Control of RelB during dendritic cell activation integrates canonical and noncanonical NF-κB pathways

Nature Immunology

Volumn 13, Issue 12, 2012, Pages 1162-1170

  Shih, Vincent F S ^a   Davis Turak, Jeremy ^a   MacAl, Monica ^b   Huang, Jenny Q ^a   Ponomarenko, Julia ^c   Kearns, Jeffrey D ^a,e   Yu, Tony ^a   Fagerlund, Riku ^a   Asagiri, Masataka ^a,d   Zuniga, Elina I ^b   Hoffmann, Alexander ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d KYOTO UNIVERSITY   (Japan)

^e MERRIMACK PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR RELB;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; FIBROBLAST; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; DENDRITIC CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION; I-KAPPA B KINASE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 9; TRANSCRIPTION FACTOR RELB;

EID: 84869411578     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2446     Document Type: Article

References (47)

1. Banchereau, J. & Steinman, R.M. Dendritic cells and the control of immunity. Nature 392, 245-252 (1998). (Pubitemid 28155090)
2. Liu, Y.J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23, 275-306 (2005).
3. Serbina, N.V., Salazar-Mather, T.P., Biron, C.A., Kuziel, W.A. & Pamer, E.G. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19, 59-70 (2003). (Pubitemid 36859901)
4. Steinman, R.M. & Banchereau, J. Taking dendritic cells into medicine. Nature 449, 419-426 (2007). (Pubitemid 47509552)
5. Carrasco, D., Ryseck, R.P. & Bravo, R. Expression of relB transcripts during lymphoid organ development: specific expression in dendritic antigen-presenting cells. Development 118, 1221-1231 (1993). (Pubitemid 23252410)
6. Zanetti, M., Castiglioni, P., Schoenberger, S. & Gerloni, M. The role of relB in regulating the adaptive immune response. Ann. NY Acad. Sci. 987, 249-257 (2003). (Pubitemid 36584030)
7. Li, M. et al. Immune modulation and tolerance induction by RelB-silenced dendritic cells through RNA interference. J. Immunol. 178, 5480-5487 (2007). (Pubitemid 46674342)
8. Wu, L. et al. RelB is essential for the development of myeloid-related CD8α-dendritic cells but not of lymphoid-related CD8α+ dendritic cells. Immunity 9, 839-847 (1998). (Pubitemid 29024463)
9. Kobayashi, T. et al. TRAF6 is a critical factor for dendritic cell maturation and development. Immunity 19, 353-363 (2003). (Pubitemid 37153412)
10. Hofmann, J., Mair, F., Greter, M., Schmidt-Supprian, M. & Becher, B. NIK signaling in dendritic cells but not in T cells is required for the development of effector T cells and cell-mediated immune responses. J. Exp. Med. 208, 1917-1929 (2011).
11. Yang, H. et al. Suppression of ongoing experimental autoimmune myasthenia gravis by transfer of RelB-silenced bone marrow dentritic cells is associated with a change from a T helper Th17/Th1 to a Th2 and FoxP3+ regulatory T-cell profile. Inflamm. Res. 59, 197-205 (2010).
12. Pomerantz, J.L. & Baltimore, D. Two pathways to NF-κB. Mol. Cell 10, 693-695 (2002).
13. Oeckinghaus, A., Hayden, M.S. & Ghosh, S. Crosstalk in NF-κB signaling pathways. Nat. Immunol. 12, 695-708 (2011).
14. Derudder, E. et al. RelB/p50 dimers are differentially regulated by tumor necrosis factor-alpha and lymphotoxin-beta receptor activation: critical roles for p100. J. Biol. Chem. 278, 23278-23284 (2003). (Pubitemid 36830141)
15. Lind, E.F. et al. Dendritic cells require the NF-κB2 pathway for cross-presentation of soluble antigens. J. Immunol. 181, 354-363 (2008).
16. O'Sullivan, B.J. & Thomas, R. CD40 ligation conditions dendritic cell antigen-presenting function through sustained activation of NF-κB. J. Immunol. 168, 5491-5498 (2002). (Pubitemid 34556127)
17. Saccani, S., Pantano, S. & Natoli, G. Modulation of NF-κB activity by exchange of dimers. Mol. Cell 11, 1563-1574 (2003). (Pubitemid 36776542)
18. Ammon, C., Mondal, K., Andreesen, R. & Krause, S.W. Differential expression of the transcription factor NF-κB during human mononuclear phagocyte differentiation to macrophages and dendritic cells. Biochem. Biophys. Res. Commun. 268, 99-105 (2000). (Pubitemid 30116618)
19. Gasparini, C., Foxwell, B.M. & Feldmann, M. RelB/p50 regulates CCL19 production, but fails to promote human DC maturation. Eur. J. Immunol. 39, 2215-2223 (2009).
20. Basak, S., Shih, V.F. & Hoffmann, A. Generation and activation of multiple dimeric transcription factors within the NF-κB signaling system. Mol. Cell. Biol. 28, 3139-3150 (2008). (Pubitemid 351657080)
