IL-4-stimulated NF-κB activity is required for Stat6 DNA binding

Journal of Leukocyte Biology

Volumn 82, Issue 2, 2007, Pages 370-379

  Thieu, Vivian T ^a   Nguyen, Evelyn T ^a   McCarthy, Brian P ^a   Bruns, Heather A ^a   Kapur, Reuben ^a   Chang, Cheong Hee ^a   Kaplan, Mark H ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Gene regulation; p100 processing; Transcription factors

Indexed keywords

CD86 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P100; PROTEIN P52; STAT6 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DNA BINDING; ENZYME PHOSPHORYLATION; GENE EXPRESSION; IMMUNE RESPONSE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; CELLS, CULTURED; DNA; GENES, REPORTER; INTERLEUKIN-4; LUCIFERASES; MICE; MICE, INBRED C57BL; NF-KAPPA B; STAT6 TRANSCRIPTION FACTOR;

EID: 34547777485     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1106707     Document Type: Article

References (64)

1. Kelly-Welch, A., Hanson, E. M., Keegan, A. D. (2005) Interleukin-4 (IL-4) pathway. Sci. STKE 2005, cm9.
2. Nelms, K., Huang, H., Ryan, J., Keegan, A., Paul, W. E. (1998) Interleukin-4 receptor signaling mechanisms and their biological significance. Adv. Exp. Med. Biol. 452, 37-43.
3. Nelms, K., Keegan, A. D., Zamorano, J., Ryan, J. J., Paul, W. E. (1999) The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17, 701-738.
4. Seder, R. A., Paul, W. E., Davis, M. M., Fazekas de St Groth, B. (1992) The presence of interleukin 4 during in vitro priming determines the lymphokine-producing potential of CD4+ T cells from T cell receptor transgenic mice. J. Exp. Med. 176, 1091-1098.
5. Swain, S. L., Weinberg, A. D., English, M., Huston, G. (1990) IL-4 directs the development of Th2-like helper effectors. J. Immunol. 145, 3796-3806.
6. Conrad, D. H., Waldschmidt, T. J., Lee, W. T., Rao, M., Keegan, A. D., Noelle, R. J., Lynch, R. G., Kehry, M. R. (1987) Effect of B cell stimulatory factor-1 (interleukin 4) on Fc ε and Fc γ receptor expression on murine B lymphocytes and B cell lines. J. Immunol. 139, 2290-2296.
7. Ohara, J., Paul, W. E. (1988) Up-regulation of interleukin 4/B-cell stimulatory factor 1 receptor expression. Proc. Natl. Acad. Sci. USA 85, 8221-8225.
8. Noelle, R., Krammer, P. H., Ohara, J., Uhr, J. W., Vitetta, E. S. (1984) Increased expression of Ia antigens on resting B cells: an additional role for B-cell growth factor. Proc. Natl. Acad. Sci. USA 81, 6149-6153.
9. Noelle, R. J., Kuziel, W. A., Maliszewski, C. R., McAdams, E., Vitetta, E. S., Tucker, P. W. (1986) Regulation of the expression of multiple class II genes in murine B cells by B cell stimulatory factor-1 (BSF-1). J. Immunol. 137, 1718-1723.
10. Stack, R. M., Lenschow, D. J., Gray, G. S., Bluestone, J. A., Fitch, F. W. (1994) IL-4 treatment of small splenic B cells induces costimulatory molecules B7-1 and B7-2. J. Immunol. 152, 5723-5733.
11. Coffman, R. L., Ohara, J., Bond, M. W., Carty, J., Zlotnik, A., Paul, W. E. (1986) B cell stimulatory factor-1 enhances the IgE response of lipopolysaccharide-activated B cells. J. Immunol. 136, 4538-4541.
12. Vitetta, E. S., Ohara, J., Myers, C. D., Layton, J. E., Krammer, P. H., Paul, W. E. (1985) Serological, biochemical, and functional identity of B cell-stimulatory factor 1 and B cell differentiation factor for IgG1. J. Exp. Med. 162, 1726-1731.
13. Kotanides, H., Reich, N. C. (1996) Interleukin-4-induced STAT6 recognizes and activates a target site in the promoter of the interleukin-4 receptor gene. J. Biol. Chem. 271, 25555-25561.
