The signaling adaptor TRAF1 negatively regulates Toll-like receptor signaling and this underlies its role in rheumatic disease

Nature Immunology

Volumn 18, Issue 1, 2017, Pages 26-35

  Abdul Sater, Ali A ^a,c   Edilova, Maria I ^a   Clouthier, Derek L ^a   Mbanwi, Achire ^a   Kremmer, Elisabeth ^a   Watts, Tania H ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b Inst F Klin Molekularbiologie/T   (Germany)

^c York University   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; CYTOKINE; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; PROTEIN; SHANK ASSOCIATED RH DOMAIN INTERACTOR; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE 1; UBIQUITIN PROTEIN LIGASE 1 INTERACTING PROTEIN; UNCLASSIFIED DRUG; AUTACOID; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; GENE; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SEPTIC SHOCK; SIGNAL TRANSDUCTION; TRAF1 GENE; UBIQUITINATION; ANIMAL; C57BL MOUSE; GENETIC PREDISPOSITION; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MONONUCLEAR CELL; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; ARTHRITIS, RHEUMATOID; CYTOKINES; GENETIC PREDISPOSITION TO DISEASE; HEK293 CELLS; HUMANS; INFLAMMATION MEDIATORS; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 1; TOLL-LIKE RECEPTORS;

EID: 84997766110     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3618     Document Type: Article

References (49)