21. Basak, S. et al. A fourth IκB protein within the NF-κB signaling module. Cell 128, 369-381 (2007). (Pubitemid 46123518)
22. Shih, V.F. et al. Kinetic control of negative feedback regulators of NF-κB/RelA determines their pathogen-and cytokine-receptor signaling specificity. Proc. Natl. Acad. Sci. USA 106, 9619-9624 (2009).
23. Li, T. et al. MicroRNAs modulate the noncanonical transcription factor NF-κB pathway by regulating expression of the kinase IKKα during macrophage differentiation. Nat. Immunol. 11, 799-805 (2010).
24. Wuerzberger-Davis, S.M. et al. Nuclear export of the NF-κB inhibitor IκBα is required for proper B cell and secondary lymphoid tissue formation. Immunity 34, 188-200 (2011).
25. Shih, V.F., Tsui, R., Caldwell, A. & Hoffmann, A. A single NFκB system for both canonical and non-canonical signaling. Cell Res. 21, 86-102 (2011).
26. Waterfield, M., Jin, W., Reiley, W., Zhang, M. & Sun, S.C. IκB kinase is an essential component of the Tpl2 signaling pathway. Mol. Cell. Biol. 24, 6040-6048 (2004). (Pubitemid 38787986)
27. He, J.Q. et al. Rescue of TRAF3-null mice by p100 NF-κB deficiency. J. Exp. Med. 203, 2413-2418 (2006). (Pubitemid 44664610)
28. Hoffmann, A., Natoli, G. & Ghosh, G. Transcriptional regulation via the NF-κB signaling module. Oncogene 25, 6706-6716 (2006). (Pubitemid 44657847)
29. Bonizzi, G. et al. Activation of IKKα target genes depends on recognition of specific κB binding sites by RelB:p52 dimers. EMBO J. 23, 4202-4210 (2004). (Pubitemid 39546158)
30. Lernbecher, T., Kistler, B. & Wirth, T. Two distinct mechanisms contribute to the constitutive activation of RelB in lymphoid cells. EMBO J. 13, 4060-4069 (1994). (Pubitemid 24275862)
31. Dobrzanski, P., Ryseck, R.P. & Bravo, R. Differential interactions of Rel-NF-κB complexes with IκBα determine pools of constitutive and inducible NF-κB activity. EMBO J. 13, 4608-4616 (1994).
32. Fusco, A.J. et al. NF-κB p52:RelB heterodimer recognizes two classes of κB sites with two distinct modes. EMBO Rep. 10, 152-159 (2009).
33. Moorthy, A.K., Huang, D.B., Wang, V.Y., Vu, D. & Ghosh, G. X-ray structure of a NF-κB p50/RelB/DNA complex reveals assembly of multiple dimers on tandem κB sites. J. Mol. Biol. 373, 723-734 (2007). (Pubitemid 47488406)
34. Weih, F., Warr, G., Yang, H. & Bravo, R. Multifocal defects in immune responses in RelB-deficient mice. J. Immunol. 158, 5211-5218 (1997). (Pubitemid 127681224)
35. Sasaki, C.Y., Ghosh, P. & Longo, D.L. Recruitment of RelB to the Csf2 promoter enhances RelA-mediated transcription of granulocyte-macrophage colony-stimulating factor. J. Biol. Chem. 286, 1093-1102 (2011).
36. Bergqvist, S. et al. Kinetic enhancement of NF-κBxDNA dissociation by IκBα. Proc. Natl. Acad. Sci. USA 106, 19328-19333 (2009).
37. Werner, S.L., Barken, D. & Hoffmann, A. Stimulus specificity of gene expression programs determined by temporal control of IKK activity. Science 309, 1857-1861 (2005). (Pubitemid 41325096)
38. O'Dea, E.L., Kearns, J.D. & Hoffmann, A. UV as an amplifier rather than inducer of NF-κB activity. Mol. Cell 30, 632-641 (2008). (Pubitemid 351755056)
39. O'Dea, E.L. et al. A homeostatic model of IκB metabolism to control constitutive NF-κB activity. Mol. Syst. Biol. 3, 111 (2007).
40. Kearns, J.D., Basak, S., Werner, S.L., Huang, C.S. & Hoffmann, A. IκBepsilon provides negative feedback to control NF-κB oscillations, signaling dynamics, and inflammatory gene expression. J. Cell Biol. 173, 659-664 (2006). (Pubitemid 46165574)
41. Hoffmann, A., Levchenko, A., Scott, M.L. & Baltimore, D. The IκB-NF-κB signaling module: temporal control and selective gene activation. Science 298, 1241-1245 (2002). (Pubitemid 35285493)
42. Lutz, M.B. et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223, 77-92 (1999). (Pubitemid 29096240)
43. Boonstra, A. et al. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J. Exp. Med. 197, 101-109 (2003). (Pubitemid 36110261)
44. Cheng, C.S. et al. The specificity of innate immune responses is enforced by repression of interferon response elements by NF-κB p50. Sci. Signal. 4, ra11 (2011).
45. Sasik, R., Woelk, C.H. & Corbeil, J. Microarray truths and consequences. J. Mol. Endocrinol. 33, 1-9 (2004). (Pubitemid 39206343)
46. Tusher, V.G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116-5121 (2001). (Pubitemid 32397092)
47. Saeed, A.I. et al. TM4 microarray software suite. Methods Enzymol. 411, 134-193 (2006).