The role of ubiquitination in regulation of innate immune signaling

Current Issues in Molecular Biology

Volumn 18, Issue 1, 2016, Pages 1-10

  Zohaib, Ali ^a   Duan, Xiaodong ^a   Zhu, Bibo ^a   Ye, Jing ^a   Wan, Shengfeng ^a   Chen, Huanchun ^a   Liu, Xueqin ^a   Cao, Shengbo ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; DEUBIQUITINASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; PROTEIN LGP2; PROTEIN MDA5; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; IMMUNE SYSTEM; IMMUNOREACTIVITY; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; PHYSIOLOGY;

ANIMALS; HUMANS; IMMUNITY, INNATE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; UBIQUITINATION;

EID: 84937825161     PISSN: 14673037     EISSN: 14673045     Source Type: Journal    
DOI: None     Document Type: Article

References (107)

1. Arimoto, K., Takahashi, H., Hishiki, T., Konishi, H., Fujita, T., and Shimotohno, K. (2007). Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. U. S. A. 104, 7500-7505.
2. Bauler, L.D., Duckett, C.S., and O’Riordan, M.X.D. (2008). XIAP regulates cytosol-specific innate immunity to Listeria infection. PLoS Pathog. 4, e1000142.
3. Belgnaoui, S.M., Paz, S., Samuel, S., Goulet, M.-L., Sun, Q., Kikkert, M., Iwai, K., Dikic, I., Hiscott, J., and Lin, R. (2012). Linear ubiquitination of NEMO negatively regulates the interferon antiviral response through disruption of the MAVS-TRAF3 complex. Cell Host Microbe 12, 211-222.
4. Bertrand, M.J.M., Milutinovic, S., Dickson, K.M., Ho, W.C., Boudreault, A., Durkin, J., Gillard, J.W., Jaquith, J.B., Morris, S.J., and Barker, P.A. (2008). cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700.
5. Bertrand, M.J.M., Doiron, K., Labbé, K., Korneluk, R.G., Barker, P.A., and Saleh, M. (2009). Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immunity signaling by the pattern recognition receptors NOD1 and NOD2. Immunity 30, 789-801.
6. Blonska, M., Shambharkar, P.B., Kobayashi, M., Zhang, D., Sakurai, H., Su, B., and Lin, X. (2005). TAK1 is recruited to the tumor necrosis factor-alpha (TNF-alpha) receptor 1 complex in a receptor-interacting protein (RIP)- dependent manner and cooperates with MEKK3 leading to NF-kappaB activation. J. Biol. Chem. 280, 43056-43063.
7. Boname, J.M., Thomas, M., Stagg, H.R., Xu, P., Peng, J., and Lehner, P.J. (2010). Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic Cph. Den. 11, 210-220.
8. Boone, D.L., Turer, E.E., Lee, E.G., Ahmad, R.-C., Wheeler, M.T., Tsui, C., Hurley, P., Chien, M., Chai, S., Hitotsumatsu, O., et al. (2004). The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5, 1052-1060.
9. Brummelkamp, T.R., Nijman, S.M.B., Dirac, A.M.G., and Bernards, R. (2003). Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424, 797-801.
10. Chang, M., Jin, W., and Sun, S.-C. (2009). Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nat. Immunol. 10, 1089-1095.
11. Chen, Z.J., and Sun, L.J. (2009). Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33, 275-286.
12. Colleran, A., Collins, P.E., O’Carroll, C., Ahmed, A., Mao, X., McManus, B., Kiely, P.A., Burstein, E., and Carmody, R.J. (2013). Deubiquitination of NF-κB by Ubiquitin- Specific Protease-7 promotes transcription. Proc. Natl. Acad. Sci. U. S. A. 110, 618-623.
13. Conze, D.B., Wu, C.-J., Thomas, J.A., Landstrom, A., and Ashwell, J.D. (2008). Lys63-linked polyubiquitination of IRAK-1 is required for interleukin-1 receptor- and toll-like receptor-mediated NF-kappaB activation. Mol. Cell. Biol. 28, 3538-3547.
