The deubiquitinase A20 mediates feedback inhibition of interleukin-17 receptor signaling

Science Signaling

Volumn 6, Issue 278, 2013, Pages

  Garg, Abhishek V ^a   Ahmed, Mushtaq ^a   Vallejo, Abbe N ^b   Ma, Averil ^c   Gaffen, Sarah L ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE A20; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; FEEDBACK SYSTEM; FIBROBLAST; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; ZINC FINGER MOTIF;

HUMANS; NF-KAPPA B; PROMOTER REGIONS, GENETIC; RECEPTORS, INTERLEUKIN-17; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; UBIQUITIN-SPECIFIC PROTEASES;

EID: 84878912610     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003699     Document Type: Article

References (88)

1. I. B. McInnes, G. Schett, Cytokines in the pathogenesis of rheumatoid arthritis. Nat. Rev. Immunol. 7, 429-442 (2007).
2. M. C. Genovese, F. Van den Bosch, S. A. Roberson, S. Bojin, I. M. Biagini, P. Ryan, J. Sloan-Lancaster, LY2439821, a humanized anti-interleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: A phase I randomized, double-blind, placebo-controlled, proof-of-concept study. Arthritis Rheum. 62, 929-939 (2010).
3. K. A. Papp, C. Leonardi, A. Menter, J. P. Ortonne, J. G. Krueger, G. Kricorian, G. Aras, J. Li, C. B. Russell, E. H. Thompson, S. Baumgartner, Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N. Engl. J. Med. 366, 1181-1189 (2012).
4. W. Hueber, D. D. Patel, T. Dryja, A. M. Wright, I. Koroleva, G. Bruin, C. Antoni, Z. Draelos, M. H. Gold, Psoriasis Study Group, P. Durez, P. P. Tak, J. J. Gomez-Reino, Rheumatoid Arthritis Study Group, C. S. Foster, R. Y. Kim, C. M. Samson, N. S. Falk, D. S. Chu, D. Callanan, Q. D. Nguyen, Uveitis Study Group, K. Rose, A. Haider, F. Di Padova, Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci. Transl. Med. 2, 52ra72 (2010).
5. C. Leonardi, R. Matheson, C. Zachariae, G. Cameron, L. Li, E. Edson-Heredia, D. Braun, S. Banerjee, Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N. Engl. J. Med. 366, 1190-1199 (2012).
6. T. Korn, E. Bettelli, M. Oukka, V. K. Kuchroo, IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517 (2009).
7. J. M. Reynolds, P. Angkasekwinai, C. Dong, IL-17 family member cytokines: Regulation and function in innate immunity. Cytokine Growth Factor Rev. 21, 413-423 (2010).
8. D. J. Cua, C. M. Tato, Innate IL-17-producing cells: The sentinels of the immune system. Nat. Rev. Immunol. 10, 479-489 (2010).
9. S. L. Gaffen, Recent advances in the IL-17 cytokine family. Curr. Opin. Immunol. 23, 613-619 (2011).
10. R. M. Onishi, S. L. Gaffen, IL-17 and its target genes: Mechanisms of IL-17 function in disease. Immunology 129, 311-321 (2010).
11. A. R. Huppler, S. Bishu, S. L. Gaffen, Mucocutaneous candidiasis: The IL-17 pathway and implications for targeted immunotherapy. Arthritis Res. Ther. 14, 217 (2012).
12. A. Puel, C. Picard, S. Cypowyj, D. Lilic, L. Abel, J. L. Casanova, Inborn errors of mucocutaneous immunity to Candida albicans in humans: A role for IL-17 cytokines? Curr. Opin. Immunol. 22, 467-474 (2010).
13. L. A. Zenewicz, C. Abraham, R. A. Flavell, J. H. Cho, Unraveling the genetics of autoimmunity. Cell 140, 791-797 (2010).
