The Role of Ubiquitination in NF-κB Signaling during Virus Infection
Abstract
:1. Introduction
2. NF-κB Signaling Pathways
3. Ubiquitination
3.1. Ubiquitination Process
3.2. Ubiquitination Types
3.2.1. K48-Linked Polyubiquitination
3.2.2. K63-Linked Polyubiquitination
3.2.3. Met1-Linked Polyubiquitination
3.2.4. Unanchored Polyubiquitin
4. Ubiquitination in NF-κB Signaling Pathways
4.1. Ubiquitination in the TNFR1 Signaling Pathway
4.2. Ubiquitination in the RIG-I Signaling Pathway
5. Modulation of the Ubiquitination in NF-κB Pathways by Viruses
5.1. Virus-Mediated Inhibition of NF-κB Signaling by Modulation of Ubiquitination
5.1.1. Virus-Encoded E3 Ligases and DUBs
5.1.2. Viruses Hijack Host Proteolytic Ubiquitination
5.1.3. Viruses Subverts Host K63-Linked and Met1-Linked Ubiquitination
5.2. Virus-Mediated Activation of NF-κB Signaling by Modulation of Ubiquitination
6. Conclusions and Perspectives
Author Contributions
Funding
Conflicts of Interest
References
- Hayden, M.S.; Ghosh, S. NF-kappaB, the first quarter-century: Remarkable progress and outstanding questions. Genes Dev. 2012, 26, 203–234. [Google Scholar] [CrossRef] [Green Version]
- Patil, G.; Li, S. Tripartite motif proteins: An emerging antiviral protein family. Future Virol. 2019, 14, 107–122. [Google Scholar] [CrossRef] [PubMed]
- Henkel, T.; Zabel, U.; van Zee, K.; Muller, J.M.; Fanning, E.; Baeuerle, P.A. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-kappa B subunit. Cell 1992, 68, 1121–1133. [Google Scholar] [CrossRef]
- Hinz, M.; Scheidereit, C. The IkappaB kinase complex in NF-kappaB regulation and beyond. EMBO Rep. 2014, 15, 46–61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, S.C. The non-canonical NF-kappaB pathway in immunity and inflammation. Nat. Rev. Immunol. 2017, 17, 545–558. [Google Scholar] [CrossRef] [PubMed]
- Iwai, K. Diverse ubiquitin signaling in NF-kappaB activation. Trends Cell Biol. 2012, 22, 355–364. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Chen, Z.J. Regulation of NF-kappaB by ubiquitination. Curr. Opin. Immunol. 2013, 25, 4–12. [Google Scholar] [CrossRef] [Green Version]
- McClellan, A.J.; Laugesen, S.H.; Ellgaard, L. Cellular functions and molecular mechanisms of non-lysine ubiquitination. Open Biol. 2019, 9, 190147. [Google Scholar] [CrossRef] [Green Version]
- Berndsen, C.E.; Wolberger, C. New insights into ubiquitin E3 ligase mechanism. Nat. Struct. Mol. Biol. 2014, 21, 301–307. [Google Scholar] [CrossRef]
- Komander, D.; Rape, M. The Ubiquitin Code. Annu. Rev. Biochem. 2012, 81, 203–229. [Google Scholar] [CrossRef] [Green Version]
- Collins, P.E.; Mitxitorena, I.; Carmody, R.J. The Ubiquitination of NF-kappaB Subunits in the Control of Transcription. Cells 2016, 5, 23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nijman, S.M.; Luna-Vargas, M.P.; Velds, A.; Brummelkamp, T.R.; Dirac, A.M.; Sixma, T.K.; Bernards, R. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005, 123, 773–786. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fiil, B.K.; Damgaard, R.B.; Wagner, S.A.; Keusekotten, K.; Fritsch, M.; Bekker-Jensen, S.; Mailand, N.; Choudhary, C.; Komander, D.; Gyrd-Hansen, M. OTULIN restricts Met1-linked ubiquitination to control innate immune signaling. Mol. Cell 2013, 50, 818–830. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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. OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 2013, 153, 1312–1326. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akutsu, M.; Dikic, I.; Bremm, A. Ubiquitin chain diversity at a glance. J. Cell Sci. 2016, 129, 875–880. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yuan, W.C.; Lee, Y.R.; Lin, S.Y.; Chang, L.Y.; Tan, Y.P.; Hung, C.C.; Kuo, J.C.; Liu, C.H.; Lin, M.Y.; Xu, M.; et al. K33-Linked Polyubiquitination of Coronin 7 by Cul3-KLHL20 Ubiquitin E3 Ligase Regulates Protein Trafficking. Mol. Cell 2014, 54, 586–600. [Google Scholar] [CrossRef] [Green Version]
- Spencer, E.; Jiang, J.; Chen, Z.J. Signal-induced ubiquitination of IkappaBalpha by the F-box protein Slimb/beta-TrCP. Genes Dev. 1999, 13, 284–294. [Google Scholar] [CrossRef] [Green Version]
- Winston, J.T.; Strack, P.; Beer-Romero, P.; Chu, C.Y.; Elledge, S.J.; Harper, J.W. The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and beta-catenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev. 1999, 13, 270–283. [Google Scholar] [CrossRef]
- Schweitzer, K.; Bozko, P.M.; Dubiel, W.; Naumann, M. CSN controls NF-kappaB by deubiquitinylation of IkappaBalpha. EMBO J. 2007, 26, 1532–1541. [Google Scholar] [CrossRef]
- Sun, W.; Tan, X.; Shi, Y.; Xu, G.; Mao, R.; Gu, X.; Fan, Y.; Yu, Y.; Burlingame, S.; Zhang, H.; et al. USP11 negatively regulates TNFalpha-induced NF-kappaB activation by targeting on IkappaBalpha. Cell Signal. 2010, 22, 386–394. [Google Scholar] [CrossRef] [Green Version]
- Fukushima, H.; Matsumoto, A.; Inuzuka, H.; Zhai, B.; Lau, A.W.; Wan, L.; Gao, D.; Shaik, S.; Yuan, M.; Gygi, S.P.; et al. SCF(Fbw7) modulates the NFkB signaling pathway by targeting NFkB2 for ubiquitination and destruction. Cell Rep. 2012, 1, 434–443. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Busino, L.; Millman, S.E.; Scotto, L.; Kyratsous, C.A.; Basrur, V.; O’Connor, O.; Hoffmann, A.; Elenitoba-Johnson, K.S.; Pagano, M. Fbxw7alpha- and GSK3-mediated degradation of p100 is a pro-survival mechanism in multiple myeloma. Nat. Cell Biol. 2012, 14, 375–385. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamamoto, M.; Okamoto, T.; Takeda, K.; Sato, S.; Sanjo, H.; Uematsu, S.; Saitoh, T.; Yamamoto, N.; Sakurai, H.; Ishii, K.J.; et al. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat. Immunol. 2006, 7, 962–970. [Google Scholar] [CrossRef] [PubMed]
- Yamazaki, K.; Gohda, J.; Kanayama, A.; Miyamoto, Y.; Sakurai, H.; Yamamoto, M.; Akira, S.; Hayashi, H.; Su, B.; Inoue, J. Two mechanistically and temporally distinct NF-kappaB activation pathways in IL-1 signaling. Sci. Signal. 2009, 2, ra66. [Google Scholar] [CrossRef]
- Xu, M.; Skaug, B.; Zeng, W.; Chen, Z.J. A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta. Mol. Cell 2009, 36, 302–314. [Google Scholar] [CrossRef] [Green Version]
- Iwai, K.; Tokunaga, F. Linear polyubiquitination: A new regulator of NF-kappaB activation. EMBO Rep. 2009, 10, 706–713. [Google Scholar] [CrossRef] [Green Version]
- 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. Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol. Cell 2009, 36, 831–844. [Google Scholar] [CrossRef]
