. Avraham, O. Gerlitz, I. Pashut-Lavon, and Y. Ben-Neriah. 1995. In vivo stimulation of IκB phosphorylation is not sufficient to activate NF-κB. Mol. Cell. Biol. 15:1294-1301.
2. 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.
3. Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
4. Aoki, T., Y. Sano, T. Yamamoto, and J. Inoue. 1996. The ankyrin repeats but not the PEST-like sequences are required for signal-dependent degradation of IkBa. Oncogene 12:1159-1164.
5. 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.
6. Auphan, N., J. A. DiDonato, C. Rosette, A. Helmberg, and M. Karin. 1995. Immunosuppression by glucocorticoids: inhibition of NF-kappa B activity through induction of I kappa B synthesis. Science 270:286-290.
7. Baeuerle, P., and D. Baltimore. 1988. IκB: a specific inhibitor of the NF-κB transcription factor. Science 242:540-546.
8. Baldi, L., K. Brown, G. Franzoso, and U. Siebenlist. 1996. Mutation of lysines 21/22 in IkB-a block NF-κB activation. J. Biol. Chem. 271:376-379.
9. Ballard, D. W., H. Walker, S. Doerre, P. Sista, J. A. Molitor, E. P. Dixon, N. J. Peffer, M. Hannink, and W. C. Greene. 1990. The v-rel oncogene encodes a κB enhancer binding protein that inhibits NF-κB function. Cell 63:803-814.
10. Barroga, C. F., J. K. Stevenson, E. M. Schwarz, and I. M. Verma. 1995. Constitutive phosphorylation of I kappa B alpha by casein kinase II. Proc. Natl. Acad. Sci. USA 92:7637-7641.
11. Beg, A. A., and A. S. Baldwin, Jr. 1993. The I kappa B proteins: multifunctional regulators of Rel/NF-kappa B transcription factors. Genes Dev. 7:2064-2070.
12. Beg, A. A., S. M. Ruben, R. I. Scheinman, S. Haskill, C. A. Rosen, and A. S. Baldwin, Jr. 1992. I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: a mechanism for cytoplasmic retention. Genes Dev. 6:1899-1913. (Erratum, 6:2664-2665.)
13. Beg, A. A., W. C. Sha, R. T. Bronson, and D. Baltimore. 1995. Constitutive NF-kappa B activation, enhanced granulopoiesis, and neonatal lethality in I kappa B alpha-deficient mice. Genes Dev. 9:2736-2746.
14. Belvin, M. P., Y. Jin, and K. V. Anderson. 1995. Cactus protein degradation mediates Drosophila dorsal-ventral signaling. Genes Dev. 9:783-793.
15. 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.
16. Brown, K., S. Gerstberger, L. Carlson, G. Franzoso, and U. Siebenlist. 1995. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267:1485-1488.
17. Brown, K., S. Park, T. Kanno, G. Franzoso, and U. Siebenlist. 1993. Mutual regulation of the transcriptional activator NF-kappa B and its inhibitor, I kappa B-alpha. Proc. Natl. Acad. Sci. USA 90:2532-2536.
18. Cauley, K., and I. M. Verma. 1994. κB enhancer-binding complexes that do not contain NF-κB are developmentally regulated in mammalian brain. Proc. Natl. Acad. Sci. USA 91:390-394.
19. Chen, Z., J. Hagler, V. J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
20. Chiao, P. J., S. Miyamoto, and I. M. Verma. 1994. Autoregulation of I kappa B alpha activity. Proc. Natl. Acad. Sci. USA 91:28-32.
21. 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.
22. 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.
23. Ganchi, P. A., 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.
24. Geisler, R., A. Bergmann, Y. Hiromi, and C. Nusslein-Volhard. 1992. cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the I kappa B gene family of vertebrates. Cell 71:613-621.
25. Ghosh, S., A. M. Gifford, L. R. Riviere, P. Tempst, G. P. Nolan, and D. Baltimore. 1990. Cloning of the p50 subunit of NF-κB-homology to Rel and Dorsal. Cell 62:1019-1029.