14. Damgaard, R.B., Nachbur, U., Yabal, M., Wong, W.W.-L., Fiil, B.K., Kastirr, M., Rieser, E., Rickard, J.A., Bankovacki, A., Peschel, C., et al. (2012). The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol. Cell 46, 746-758.
15. Daubeuf, S., Singh, D., Tan, Y., Liu, H., Federoff, H.J., Bowers, W.J., and Tolba, K. (2009). HSV ICP0 recruits USP7 to modulate TLR-mediated innate response. Blood 113, 3264-3275.
16. Dempsey, L.A. (2013). NLRP3 ubiquitination. Nat. Immunol. 14, 118-118.
17. Deng, L., Wang, C., Spencer, E., Yang, L., Braun, A., You, J., Slaughter, C., Pickart, C., and Chen, Z.J. (2000). Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351-361.
18. Dynek, J.N., Goncharov, T., Dueber, E.C., Fedorova, A.V., Izrael-Tomasevic, A., Phu, L., Helgason, E., Fairbrother, W.J., Deshayes, K., Kirkpatrick, D.S., et al. (2010). c- IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J. 29, 4198-4209.
19. Ea, C.-K., Deng, L., Xia, Z.-P., Pineda, G., and Chen, Z.J. (2006). Activation of IKK by TNFalpha requires sitespecific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22, 245-257.
20. Emmerich, C.H., Ordureau, A., Strickson, S., Arthur, J.S.C., Pedrioli, P.G.A., Komander, D., and Cohen, P. (2013). Activation of the canonical IKK complex by K63/M1- linked hybrid ubiquitin chains. Proc. Natl. Acad. Sci. U. S. A. 110, 15247-15252.
21. Enesa, K., Zakkar, M., Chaudhury, H., Luong, L.A., Rawlinson, L., Mason, J.C., Haskard, D.O., Dean, J.L.E., and Evans, P.C. (2008). NF-kappaB suppression by the deubiquitinating enzyme Cezanne: a novel negative feedback loop in pro-inflammatory signaling. J. Biol. Chem. 283, 7036-7045.
22. Estornes, Y., Toscano, F., Virard, F., Jacquemin, G., Pierrot, A., Vanbervliet, B., Bonnin, M., Lalaoui, N., Mercier- Gouy, P., Pachéco, Y., et al. (2012). dsRNA induces apoptosis through an atypical death complex associating TLR3 to caspase-8. Cell Death Differ. 19, 1482-1494.
23. Feoktistova, M., Geserick, P., Kellert, B., Dimitrova, D.P., Langlais, C., Hupe, M., Cain, K., MacFarlane, M., Häcker, G., and Leverkus, M. (2011). cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 43, 449-463.
24. Fiil, B.K., Damgaard, R.B., Wagner, S.A., Keusekotten, K., Fritsch, M., Bekker-Jensen, S., Mailand, N., Choudhary, C., Komander, D., and Gyrd-Hansen, M. (2013). OTULIN restricts Met1-linked ubiquitination to control innate immune signaling. Mol. Cell 50, 818-830.
25. Friedman, C.S., O’Donnell, M.A., Legarda-Addison, D., Ng, A., Cárdenas, W.B., Yount, J.S., Moran, T.M., Basler, C.F., Komuro, A., Horvath, C.M., et al. (2008). The tumour suppressor CYLD is a negative regulator of RIGI- mediated antiviral response. EMBO Rep. 9, 930-936.
26. Fukushima, T., Matsuzawa, S., Kress, C.L., Bruey, J.M., Krajewska, M., Lefebvre, S., Zapata, J.M., Ronai, Z., and Reed, J.C. (2007). Ubiquitin-conjugating enzyme Ubc13 is a critical component of TNF receptor-associated factor (TRAF)-mediated inflammatory responses. Proc. Natl. Acad. Sci. U. S. A. 104, 6371-6376.