- Tokunaga, F.; Sakata, S.; Saeki, Y.; Satomi, Y.; Kirisako, T.; Kamei, K.; Nakagawa, T.; Kato, M.; Murata, S.; Yamaoka, S.; et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 2009, 11, 123–132. [Google Scholar] [CrossRef]
- Tokunaga, F.; Nakagawa, T.; Nakahara, M.; Saeki, Y.; Taniguchi, M.; Sakata, S.; Tanaka, K.; Nakano, H.; Iwai, K. SHARPIN is a component of the NF-kappaB-activating linear ubiquitin chain assembly complex. Nature 2011, 471, 633–636. [Google Scholar] [CrossRef]
- Ikeda, F.; Deribe, Y.L.; Skanland, S.S.; Stieglitz, B.; Grabbe, C.; Franz-Wachtel, M.; van Wijk, S.J.; Goswami, P.; Nagy, V.; Terzic, J.; et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappaB activity and apoptosis. Nature 2011, 471, 637–641. [Google Scholar] [CrossRef]
- 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.; et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 2011, 471, 591–596. [Google Scholar] [CrossRef] [PubMed]
- Fu, B.; Li, S.; Wang, L.; Berman, M.A.; Dorf, M.E. The ubiquitin conjugating enzyme UBE2L3 regulates TNFalpha-induced linear ubiquitination. Cell Res. 2014, 24, 376–379. [Google Scholar] [CrossRef] [PubMed]
- Inn, K.S.; Gack, M.U.; Tokunaga, F.; Shi, M.; Wong, L.Y.; Iwai, K.; Jung, J.U. Linear ubiquitin assembly complex negatively regulates RIG-I- and TRIM25-mediated type I interferon induction. Mol. Cell 2011, 41, 354–365. [Google Scholar] [CrossRef] [Green Version]
- Xia, Z.P.; Sun, L.; Chen, X.; Pineda, G.; Jiang, X.; Adhikari, A.; Zeng, W.; Chen, Z.J. Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 2009, 461, 114–119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zeng, W.; Sun, L.; Jiang, X.; Chen, X.; Hou, F.; Adhikari, A.; Xu, M.; Chen, Z.J. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010, 141, 315–330. [Google Scholar] [CrossRef] [Green Version]
- Enesa, K.; Zakkar, M.; Chaudhury, H.; Luong, L.A.; Rawlinson, L.; Mason, J.C.; Haskard, D.O.; Dean, J.L.; Evans, P.C. NF-kappaB suppression by the deubiquitinating enzyme Cezanne: A novel negative feedback loop in pro-inflammatory signaling. J. Biol. Chem. 2008, 283, 7036–7045. [Google Scholar] [CrossRef] [Green Version]
- Xu, G.; Tan, X.; Wang, H.; Sun, W.; Shi, Y.; Burlingame, S.; Gu, X.; Cao, G.; Zhang, T.; Qin, J.; et al. 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. 2010, 285, 969–978. [Google Scholar] [CrossRef] [Green Version]
- Tzimas, C.; Michailidou, G.; Arsenakis, M.; Kieff, E.; Mosialos, G.; Hatzivassiliou, E.G. Human ubiquitin specific protease 31 is a deubiquitinating enzyme implicated in activation of nuclear factor-kappaB. Cell Signal. 2006, 18, 83–92. [Google Scholar] [CrossRef]
- Daubeuf, S.; Singh, D.; Tan, Y.; Liu, H.; Federoff, H.J.; Bowers, W.J.; Tolba, K. HSV ICP0 recruits USP7 to modulate TLR-mediated innate response. Blood 2009, 113, 3264–3275. [Google Scholar] [CrossRef] [Green Version]
- Liang, J.; Saad, Y.; Lei, T.; Wang, J.; Qi, D.; Yang, Q.; Kolattukudy, P.E.; Fu, M. MCP-induced protein 1 deubiquitinates TRAF proteins and negatively regulates JNK and NF-kappaB signaling. J. Exp. Med. 2010, 207, 2959–2973. [Google Scholar] [CrossRef] [Green Version]
- Metzig, M.; Nickles, D.; Falschlehner, C.; Lehmann-Koch, J.; Straub, B.K.; Roth, W.; Boutros, M. An RNAi screen identifies USP2 as a factor required for TNF-alpha-induced NF-kappaB signaling. Int. J. Cancer 2011, 129, 607–618. [Google Scholar] [CrossRef] [PubMed]