14. R. H. Duerr, K. D. Taylor, S. R. Brant, J. D. Rioux, M. S. Silverberg, M. J. Daly, A. H. Steinhart, C. Abraham, M. Regueiro, A. Griffiths, T. Dassopoulos, A. Bitton, H. Yang, S. Targan, L. W. Datta, E. O. Kistner, L. P. Schumm, A. T. Lee, P. K. Gregersen, M. M. Barmada, J. I. Rotter, D. L. Nicolae, J. H. Cho, A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314, 1461-1463 (2006).
15. S. L. Gaffen, Structure and signalling in the IL-17 receptor family. Nat. Rev. Immunol. 9, 556-567 (2009).
16. M. Novatchkova, A. Leibbrandt, J. Werzowa, A. Neubüser, F. Eisenhaber, The STIRdomain superfamily in signal transduction, development and immunity. Trends Biochem. Sci. 28, 226-229 (2003).
17. C. Liu, W. Qian, Y. Qian, N. V. Giltiay, Y. Lu, S. Swaidani, S. Misra, L. Deng, Z. J. Chen, X. Li, Act1, a U-box E3 ubiquitin ligase for IL-17 signaling. Sci. Signal. 2, ra63 (2009).
18. S. H. Chang, H. Park, C. Dong, Act1 adaptor protein is an immediate and essential signaling component of interleukin-17 receptor. J. Biol. Chem. 281, 35603-35607 (2006).
19. Y. Qian, C. Liu, J. Hartupee, C. Z. Altuntas, M. F. Gulen, D. Jane-Wit, J. Xiao, Y. Lu, N. Giltiay, J. Liu, T. Kordula, Q. W. Zhang, B. Vallance, S. Swaidani, M. Aronica, V. K. Tuohy, T. Hamilton, X. Li, The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat. Immunol. 8, 247-256 (2007).
20. A. Leonardi, A. Chariot, E. Claudio, K. Cunningham, U. Siebenlist, CIKS, a connection to IκB kinase and stress-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 97, 10494-10499 (2000).
21. J. Zepp, L. Wu, X. Li, IL-17 receptor signaling and T helper 17-mediated autoimmune demyelinating disease. Trends Immunol. 32, 232-239 (2011).
22. Y. Iwakura, H. Ishigame, S. Saijo, S. Nakae, Functional specialization of interleukin-17 family members. Immunity 34, 149-162 (2011).
23. A. Maitra, F. Shen, W. Hanel, K. Mossman, J. Tocker, D. Swart, S. L. Gaffen, Distinct functional motifs within the IL-17 receptor regulate signal transduction and target gene expression. Proc. Natl. Acad. Sci. U.S.A. 104, 7506-7511 (2007).
24. R. M. Onishi, S. J. Park, W. Hanel, A. W. Ho, A. Maitra, S. L. Gaffen, SEF/IL-17R (SEFIR) is not enough: An extended SEFIR domain is required for IL-17RA-mediated signal transduction. J. Biol. Chem. 285, 32751-32759 (2010).
25. F. Shen, N. Li, P. Gade, D. V. Kalvakolanu, T. Weibley, B. Doble, J. R. Woodgett, T. D. Wood, S. L. Gaffen, IL-17 receptor signaling inhibits C/EBPb by sequential phosphorylation of the regulatory 2 domain. Sci. Signal. 2, ra8 (2009).
26. S. Zhu, W. Pan, P. Shi, H. Gao, F. Zhao, X. Song, Y. Liu, L. Zhao, X. Li, Y. Shi, Y. Qian, Modulation of experimental autoimmune encephalomyelitis through TRAF3-mediated suppression of interleukin 17 receptor signaling. J. Exp. Med. 207, 2647-2662 (2010).
27. X. Jiang, Z. J. Chen, The role of ubiquitylation in immune defence and pathogen evasion. Nat. Rev. Immunol. 12, 35-48 (2012).
28. B. A. Malynn, A. Ma, Ubiquitin makes its mark on immune regulation. Immunity 33, 843-852 (2010).
29. X. Li, Act1 modulates autoimmunity through its dual functions in CD40L/BAFF and IL-17 signaling. Cytokine 41, 105-113 (2008).
