Basal phosphorylation of the PEST domain in IκBβ regulates its functional interaction with the c-rel proto-oncogene product

Molecular and Cellular Biology

Volumn 16, Issue 11, 1996, Pages 5974-5984

  Chu, Zhi Liang ^a   Mckinsey, Timothy A ^a   Liu, Lily ^a   Qi, Xiaoxia ^a   Ballard, Dean W ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; DNA; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEPTIDE; PROTEIN KINASE; TRANSCRIPTION FACTOR;

ANTIGENICITY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA BINDING; ELECTROPHORETIC MOBILITY; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PHOSPHORYLATION; POINT MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTO ONCOGENE; T LYMPHOCYTE;

MAMMALIA;

EID: 0029808167     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.11.5974     Document Type: Article

References (76)

1. Abbadie, C., N. Kabrun, F. Bouali, J. Smardova, D. Stéhelin, B. Vanderbunder, and P. J. Enrietto. 1993. High levels of c-rel expression are associated with programmed cell death in the developing avian embryo and in bone marrow cells in vitro. Cell 75:899-912.
2. Alkalay, I., A. Yaron, A. Hatzubai, A. Orian, A. Ciechanover, and Y. Ben-Neriah. 1995. Stimulation-dependent IκBα phosphorylation marks the NF-κB inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 92:10599-10603.
3. Andersson, S., D. L. Davis, H. Dahlback, H. Jörnvall, and D. W. Russell. 1989. Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme. J. Biol. Chem. 264:8222-8229.
4. Baldwin, A. S., Jr. 1996. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-681.
5. Ballard, D. W., E. Böhnlein, J. A. Hoffman, H. P. Bogerd, E. P. Dixon, B. R. Franza, and W. C. Greene. 1989. Activation of the interleukin-2 receptor α gene: regulatory role for DNA-protein interactions flanking the κB enhancer. New Biol. 1:83-92.
6. 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.
7. Ballard, D. W., 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.
8. 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.
9. 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.
10. Beg, A. A., W. C. Sha, R. T. Bronson, and D. Baltimore. 1995. Constitutive NF-κB activation, enhanced granulopoiesis, and neonatal lethality in IκBα-deficient mice. Genes Dev. 9:2736-2746.
11. Blanar, M., and W. J. Rutter. 1992. Interaction cloning: identification of a helix-loop-helix zipper protein that interacts with c-fos. Science 256:1014-1018.
12. Böhnlein, E., J. W. Lowenthal, M. Siekevitz, D. W. Ballard, B. R. Franz, and W. C. Greene. 1988. The same inducible nuclear protein(s) regulate mitogen activation of both the interleukin-2 receptor-alpha gene and type I human immunodeficiency virus. Cell 53:827-836.
13. Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110-149.
14. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
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 IκB-α proteotysis by site-specific, signal-induced phosphorylation. Science 267:1485-1488.
17. Bryan, R. G., Y. Li, J.-H. Lai, M. Van, N. R. Rice, R. R. Rich, and T.-H. Tan. 1994. Effect of CD28 signal transduction on c-Rel in human peripheral blood T cells. Mol. Cell. Biol. 14:7933-7942.
18. Chen, Z., J. Hagler, V. J. Palorabella, 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.
19. Costello, R., C. Lipcey, M. Algarte, C. Cerdan, P. A. Baeuerle, D. Olive, and J. Imbert. 1993. Activation of primary human T-lymphocytes through CD2 plus CD28 adhesion molecules induces long-term nuclear expression of NF-κB. Cell Growth Differ. 4:329-339.
20. Cullen, B. R. 1987. Use of eukaryotic expression technology in functional analysis of cloned genes. Methods Enzymol. 152:684-703.
21. DiDonato, J., F. Mercurio, C. Rosette, J. Wu-Li, H. Suyang, S. Ghosh, and M. Karin. 1996. Mapping of the inducible IκB phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol. 16:1295-1304.
22. DiDonato, J. A., F. Mercurio, and M. Karin. 1995. Phosphorylation of IκBα precedes but is not sufficient for ils dissociation from NF-κB. Mol. Cell. Biol. 15:1302-1316.
23. Doerre, S., P. Sista, S.-C. Sun, D. W. Ballard, and W. C. Greene. 1993. The c-rel protooncogene product represses NF-κB p65-mediated transcriptional activation of the long terminal repeat of type 1 human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 90:1023-1027.
