Noncanonical NF-κB signaling is limited by classical NF-κB activity

Science Signaling

Volumn 7, Issue 311, 2014, Pages

  Gray, Carolyn M ^a   Remouchamps, Caroline ^b   McCorkell, Kelly A ^a   Solt, Laura A ^c   Dejardin, Emmanuel ^b   Orange, Jordan S ^d,e   May, Michael J ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELLS, CULTURED; GENE EXPRESSION; HUMANS; I-KAPPA B KINASE; IMMUNOBLOTTING; IMMUNOLOGIC DEFICIENCY SYNDROMES; JURKAT CELLS; LEUKOCYTES, MONONUCLEAR; MICE; MUTATION; NF-KAPPA B; NF-KAPPA B P52 SUBUNIT; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 14;

EID: 84894232387     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004557     Document Type: Article

References (46)

1. M. S. Hayden, S. Ghosh, Shared principles in NF-κB signaling. Cell 132, 344-362 (2008).
2. M. S. Hayden, S. Ghosh, NF-κB in immunobiology. Cell Res. 21, 223-244 (2011).
3. T. Kawai, R. Nishikomori, T. Heike, Diagnosis and treatment in anhidrotic ectodermal dysplasia with immunodeficiency. Allergol. Int. 61, 207-217 (2012).
4. L. A. Solt, M. J. May, The IκB kinase complex: Master regulator of NF-κB signaling. Immunol. Res. 42, 3-18 (2008).
5. D. Rudolph, W. C. Yeh, A. Wakeham, B. Rudolph, D. Nallainathan, J. Potter, A. J. Elia, T. W. Mak, Severe liver degeneration and lack of NF-κB activation in NEMO/IKKγ-deficient mice. Genes Dev. 14, 854-862 (2000).
6. E. Zandi, D. M. Rothwarf, M. Delhase, M. Hayakawa, M. Karin, The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell 91, 243-252 (1997).
7. D. M. Rothwarf, E. Zandi, G. Natoli, M. Karin, IKK-γ is an essential regulatory subunit of the IκB kinase complex. Nature 395, 297-300 (1998).
8. J. A. DiDonato, M. Hayakawa, D. M. Rothwarf, E. Zandi, M. Karin, A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388, 548-554 (1997).
9. Q. Li, D. Van Antwerp, F. Mercurio, K. F. Lee, I. M. Verma, Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science 284, 321-325 (1999).
10. Z. W. Li, W. Chu, Y. Hu, M. Delhase, T. Deerinck, M. Ellisman, R. Johnson, M. Karin, The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189, 1839-1845 (1999).
11. F. Mercurio, B. W. Murray, A. Shevchenko, B. L. Bennett, D. B. Young, J.W. Li, G. Pascual, A. Motiwala, H. Zhu, M. Mann, A. M. Manning, IκB kinase (IKK)-associated protein 1, a common component of the heterogeneous IKK complex. Mol. Cell. Biol. 19, 1526-1538 (1999).
12. L. A. Solt, L. A. Madge, J. S. Orange, M. J. May, Interleukin-1-induced NF-κB activation is NEMO-dependent but does not require IKKb. J. Biol. Chem. 282, 8724-8733 (2007).
13. Y. Yamamoto, U. N. Verma, S. Prajapati, Y. T. Kwak, R. B. Gaynor, Histone H3 phosphorylation by IKK-α is critical for cytokine-induced gene expression. Nature 423, 655-659 (2003).
14. V. Anest, J. L. Hanson, P. C. Cogswell, K. A. Steinbrecher, B. D. Strahl, A. S. Baldwin, A nucleosomal function for IκB kinase-α in NF-κB-dependent gene expression. Nature 423, 659-663 (2003).
15. M. Adli, E. Merkhofer, P. Cogswell, A. S. Baldwin, IKKα and IKKβ each function to regulate NF-κB activation in the TNF-induced/canonical pathway. PLOS One 5, e9428 (2010).
16. T. Lawrence, M. Bebien, G. Y. Liu, V. Nizet, M. Karin, IKKα limits macrophage NF-κB activation and contributes to the resolution of inflammation. Nature 434, 1138-1143 (2005).