27. Gerlach, B., Cordier, S.M., Schmukle, A.C., Emmerich, C.H., Rieser, E., Haas, T.L., Webb, A.I., Rickard, J.A., Anderton, H., Wong, W.W.-L., et al. (2011). Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471, 591-596.
28. Haas, T.L., Emmerich, C.H., Gerlach, B., Schmukle, A.C., Cordier, S.M., Rieser, E., Feltham, R., Vince, J., Warnken, U., Wenger, T., et al. (2009). Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNFmediated gene induction. Mol. Cell 36, 831-844.
29. Harhaj, E.W., and Dixit, V.M. (2012). Regulation of NF-κB by deubiquitinases. Immunol. Rev. 246, 107-124.
30. Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
31. Hitotsumatsu, O., Ahmad, R.-C., Tavares, R., Wang, M., Philpott, D., Turer, E.E., Lee, B.L., Shiffin, N., Advincula, R., Malynn, B.A., et al. (2008). The ubiquitin-editing enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 28, 381-390.
32. Ikeda, F., Deribe, Y.L., Skånland, S.S., Stieglitz, B., Grabbe, C., Franz-Wachtel, M., van Wijk, S.J.L., Goswami, P., Nagy, V., Terzic, J., et al. (2011). SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature 471, 637-641.
33. Inn, K.-S., Gack, M.U., Tokunaga, F., Shi, M., Wong, L.-Y., Iwai, K., and Jung, J.U. (2011). Linear ubiquitin assembly complex negatively regulates RIG-I- and TRIM25- mediated type I interferon induction. Mol. Cell 41, 354-365.
34. Iwai, K. (2012). Diverse ubiquitin signaling in NF-κB activation. Trends Cell Biol. 22, 355-364.
35. Jiang, X., Kinch, L.N., Brautigam, C.A., Chen, X., Du, F., Grishin, N.V., and Chen, Z.J. (2012). Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36, 959-973.
36. Jono, H., Lim, J.H., Chen, L.-F., Xu, H., Trompouki, E., Pan, Z.K., Mosialos, G., and Li, J.-D. (2004). NF-kappaB is essential for induction of CYLD, the negative regulator of NF-kappaB: evidence for a novel inducible autoregulatory feedback pathway. J. Biol. Chem. 279, 36171-36174.
37. Kaiser, W.J., Sridharan, H., Huang, C., Mandal, P., Upton, J.W., Gough, P.J., Sehon, C.A., Marquis, R.W., Bertin, J., and Mocarski, E.S. (2013). Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J. Biol. Chem. 288, 31268-31279.
38. Kanayama, A., Seth, R.B., Sun, L., Ea, C.-K., Hong, M., Shaito, A., Chiu, Y.-H., Deng, L., and Chen, Z.J. (2004). TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell 15, 535-548.
39. Kayagaki, N., Phung, Q., Chan, S., Chaudhari, R., Quan, C., O’Rourke, K.M., Eby, M., Pietras, E., Cheng, G., Bazan, J.F., et al. (2007). DUBA: a deubiquitinase that regulates type I interferon production. Science 318, 1628-1632.
40. Keusekotten, K., Elliott, P.R., Glockner, L., Fiil, B.K., Damgaard, R.B., Kulathu, Y., Wauer, T., Hospenthal, M.K., Gyrd-Hansen, M., Krappmann, D., et al. (2013). OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 153, 1312-1326.
41. Kho, Y., Kim, S.C., Jiang, C., Barma, D., Kwon, S.W., Cheng, J., Jaunbergs, J., Weinbaum, C., Tamanoi, F., Falck, J., et al. (2004). A tagging-via-substrate technology for detection and proteomics of farnesylated proteins. Proc. Natl. Acad. Sci. U. S. A. 101, 12479-12484.
42. Kirisako, T., Kamei, K., Murata, S., Kato, M., Fukumoto, H., Kanie, M., Sano, S., Tokunaga, F., Tanaka, K., and Iwai, K. (2006). A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25, 4877-4887.