24. DuBridge, R. B., P. Tang, H. C. Hsia, P. M. Leong, J. H. Miller, and M. P. Calos. 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379-387.
25. 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.
26. Finco, T., and A. S. Baldwin. 1995. Mechanistic aspects of NF-κB regulation: the emerging role of phosphorylation and proteolysis. Immunity 3:263-272.
27. Ganchi, P., S.-C. Sun, W. C. Greene, and D. W. Ballard. 1993. A novel NF-κB complex containing p65 homodimers: implications for transcriptional control at the level of subunit dimerization. Mol. Cell. Biol. 13:7826-7835.
28. Ghosh, P., T.-H. Tan, N. R. Rice, and H. A. Young. 1993. The IL-2 CD28-responsive complex contains at least three members of the NF-κB family: c-Rel, p50, and p65. Proc. Natl. Acad. Sci. USA 90:1696-1700.
29. Grilli, M., J. Chiu, and M. Lenardo. 1993. NF-κB and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143:1-62.
30. 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.
31. Hathaway, G. M., T. H. Lubben, and J. A. Traugh. 1980. Inhibition of casein kinase II by heparin. J. Biol. Chem. 255:8038-8044.
32. 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 the c-Jun activation domain. Genes Dev. 7:2135-2148.
33. Inoue, J.-I., L. D. Kerr, D. Rashid, H. R. Bose, Jr., and I. M. Verma. 1992. Direct association of pp40/IκBβ 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.
34. Ito, C. Y., A. G. Kazantsev, and A. S. Baldwin, Jr. 1994. Three NF-κB sites in the IκBα promoter are required for induction of gene expression by TNFα. Nucleic Acids Res. 22:3787-3792.
35. Jaffray, E., K. Wood, and R. Hay. 1995. Domain organization of IκBα and the sites of interaction with NF-κB p65. Mol. Cell. Biol. 15:2166-2172.
36. Janknecht, R., G. de Martynoff, J. Lou, R. A. Hipskind, A. Nordheim, and H. G. Stunnenberg. 1991. Rapid and efficient purification of native histidine-tagged protein expressed by recombinant vaccinia virus. Proc. Natl. Acad. Sci. USA 88:8972-8976.
37. 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 IκBβ and regulation by phosphorylation. Genes Dev. 5:1464-1476.
38. Kieran, M., V. Blank, F. Logeat, J. Vandekerckhove, F. Lottspeich, O. LeBail, M. B. Urban, P. Kourilsky, P. A. Baeuerle, and A. Israël. 1990. The DNA binding subunit of NF-κB is identified to factor KBF1 and homologous to the rel oncogene product. Cell 62:1007-1018.
39. Köntgen, F., R. J. Grumont, A. Strasser, D. Metcalf, R. Li, D. Tarlinton, and S. Gerondakis. 1995. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9:1965-1977.
40. Kuenzel, E. A., J. A. Mulligan, J. Sommercorn, and E. G. Krebs. 1987. Substrate specificity determinants for casein kinase II as deduced from studies with synthetic peptides. J. Biol. Chem. 262:9136-9140.
41. Kunsch, C., and C. A. Rosen. 1993. NF-κB subunit-specific regulation of the interleukin-8 promoter. Mol. Cell. Biol. 13:6137-6146.
42. Lai, J.-H., G. Horvath, Y. Li, and T.-H. Tan. 1995. Mechanisms of enhanced nuclear translocation of the transcription factors c-Rel and NF-κB by CD28 costimulation in human T lymphocytes. Ann. N. Y. Acad. Sci. 766:220-223.
43. Lai, J.-H., and T.-H. Tan. 1994. CD28 signaling causes a sustained down-regulation of IκBα which can be prevented by the immunosuppressant rapamycin. J. Biol. Chem. 269:30077-30080.
44. LeBail, O., R. Schmidt-Ullrich, and A. Israël. 1993. Promoter analysis of the gene encoding the IκBα/MAD3 inhibitor of NF-κB: positive regulation by members of the rel/NF-κB family. EMBO J. 12:5043-5049.
45. Lee, J. W., H.-S. Choi, J. Gyuris, R. Brent, and D. D. Moore. 1995. Two classes of proteins dependent on either the presence or absence of thyroid hormone for interaction with the thyroid hormone receptor. Mol. Endocrinol. 9:243-254.
46. 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.
47. Link, E., L. D. Kerr, R. Schreck, U. Zabel, I. Verma, and P. A. Baeuerle. 1992. Purified IκB-β is inactivated upon dephosphorylation. J. Biol. Chem. 267:239-246.
48. 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-288, S-293, and T-291 and is required for its degradation. Mol. Cell. Biol. 16:899-906.
49. McKinsey, T. A., J. A. Brockman, D. C. Scherer, S. W. Al-Murrani, P. L. Greene, 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.
