Epigenetic regulation of the expression of Il12 and Il23 and autoimmune inflammation by the deubiquitinase Trabid

Nature Immunology

Volumn 17, Issue 3, 2016, Pages 259-268

  Jin, Jin ^a,b   Xie, Xiaoping ^b   Xiao, Yichuan ^b,c   Hu, Hongbo ^b,d   Zou, Qiang ^b   Cheng, Xuhong ^b   Sun, Shao Cong ^b,e  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF TEXAS   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

^d SICHUAN UNIVERSITY   (China)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; DEUBIQUITINASE; GAMMA INTERFERON; HISTONE DEMETHYLASE; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 4; JMJD2D PROTEIN; MESSENGER RNA; TOLL LIKE RECEPTOR; TRABID PROTEIN; UNCLASSIFIED DRUG; KDM4D PROTEIN, MOUSE; RNA BINDING PROTEIN; ZINC FINGER PROTEIN; ZRANB1 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; EPIGENETICS; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENE; GENE DELETION; GENE EXPRESSION REGULATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; IL12 GENE; IL23 GENE; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN STABILITY; T LYMPHOCYTE; ZRANB1 GENE; ANIMAL; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; FLOW CYTOMETRY; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; IMMUNOBLOTTING; IMMUNOLOGY; IMMUNOPRECIPITATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EPIGENESIS, GENETIC; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTERLEUKIN-12; INTERLEUKIN-23; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MICE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; UBIQUITIN-SPECIFIC PROTEASES; ZINC FINGERS;

EID: 84955614434     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3347     Document Type: Article

References (44)