1. Rothe, M., Wong, S. C., Henzel, W. J. & Goeddel, D. V. A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell 78, 681-692 (1994).
2. Wang, C. Y., Mayo, M. W., Korneluk, R. G., Goeddel, D. V. & Baldwin, A. S. Jr. NF-?B antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281, 1680-1683 (1998).
3. Carpentier, I. & Beyaert, R. TRAF1 is a TNF inducible regulator of NF-?B activation. FEBS Lett. 460, 246-250 (1999).
4. Tsitsikov, E. N. et al. TRAF1 is a negative regulator of TNF signaling. enhanced TNF signaling in TRAF1-deficient mice. Immunity 15, 647-657 (2001).
5. McPherson, A. J., Snell, L. M., Mak, T. W. & Watts, T. H. Opposing roles for TRAF1 in the alternative versus classical NF-?B pathway in T cells. J. Biol. Chem. 287, 23010-23019 (2012).
6. Wicovsky, A. et al. Tumor necrosis factor receptor-associated factor-1 enhances proinflammatory TNF receptor-2 signaling and modifies TNFR1-TNFR2 cooperation. Oncogene 28, 1769-1781 (2009).
7. Xie, P., Hostager, B. S., Munroe, M. E., Moore, C. R. & Bishop, G. A. Cooperation between TNF receptor-associated factors 1 and 2 in CD40 signaling. J. Immunol. 176, 5388-5400 (2006).
8. Arron, J. R., Pewzner-Jung, Y., Walsh, M. C., Kobayashi, T. & Choi, Y. Regulation of the subcellular localization of tumor necrosis factor receptor-associated factor (TRAF)2 by TRAF1 reveals mechanisms of TRAF2 signaling. J. Exp. Med. 196, 923-934 (2002).
9. Sabbagh, L., Pulle, G., Liu, Y., Tsitsikov, E. N. & Watts, T. H. ERK-dependent Bim modulation downstream of the 4-1BB-TRAF1 signaling axis is a critical mediator of CD8 T cell survival in vivo. J. Immunol. 180, 8093-8101 (2008).
10. Sabbagh, L. et al. A critical role for TNF receptor-associated factor 1 and Bim down-regulation in CD8 memory T cell survival. Proc. Natl. Acad. Sci. USA 103, 18703-18708 (2006).
11. Speiser, D. E. et al. A regulatory role for TRAF1 in antigen-induced apoptosis of T cells. J. Exp. Med. 185, 1777-1783 (1997).
12. Lee, S. Y. & Choi, Y. TRAF1 and its biological functions. Adv. Exp. Med. Biol. 597, 25-31 (2007).
13. Zheng, C., Kabaleeswaran, V., Wang, Y., Cheng, G. & Wu, H. Crystal structures of the TRAF2: cIAP2 and the TRAF1: TRAF2: cIAP2 complexes: affinity, specificity, and regulation. Mol. Cell 38, 101-113 (2010).
14. Vallabhapurapu, S. & Karin, M. Regulation and function of NF-?B transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733 (2009).
15. Gerlach, B. et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471, 591-596 (2011).
16. Ikeda, F. et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-?B activity and apoptosis. Nature 471, 637-641 (2011).
17. Tokunaga, F. et al. SHARPIN is a component of the NF-?B-activating linear ubiquitin chain assembly complex. Nature 471, 633-636 (2011).
18. Damgaard, R. B. et al. The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol. Cell 46, 746-758 (2012).
19. Warner, N. et al. A genome-wide siRNA screen reveals positive and negative regulators of the NOD2 and NF-?B signaling pathways. Sci. Signal. 6, rs3 (2013).
20. Kirisako, T. et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25, 4877-4887 (2006).
21. Chang, M. et al. A large-scale rheumatoid arthritis genetic study identifies association at chromosome 9q33. 2. PLoS Genet. 4, e1000107 (2008).
22. Plenge, R. M. et al. TRAF1-C5 as a risk locus for rheumatoid arthritis-a genomewide study. N. Engl. J. Med. 357, 1199-1209 (2007).
23. Kurreeman, F. A. et al. A candidate gene approach identifies the TRAF1/C5 region as a risk factor for rheumatoid arthritis. PLoS Med. 4, e278 (2007).
24. Panoulas, V. F., Smith, J. P., Nightingale, P. & Kitas, G. D. Association of the TRAF1/C5 locus with increased mortality, particularly from malignancy or sepsis, in patients with rheumatoid arthritis. Arthritis Rheum. 60, 39-46 (2009).
25. Nishimoto, K. et al. Association study of TRAF1-C5 polymorphisms with susceptibility to rheumatoid arthritis and systemic lupus erythematosus in Japanese. Ann. Rheum. Dis. 69, 368-373 (2010).
26. Song, G. G., Bae, S. C., Kim, J. H. & Lee, Y. H. Associations between TRAF1-C5 gene polymorphisms and rheumatoid arthritis: a meta-analysis. Immunol. Invest. 43, 97-112 (2014).
27. McInnes, I. B. & O'Dell, J. R. State-of-the-art: rheumatoid arthritis. Ann. Rheum. Dis. 69, 1898-1906 (2010).
28. McInnes, I. B. & Schett, G. The pathogenesis of rheumatoid arthritis. N. Engl. J. Med. 365, 2205-2219 (2011).
29. Davignon, J. L. et al. Targeting monocytes/macrophages in the treatment of rheumatoid arthritis. Rheumatology (Oxford) 52, 590-598 (2013).
30. Li, S., Wang, L., Berman, M., Kong, Y. Y. & Dorf, M. E. Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 35, 426-440 (2011).
31. Fujita, H. et al. Mechanism underlying I?B kinase activation mediated by the linear ubiquitin chain assembly complex. Mol. Cell. Biol. 34, 1322-1335 (2014).
32. Rieser, E., Cordier, S. M. & Walczak, H. Linear ubiquitination: a newly discovered regulator of cell signalling. Trends Biochem. Sci. 38, 94-102 (2013).
33. Keusekotten, K. et al. OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 153, 1312-1326 (2013).
34. Rothe, M., Sarma, V., Dixit, V. M. & Goeddel, D. V. TRAF2-mediated activation of NF-kappa B by TNF receptor 2 and CD40. Science 269, 1424-1427 (1995).
35. Sakamoto, H. et al. Gliotoxin suppresses NF-?B activation by selectively inhibiting linear ubiquitin chain assembly complex (LUBAC). ACS Chem. Biol. 10, 675-681 (2015).
36. Aderem, A. & Ulevitch, R. J. Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787 (2000).
37. Masters, S. L., Simon, A., Aksentijevich, I. & Kastner, D. L. Horror autoinflammaticus: the molecular pathophysiology of autoinflammatory disease (). Annu. Rev. Immunol. 27, 621-668 (2009).
38. Kondo, T., Kawai, T. & Akira, S. Dissecting negative regulation of Toll-like receptor signaling. Trends Immunol. 33, 449-458 (2012).
39. Ma, A. & Malynn, B. A. A20: linking a complex regulator of ubiquitylation to immunity and human disease. Nat. Rev. Immunol. 12, 774-785 (2012).
40. Feldmann, M. & Maini, R. N. Anti-TNF alpha therapy of rheumatoid arthritis: what have we learned? Annu. Rev. Immunol. 19, 163-196 (2001).
41. Abdul-Sater, A. A. et al. Cyclic-di-GMP and cyclic-di-AMP activate the NLRP3 inflammasome. EMBO Rep. 14, 900-906 (2013).
42. Siegler, G., Kremmer, E., Gonnella, R. & Niedobitek, G. Epstein-Barr virus encoded latent membrane protein 1 (LMP1) and TNF receptor associated factors (TRAF): colocalisation of LMP1 and TRAF1 in primary EBV infection and in EBV associated Hodgkin lymphoma. Mol. Pathol. 56, 156-161 (2003).
43. Newton, K. et al. Using linkage-specific monoclonal antibodies to analyze cellular ubiquitylation. Methods Mol. Biol. 832, 185-196 (2012).
44. Newton, K. et al. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134, 668-678 (2008).
45. Matsumoto, M. L. et al. Engineering and structural characterization of a linear polyubiquitin-specific antibody. J. Mol. Biol. 418, 134-144 (2012).
46. Wertz, I. E. et al. Phosphorylation and linear ubiquitin direct A20 inhibition of inflammation. Nature 528, 370-375 (2015).
47. Sanjabi, S. et al. A c-Rel subdomain responsible for enhanced DNA-binding affinity and selective gene activation. Genes Dev. 19, 2138-2151 (2005).
48. Fu, B., Li, S., Wang, L., Berman, M. A. & Dorf, M. E. The ubiquitin conjugating enzyme UBE2L3 regulates TNF?-induced linear ubiquitination. Cell Res. 24, 376-379 (2014).
49. Smit, J. J. et al. The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J. 31, 3833-3844 (2012).