50. Molitor, J. A., W. H. Walker, S. Doerre, D. W. Ballard, and W. C. Greene. 1990. NF-κB: a family of inducible and differentially expressed enhancer-binding proteins in human T cells. Proc. Natl. Acad. Sci. USA 87:10028-10032.
51. Muller, E., B. Boldyreff, and K. H. Scheidtmann. 1993. Characterization of protein kinase activities associated with p53-large-T immune complexes from SV40-transformed rat cells. Oncogene 8:2193-2205.
52. Nakamaya, K., H. Shimizu, K. Mitomo, T. Watanabe, S.-I. Okamoto, and K.-I. Yamamoto. 1992. A lymphoid cell-specific nuclear factor containing c-Rel-like proteins preferentially interacts with interleukin-6 κB-related motifs whose activities are repressed in lymphoid cells. Mol. Cell. Biol. 12:1736-1746.
53. Neumann, J., C. Morency, and K. Russian. 1987. A novel rapid assay for chloramphenicol acetyltransferase gene expression. BioTechniques 5:444-447.
54. Palombella, V. J., O. J. Rando, A. L. Goldberg, and T. Manialis. 1994. Ubiquitin and the proteasome are required for processing the NF-κB1 precursor and the activation of NF-κB. Cell 78:773-785.
55. Prickett, K. S., D. C. Amberg, and T. P. Hopp. 1989. A calcium-dependent antibody for identification and purification of recombinant proteins. BioTechniques 7:580-589.
56. Rechsteiner, M., and S. W. Rogers. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:267-271.
57. Rogers, S., R. Wells, and M. Rechsteiner. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234: 364-368.
58. 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 p65-kD subunit of NF-κB. Science 251:1490-1493.
59. 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-terminal serine residues of IκB-α is specifically required for inhibition of DNA-binding. Oncogene 11: 811-823.
60. Sawada, K., S. B. Krantz, J. S. Kans, E. D. Dessypris, S. Sawyer, A. D. Glick, C. I. Civin. 1987. Purification of human erythroid colony forming units and demonstration of specific binding of erythropoietin. J. Clin. Invest. 80:357-364.
61. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range of 1 to 100 kDa. Anal. Biochem. 166:368-379.
62. 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.
63. Schreiber, E., P. Matthias, M. Muller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17:6419.
64. Schwarz, E. M., D. van Antwerp, and I. M. Verma. 1996. Constitutive phosphorylation of IκBα by casein kinase II occurs preferentially at serine 293: requirement for degradation of free IκBα. Mol. Cell. Biol. 16:3554-3559.
65. Sha, W. C., H.-C. Liou, E. I. Tuomanen, and D. Baltimore. 1995. Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell 80:321-330.
66. Siebenlist, U., G. Franzoso, and K. Brown. 1994. Structure, regulation and function of NF-κB. Annu. Rev. Cell Biol. 10:405-455.
67. Stein, B., H. J. Rahmsdorf, A. Steffen, M. Litfin, and P. Herrlich. 1989. UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothioncin. Mol. Cell. Biol. 9:5169-5181.
68. 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.
69. Suyang, H., R. Phillips, I. Douglas, and S. Ghosh. 1996. Role of unphosphorylated, newly synthesized IκBβ in persistent activation of NF-κB. Mol. Cell. Biol. 16:5444-5449.
70. Tan, T.-H., G. P. Huang, A. Sica, P. Ghosh, H. A. Young, D. L. Longo, and N. R. Rice. 1992. κB site-dependent activation of the interleukin-2 receptor α-chain gene promoter by human c-Rel. Mol. Cell. Biol. 12:4067-4075.
71. Thanos, D., and T. Maniatis. 1995. NF-κB: a lesson in family values. Cell 80:529-532.
72. Thompson, J. E., R. J. Phillips, H. Erdjument-Bromage, P. Tempst, and S. Ghosh. 1995. IκB-β regulates the persistent response in a biphasic activation of NF-κB. Cell 80:573-582.
73. Traenckner, E. B.-M., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human IκB-α on serines 32 and 36 controls IκB-α proteolysis and NF-κB activation in response to diverse stimuli. EMBO J. 14:2876-2883.
74. 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.
75. Weil, F., D. Carrasco, S. K. Durham, D. S. Barton, C. A. Rizzo, R.-P. Ryseck, S. A. Lira, and R. Bravo. 1995. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-κB/Rel family. Cell 80:331-340.
76. 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.