26. Gilmore, T. 1991. Malignant transformation by mutant Rel proteins. Trends Genet. 7:318-322.
27. Glotzer, M., A. W. Murray, and M. W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature (London) 349:132-138.
28. Grilli, M., J. J.-S. Chiu, and M. J. Leonardo. 1993. NF-κB and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143:1-62.
29. Hatada, E. N., M. Naumann, and C. Scheidereit. 1993. Common structural constituents confer I kappa B activity to NF-kappa B p105 and I kappa B/MAD-3. EMBO J. 12:2781-2788.
30. Henkel, T., T. Machleidt, I. Alkalay, M. Kronke, Y. Ben-Neriah, and P. A. Baeuerle. 1993. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature (London) 365:182-185.
31. Higgins, H. A., J. R. Perez, T. A. Coleman, K. Dorshkind, W. A. McComas, U. M. Sarmiento, C. A. Rosen, and R. Narayanan. 1993. Antisense inhibition of p65 subunit of NF-κB blocks tumorigenesis and causes tumor regression. Proc. Natl. Acad. Sci. USA 90:9901-9905.
32. Hochstrasser, M., M. J. Ellison, V. Chau, and A. Varshavsky. 1991. The short-lived MATα2 repressor is ubiquitinated in vivo. Proc. Natl. Acad. Sci. USA 88:4606-4610.
33. Inoue, J., L. D. Kerr, A. Kakizuka, and I. M. Verma. 1992. 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 68:1109-1120.
34. Inoue, J., L. D. Kerr, L. J. Ransone, E. Bengal, T. Hunter, and I. M. Verma. 1991. c-rel activates but v-rel suppresses transcription from kappa B sites. Proc. Natl. Acad. Sci. USA 88:3715-3719.
35. Inoue, J., L. D. Kerr, D. Rashid, N. Davis, H. R. Bose, Jr., and I. M. Verma. 1992. Direct association of pp40/I kappa B beta with rel/NF-kappa B transcription factors: role of ankyrin repeats in the inhibition of DNA binding activity. Proc. Natl. Acad. Sci. USA 89:4333-4337.
36. 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.
37. Kitajima, I., T. Shinohara, J. Bilakovics, D. A. Brown, X. Xu, and M. Nerenberg. 1992. Ablation of transplanted HTLV-I Tax-transformed tumors in mice by antisense inhibition of NF-kappa B. Science 258:1792-1795. (Erratum, 259:1523, 1993.)
38. Leveillard, T., and I. M. Verma. 1993. Diverse molecular mechanisms of inhibition of NF-kappa B/DNA binding complexes by I kappa B proteins. Gene Expr. 3:135-150.
39. Luca, F. C., E. K. Shibuya, C. E. Dohrmann, and J. V. Ruderman. 1991. Both cyclin AΔ60 and BΔ97 are stable and arrest cells in M-phase, but only cyclin BΔ97 turns on cyclin destruction. EMBO J. 10:4311-4320.
40. Lucklow, B., and G. Schultz. 1987. CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res. 15:5490.
41. Mercurio, F., J. A. DiDonato, C. Rosette, and M. Karin. 1992. Molecular cloning and characterization of a novel Rel/NF-κB family member displaying structural and functional homology to NF-κB p50-p105. DNA Cell Biol. 11:523-537.
42. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-982, 984-986, 989-990.
43. Miyamoto, S., P. J. Chiao, and I. M. Verma. 1994. Enhanced IκBα degradation is responsible for constitutive NF-κB activity in mature murine B-cell lines. Mol. Cell. Biol. 14:3276-3282.
44. Miyamoto, S., M. Maki, M. J. Schmitt, M. Hatanaka, and I. M. Verma. 1994. Tumor necrosis factor alpha-induced phosphorylation of I kappa B alpha is a signal for its degradation but not dissociation from NF-kappa B. Proc. Natl. Acad. Sci. USA 91:12740-12744.
45. Naviaux, R. K., E. Costanzi, M. Haas, and I. M. Verma. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70:5701-5705.