30. A. Lindén, A role for the cytoplasmic adaptor proteins Act1 in mediating IL-17 signaling. Sci. STKE 2007, re4 (2007).
31. R. Schwandner, K. Yamaguchi, Z. Cao, Requirement of tumor necrosis factor-associated factor (TRAF)6 in interleukin 17 signal transduction. J. Exp. Med. 191, 1233-1240 (2000).
32. N. Shembade, A. Ma, E. W. Harhaj, Inhibition of NF-κB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 327, 1135-1139 (2010).
33. J. Ruland, Return to homeostasis: Downregulation of NF-κB responses. Nat. Immunol. 12, 709-714 (2011).
34. S. C. Sun, Deubiquitylation and regulation of the immune response. Nat. Rev. Immunol. 8, 501-511 (2008).
35. N. Shembade, E. W. Harhaj, Regulation of NF-κB signaling by the A20 deubiquitinase. Cell. Mol. Immunol. 9, 123-130 (2012).
36. L. Verstrepen, K. Verhelst, G. van Loo, I. Carpentier, S. C. Ley, R. Beyaert, Expression, biological activities and mechanisms of action of A20 (TNFAIP3). Biochem. Pharmacol. 80, 2009-2020 (2010).
37. D. L. Boone, E. E. Turer, E. G. Lee, R. C. Ahmad, M. T. Wheeler, C. Tsui, P. Hurley, M. Chien, S. Chai, O. Hitotsumatsu, E. McNally, C. Pickart, A. Ma, The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5, 1052-1060 (2004).
38. O. Hitotsumatsu, R. C. Ahmad, R. Tavares, M. Wang, D. Philpott, E. E. Turer, B. L. Lee, N. Shiffin, R. Advincula, B. A. Malynn, C. Werts, A. Ma, The ubiquitin-editing enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 28, 381-390 (2008).
39. E. G. Lee, D. L. Boone, S. Chai, S. L. Libby, M. Chien, J. P. Lodolce, A. Ma, Failure to regulate TNF-induced NF-κB and cell death responses in A20-deficient mice. Science 289, 2350-2354 (2000).
40. J. Maelfait, K. Roose, P. Bogaert, M. Sze, X. Saelens, M. Pasparakis, I. Carpentier, G. van Loo, R. Beyaert, A20 (Tnfaip3) deficiency in myeloid cells protects against influenza A virus infection. PLoS Pathog. 8, e1002570 (2012).
41. M. Matmati, P. Jacques, J. Maelfait, E. Verheugen, M. Kool, M. Sze, L. Geboes, E. Louagie, C. Mc Guire, L. Vereecke, Y. Chu, L. Boon, S. Staelens, P. Matthys, B. N. Lambrecht, M. Schmidt-Supprian, M. Pasparakis, D. Elewaut, R. Beyaert, G. van Loo, A20 (TNFAIP3) deficiency in myeloid cells triggers erosive polyarthritis resembling rheumatoid arthritis. Nat. Genet. 43, 908-912 (2011).
42. G. E. Hammer, E. E. Turer, K. E. Taylor, C. J. Fang, R. Advincula, S. Oshima, J. Barrera, E. J. Huang, B. Hou, B. A. Malynn, B. Reizis, A. DeFranco, L. A. Criswell, M. C. Nakamura, A. Ma, Expression of A20 by dendritic cells preserves immune homeostasis and prevents colitis and spondyloarthritis. Nat. Immunol. 12, 1184-1193 (2011).
43. S. L. Musone, K. E. Taylor, T. T. Lu, J. Nititham, R. C. Ferreira, W. Ortmann, N. Shifrin, M. A. Petri, M. I. Kamboh, S. Manzi, M. F. Seldin, P. K. Gregersen, T. W. Behrens, A. Ma, P. Y. Kwok, L. A. Criswell, Multiple polymorphisms in the TNFAIP3 region are independently associated with systemic lupus erythematosus. Nat. Genet. 40, 1062-1064 (2008).