17. U. Senftleben, Y. Cao, G. Xiao, F. R. Greten, G. Krähn, G. Bonizzi, Y. Chen, Y. Hu, A. Fong, S. C. Sun, M. Karin, Activation by IKKα of a second, evolutionary conserved, NF-κB signaling pathway. Science 293, 1495-1499 (2001).
18. E. Dejardin, N. M. Droin, M. Delhase, E. Haas, Y. Cao, C. Makris, Z. W. Li, M. Karin, C. F. Ware, D. R. Green, The lymphotoxin-β receptor induces different patterns of gene expression via two NF-κB pathways. Immunity 17, 525-535 (2002).
19. S. C. Sun, Non-canonical NF-κB signaling pathway. Cell Res. 21, 71-85 (2011).
20. S. C. Sun, The noncanonical NF-κB pathway. Immunol. Rev. 246, 125-140 (2012).
21. E. Derudder, E. Dejardin, L. L. Pritchard, D. R. Green, M. Korner, V. Baud, RelB/p50 dimers are differentially regulated by tumor necrosis factor-α and lymphotoxin-β receptor activation: Critical roles for p100. J. Biol. Chem. 278, 23278-23284 (2003).
22. S. C. Sun, Controlling the fate of NIK: A central stage in noncanonical NF-κB signaling. Sci. Signal. 3, pe18 (2010).
23. G. Liao, M. Zhang, E. W. Harhaj, S. C. Sun, Regulation of the NF-κB-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J. Biol. Chem. 279, 26243-26250 (2004).
24. S. Vallabhapurapu, A. Matsuzawa, W. Zhang, P. H. Tseng, J. J. Keats, H. Wang, D. A. Vignali, P. L. Bergsagel, M. Karin, Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-κB signaling. Nat. Immunol. 9, 1364-1370 (2008).
25. B. J. Zarnegar, Y. Wang, D. J. Mahoney, P. W. Dempsey, H. H. Cheung, J. He, T. Shiba, X. Yang, W. C. Yeh, T. W. Mak, R. G. Korneluk, G. Cheng, Noncanonical NF-κB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat. Immunol. 9, 1371-1378 (2008).
26. E. Varfolomeev, J. W. Blankenship, S. M. Wayson, A. V. Fedorova, N. Kayagaki, P. Garg, K. Zobel, J. N. Dynek, L. O. Elliott, H. J. Wallweber, J. A. Flygare, W. J. Fairbrother, K. Deshayes, V. M. Dixit, D. Vucic, IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell 131, 669-681 (2007).
27. B. Razani, B. Zarnegar, A. J. Ytterberg, T. Shiba, P. W. Dempsey, C. F. Ware, J. A. Loo, G. Cheng, Negative feedback in noncanonical NF-κB signaling modulates NIK stability through IKKα-mediated phosphorylation. Sci. Signal. 3, ra41 (2010).
28. J. Jin, Y. Xiao, J. H. Chang, J. Yu, H. Hu, R. Starr, G. C. Brittain, M. Chang, X. Cheng, S. C. Sun, The kinase TBK1 controls IgA class switching by negatively regulating noncanonical NF-κB signaling. Nat. Immunol. 13, 1101-1109 (2012).
29. J. S. Orange, A. Jain, Z. K. Ballas, L. C. Schneider, R. S. Geha, F. A. Bonilla, The presentation and natural history of immunodeficiency caused by nuclear factor κB essential modulator mutation. J. Allergy Clin. Immunol. 113, 725-733 (2004).
30. E. P. Hanson, L. Monaco-Shawver, L. A. Solt, L. A. Madge, P. P. Banerjee, M. J. May, J. S. Orange, Hypomorphic nuclear factor-κB essential modulator mutation database and reconstitution system identifies phenotypic and immunologic diversity. J. Allergy Clin. Immunol. 122, 1169-1177.e1116 (2008).
31. L. A. Madge, M. S. Kluger, J. S. Orange, M. J. May, Lymphotoxin-α 1β2 and LIGHT induce classical and noncanonical NF-κB-dependent proinflammatory gene expression in vascular endothelial cells. J. Immunol. 180, 3467-3477 (2008).
