The ubiquitin ligase Peli1 negatively regulates T cell activation and prevents autoimmunity

Nature Immunology

Volumn 12, Issue 10, 2011, Pages 1002-1009

  Chang, Mikyoung ^a   Jin, Wei ^a,c   Chang, Jae Hoon ^a   Xiao, Yichuan ^a   Brittain, George C ^a   Yu, Jiayi ^a   Zhou, Xiaofei ^a   Wang, Yi Hong ^a   Cheng, Xuhong ^a   Li, Pingwei ^b   Rabinovich, Brian A ^a   Hwu, Patrick ^a   Sun, Shao Cong ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR REL; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; AUTOIMMUNITY; MOUSE; MULTIPLE ORGAN FAILURE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD28; AUTOIMMUNITY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NF-KAPPA B; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS C-REL; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; UBIQUITINATION;

EID: 80052971340     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2090     Document Type: Article

References (50)

1. Smith-Garvin, J.E., Koretzky, G.A. & Jordan, M.S. T cell activation. Annu. Rev. Immunol. 27, 591-619 (2009).
2. Goodnow, C.C., Sprent, J., Fazekas de St Groth, B. & Vinuesa, C.G. Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 435, 590-597 (2005). (Pubitemid 40825498)
3. Tzachanis, D., Lafuente, E.M., Li, L. & Boussiotis, V.A. Intrinsic and extrinsic regulation of T lymphocyte quiescence. Leuk. Lymphoma 45, 1959-1967 (2004). (Pubitemid 39232844)
4. von Boehmer, H. Mechanisms of suppression by suppressor T cells. Nat. Immunol. 6, 338-344 (2005). (Pubitemid 41716770)
5. Sojka, D.K., Huang, Y.H. & Fowell, D.J. Mechanisms of regulatory T-cell suppression-a diverse arsenal for a moving target. Immunology 124, 13-22 (2008). (Pubitemid 351537583)
6. Lu, L.F. & Rudensky, A. Molecular orchestration of differentiation and function of regulatory T cells. Genes Dev. 23, 1270-1282 (2009).
7. Wan, Y.Y. Regulatory T cells: immune suppression and beyond. Cell Mol. Immunol. 7, 204-210 (2010).
8. Wells, A.D. New insights into the molecular basis of T cell anergy: anergy factors, avoidance sensors, and epigenetic imprinting. J. Immunol. 182, 7331-7341 (2009).
9. Liu, Y.C. Ubiquitin ligases and the immune response. Annu. Rev. Immunol. 22, 81-127 (2004).
10. Hayden, M.S. & Ghosh, S. Shared principles in NF-κB signaling. Cell 132, 344-362 (2008).
11. Vallabhapurapu, S. & Karin, M. Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733 (2009).
12. Köntgen, F. et al. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoural immunity, and interleukin-2 expression. Genes Dev. 9, 1965-1977 (1995).
13. Liou, H.C. et al. c-Rel is crucial for lymphocyte proliferation but dispensable for T cell effector function. Int. Immunol. 11, 361-371 (1999).
14. Hilliard, B.A. et al. Critical roles of c-Rel in autoimmune inflammation and helper T cell differentiation. J. Clin. Invest. 110, 843-850 (2002).
15. Mason, N.J., Liou, H.C. & Hunter, C.A. T cell-intrinsic expression of c-Rel regulates Th1 cell responses essential for resistance to Toxoplasma gondii. J. Immunol. 172, 3704-3711 (2004). (Pubitemid 38337954)
16. Banerjee, D., Liou, H.C. & Sen, R. c-Rel-dependent priming of naive T cells by inflammatory cytokines. Immunity 23, 445-458 (2005). (Pubitemid 41443445)
17. Chen, G. et al. Regulation of the IL-21 gene by the NF-κB transcription factor c-Rel. J. Immunol. 185, 2350-2359 (2010).
18. Deenick, E.K. et al. c-Rel phenocopies PKC but not Bcl-10 in regulating CD8+ T-cell activation versus tolerance. Eur. J. Immunol. 40, 867-877 (2010).
19. Maggirwar, S.B., Harhaj, E.W. & Sun, S.-C. Regulation of the interleukin-2 CD28 responsive element by NF-ATp and various NF-κB/Rel transcription factors. Mol. Cell Biol. 17, 2605-2614 (1997). (Pubitemid 27175142)
20. Zhou, X.Y. et al. Molecular mechanisms underlying differential contribution of CD28 versus non-CD28 costimulatory molecules to IL-2 promoter activation. J. Immunol. 168, 3847-3854 (2002).
21. Sen, R. & Smale, S.T. Selectivity of the NF-κB response. Cold Spring Harb. Perspect. Biol. 2, a000257 (2009).
22. Bhoj, V.G. & Chen, Z.J. Ubiquitylation in innate and adaptive immunity. Nature 458, 430-437 (2009).
23. Loeser, S. & Penninger, J.M. Regulation of peripheral T cell tolerance by the E3 ubiquitin ligase Cbl-b. Semin. Immunol. 19, 206-214 (2007). (Pubitemid 46810290)
24. Huang, F. & Gu, H. Negative regulation of lymphocyte development and function by the Cbl family of proteins. Immunol. Rev. 224, 229-238 (2008).