44. A. Krikos, C. D. Laherty, V. M. Dixit, Transcriptional activation of the tumor necrosis factor α-inducible zinc finger protein, A20, is mediated by κB elements. J. Biol. Chem. 267, 17971-17976 (1992).
45. P. Miossec, Interleukin-17 in rheumatoid arthritis: If T cells were to contribute to inflammation and destruction through synergy. Arthritis Rheum. 48, 594-601 (2003).
46. M. J. Ruddy, G. C. Wong, X. K. Liu, H. Yamamoto, S. Kasayama, K. L. Kirkwood, S. L. Gaffen, Functional cooperation between interleukin-17 and tumor necrosis factor-α is mediated by CCAAT/enhancer binding protein family members. J. Biol. Chem. 279, 2559-2567 (2004).
47. S. U. Sønder, S. Saret, W. Tang, D. E. Sturdevant, S. F. Porcella, U. Siebenlist, IL-17-induced NF-κB activation via CIKS/Act1: Physiologic significance and signaling mechanisms. J. Biol. Chem. 286, 12881-12890 (2011).
48. F. Shen, M. J. Ruddy, P. Plamondon, S. L. Gaffen, Cytokines link osteoblasts and inflammation: Microarray analysis of interleukin-17- and TNF-α-induced genes in bone cells. J. Leukoc. Biol. 77, 388-399 (2005).
49. S. L. Gaffen, The role of interleukin-17 in the pathogenesis of rheumatoid arthritis. Curr. Rheumatol. Rep. 11, 365-370 (2009).
50. F. Shen, Z. Hu, J. Goswami, S. L. Gaffen, Identification of common transcriptional regulatory elements in interleukin-17 target genes. J. Biol. Chem. 281, 24138-24148 (2006).
51. H. Y. Song, M. Rothe, D. V. Goeddel, The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-κB activation. Proc. Natl. Acad. Sci. U.S.A. 93, 6721-6725 (1996).
52. K. Heyninck, R. Beyaert, The cytokine-inducible zinc finger protein A20 inhibits IL-1-induced NF-κB activation at the level of TRAF6. FEBS Lett. 442, 147-150 (1999).
53. B. Zhong, X. Liu, X. Wang, S. H. Chang, X. Liu, A. Wang, J. M. Reynolds, C. Dong, Negative regulation of IL-17-mediated signalling and inflammation by the ubiquitin-specific protease USP25. Nat. Immunol. 13, 1110-1117 (2012).
54. Z. Yao, W. C. Fanslow, M. F. Seldin, A. M. Rousseau, S. L. Painter, M. R. Comeau, J. I. Cohen, M. K. Spriggs, Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3, 811-821 (1995).
55. I. E.Wertz, K. M. O'Rourke, H. Zhou, M. Eby, L. Aravind, S. Seshagiri, P.Wu, C. Wiesmann, R. Baker, D. L. Boone, A. Ma, E. V. Koonin, V. M. Dixit, De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling. Nature 430, 694-699 (2004).
56. A. Ma, B. A. Malynn, A20: Linking a complex regulator of ubiquitylation to immunity and human disease. Nat. Rev. Immunol. 12, 774-785 (2012).
57. K. Verhelst, I. Carpentier, M. Kreike, L. Meloni, L. Verstrepen, T. Kensche, I. Dikic, R. Beyaert, A20 inhibits LUBAC-mediated NF-κB activation by binding linear polyubiquitin chains via its zinc finger 7. EMBO J. 31, 3845-3855 (2012).
58. F. Tokunaga, H. Nishimasu, R. Ishitani, E. Goto, T. Noguchi, K. Mio, K. Kamei, A. Ma, K. Iwai, O. Nureki, Specific recognition of linear polyubiquitin by A20 zinc finger 7 is involved in NF-κB regulation. EMBO J. 31, 3856-3870 (2012).
59. I. Bosanac, I. E. Wertz, B. Pan, C. Yu, S. Kusam, C. Lam, L. Phu, Q. Phung, B. Maurer, D. Arnott, D. S. Kirkpatrick, V. M. Dixit, S. G. Hymowitz, Ubiquitin binding to A20 ZnF4 is required for modulation of NF-κB signaling. Mol. Cell 40, 548-557 (2010).