43. Kobayashi, N., Kadono, Y., Naito, A., Matsumoto, K., Yamamoto, T., Tanaka, S., and Inoue, J. (2001). Segregation of TRAF6-mediated signaling pathways clarifies its role in osteoclastogenesis. EMBO J. 20, 1271-1280.
44. Komander, D., Clague, M.J., and Urbé, S. (2009a). Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563.
45. Komander, D., Reyes-Turcu, F., Licchesi, J.D.F., Odenwaelder, P., Wilkinson, K.D., and Barford, D. (2009b). Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10, 466-473.
46. Kovalenko, A., Chable-Bessia, C., Cantarella, G., Israël, A., Wallach, D., and Courtois, G. (2003). The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 424, 801-805.
47. Labbé, K., McIntire, C.R., Doiron, K., Leblanc, P.M., and Saleh, M. (2011). Cellular inhibitors of apoptosis proteins cIAP1 and cIAP2 are required for efficient caspase-1 activation by the inflammasome. Immunity 35, 897-907.
48. Lamothe, B., Besse, A., Campos, A.D., Webster, W.K., Wu, H., and Darnay, B.G. (2007). Site-specific Lys-63-linked tumor necrosis factor receptor-associated factor 6 autoubiquitination is a critical determinant of I kappa B kinase activation. J. Biol. Chem. 282, 4102-4112.
49. Lee, E.G., Boone, D.L., Chai, S., Libby, S.L., Chien, M., Lodolce, J.P., and Ma, A. (2000). Failure to regulate TNFinduced NF-kappaB and cell death responses in A20- deficient mice. Science 289, 2350-2354.
50. Lee, T.H., Shank, J., Cusson, N., and Kelliher, M.A. (2004). The Kinase Activity of Rip1 Is Not Required for Tumor Necrosis Factor-α-induced IκB Kinase or p38 MAP Kinase Activation or for the Ubiquitination of Rip1 by Traf2. J. Biol. Chem. 279, 33185-33191.
51. Lin, R., Yang, L., Nakhaei, P., Sun, Q., Sharif-Askari, E., Julkunen, I., and Hiscott, J. (2006). Negative regulation of the retinoic acid-inducible gene I-induced antiviral state by the ubiquitin-editing protein A20. J. Biol. Chem. 281, 2095-2103.
52. Lin, S.-C., Chung, J.Y., Lamothe, B., Rajashankar, K., Lu, M., Lo, Y.-C., Lam, A.Y., Darnay, B.G., and Wu, H. (2008). Molecular basis for the unique deubiquitinating activity of the NF-kappaB inhibitor A20. J. Mol. Biol. 376, 526-540.
53. Liu, S., Chen, J., Cai, X., Wu, J., Chen, X., Wu, Y.-T., Sun, L., and Chen, Z.J. (2013). MAVS recruits multiple ubiquitin E3 ligases to activate antiviral signaling cascades. eLife 2, e00785.
54. Lomaga, M.A., Yeh, W.C., Sarosi, I., Duncan, G.S., Furlonger, C., Ho, A., Morony, S., Capparelli, C., Van, G., Kaufman, S., et al. (1999). TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13, 1015-1024.
55. Lopez, J., and Meier, P. (2010). To fight or die - inhibitor of apoptosis proteins at the crossroad of innate immunity and death. Curr. Opin. Cell Biol. 22, 872-881.
56. Mahoney, D.J., Cheung, H.H., Mrad, R.L., Plenchette, S., Simard, C., Enwere, E., Arora, V., Mak, T.W., Lacasse, E.C., Waring, J., et al. (2008). Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc. Natl. Acad. Sci. U. S. A. 105, 11778-11783.
57. Mao, A.-P., Li, S., Zhong, B., Li, Y., Yan, J., Li, Q., Teng, C., and Shu, H.-B. (2010). Virus-triggered ubiquitination of TRAF3/6 by cIAP1/2 is essential for induction of interferon-beta (IFN-beta) and cellular antiviral response. J. Biol. Chem. 285, 9470-9476.