14. Keegan, A., Nelms, K., Paul, W. E. (1994) The IL-4 receptor - signaling mechanisms. Adv. Exp. Med. Biol. 365, 211-215.
15. Quelle, F. W., Shimoda, K., Thierfelder, W., Fischer, C., Kim, A., Ruben, S. M., Cleveland, J. L., Pierce, J. H., Keegan, A. D., Nelms, K. (1995) Cloning of murine Stat6 and human Stat6, Stat proteins that are tyrosine phosphorylated in responses to IL-4 and IL-3 but are not required for mitogenesis. Mol. Cell. Biol. 15, 3336-3343.
16. Kaplan, M. H., Schindler, U., Smiley, S. T., Grusby, M. J. (1996) Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4, 313-319.
17. Takeda, K., Tanaka, T., Shi, W., Matsumoto, M., Minami, M., Kashiwamura, S., Nakanishi, K., Yoshida, N., Kishimoto, T., Akira, S. (1996) Essential role of Stat6 in IL-4 signaling. Nature 380, 627-630.
18. Shimoda, K., van Deursen, J., Sangster, M. Y., Sarawar, S. R., Carson, R. T., Tripp, R. A., Chu, C., Quelle, F. W., Nosaka, T., Vignali, D. A., Doherty, P. C., Grosveld, G., Paul, W. E., Ihle, J. N. (1996) Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380, 630-633.
19. Zamorano, J., Wang, H. Y., Wang, L. M., Pierce, J. H., Keegan, A. D. (1996) IL-4 protects cells from apoptosis via the insulin receptor substrate pathway and a second independent signaling pathway. J. Immunol. 157, 4926-4934.
20. Kelly-Welch, A. E., Wang, H. Y., Wang, L-M., Pierce, J. H., Jay, G., Finkelman, F., Keegan, A. D. (2004) Transgenic expression of insulin receptor substrate 2 in murine B cells alters the cell density-dependence of IgE production in vitro and enhances IgE production in vivo. J. Immunol. 172, 2803-2810.
21. Zamorano, J., Kelly, A. E., Austrian, J., Wang, H. Y., Keegan, A. D. (2001) Costimulation of resting B lymphocytes alters the IL-4-activated IRS2 signaling pathway in a STAT6 independent manner: implications for cell survival and proliferation. Cell Res. 11, 44-54.
22. Siebenlist, U., Brown, K., Claudio, E. (2005) Control of lymphocyte development by nuclear factor-[κ]B. Nat. Rev. Immunol. 5, 435-445.
23. Bonizzi, G., Karin, M. (2004) The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25, 280-288.
24. Beinke, S., Ley, S. C. (2004) Functions of NF-κB1 and NF-κB2 in immune cell biology. Biochem. J. 382, 393-409.
25. Viatour, P., Bentires-Alj, M., Chariot, A., Deregowski, V., de Leval, L., Merville, M. P., Bours, V. (2003) NF-κ B2/p100 induces Bcl-2 expression. Leukemia 17, 1349-1356.
26. Claudio, E., Brown, K., Park, S., Wang, H., Siebenlist, U. (2002) BAFFinduced NEMO-independent processing of NF-[κ]B2 in maturing B cells. Nat. Immunol. 3, 958-965.
27. Kayagaki, N., Yan, M., Seshasayee, D., Wang, H., Lee, W., French, D. M., Grewal, I. S., Cochran, A. G., Gordon, N. C., Yin, J., Starovasnik, M. A., Dixit, V. M. (2002) BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-κB2. Immunity 17, 515-524.
28. Dejardin, E., Droin, N. M., Delhase, M., Haas, E., Cao, Y., Makris, C., Li, Z. W., Karin, M., Ware, C. F., Green, D. R. (2002) The lymphotoxin-β receptor induces different patterns of gene expression via two NF-κB pathways. Immunity 17, 525-535.
29. Mordmuller, B., Krappmann, D., Esen, M., Wegener, E., Scheidereit, C. (2003) Lymphotoxin and lipopolysaccharide induce NF-κB-p52 generation by a co-translational mechanism. EMBO Rep. 4, 82-87.
30. Muller, J. R., Siebenlist, U. (2003) Lymphotoxin β receptor induces sequential activation of distinct NF-κ B factors via separate signaling pathways. J. Biol. Chem. 278, 12006-12012.
