The Anaphase-Promoting Complex Protein 5 (AnapC5) Associates with A20 and Inhibits IL-17-Mediated Signal Transduction

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Ho, Allen W ^a,b   Garg, Abhishek V ^a   Monin, Leticia ^a   Simpson Abelson, Michelle R ^a   Kinner, Lauren ^a   Gaffen, Sarah L ^a  

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

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; ANAPHASE PROMOTING COMPLEX PROTEIN 5; ANAPHASE PROMOTING COMPLEX PROTEIN 7; BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 17 RECEPTOR A; INTERLEUKIN 17 RECEPTOR C; PROTEIN A20; PROTEIN ITCH; SCAFFOLD PROTEIN; SMALL INTERFERING RNA; TAX BINDING PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; ANIMALS; APC5 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; APC7 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; CARRIER PROTEINS; CELL LINE; COMPLEMENT FACTOR D; DNA-BINDING PROTEINS; INTERLEUKIN-17; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN SUBUNITS; RAS PROTEINS; RECEPTORS, INTERLEUKIN-17; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN-PROTEIN LIGASES;

EID: 84880844999     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070168     Document Type: Article

References (71)

1. Korn T, Bettelli E, Oukka M, Kuchroo VK, (2009) IL-17 and Th17 Cells. Annu Rev Immunol 27: 485-518.
2. Iwakura Y, Ishigame H, Saijo S, Nakae S, (2011) Functional specialization of interleukin-17 family members. Immunity 34: 149-162.
3. Wright JF, Guo Y, Quazi A, Luxenberg DP, Bennett F, et al. (2007) Identification of an Interleukin 17F/17A Heterodimer in Activated Human CD4+ T Cells. J Biol Chem 282: 13447-13455.
4. Chang SH, Dong C, (2007) A novel heterodimeric cytokine consisting of IL-17 and IL-17F regulates inflammatory responses. Cell Res 17: 435-440.
5. Yang XO, Chang SH, Park H, Nurieva R, Shah B, et al. (2008) Regulation of inflammatory responses by IL-17F. J Exp Med 205: 1063-1075.
6. Onishi R, Gaffen SL, (2010) IL-17 and its Target Genes: Mechanisms of IL-17 Function in Disease. Immunology 129: 311-321.
7. Hueber W, Patel DD, Dryja T, Wright AM, Koroleva I, et al. (2010) Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med 2: 52ra72.
8. Genovese M, Van den Bosch F, Roberson S, Bojin S, Biagini I, et al. (2010) LY2439821, a humanized anti-interleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis. Arth Rheum 62: 929-939.
9. Leonardi C, Matheson R, Zachariae C, Cameron G, Li L, et al. (2012) Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Engl J Med 366: 1190-1199.
10. Papp KA, Leonardi C, Menter A, Ortonne JP, Krueger JG, et al. (2012) Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N Engl J Med 366: 1181-1189.
11. Gaffen SL, (2009) Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 9: 556-567.
12. Aggarwal S, Gurney AL, (2002) IL-17: A prototype member of an emerging family. J Leukoc Biol 71: 1-8.
13. Toy D, Kugler D, Wolfson M, Vanden Bos T, Gurgel J, et al. (2006) Cutting Edge: Interleukin-17 signals through a heteromeric receptor complex. J Immunol 177: 36-39.
14. Yao Z, Fanslow WC, Seldin MF, Rousseau A-M, Painter SL, et al. (1995) Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3: 811-821.
15. Wright JF, Bennett F, Li B, Brooks J, Luxenberg DP, et al. (2008) The human IL-17F/IL-17A heterodimeric cytokine signals through the IL-17RA/IL-17RC receptor complex. J Immunol 181: 2799-2805.
16. Kuestner R, Taft D, Haran A, Brandt C, Brender T, et al. (2007) Identification of the IL-17 receptor related molecule, IL-17RC, as the receptor for IL-17F. J Immunol 179: 5462-5473.
17. Rickel EA, Siegel LA, Yoon BR, Rottman JB, Kugler DG, et al. (2008) Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J Immunol 181: 4299-4310.
18. Chang SH, Reynolds JM, Pappu BP, Chen G, Martinez GJ, et al. (2011) Interleukin-17C promotes Th17 cell responses and autoimmune disease via interleukin-17 receptor E. Immunity. 35: 611-621.
19. Ramirez-Carrozzi V, Sambandam A, Luis E, Lin Z, Jeet S, et al. (2011) IL-17C regulates the innate immune function of epithelial cells in an autocrine manner. Nat Immunol 12: 1159-1166.