60. M. Klinkenberg, S. Van Huffel, K. Heyninck, R. Beyaert, Functional redundancy of the zinc fingers of A20 for inhibition of NF-κB activation and protein-protein interactions. FEBS Lett. 498, 93-97 (2001).
61. A. W. Ho, F. Shen, H. R. Conti, N. Patel, E. E. Childs, A. Peterson, N. Hernández-Santos, J. K. Kolls, L. P. Kane, W. Ouyang, S. L. Gaffen, IL-17RC is required for immune signaling via an extended SEFIR domain in the cytoplasmic tail. J. Immunol. 185, 1063-1070 (2010).
62. C. T. Weaver, R. D. Hatton, P. R. Mangan, L. E. Harrington, IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25, 821-852 (2007).
63. J. S. Stumhofer, J. Silver, C. A. Hunter, Negative regulation of Th17 responses. Semin. Immunol. 19, 394-399 (2007).
64. C. Diveu, M. J. McGeachy, D. J. Cua, Cytokines that regulate autoimmunity. Curr. Opin. Immunol. 20, 663-668 (2008).
65. A. Laurence, C. M. Tato, T. S. Davidson, Y. Kanno, Z. Chen, Z. Yao, R. B. Blank, F. Meylan, R. Siegel, L. Hennighausen, E. M. Shevach, J. J. O'Shea, Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26, 371-381 (2007).
66. H. Park, Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H.Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, C. Dong, A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141 (2005).
67. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6, 1123-1132 (2005).
68. K. Hirota, J. H. Duarte, M. Veldhoen, E. Hornsby, Y. Li, D. J. Cua, H. Ahlfors, C. Wilhelm, M. Tolaini, U. Menzel, A. Garefalaki, A. J. Potocnik, B. Stockinger, Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12, 255-263 (2011).
69. J. A. Bluestone, C. R. Mackay, J. J. O'Shea, B. Stockinger, The functional plasticity of T cell subsets. Nat. Rev. Immunol. 9, 811-816 (2009).
70. X. O. Yang, R. Nurieva, G. J. Martinez, H. S. Kang, Y. Chung, B. P. Pappu, B. Shah, S. H. Chang, K. S. Schluns, S. S. Watowich, X. H. Feng, A. M. Jetten, C. Dong, Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29, 44-56 (2008).
71. J. S. Stumhofer, C. A. Hunter, Advances in understanding the anti-inflammatory properties of IL-27. Immunol. Lett. 117, 123-130 (2008).
72. J. S. Stumhofer, A. Laurence, E. H. Wilson, E. Huang, C. M. Tato, L. M. Johnson, A. V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, C. J. Saris, J. J. O'Shea, L. Hennighausen, M. Ernst, C. A. Hunter, Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7, 937-945 (2006).
73. M. A. Kleinschek, A. M. Owyang, B. Joyce-Shaikh, C. L. Langrish, Y. Chen, D. M. Gorman, W. M. Blumenschein, T. McClanahan, F. Brombacher, S. D. Hurst, R. A. Kastelein, D. J. Cua, IL-25 regulates Th17 function in autoimmune inflammation. J. Exp. Med. 204, 161-170 (2007).
74. F. Shen, S. L. Gaffen, Structure-function relationships in the IL-17 receptor: Implications for signal transduction and therapy. Cytokine 41, 92-104 (2008).
75. S. Zhu, W. Pan, X. Song, Y. Liu, X. Shao, Y. Tang, D. Liang, D. He, H. Wang, W. Liu, Y. Shi, J. B. Harley, N. Shen, Y. Qian, The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-α. Nat. Med. 18, 1077-1086 (2012).
76. β-TrCP-mediated degradation of Act1. Sci. Signal. 4, ra73 (2011).
