Roles of ubiquitination in pattern-recognition receptors and type I interferon receptor signaling

Cytokine

Volumn 43, Issue 3, 2008, Pages 359-367

  Bibeau Poirier, Annie ^a   Servant, Marc J ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Innate immunity; Interferon; Pattern recognition receptors; Phosphorylation; Ubiquitination

Indexed keywords

BACTERIAL PROTEIN; CULLIN; DNA BINDING PROTEIN; ELONGIN BC; INTERFERON RECEPTOR; INTERFERON RECEPTOR 1; NUCLEIC ACID BINDING PROTEIN; PATTERN RECOGNITION RECEPTOR; PROTEIN A20; PROTEIN CYLD; PROTEIN DUBA; PROTEIN RNF125; PROTEIN SLIM; PROTEIN TRIAD3; PROTEIN TRIM; PROTEIN TRIM21; PROTEIN TRIM25; PROTEIN TRIM30ALPHA; PROTEIN YOPJ; STAT PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

CELL FUNCTION; CYTOKINE PRODUCTION; ENZYME ACTIVITY; GENE CONTROL; HUMAN; INNATE IMMUNITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; REVIEW; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NUCLEAR PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR, INTERFERON ALPHA-BETA; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 51349083101     PISSN: 10434666     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cyto.2008.07.012     Document Type: Review

References (91)