58. Matsuzawa, A., Tseng, P.-H., Vallabhapurapu, S., Luo, J.- L., Zhang, W., Wang, H., Vignali, D.A.A., Gallagher, E., and Karin, M. (2008). Essential cytoplasmic translocation of a cytokine receptor-assembled signaling complex. Science 321, 663-668.
59. Michallet, M.-C., Meylan, E., Ermolaeva, M.A., Vazquez, J., Rebsamen, M., Curran, J., Poeck, H., Bscheider, M., Hartmann, G., König, M., et al. (2008). TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 28, 651-661.
60. Micheau, O., and Tschopp, J. (2003). Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181-190.
61. Morris, J.R., and Solomon, E. (2004). BRCA1 : BARD1 induces the formation of conjugated ubiquitin structures, dependent on K6 of ubiquitin, in cells during DNA replication and repair. Hum. Mol. Genet. 13, 807-817.
62. Nijman, S.M.B., Luna-Vargas, M.P.A., Velds, A., Brummelkamp, T.R., Dirac, A.M.G., Sixma, T.K., and Bernards, R. (2005). A Genomic and Functional Inventory of Deubiquitinating Enzymes. Cell 123, 773-786.
63. Pickart, C.M. (2001). Mechanisms under lying ubiquitination. Annu. Rev. Biochem. 70, 503-533.
64. Prakash, H., Albrecht, M., Becker, D., Kuhlmann, T., and Rudel, T. (2010). Deficiency of XIAP leads to sensitization for Chlamydophila pneumoniae pulmonary infection and dysregulation of innate immune response in mice. J. Biol. Chem. 285, 20291-20302.
65. Py, B.F., Kim, M.-S., Vakifahmetoglu-Norberg, H., and Yuan, J. (2013). Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol. Cell 49, 331-338.
66. Rajput, A., Kovalenko, A., Bogdanov, K., Yang, S.-H., Kang, T.-B., Kim, J.-C., Du, J., and Wallach, D. (2011). RIG-I RNA helicase activation of IRF3 transcription factor is negatively regulated by caspase-8-mediated cleavage of the RIP1 protein. Immunity 34, 340-351.
67. Reyes-Turcu, F.E., Ventii, K.H., and Wilkinson, K.D. (2009). Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78, 363-397.
68. Rotin, D., and Kumar, S. (2009). Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10, 398-409.
69. Sasaki, Y., Sano, S., Nakahara, M., Murata, S., Kometani, K., Aiba, Y., Sakamoto, S., Watanabe, Y., Tanaka, K., Kurosaki, T., et al. (2013). Defective immune responses in mice lacking LUBAC-mediated linear ubiquitination in B cells. EMBO J. 32, 2463-2476.
70. Shembade, N., Harhaj, N.S., Liebl, D.J., and Harhaj, E.W. (2007). Essential role for TAX1BP1 in the termination of TNF-alpha-, IL-1- and LPS-mediated NF-kappaB and JNK signaling. EMBO J. 26, 3910-3922.
71. Shembade, N., Harhaj, N.S., Parvatiyar, K., Copeland, N.G., Jenkins, N.A., Matesic, L.E., and Harhaj, E.W. (2008). The E3 ligase Itch negatively regulates inflammatory signaling pathways by controlling the function of the ubiquitin-editing enzyme A20. Nat. Immunol. 9, 254-262.
72. Shembade, N., Parvatiyar, K., Harhaj, N.S., and Harhaj, E.W. (2009). The ubiquitin-editing enzyme A20 requires RNF11 to downregulate NF-kappaB signalling. EMBO J. 28, 513-522.
73. Shembade, N., Ma, A., and Harhaj, E.W. (2010a). Inhibition of NF-κB Signaling by A20 Through Disruption of Ubiquitin Enzyme Complexes. Science 327, 1135-1139.
74. Shembade, N., Ma, A., and Harhaj, E.W. (2010b). Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 327, 1135-1139.
75. Smit, J.J., Monteferrario, D., Noordermeer, S.M., van Dijk, W.J., van der Reijden, B.A., and Sixma, T.K. (2012). The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J. 31, 3833-3844.