32. L. A. Madge, M. J. May, Classical NF-κB activation negatively regulates noncanonical NF-κB-dependent CXCL12 expression. J. Biol. Chem. 285, 38069-38077 (2010).
33. K. L. He, A. T. Ting, A20 inhibits tumor necrosis factor (TNF) alpha-induced apoptosis by disrupting recruitment of TRADD and RIP to the TNF receptor 1 complex in Jurkat T cells. Mol. Cell. Biol. 22, 6034-6045 (2002).
34. G. Xiao, E. W. Harhaj, S. C. Sun, NF-κB-inducing kinase regulates the processing of NF-κB2 p100. Mol. Cell 7, 401-409 (2001).
35. L. A. Solt, L. A. Madge, M. J. May, NEMO-binding domains of both IKKα and IKKβ regulate IκB kinase complex assembly and classical NF-κB activation. J. Biol. Chem. 284, 27596-27608 (2009).
36. J. Q. He, B. Zarnegar, G. Oganesyan, S. K. Saha, S. Yamazaki, S. E. Doyle, P. W. Dempsey, G. Cheng, Rescue of TRAF3-null mice by p100 NF-κB deficiency. J. Exp. Med. 203, 2413-2418 (2006).
37. Y. Sasaki, D. P. Calado, E. Derudder, B. Zhang, Y. Shimizu, F. Mackay, S. Nishikawa, K. Rajewsky, M. Schmidt-Supprian, NIK overexpression amplifies, whereas ablation of its TRAF3-binding domain replaces BAFF:BAFF-R-mediated survival signals in B cells. Proc. Natl. Acad. Sci. U.S.A. 105, 10883-10888 (2008).
38. Z. L. Chu, T. A. McKinsey, L. Liu, J. J. Gentry, M. H. Malim, D.W. Ballard, Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-κB control. Proc. Natl. Acad. Sci. U.S.A. 94, 10057-10062 (1997).
39. J. S. Orange, S. R. Brodeur, A. Jain, F. A. Bonilla, L. C. Schneider, R. Kretschmer, S. Nurko, W. L. Rasmussen, J. R. Köhler, S. E. Gellis, B. M. Ferguson, J. L. Strominger, J. Zonana, N. Ramesh, Z. K. Ballas, R. S. Geha, Deficient natural killer cell cytotoxicity in patients with IKK-γ/NEMO mutations. J. Clin. Invest. 109, 1501-1509 (2002).
40. J. S. Orange, R. S. Geha, Finding NEMO: Genetic disorders of NF-κB activation. J. Clin. Invest. 112, 983-985 (2003).
41. E. Claudio, K. Brown, S. Park, H. Wang, U. Siebenlist, BAFF-induced NEMO-independent processing of NF-κB2 in maturing B cells. Nat. Immunol. 3, 958-965 (2002).
42. C. Makris, J. L. Roberts, M. Karin, The carboxyl-terminal region of IκB kinase γ (IKKγ) is required for full IKK activation. Mol. Cell. Biol. 22, 6573- 6581 (2002).
43. F. Cordier, E. Vinolo, M. Véron, M. Delepierre, F. Agou, Solution structure of NEMO zinc finger and impact of an anhidrotic ectodermal dysplasia with immunodeficiencyrelated point mutation. J. Mol. Biol. 377, 1419-1432 (2008).
44. H. Hu, G. C. Brittain, J. H. Chang, N. Puebla-Osorio, J. Jin, A. Zal, Y. Xiao, X. Cheng, M. Chang, Y. X. Fu, T. Zal, C. Zhu, S. C. Sun, OTUD7B controls non-canonical NF-κB activation through deubiquitination of TRAF3. Nature 494, 371-374 (2013).
45. S. Gardam, V. M. Turner, H. Anderton, S. Limaye, A. Basten, F. Koentgen, D. L. Vaux, J. Silke, R. Brink, Deletion of cIAP1 and cIAP2 in murine B lymphocytes constitutively activates cell survival pathways and inactivates the germinal center response. Blood 117, 4041-4051 (2011).
46. W. S. Pear, J. P. Miller, L. Xu, J. C. Pui, B. Soffer, R. C. Quackenbush, A. M. Pendergast, R. Bronson, J. C. Aster, M. L. Scott, D. Baltimore, Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92, 3780-3792 (1998).