31. Coope, H. J., Atkinson, P. G., Huhse, B., Belich, M., Janzen, J., Holman, M. J., Klaus, G. G., Johnston, L. H., Ley, S. C. (2002) CD40 regulates the processing of NF-κB2 p100 to p52. EMBO J. 21, 5375-5385.
32. Zarnegar, B., He, J. Q., Oganesyan, G., Hoffmann, A., Baltimore, D., Cheng, G. (2004) Unique CD40-mediated biological program in B cell activation requires both type 1 and type 2 NF-κB activation pathways. Proc. Natl. Acad. Sci. USA 101, 8108-8113.
33. Senftleben, U., Cao, Y., Xiao, G., Greten, F. R., Krahn, G., Bonizzi, G., Chen, Y., Hu, Y., Fong, A., Sun, S. C., Karin, M. (2001) Activation by IKKα of a second, evolutionary conserved, NF-κ B signaling pathway. Science 293, 1495-1499.
34. Senftleben, U., Karin, M. (2002) The IKK/NF-κ B pathway. Crit. Care Med. 30, S18-S26.
35. Xiao, G., Harhaj, E. W., Sun, S. C. (2001) NF-κB-inducing kinase regulates the processing of NF-κB2 p100. Mol. Cell 7, 401-409.
36. Xiao, G., Fong, A., Sun, S. C. (2004) Induction of p100 processing by NF-κB-inducing kinase involves docking IκB kinase α (IKKα) to p100 and IKKα-mediated phosphorylation. J. Biol. Chem. 279, 30099-30105.
37. Brown, K. D., Hostager, B. S., Bishop, G. A. (2001) Differential signaling and tumor necrosis factor receptor-associated factor (TRAF) degradation mediated by CD40 and the Epstein-Barr virus oncoprotein latent membrane protein 1 (LMP1). J. Exp. Med. 193, 943-954.
38. Moore, C. R., Bishop, G. A. (2005) Differential regulation of CD40-mediated TNF receptor-associated factor degradation in B lymphocytes. J. Immunol. 175, 3780-3789.
39. Karin, M., Lin, A. (2002) NF-κB at the crossroads of life and death. Nat. Immunol. 3, 221-227.
40. Chang, H. C., Zhang, S., Thieu, V. T., Slee, R. B., Bruns, H. A., Laribee, R. N., Klemsz, M. J., Kaplan, M. H. (2005) PU.1 expression delineates heterogeneity in primary Th2 cells. Immunity 22, 693-703.
41. Bruns, H. A., Schindler, U., Kaplan, M. H. (2003) Expression of a constitutively active Stat6 in vivo alters lymphocyte homeostasis with distinct effects in T and B cells. J. Immunol. 170, 3478-3487.
42. Hayden, M. S., Ghosh, S. (2004) Signaling to NF-κB. Genes Dev. 18, 2195-2224.
43. Liao, G., Zhang, M., Harhaj, E. W., Sun, S-C. (2004) Regulation of the NF-{κ}B-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J. Biol. Chem. 279, 26243-26250.
44. Ozes, O. N., Mayo, L. D., Gustin, J. A., Pfeffer, S. R., Pfeffer, L. M., Donner, D. B. (1999) NF-[κ]B activation by tumor necrosis factor requires the Akt serine-threonine kinase. Nature 401, 82-85.
45. Gustin, J. A., Ozes, O. N., Akca, H., Pincheira, R., Mayo, L. D., Li, Q., Guzman, J. R., Korgaonkar, C. K., Donner, D. B. (2004) Cell type-specific expression of the I{κ}B kinases determines the significance of phosphatidylinositol 3-kinase/Akt signaling to NF-{κ}B activation. J. Biol. Chem. 279, 1615-1620.
46. Gustin, J. A., Korgaonkar, C. K., Pincheira, R., Li, Q., Donner, D. B. (2006) Akt regulates basal and induced processing of NF-{κ}B2 (p100) to p52. J. Biol. Chem. 281, 16473-16481.
47. Schnyder, B., Schnyder-Candrian, S., Panski, A., Bommel, H., Heim, M., Duschl, A., Moser, R. (2002) Phytochemical inhibition of interleukin-4-activated Stat6 and expression of VCAM-1. Biochem. Biophys. Res. Commun. 292, 841-847.
48. Oomizu, S., Yanase, Y., Suzuki, H., Kameyoshi, Y., Hide, M. (2006) Fucoidan prevents C[ε] germline transcription and NF[κ]B p52 translocation for IgE production in B cells. Biochem. Biophys. Res. Commun. 350, 501-507.