76. Sun, S.-C. (2010). CYLD: a tumor suppressor deubiquitinase regulating NF-kappaB activation and diverse biological processes. Cell Death Differ. 17, 25-34.
77. Sun, W., Tan, X., Shi, Y., Xu, G., Mao, R., Gu, X., Fan, Y., Yu, Y., Burlingame, S., Zhang, H., et al. (2010). USP11 negatively regulates TNFalpha-induced NF-kappaB activation by targeting on IkappaBalpha. Cell. Signal. 22, 386-394.
78. Takahashi, K., Kawai, T., Kumar, H., Sato, S., Yonehara, S., and Akira, S. (2006). Cutting Edge: Roles of Caspase-8 and Caspase-10 in Innate Immune Responses to Double-Stranded RNA. J. Immunol. 176, 4520-4524.
79. Takeda, K., Kaisho, T., and Akira, S. (2003). Toll-Like Receptors. Annu. Rev. Immunol. 21, 335-376.
80. Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820.
81. Tokunaga, F., Sakata, S., Saeki, Y., Satomi, Y., Kirisako, T., Kamei, K., Nakagawa, T., Kato, M., Murata, S., Yamaoka, S., et al. (2009). Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 11, 123-132.
82. Tokunaga, F., Nakagawa, T., Nakahara, M., Saeki, Y., Taniguchi, M., Sakata, S., Tanaka, K., Nakano, H., and Iwai, K. (2011). SHARPIN is a component of the NF-κBactivating linear ubiquitin chain assembly complex. Nature 471, 633-636.
83. Tokunaga, F., Nishimasu, H., Ishitani, R., Goto, E., Noguchi, T., Mio, K., Kamei, K., Ma, A., Iwai, K., and Nureki, O. (2012). Specific recognition of linear polyubiquitin by A20 zinc finger 7 is involved in NF-κB regulation. EMBO J. 31, 3856-3870.
84. Trompouki, E., Hatzivassiliou, E., Tsichritzis, T., Farmer, H., Ashworth, A., and Mosialos, G. (2003). CYLD is a deubiquitinating enzyme that negatively regulates NFkappaB activation by TNFR family members. Nature 424, 793-796.
85. Tseng, P.-H., Matsuzawa, A., Zhang, W., Mino, T., Vignali, D.A.A., and Karin, M. (2010). Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat. Immunol. 11, 70-75.
86. Tzimas, C., Michailidou, G., Arsenakis, M., Kieff, E., Mosialos, G., and Hatzivassiliou, E.G. (2006). Human ubiquitin specific protease 31 is a deubiquitinating enzyme implicated in activation of nuclear factor-kappaB. Cell. Signal. 18, 83-92.
87. Vallabhapurapu, S., and Karin, M. (2009). Regulation and Function of NF-κB Transcription Factors in the Immune System. Annu. Rev. Immunol. 27, 693-733.
88. Varfolomeev, E., Goncharov, T., Fedorova, A.V., Dynek, J.N., Zobel, K., Deshayes, K., Fairbrother, W.J., and Vucic, D. (2008). c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)- induced NF-kappaB activation. J. Biol. Chem. 283, 24295-24299.
89. Verhelst, K., Carpentier, I., Kreike, M., Meloni, L., Verstrepen, L., Kensche, T., Dikic, I., and Beyaert, R. (2012). A20 inhibits LUBAC-mediated NF-κB activation by binding linear polyubiquitin chains via its zinc finger 7. EMBO J. 31, 3845-3855.
90. Vince, J.E., Wong, W.W.-L., Gentle, I., Lawlor, K.E., Allam, R., O’Reilly, L., Mason, K., Gross, O., Ma, S., Guarda, G., et al. (2012). Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36, 215-227.
91. Wang, C., Deng, L., Hong, M., Akkaraju, G.R., Inoue, J., and Chen, Z.J. (2001). TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351.