20. Song X, Zhu S, Shi P, Liu Y, Shi Y, et al. (2011) IL-17RE is the functional receptor for IL-17C and mediates mucosal immunity to infection with intestinal pathogens. Nat Immunol 12: 1151-1158.
21. Ho A, Gaffen SL, (2010) IL-17RC: A partner in IL-17 signaling and beyond. Semin Immunopathol 32: 33-42.
22. Novatchkova M, Leibbrandt A, Werzowa J, Neubuser A, Eisenhaber F, (2003) The STIR-domain superfamily in signal transduction, development and immunity. Trends Biochem Sci 28: 226-229.
23. Zhang B, Liu C, Qian W, Han Y, Li X, et al. (2013) Crystal Structure of IL-17 Receptor B SEFIR Domain. J Immunol 190: 2320-2326.
24. Maitra A, Shen F, Hanel W, Mossman K, Tocker J, et al. (2007) Distinct functional motifs within the IL-17 receptor regulate signal transduction and target gene expression. Proc Natl Acad Sci, USA 104: 7506-7511.
25. Qian Y, Liu C, Hartupee J, Altuntas CZ, Gulen MF, et al. (2007) The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 8: 247-256.
26. Chang SH, Park H, Dong C, (2006) Act1 adaptor protein is an immediate and essential signaling component of interleukin-17 receptor. J Biol Chem 281: 35603-35607.
27. Li X, (2008) Act1 modulates autoimmunity through its dual functions in CD40L/BAFF and IL-17 signaling. Cytokine 41: 105-113.
28. Liu C, Qian W, Qian Y, Giltiay NV, Lu Y, et al. (2009) Act1, a U-box E3 ubiquitin ligase for IL-17 signaling. Sci Signal 2: ra63.
29. Linden A, (2007) A role for the cytoplasmic adaptor proteins Act1 in mediating IL-17 signaling. Sci STKE re4: 1-8.
30. Schwandner R, Yamaguchi K, Cao Z, (2000) Requirement of tumor necrosis factor-associated factor (TRAF)6 in interleukin 17 signal transduction. J Exp Med 191: 1233-1239.
31. Shen F, Hu Z, Goswami J, Gaffen SL, (2006) Identification of common transcriptional regulatory elements in interleukin-17 target genes. J Biol Chem 281: 24138-24148.
32. Sun D, Novotny M, Bulek K, Liu C, Li X, et al. (2011) Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing regulatory factor SF2 (ASF). Nat Immunol in press.
33. Hartupee J, Liu C, Novotny M, Sun D, Li X, et al. (2009) IL-17 signaling for mRNA stabilization does not require TNF receptor-associated factor 6. J Immunol 182: 1660-1666.
34. Shen F, Gaffen SL, (2008) Structure-function relationships in the IL-17 receptor: Implications for signal transduction and therapy. Cytokine 41: 92-104.
35. Shi P, Zhu S, Lin Y, Liu Y, Chen Z, et al. (2011) Persistent stimulation with interleukin-17 desensitizes cells through SCFbeta-TrCP-mediated degradation of Act1. Sci Signal 4: ra73.
36. Shen F, Li N, Gade P, Kalvakolanu DV, Weibley T, et al. (2009) IL-17 Receptor Signaling Inhibits C/EBP{beta} by Sequential Phosphorylation of the Regulatory 2 Domain. Sci Signal 2: ra8.
37. Zhu S, Pan W, Song X, Liu Y, Shao X, et al. (2012) The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-alpha. Nat Med 18: 1077-1086.
38. Zhong B, Liu X, Wang X, Chang S, Liu X, et al. (2012) Negative regulation of IL-17-mediated signalling and inflammation by the ubiquitin-specific protease USP25. Nat Immunol in press.
39. Garg A, Ahmed M, Vallejo A, Ma A, Gaffen S, (2013) The deubiquitinase A20 mediates feedback inhibition of Interleukin-17 receptor signaling. Science Signaling 6: ra44-55.
40. Zhong B, Liu X, Wang X, Li H, Darnay BG, et al. (2013) Ubiquitin-Specific Protease 25 Regulates TLR4-Dependent Innate Immune Responses Through Deubiquitination of the Adaptor Protein TRAF3. Sci Signal 6: ra35.
41. Ma A, Malynn BA, (2012) A20: linking a complex regulator of ubiquitylation to immunity and human disease. Nat Rev Immunol 12: 774-785.
42. Ho A, Shen F, Conti H, Patel N, Childs E, et al. (2010) IL-17RC is required for immune signaling via an extended SEFIR domain in the cytoplasmic tail J Immunol. 185: 1063-1070.
43. Turnell AS, Mymryk JS, (2006) Roles for the coactivators CBP and p300 and the APC/C E3 ubiquitin ligase in E1A-dependent cell transformation. Br J Cancer 95: 555-560.
44. Shembade N, Harhaj EW, (2012) Regulation of NF-kappaB signaling by the A20 deubiquitinase. Cell Mol Immunol 9: 123-130.
45. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, et al. (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14: 282-289.
46. Chang L, Zhang J, Tseng YH, Xie CQ, Ilany J, et al. (2007) Rad GTPase deficiency leads to cardiac hypertrophy. Circulation 116: 2976-2983.
47. Xu Y, Ma M, Ippolito GC, Schroeder HW Jr, Carroll MC, et al. (2001) Complement activation in factor D-deficient mice. Proc Natl Acad Sci U S A 98: 14577-14582.
48. Ding J, Nagai K, Woo JT, (2003) Insulin-dependent adipogenesis in stromal ST2 cells derived from murine bone marrow. Biosci Biotechnol Biochem 67: 314-321.
49. Maitra A, Shen F, Hanel W, Mossman K, Tocker J, et al. (2007) 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.
50. Xu C, Mendelsohn A, Brent R, (1997) Cells that register logical relationships among proteins. Proc Natl Acad Sci U S A 94: 12473-12478.
51. Li X, Commane M, Nie H, Hua X, Chatterjee-Kishore M, et al. (2000) Act1, an NF-kappa B-activating protein. Proc Natl Acad Sci U S A 97: 10489-10493.
52. Reynet C, Kahn CR, (1993) Rad: a member of the Ras family overexpressed in muscle of type II diabetic humans. Science 262: 1441-1444.
53. Conti H, Shen F, Nayyar N, Stocum E, JN S, et al. (2009) Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 206: 299-311.
54. Xu Y, Ponnuraj K, Narayana S, Volanakis J (2005) Factors D and B: Substrate-inducible serine proteases of the alternative pathway of complement activation. In: Morikis D, Lambris J, editors. Structural Biology of the Complement System. Boca Raton: CRC Press. 91-110.
55. Turnell AS, Stewart GS, Grand RJ, Rookes SM, Martin A, et al. (2005) The APC/C and CBP/p300 cooperate to regulate transcription and cell-cycle progression. Nature 438: 690-695.
56. Shen F, Li N, Gade P, Kalvakolanu DV, Weibley T, et al. (2009) IL-17 receptor signaling inhibits C/EBPbeta by sequential phosphorylation of the regulatory 2 domain. Sci Signal 2: ra8.
57. Zhu S, Pan W, Shi P, Gao H, Zhao F, et al. (2010) Modulation of experimental autoimmune encephalomyelitis through TRAF3-mediated suppression of interleukin 17 receptor signaling. J Exp Med 207: 2647-2662.
58. Onishi R, Park S, Hanel W, Maitra A, Gaffen S, (2010) The SEFIR is not enough: An extended region downstream of the Interleukin-17RA SEFIR domain is required for IL-17-dependent signal transduction. J Biol Chem 285: 32751-32759.
59. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, et al. (2003) Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748.
60. Hue S, Ahern P, Buonocore S, Kullberg M, Cua D, et al. (2006) Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med.
61. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201: 233-240.
62. McGeachy MJ, Cua DJ, (2007) The link between IL-23 and Th17 cell-mediated immune pathologies. Semin Immunol 19: 372-376.
63. Patel DD, Lee DM, Kolbinger F, Antoni C (2012) Effect of IL-17A blockade with secukinumab in autoimmune diseases. Ann Rheum Dis.
64. Hernández-Santos N, Gaffen SL, (2012) Th17 cells in immunity to Candida albicans. Cell Host Microbe 11: 425-435.
65. Huppler AR, Bishu S, Gaffen SL, (2012) Mucocutaneous candidiasis: the IL-17 pathway and implications for targeted immunotherapy. Arthritis Res Ther 14: 217.
66. Hymowitz SG, Filvaroff EH, Yin JP, Lee J, Cai L, et al. (2001) IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. Embo J 20: 5332-5341.
67. Ely LK, Fischer S, Garcia KC, (2009) Structural basis of receptor sharing by interleukin 17 cytokines. Nat Immunol 10: 1245-1251.
68. Hamilton T, Novotny M, Pavicic PJ Jr, Herjan T, Hartupee J, et al. (2010) Diversity in post-transcriptional control of neutrophil chemoattractant cytokine gene expression. Cytokine 52: 116-122.
69. Hymowitz SG, Wertz IE, (2010) A20: from ubiquitin editing to tumour suppression. Nat Rev Cancer 10: 332-341.
70. Sun SC, (2008) Deubiquitylation and regulation of the immune response. Nat Rev Immunol 8: 501-511.
71. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, et al. (2004) De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430: 694-699.