49. Schaffer, A., Cerutti, A., Shah, S., Zan, H., Casali, P. (1999) The evolutionarily conserved sequence upstream of the human Ig heavy chain S{γ}3 region is an inducible promoter: synergistic activation by CD40 ligand and IL-4 via cooperative NF-{κ}B and STAT-6 binding sites. J. Immunol. 162, 5327-5336.
50. Tinnell, S. B., Jacobs-Helber, S. M., Sterneck, E., Sawyer, S. T., Conrad, D. H. (1998) STAT6, NF-κB and C/EBP in CD23 expression and IgE production. Int. Immunol. 10, 1529-1538.
51. Lin, S. C., Stavnezer, J. (1996) Activation of NF-κB/Rel by CD40 engagement induces the mouse germ line immunoglobulin Cγ1 promoter. Mol. Cell. Biol. 16, 4591-4603.
52. Dedeoglu, F., Horwitz, B., Chaudhuri, J., Alt, F. W., Geha, R. S. (2004) Induction of activation-induced cytidine deaminase gene expression by IL-4 and CD40 ligation is dependent on STAT6 and NF{κ}B. Int. Immunol. 16, 395-404.
53. Stutz, A. M., Woisetschlager, M. (1999) Functional synergism of STAT6 with either NF-{κ}B or PU.1 to mediate IL-4-induced activation of IgE germline gene transcription. J. Immunol. 163, 4383-4391.
54. Messner, B., Stutz, A. M., Albrecht, B., Peiritsch, S., Woisetschlager, M. (1997) Cooperation of binding sites for STAT6 and NF κ B/rel in the IL-4-induced up-regulation of the human IgE germline promoter. J. Immunol. 159, 3330-3337.
55. Warren, W. D., Roberts, K. L., Linehan, L. A., Berton, M. T. (1999) Regulation of the germline immunoglobulin C[γ]1 promoter by CD40 ligand and IL-4: dual role for tandem NF-[κ]B binding sites. Mol. Immunol. 36, 31-44.
56. Shen, C-H., Stavnezer, J. (1998) Interaction of Stat6 and NF-κ B: direct association and synergistic activation of interleukin-4-induced transcription. Mol. Cell. Biol. 18, 3395-3404.
57. Iciek, L. A., Delphin, S. A., Stavnezer, J. (1997) CD40 cross-linking induces Ig ε germline transcripts in B cells via activation of NF-κB: synergy with IL-4 induction. J. Immunol. 158, 4769-4779.
58. Berton, M. T., Linehan, L. A., Wick, K. R., Dunnick, W. A. (2004) NF-{κ}B elements associated with the Stat6 site in the germline {γ}1 immunoglobulin promoter are not necessary for the transcriptional response to CD40 ligand. Int. Immunol. 16, 1741-1749.
59. Gupta, S., Jiang, M., Anthony, A., Pernis, A. B. (1999) Lineage-specific modulation of interleukin 4 signaling by interferon regulatory factor 4. J. Exp. Med. 190, 1837-1848.
60. Lischke, A., Moriggl, R., Brandlein, S., Berchtold, S., Kammer, W., Sebald, W., Groner, B., Liu, X., Hennighausen, L., Friedrich, K. (1998) The interleukin-4 receptor activates STAT5 by a mechanism that relies upon common γ-chain. J. Biol. Chem. 273, 31222-31229.
61. Kuchtey, J., Pennini, M., Pai, R. K., Harding, C. V. (2003) CpG DNA induces a class II transactivator-independent increase in class II MHC by stabilizing class II MHC mRNA in B lymphocytes. J. Immunol. 171, 2320-2325.
62. Pai, R. K., Askew, D., Boom, W. H., Harding, C. V. (2002) Regulation of class II MHC expression in APCs: roles of types I, III, and IV class II transactivator. J. Immunol. 169, 1326-1333.
63. Finn, P. W., Kara, C. J., Grusby, M. J., Folsom, V., Glimcher, L. H. (1991) Upstream elements of the MHC class II E β gene active in B cells. J. Immunol. 146, 4011-4015.
64. Kretsovali, A., Papamatheakis, J. (1995) A novel IL-4 responsive element of the E α MHC class II promoter that binds to an inducible factor. Nucleic Acids Res. 23, 2919-2928.