92. Wenzel, D.M., Lissounov, A., Brzovic, P.S., and Klevit, R.E. (2011). UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 474, 105-108.
93. Wertz, I.E., O’Rourke, K.M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., Wu, P., Wiesmann, C., Baker, R., Boone, D.L., et al. (2004). De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430, 694-699.
94. Wickliffe, K.E., Williamson, A., Meyer, H.-J., Kelly, A., and Rape, M. (2011). K11-linked ubiquitin chains as novel regulators of cell division. Trends Cell Biol. 21, 656-663.
95. Windheim, M., Stafford, M., Peggie, M., and Cohen, P. (2008). 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, 1783-1791.
96. Wu, C.-J., Conze, D.B., Li, T., Srinivasula, S.M., and Ashwell, J.D. (2006). Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat. Cell Biol. 8, 398-406.
97. Xia, Z.-P., Sun, L., Chen, X., Pineda, G., Jiang, X., Adhikari, A., Zeng, W., and Chen, Z.J. (2009). Direct Activation of Protein Kinases by Unanchored Polyubiquitin Chains. Nature 461, 114-119.
98. Xu, G., Tan, X., Wang, H., Sun, W., Shi, Y., Burlingame, S., Gu, X., Cao, G., Zhang, T., Qin, J., et al. (2010). Ubiquitin-specific peptidase 21 inhibits tumor necrosis factor alpha-induced nuclear factor kappaB activation via binding to and deubiquitinating receptor-interacting protein 1. J. Biol. Chem. 285, 969-978.
99. Xu, M., Skaug, B., Zeng, W., and Chen, Z.J. (2009). A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta. Mol. Cell 36, 302-314.
100. Yamaguchi, T., Kimura, J., Miki, Y., and Yoshida, K. (2007). The deubiquitinating enzyme USP11 controls an IkappaB kinase alpha (IKKalpha)-p53 signaling pathway in response to tumor necrosis factor alpha (TNFalpha). J. Biol. Chem. 282, 33943-33948.
101. Yamamoto, M., Okamoto, T., Takeda, K., Sato, S., Sanjo, H., Uematsu, S., Saitoh, T., Yamamoto, N., Sakurai, H., Ishii, K.J., et al. (2006). Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat. Immunol. 7, 962-970.
102. You, F., Sun, H., Zhou, X., Sun, W., Liang, S., Zhai, Z., and Jiang, Z. (2009). PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat. Immunol. 10, 1300-1308.
103. Zak, D.E., Schmitz, F., Gold, E.S., Diercks, A.H., Peschon, J.J., Valvo, J.S., Niemistö, A., Podolsky, I., Fallen, S.G., Suen, R., et al. (2011). Systems analysis identifies an essential role for SHANK-associated RH domaininteracting protein (SHARPIN) in macrophage Toll-like receptor 2 (TLR2) responses. Proc. Natl. Acad. Sci. U. S. A. 108, 11536-11541.
104. Zhang, M., Wu, X., Lee, A.J., Jin, W., Chang, M., Wright, A., Imaizumi, T., and Sun, S.-C. (2008). Regulation of IkappaB kinase-related kinases and antiviral responses by tumor suppressor CYLD. J. Biol. Chem. 283, 18621-18626.
105. Zhong, B., Liu, X., Wang, X., Liu, X., Li, H., Darnay, B.G., Lin, X., Sun, S.-C., and Dong, C. (2013). Ubiquitinspecific protease 25 regulates TLR4-dependent innate immune responses through deubiquitination of the adaptor protein TRAF3. Sci. Signal. 6, ra35.
106. Zhou, F., Zhang, X., van Dam, H., Ten Dijke, P., Huang, H., and Zhang, L. (2012). Ubiquitin-specific protease 4 mitigates Toll-like/interleukin-1 receptor signaling and regulates innate immune activation. J. Biol. Chem. 287, 11002-11010.
107. Zinngrebe, J., Montinaro, A., Peltzer, N., and Walczak, H. (2014). Ubiquitin in the immune system. EMBO Rep. 15, 28-45.