25. Butler, M.P., Hanly, J.A. & Moynagh, P.N. Kinase-active interleukin-1 receptorassociated kinases promote polyubiquitination and degradation of the Pellino family: direct evidence for PELLINO proteins being ubiquitin-protein isopeptide ligases. J. Biol. Chem. 282, 29729-29737 (2007). (Pubitemid 350035285)
26. Ordureau, A. et al. The IRAK-catalysed activation of the E3 ligase function of Pellino isoforms induces the Lys63-linked polyubiquitination of IRAK1. Biochem. J. 409, 43-52 (2008).
27. Schauvliege, R., Janssens, S. & Beyaert, R. Pellino proteins are more than scaffold proteins in TLR/IL-1R signalling: a role as novel RING E3-ubiquitin-ligases. FEBS Lett. 580, 4697-4702 (2006). (Pubitemid 44189391)
28. Schauvliege, R., Janssens, S. & Beyaert, R. Pellino proteins: novel players in TLR and IL-1R signalling. J. Cell Mol. Med. 11, 453-461 (2007). (Pubitemid 47153457)
29. Moynagh, P.N. The Pellino family: IRAK E3 ligases with emerging roles in innate immune signalling. Trends Immunol. 30, 33-42 (2009).
30. Chang, M., Jin, W. & Sun, S.C. Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nat. Immunol. 10, 1089-1095 (2009).
31. Li, M.O., Wan, Y.Y., Sanjabi, S., Robertson, A.K. & Flavell, R.A. Transforming growth factor-regulation of immune responses. Annu. Rev. Immunol. 24, 99-146 (2006).
32. Rubtsov, Y.P. & Rudensky, A.Y. TGFΒ signalling in control of T-cell-mediated selfreactivity. Nat. Rev. Immunol. 7, 443-453 (2007). (Pubitemid 46834850)
33. Appleman, L.J. & Boussiotis, V.A. T cell anergy and costimulation. Immunol. Rev. 192, 161-180 (2003). (Pubitemid 36613331)
34. Wohlfert, E.A., Callahan, M.K. & Clark, R.B. Resistance to CD4+CD25+ regulatory T cells and TGF-Βin Cbl-b-/-mice. J. Immunol. 173, 1059-1065 (2004).
35. King, C.G. et al. TRAF6 is a T cell-intrinsic negative regulator required for the maintenance of immune homeostasis. Nat. Immunol. 12, 1088-1092 (2006). (Pubitemid 44353391)
36. Liou, H.C. & Smith, K.A. The roles of c-rel and interleukin-2 in tolerance: a molecular explanation of self-nonself discrimination. Immunol. Cell Biol. 89, 27-32 (2011).
37. Chen, E. et al. Degradation of proto-oncoprotein c-Rel by the ubiquitin-proteasome pathway. J. Biol. Chem. 273, 35201-35207 (1998). (Pubitemid 29028225)
38. Lim, K.L. et al. Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J. Neurosci. 25, 2002-2009 (2005).
39. Kumar, K.G. et al. Site-specific ubiquitination exposes a linear motif to promote interferon-receptor endocytosis. J. Cell Biol. 179, 935-950 (2007). (Pubitemid 350223490)
40. Varfolomeev, E. et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell 131, 669-681 (2007). (Pubitemid 350087204)
41. Bertrand, M.J. et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700 (2008). (Pubitemid 351818251)
42. Bryan, R.G. et al. Effect of CD28 signal transduction on c-Rel in human peripheral blood T cells. Mol. Cell Biol. 14, 7933-7942 (1994). (Pubitemid 24373542)
43. Shapiro, V.S., Truitt, K.E., Imboden, J.B. & Weiss, A. CD28 mediates transcriptional upregulation of the interleukin-2 (IL-2) promoter through a composite element containing the CD28RE and NF-IL-2B AP-1 sites. Mol. Cell Biol. 17, 4051-4058 (1997). (Pubitemid 27281881)
44. Chang, M., Lee, A.J., Fitzpatrick, L., Zhang, M. & Sun, S.C. NF-κB1 p105 regulates T cell homeostasis and prevents chronic inflammation. J. Immunol. 182, 3131-3138 (2009).
45. Lee, Y.S. et al. Smad7 and Smad6 bind to discrete regions of Pellino-1 via their MH2 domains to mediate TGF-Β1-induced negative regulation of IL-1R/TLR signaling. Biochem. Biophys. Res. Commun. 393, 836-843 (2010).
46. Xiao, G., Harhaj, E.W. & Sun, S.C. NF-κB-inducing kinase regulates the processing of NF-κB2 p100. Mol. Cell 7, 401-409 (2001). (Pubitemid 32206507)
47. Jin, W., Zhou, X.F., Yu, J., Cheng, X. & Sun, S.C. Regulation of Th17 cell differentiation and EAE induction by the MAP3K NIK. Blood 113, 6603-6610 (2009).
48. Reiley, W.W. et al. Deubiquitinating enzyme CYLD negatively regulates the ubiquitindependent kinase Tak1 and prevents abnormal T cell responses. J. Exp. Med. 204, 1475-1485 (2007). (Pubitemid 46919884)
49. Uhlik, M. et al. NF-κB-inducing kinase and I-B kinase participate in human T-cell leukemia virus I Tax-mediated NF-κB activation. J. Biol. Chem. 273, 21132-21136 (1998). (Pubitemid 28385401)
50. Reiley, W.W. et al. Regulation of T cell development by the deubiquitinating enzyme CYLD. Nat. Immunol. 7, 411-417 (2006).