46. 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 oncogene lyt-10, homologous to NF-kB p50. Cell 67:1075-1087.
47. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199.
48. Nolan, G. P., S. Ghosh, H. C. Liou, P. Tempst, and D. Baltimore. 1991. DNA binding and I kappa B inhibition of the cloned p65 subunit of NF-kappa B, a rel-related polypeptide. Cell 64:961-969.
49. Ohno, H., G. Takimoto, and T. W. McKeithan. 1990. The candidate protooncogene bcl-3 is related to genes implicated in cell lineage determination and cell cycle control. Cell 60:991-997.
50. Palombella, V. J., O. J. Rando, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 78:773-785.
51. Ray, P., D. H. Zhang, J. A. Elias, and A. Ray. 1995. Cloning of a differentially expressed I kappa B-related protein. J. Biol. Chem. 270:10680-10685.
52. Rice, N. R., and M. K. Ernst. 1993. In vivo control of NF-kappa B activation by I kappa B alpha. EMBO J. 12:4685-4695.
53. 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.
54. Rogers, S., R. Wells, and M. Rechsteiner. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234: 364-368.
55. Schall, T. J., M. Lewis, K. J. Koller, A. Lee, G. C. Rice, G. H. Wong, T. Gatanaga, G. A. Granger, R. Lentz, H. Raab, et al. 1990. Molecular cloning and expression of a receptor for human tumor necrosis factor. Cell 61:361-370.
56. Scharfmann, R., J. H. Axelrod, and I. M. Verma. 1991. Long-term in vivo expression of retrovirus-mediated gene transfer in mouse fibroblast implants. Proc. Natl. Acad. Sci. USA 88:4626-4630.
57. Scheinman, R. I., P. C. Cogswell, A. K. Lofquist, and A. S. Baldwin, Jr. 1995. Role of transcriptional activation of I kappa B alpha in mediation of immunosuppression by glucocorticoids. Science 270:283-286.
58. Scherer, D. C., J. A. Brockman, Z. Chen, T. Maniatis, and D. W. Ballard. 1995. Signal-induced degradation of I kappa B alpha requires site-specific ubiquitination. Proc. Natl. Acad. Sci. USA 92:11259-11263.
59. Schwartz, E. M., D. J. Van Antwerp, and I. M. Verma. 1996. Constitutive phosphorylation of IκBα by casein kinase II occurs preferentially on serine 293: requirement for degradation of free IκBα. Mol. Cell. Biol. 16:3554-3559.
60. Sen, R., and D. Baltimore. 1986. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46:705-716.
61. Steward, R. 1987. Dorsal, an embryonic polarity gene in Drosophila is homologous to the vertebrate proto-oncogene, c-rel. Science 238:692-694.
62. Sun, S. C., J. Elwood, and W. C. Greene. 1996. Both amino and carboxyl-terminal sequences within IκBα regulate its inducible degradation. Mol. Cell. Biol. 16:1058-1065.
63. Sun, S. C., P. A. Ganchi, D. W. Ballard, and W. C. Greene. 1993. NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science 259:1912-1915.
64. Thompson, J. E., R. J. Phillips, H. Erdjument-Bromage, P. Tempst, and S. Ghosh. 1995. I kappa B-beta regulates the persistent response in a biphasic activation of NF-kappa B. Cell 80:573-582.
65. Traenckner, E. B., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J. 14:2876-2883.
66. 65a. Van Antwerp, D. J. Unpublished data.
67. 65b. Van Antwerp, D. J., and E. M. Schwarz. Unpublished data.
68. Verma, I. M., J. K. Stevenson, E. M. Schwarz, D. Van Antwerp, and S. Miyamoto. 1995. Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation. Genes Dev. 9:2723-2735.
69. 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.
70. Wigler, M., A. Pellicer, S. Silverstein, and R. Axel. 1978. Biochemical transfer of single-copy eucaryotic genes using total cellular DNA as donor. Cell 14:725-731.
71. cdc28-mediated control of cln3 cyclin degradation. Mol. Cell. Biol. 15:731-741.