1. Lee M.S., and Kim Y.J. Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem 76 (2007) 447-480
2. Hacker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006; re13 (2006).
3. Chang L., and Karin M. Mammalian MAP kinase signalling cascades. Nature 410 (2001) 37-40
4. Mamane Y., Heylbroeck C., Genin P., Algarte M., Servant M.J., LePage C., et al. Interferon regulatory factors: the next generation. Gene 237 (1999) 1-14
5. Peters R.T., Liao S.M., and Maniatis T. IKKepsilon is part of a novel PMA-inducible IkappaB kinase complex. Mol Cell 5 (2000) 513-522
6. Shimada T., Kawai T., Takeda K., Matsumoto M., Inoue J., Tatsumi Y., et al. IKK-i, a novel lipopolysaccharide-inducible kinase that is related to IkappaB kinases. Int Immunol 11 (1999) 1357-1362
7. Pomerantz J.L., and Baltimore D. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 18 (1999) 6694-6704
8. Sharma S., tenOever B.R., Grandvaux N., Zhou G.P., Lin R., and Hiscott J. Triggering the interferon antiviral response through an IKK-related pathway. Science 300 (2003) 1148-1151
9. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4 (2003) 491-496
10. Clement J.F., Bibeau-Poirier A., Gravel S.P., Grandvaux N., Bonneil E., Thibault P., et al. Phosphorylation of IRF-3 on Ser 339 generates a hyperactive form of IRF-3 through regulation of dimerization and CBP association. J Virol 82 (2008) 3984-3996
11. Panne D., McWhirter S.M., Maniatis T., and Harrison S.C. Interferon regulatory factor 3 is regulated by a dual phosphorylation-dependent switch. J Biol Chem 282 (2007) 22816-22822
12. Samuel C.E. Antiviral actions of interferons. Clin Microbiol Rev 14 (2001) 778-809
13. Liu Y.C. Ubiquitin ligases and the immune response. Annu Rev Immunol 22 (2004) 81-127
14. Liu Y.C., Penninger J., and Karin M. Immunity by ubiquitylation: a reversible process of modification. Nat Rev Immunol 5 (2005) 941-952
15. Varadan R., Assfalg M., Haririnia A., Raasi S., Pickart C., and Fushman D. Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J Biol Chem 279 (2004) 7055-7063
16. Hicke L., Schubert H.L., and Hill C.P. Ubiquitin-binding domains. Nat Rev Mol Cell Biol 6 (2005) 610-621
17. Sun L., and Chen Z.J. The novel functions of ubiquitination in signaling. Curr Opin Cell Biol 16 (2004) 119-126
18. Nijman S.M., Luna-Vargas M.P., Velds A., Brummelkamp T.R., Dirac A.M., Sixma T.K., et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 123 (2005) 773-786
19. Hoebe K., and Beutler B. TRAF3: a new component of the TLR-signaling apparatus. Trends Mol Med 12 (2006) 187-189
20. Bradley J.R., and Pober J.S. Tumor necrosis factor receptor-associated factors (TRAFs). Oncogene 20 (2001) 6482-6491
21. Hacker H., Redecke V., Blagoev B., Kratchmarova I., Hsu L.C., Wang G.G., et al. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439 (2006) 204-207
22. Oganesyan G., Saha S.K., Guo B., He J.Q., Shahangian A., Zarnegar B., et al. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 439 (2006) 208-211
23. Lomaga M.A., Yeh W.C., Sarosi I., Duncan G.S., Furlonger C., Ho A., et al. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev 13 (1999) 1015-1024
24. Gohda J., Matsumura T., and Inoue J. Cutting edge: TNFR-associated factor (TRAF) 6 is essential for MyD88-dependent pathway but not toll/IL-1 receptor domain-containing adaptor-inducing IFN-beta (TRIF)-dependent pathway in TLR signaling. J Immunol 173 (2004) 2913-2917
25. Wang C., Deng L., Hong M., Akkaraju G.R., Inoue J., and Chen Z.J. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412 (2001) 346-351
26. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., et al. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103 (2000) 351-361
27. Yamamoto M., Okamoto T., Takeda K., Sato S., Sanjo H., Uematsu S., et al. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat Immunol 7 (2006) 962-970
28. Kanayama A., Seth R.B., Sun L., Ea C.K., Hong M., Shaito A., et al. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol Cell 15 (2004) 535-548
29. Huang Q., Yang J., Lin Y., Walker C., Cheng J., Liu Z.G., et al. Differential regulation of interleukin 1 receptor and Toll-like receptor signaling by MEKK3. Nat Immunol 5 (2004) 98-103
30. Sato S., Sanjo H., Takeda K., Ninomiya-Tsuji J., Yamamoto M., Kawai T., et al. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 6 (2005) 1087-1095
31. Cusson-Hermance N., Khurana S., Lee T.H., Fitzgerald K.A., and Kelliher M.A. Rip1 mediates the Trif-dependent toll-like receptor 3- and 4-induced NF-{kappa}B activation but does not contribute to interferon regulatory factor 3 activation. J Biol Chem 280 (2005) 36560-36566
32. Conze D.B., Wu C.J., Thomas J.A., Landstrom A., and Ashwell J.D. Lys63-linked polyubiquitination of IRAK-1 is required for interleukin-1 receptor- and toll-like receptor-mediated NF-kappaB activation. Mol Cell Biol 28 (2008) 3538-3547