77. J. F. Wright, Y. Guo, A. Quazi, D. P. Luxenberg, F. Bennett, J. F. Ross, Y. Qiu, M. J.Whitters, K. N. Tomkinson, K. Dunussi-Joannopoulos, B. M. Carreno, M. Collins, N. M. Wolfman, Identification of an interleukin 17F/17A heterodimer in activated human CD4+ T cells. J. Biol. Chem. 282, 13447-13455 (2007).
78. J. F. Wright, F. Bennett, B. Li, J. Brooks, D. P. Luxenberg, M. J. Whitters, K. N. Tomkinson, L. J. Fitz, N. M. Wolfman, M. Collins, K. Dunussi-Joannopoulos, M. Chatterjee-Kishore, B. M. Carreno, The human IL-17F/IL-17A heterodimeric cytokine signals through the IL-17RA/IL-17RC receptor complex. J. Immunol. 181, 2799-2805 (2008).
79. S. H. Chang, C. Dong, A novel heterodimeric cytokine consisting of IL-17 and IL-17F regulates inflammatory responses. Cell Res. 17, 435-440 (2007).
80. B. Skaug, J. Chen, F. Du, J. He, A. Ma, Z. J. Chen, Direct, noncatalytic mechanism of IKK inhibition by A20. Mol. Cell 44, 559-571 (2011).
81. T. Hamilton, M. Novotny, P. J. Pavicic Jr., T. Herjan, J. Hartupee, D. Sun, C. Zhao, S. Datta, Diversity in post-transcriptional control of neutrophil chemoattractant cytokine gene expression. Cytokine 52, 116-122 (2010).
82. S. Datta, M. Novotny, P. G. Pavicic Jr., C. Zhao, T. Herjan, J. Hartupee, T. Hamilton, IL-17 regulates CXCL1 mRNA stability via an AUUUA/tristetraprolin- independent sequence. J. Immunol. 184, 1484-1491 (2010).
83. T. M. Tran, V. Temkin, B. Shi, L. Pagliari, S. Daniel, C. Ferran, R. M. Pope, TNFα-induced macrophage death via caspase-dependent and independent pathways. Apoptosis 14, 320-332 (2009).
84. Q. Huang, R. M. Pope, Toll-like receptor signaling: A potential link among rheumatoid arthritis, systemic lupus, and atherosclerosis. J. Leukoc. Biol. 88, 253-262 (2010).
85. S. Abdollahi-Roodsaz, F. A. van de Loo, M. I. Koenders, M. M. Helsen, B. Walgreen, L. A. van den Bersselaar, O. J. Arntz, N. Takahashi, L. A. Joosten, W. B. van den Berg, Destructive role of myeloid differentiation factor 88 and protective role of TRIF in interleukin-17-dependent arthritis in mice. Arthritis Rheum. 64, 1838-1847 (2012).
86. M. S. Maddur, P. Miossec, S. V. Kaveri, J. Bayry, Th17 cells: Biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am. J. Pathol. 181, 8-18 (2012).
87. G. Lopez-Castejon, N. M. Luheshi, V. Compan, S. High, R. C. Whitehead, S. Flitsch, A. Kirov, I. Prudovsky, E. Swanton, D. Brough, Deubiquitinases regulate the activity of caspase-1 and interleukin-1β secretion via assembly of the inflammasome. J. Biol. Chem. 288, 2721-2733 (2012).
88. A. Ernst, G. Avvakumov, J. Tong, Y. Fan, Y. Zhao, P. Alberts, A. Persaud, J. R. Walker, A. M. Neculai, D. Neculai, A. Vorobyov, P. Garg, L. Beatty, P. K. Chan, Y. C. Juang, M. C. Landry, C. Yeh, E. Zeqiraj, K. Karamboulas, A. Allali-Hassani, M. Vedadi, M. Tyers, J. Moffat, F. Sicheri, L. Pelletier, D. Durocher, B. Raught, D. Rotin, J. Yang, M. F. Moran, S. Dhe-Paganon, S. S. Sidhu, A strategy for modulation of enzymes in the ubiquitin system. Science 339, 590-595 (2013).