1. Iwasaki A., & Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 327, 291-295 (2010
2. Ganguly D., Haak S., Sisirak V., & Reizis B. The role of dendritic cells in autoimmunity. Nat. Rev. Immunol. 13, 566-577 (2013
3. Merad M., Sathe P., Helft J., Miller J., & Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31, 563-604 (2013
4. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3, 133-146 (2003
5. Gaffen S.L., Jain R., Garg A.V., & Cua D.J. The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat. Rev. Immunol. 14, 585-600 (2014
6. Teng M.W.L., et al. IL-12 and IL-23 cytokines: from discovery to targeted therapies for immune-mediated inflammatory diseases. Nat. Med. 21, 719-729 (2015
7. Langrish C.L., et al. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol. Rev. 202, 96-105 (2004
8. Sanjabi S., Hoffmann A., Liou H.C., Baltimore D., & Smale S.T. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc. Natl. Acad. Sci. USA 97, 12705-12710 (2000
9. 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
10. Weinmann A.S., et al. Nucleosome remodeling at the IL-12 p40 promoter is a TLR-dependent, Rel-independent event. Nat. Immunol. 2, 51-57 (2001
11. Weinmann A.S., Plevy S.E., & Smale S.T. Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription. Immunity 11, 665-675 (1999
12. Hayes M.P., Murphy F.J., & Burd P.R. Interferon-γ-dependent inducible expression of the human interleukin-12 p35 gene in monocytes initiates from a TATA-containing promoter distinct from the CpG-rich promoter active in Epstein-Barr virus-transformed lymphoblastoid cells. Blood 91, 4645-4651 (1998
13. Garrett S., Fitzgerald M., & Sullivan K. LPS and poly I: C induce chromatin modifications at a novel upstream region of the IL-23 p19 promoter. Inflammation 31, 235-246 (2008
14. Mise-Omata S., et al. Proximal κB site in the IL-23 p19 promoter is responsible for RelA-and c-Rel-dependent transcription. J. Immunol. 179, 6596-6603 (2007
15. Bannister A.J., & Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 21, 381-395 (2011
16. Zhu Y., Van Essen D., & Saccani S. Cell-type-specific control of enhancer activity by H3K9 Trimethylation. Mol. Cell 46, 408-423 (2012
17. Evans P.C., et al. Isolation and characterization of two novel A20-like proteins. Biochem. J. 357, 617-623 (2001
18. Licchesi J.D., et al. An ankyrin-repeat ubiquitin-binding domain determines TRABID's specificity for atypical ubiquitin chains. Nat. Struct. Mol. Biol. 19, 62-71 (2012
19. Virdee S., Ye Y., Nguyen D.P., Komander D., & Chin J.W. Engineered diubiquitin synthesis reveals Lys29-isopeptide specificity of an OTU deubiquitinase. Nat. Chem. Biol. 6, 750-757 (2010
20. Tran H., Hamada F., Schwarz-Romond T., & Bienz M. Trabid, a new positive regulator of Wnt-induced transcription with preference for binding and cleaving K63-linked ubiquitin chains. Genes Dev. 22, 528-542 (2008
21. Shi T., Bao J., Wang N., Zheng J., & Wu D. Identification of small molecule TRABID deubiquitinase inhibitors by computation-based virtual screen. BMC Chem. Biol. 12, 4 (2012
22. Peterson L.K., & Fujinami R.S. Inflammation, demyelination, neurodegeneration and neuroprotection in the pathogenesis of multiple sclerosis. J. Neuroimmunol. 184, 37-44 (2007
23. Zepp J., Wu L., & Li X. IL-17 receptor signaling and T helper 17-mediated autoimmune demyelinating disease. Trends Immunol. 32, 232-239 (2011
24. Lanzavecchia A., & Sallusto F. Regulation of T cell immunity by dendritic cells. Cell 106, 263-266 (2001
25. Feng G.J., et al. Extracellular signal-related kinase (ERK) and p38 mitogen-activated protein (MAP) kinases differentially regulate the lipopolysaccharide-mediated induction of inducible nitric oxide synthase and IL-12 in macrophages: Leishmania phosphoglycans subvert macrophage IL-12 production by targeting ERK MAP kinase. J. Immunol. 163, 6403-6412 (1999
26. Kim L., et al. p38 MAPK Autophosphorylation drives macrophage IL-12 production during intracellular infection. J. Immunol. 174, 4178-4184 (2005
27. Cho Y.-C., et al. Enhanced IL-12p40 production in LPS-stimulated macrophages by inhibiting JNK activation by artemisinin. Arch. Pharm. Res. 35, 1961-1968 (2012
28. Sanjabi S., et al. A c-Rel subdomain responsible for enhanced DNA-binding affinity and selective gene activation. Genes Dev. 19, 2138-2151 (2005
29. Zhang Y., & Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev. 15, 2343-2360 (2001
30. Cedar H., & Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304 (2009
31. Snowden A.W., Gregory P.D., Case C.C., & Pabo C.O. Gene-specific targeting of H3K9 methylation is sufficient for initiating repression in vivo. Curr. Biol. 12, 2159-2166 (2002
32. Kim J., et al. RAD6-mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137, 459-471 (2009
33. Cloos P.A.C., Christensen J., Agger K., & Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 22, 1115-1140 (2008
34. Kroenke M.A., Carlson T.J., Andjelkovic A.V., & Segal B.M. IL-12-and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 205, 1535-1541 (2008
35. Wen H., Dou Y., Hogaboam C.M., & Kunkel S.L. Epigenetic regulation of dendritic cell-derived interleukin-12 facilitates immunosuppression after a severe innate immune response. Blood 111, 1797-1804 (2008
36. Zhou L., et al. An inducible enhancer required for Il12b promoter activity in an insulated chromatin environment. Mol. Cell. Biol. 27, 2698-2712 (2007
37. Xu J., et al. Pioneer factor interactions and unmethylated CpG dinucleotides mark silent tissue-specific enhancers in embryonic stem cells. Proc. Natl. Acad. Sci. USA 104, 12377-12382 (2007
38. Van Essen D., Zhu Y., & Saccani S. A feed-forward circuit controlling inducible NF-κB target gene activation by promoter histone demethylation. Mol. Cell 39, 750-760 (2010
39. Fischle W., Wang Y., & Allis C.D. Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 15, 172-183 (2003
40. Fernando M.D.A., Kounatidis I., & Ligoxygakis P. Loss of Trabid, a new negative regulator of the Drosophila immune-deficiency pathway at the level of TAK1, reduces life span. PLoS Genet. 10, e1004117 (2014
41. Mihaly S.R., Ninomiya-Tsuji J., & Morioka S. TAK1 control of cell death. Cell Death Differ. 21, 1667-1676 (2014
42. Reiley W., Zhang M., Wu X., Graner E., & Sun S.-C. Regulation of the deubiquitinating enzyme CYLD by IκB kinase γ-dependent phosphorylation. Mol. Cell. Biol. 25, 3886-3895 (2005
43. 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
44. Nelson J.D., Denisenko O., & Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 1, 179-185 (2006