33. Wu C.J., Conze D.B., Li T., Srinivasula S.M., and Ashwell J.D. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat Cell Biol 8 (2006) 398-406
34. Windheim M., Stafford M., Peggie M., and Cohen P. Interleukin-1 (IL-1) induces the Lys63-linked polyubiquitination of IL-1 receptor-associated kinase 1 to facilitate NEMO binding and the activation of IkappaBalpha kinase. Mol Cell Biol 28 (2008) 1783-1791
35. Ea C.K., Deng L., Xia Z.P., Pineda G., and Chen Z.J. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 22 (2006) 245-257
36. Adhikari A., Xu M., and Chen Z.J. Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26 (2007) 3214-3226
37. Takaoka A., Yanai H., Kondo S., Duncan G., Negishi H., Mizutani T., et al. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434 (2005) 243-249
38. Kawai T., Sato S., Ishii K.J., Coban C., Hemmi H., Yamamoto M., et al. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 5 (2004) 1061-1068
39. Honda K., Yanai H., Mizutani T., Negishi H., Shimada N., Suzuki N., et al. Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc Natl Acad Sci USA 101 (2004) 15416-15421
40. Jiang Z., Mak T.W., Sen G., and Li X. Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc Natl Acad Sci USA 101 (2004) 3533-3538
41. Meylan E., Burns K., Hofmann K., Blancheteau V., Martinon F., Kelliher M., et al. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat Immunol 5 (2004) 503-507
42. Kayagaki N., Phung Q., Chan S., Chaudhari R., Quan C., O'Rourke K.M., et al. DUBA: a deubiquitinase that regulates type I interferon production. Science 318 (2007) 1628-1632
43. Saha S.K., Pietras E.M., He J.Q., Kang J.R., Liu S.Y., Oganesyan G., et al. Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J 25 (2006) 3257-3263
44. Gatot J.S., Gioia R., Chau T.L., Patrascu F., Warnier M., Close P., et al. Lipopolysaccharide-mediated interferon regulatory factor activation involves TBK1-IKKepsilon-dependent Lys(63)-linked polyubiquitination and phosphorylation of TANK/I-TRAF. J Biol Chem 282 (2007) 31131-31146
45. Guo B., and Cheng G. Modulation of the interferon antiviral response by the TBK1/IKKi adaptor protein TANK. J Biol Chem 282 (2007) 11817-11826
46. van der Reijden B.A., Erpelinck-Verschueren C.A., Lowenberg B., and Jansen J.H. TRIADs: a new class of proteins with a novel cysteine-rich signature. Protein Sci 8 (1999) 1557-1561
47. Chuang T.H., and Ulevitch R.J. Triad3A, an E3 ubiquitin-protein ligase regulating Toll-like receptors. Nat Immunol 5 (2004) 495-502
48. Fearns C., Pan Q., Mathison J.C., and Chuang T.H. Triad3A regulates ubiquitination and proteasomal degradation of RIP1 following disruption of Hsp90 binding. J Biol Chem 281 (2006) 34592-34600
49. Nisole S., Stoye J.P., and Saib A. TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol 3 (2005) 799-808
50. Gack M.U., Shin Y.C., Joo C.H., Urano T., Liang C., Sun L., et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446 (2007) 916-920
51. Nakasato N., Ikeda K., Urano T., Horie-Inoue K., Takeda S., and Inoue S. A ubiquitin E3 ligase Efp is up-regulated by interferons and conjugated with ISG15. Biochem Biophys Res Commun 351 (2006) 540-546
52. Higgs R., and Jefferies C.A. Targeting IRFs by ubiquitination: regulating antiviral responses. Biochem Soc Trans 36 (2008) 453-458
53. Kong H.J., Anderson D.E., Lee C.H., Jang M.K., Tamura T., Tailor P., et al. Cutting edge: autoantigen Ro52 is an interferon inducible E3 ligase that ubiquitinates IRF-8 and enhances cytokine expression in macrophages. J Immunol 179 (2007) 26-30
54. Shi M., Deng W., Bi E., Mao K., Ji Y., Lin G., et al. TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nat Immunol 9 (2008) 369-377
55. Cardozo T., and Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol 5 (2004) 739-751
56. Willems A.R., Schwab M., and Tyers M. A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695 (2004) 133-170
57. Ang X.L., and Harper J.W. SCF-mediated protein degradation and cell cycle control. Oncogene 24 (2005) 2860-2870
58. Nakayama K.I., and Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer 6 (2006) 369-381
59. Kumar K.G., Barriere H., Carbone C.J., Liu J., Swaminathan G., Xu P., et al. Site-specific ubiquitination exposes a linear motif to promote interferon-alpha receptor endocytosis. J Cell Biol 179 (2007) 935-950
60. Sato M., Suemori H., Hata N., Asagiri M., Ogasawara K., Nakao K., et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13 (2000) 539-548
61. Bibeau-Poirier A., Gravel S.P., Clement J.F., Rolland S., Rodier G., Coulombe P., et al. Involvement of the IkappaB kinase (IKK)-related kinases tank-binding kinase 1/IKKi and cullin-based ubiquitin ligases in IFN regulatory factor-3 degradation. J Immunol 177 (2006) 5059-5067
62. Saitoh T., Tun-Kyi A., Ryo A., Yamamoto M., Finn G., Fujita T., et al. Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1. Nat Immunol 7 (2006) 598-605
63. Kile B.T., Schulman B.A., Alexander W.S., Nicola N.A., Martin H.M., and Hilton D.J. The SOCS box: a tale of destruction and degradation. Trends Biochem Sci 27 (2002) 235-241
64. Yoshimura A., Naka T., and Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 7 (2007) 454-465
65. Mansell A., Smith R., Doyle S.L., Gray P., Fenner J.E., Crack P.J., et al. Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7 (2006) 148-155
66. Maine G.N., Mao X., Komarck C.M., and Burstein E. COMMD1 promotes the ubiquitination of NF-kappaB subunits through a cullin-containing ubiquitin ligase. EMBO J 26 (2007) 436-447
67. Zhao H., Li C.C., Pardo J., Chu P.C., Liao C.X., Huang J., et al. A novel E3 ubiquitin ligase TRAC-1 positively regulates T cell activation. J Immunol 174 (2005) 5288-5297
68. Giannini A.L., Gao Y., and Bijlmakers M.J. T-cell regulator RNF125/TRAC-1 belongs to a novel family of ubiquitin ligases with zinc fingers and a ubiquitin-binding domain. Biochem J 410 (2008) 101-111
69. Arimoto K., Takahashi H., Hishiki T., Konishi H., Fujita T., and Shimotohno K. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc Natl Acad Sci USA 104 (2007) 7500-7505
70. Kadrmas J.L., and Beckerle M.C. The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 5 (2004) 920-931
71. Tanaka T., Soriano M.A., and Grusby M.J. SLIM is a nuclear ubiquitin E3 ligase that negatively regulates STAT signaling. Immunity 22 (2005) 729-736
72. Tanaka T., Grusby M.J., and Kaisho T. PDLIM2-mediated termination of transcription factor NF-kappaB activation by intranuclear sequestration and degradation of the p65 subunit. Nat Immunol 8 (2007) 584-591
73. Gao C., Guo H., Mi Z., Grusby M.J., and Kuo P.C. Osteopontin induces ubiquitin-dependent degradation of STAT1 in RAW264. 7 murine macrophages. J Immunol 178 (2007) 1870-1881
74. Bignell G.R., Warren W., Seal S., Takahashi M., Rapley E., Barfoot R., et al. Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet 25 (2000) 160-165
75. Kovalenko A., Chable-Bessia C., Cantarella G., Israel A., Wallach D., and Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 424 (2003) 801-805
76. Trompouki E., Hatzivassiliou E., Tsichritzis T., Farmer H., Ashworth A., and Mosialos G. CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 424 (2003) 793-796
77. Zhang M., Wu X., Lee A.J., Jin W., Chang M., Wright A., et al. Regulation of IKK-related kinases and antiviral responses by tumor suppressor CYLD. J Biol Chem (2008)
78. Beyaert R., Heyninck K., and Van Huffel S. A20 and A20-binding proteins as cellular inhibitors of nuclear factor-kappa B-dependent gene expression and apoptosis. Biochem Pharmacol 60 (2000) 1143-1151
79. Heyninck K., and Beyaert R. A20 inhibits NF-kappaB activation by dual ubiquitin-editing functions. Trends Biochem Sci 30 (2005) 1-4
80. Chen Z.J. Ubiquitin signalling in the NF-kappaB pathway. Nat Cell Biol 7 (2005) 758-765
81. Wertz I.E., O'Rourke K.M., Zhou H., Eby M., Aravind L., Seshagiri S., et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430 (2004) 694-699
82. Boone D.L., Turer E.E., Lee E.G., Ahmad R.C., Wheeler M.T., Tsui C., et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 5 (2004) 1052-1060
83. Saitoh T., Yamamoto M., Miyagishi M., Taira K., Nakanishi M., Fujita T., et al. A20 is a negative regulator of IFN regulatory factor 3 signaling. J Immunol 174 (2005) 1507-1512
84. Wang Y.Y., Li L., Han K.J., Zhai Z., and Shu H.B. A20 is a potent inhibitor of TLR3- and Sendai virus-induced activation of NF-kappaB and ISRE and IFN-beta promoter. FEBS Lett 576 (2004) 86-90
85. Lin R., Yang L., Nakhaei P., Sun Q., Sharif-Askari E., Julkunen I., et al. Negative regulation of the retinoic acid-inducible gene I-induced antiviral state by the ubiquitin-editing protein A20. J Biol Chem 281 (2006) 2095-2103
86. Haase R., Richter K., Pfaffinger G., Courtois G., and Ruckdeschel K. Yersinia outer protein P suppresses TGF-beta-activated kinase-1 activity to impair innate immune signaling in Yersinia enterocolitica-infected cells. J Immunol 175 (2005) 8209-8217
87. Zhou H., Monack D.M., Kayagaki N., Wertz I., Yin J., Wolf B., et al. Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 202 (2005) 1327-1332
88. Thiefes A., Wolf A., Doerrie A., Grassl G.A., Matsumoto K., Autenrieth I., et al. The Yersinia enterocolitica effector YopP inhibits host cell signalling by inactivating the protein kinase TAK1 in the IL-1 signalling pathway. EMBO Rep 7 (2006) 838-844
89. Sweet C.R., Conlon J., Golenbock D.T., Goguen J., and Silverman N. YopJ targets TRAF proteins to inhibit TLR-mediated NF-kappaB, MAPK and IRF3 signal transduction. Cell Microbiol 9 (2007) 2700-2715
90. Wang Y., Tang Y., Teng L., Wu Y., Zhao X., and Pei G. Association of beta-arrestin and TRAF6 negatively regulates Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 7 (2006) 139-147
91. Michallet M.C., Meylan E., Ermolaeva M.A., Vazquez J., Rebsamen M., Curran J., et al. TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 28 (2008) 651-661