- Elliott, P.R.; Nielsen, S.V.; Marco-Casanova, P.; Fiil, B.K.; Keusekotten, K.; Mailand, N.; Freund, S.M.; Gyrd-Hansen, M.; Komander, D. Molecular basis and regulation of OTULIN-LUBAC interaction. Mol. Cell 2014, 54, 335–348. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schaeffer, V.; Akutsu, M.; Olma, M.H.; Gomes, L.C.; Kawasaki, M.; Dikic, I. Binding of OTULIN to the PUB domain of HOIP controls NF-kappaB signaling. Mol. Cell 2014, 54, 349–361. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, M.; Song, K.; Hao, W.; Wang, L.; Patil, G.; Li, Q.; Xu, L.; Hua, F.; Fu, B.; Schwamborn, J.C.; et al. Non-proteolytic ubiquitination of OTULIN regulates NF-kappaB signaling pathway. J. Mol. Cell Biol. 2019. [Google Scholar] [CrossRef]
- Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell 2010, 140, 805–820. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilkins, C.; Gale, M., Jr. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 2010, 22, 41–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pichlmair, A.; Schulz, O.; Tan, C.P.; Naslund, T.I.; Liljestrom, P.; Weber, F.; Reis e Sousa, C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 2006, 314, 997–1001. [Google Scholar] [CrossRef] [Green Version]
- Hornung, V.; Ellegast, J.; Kim, S.; Brzozka, K.; Jung, A.; Kato, H.; Poeck, H.; Akira, S.; Conzelmann, K.K.; Schlee, M.; et al. 5’-Triphosphate RNA is the ligand for RIG-I. Science 2006, 314, 994–997. [Google Scholar] [CrossRef] [Green Version]
- Yoneyama, M.; Kikuchi, M.; Natsukawa, T.; Shinobu, N.; Imaizumi, T.; Miyagishi, M.; Taira, K.; Akira, S.; Fujita, T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5, 730–737. [Google Scholar] [CrossRef]
- Kang, D.C.; Gopalkrishnan, R.V.; Wu, Q.; Jankowsky, E.; Pyle, A.M.; Fisher, P.B. mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. USA 2002, 99, 637–642. [Google Scholar] [CrossRef] [Green Version]
- Kato, H.; Takeuchi, O.; Sato, S.; Yoneyama, M.; Yamamoto, M.; Matsui, K.; Uematsu, S.; Jung, A.; Kawai, T.; Ishii, K.J.; et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441, 101–105. [Google Scholar] [CrossRef] [PubMed]
- Cui, S.; Eisenacher, K.; Kirchhofer, A.; Brzozka, K.; Lammens, A.; Lammens, K.; Fujita, T.; Conzelmann, K.K.; Krug, A.; Hopfner, K.P. The C-terminal regulatory domain is the RNA 5’-triphosphate sensor of RIG-I. Mol. Cell 2008, 29, 169–179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sharma, S.; tenOever, B.R.; Grandvaux, N.; Zhou, G.P.; Lin, R.; Hiscott, J. Triggering the interferon antiviral response through an IKK-related pathway. Science 2003, 300, 1148–1151. [Google Scholar] [CrossRef] [PubMed]
- Fitzgerald, K.A.; McWhirter, S.M.; Faia, K.L.; Rowe, D.C.; Latz, E.; Golenbock, D.T.; Coyle, A.J.; Liao, S.M.; Maniatis, T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4, 491–496. [Google Scholar] [CrossRef] [PubMed]
- Hemmi, H.; Takeuchi, O.; Sato, S.; Yamamoto, M.; Kaisho, T.; Sanjo, H.; Kawai, T.; Hoshino, K.; Takeda, K.; Akira, S. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 2004, 199, 1641–1650. [Google Scholar] [CrossRef] [Green Version]
- McWhirter, S.M.; Fitzgerald, K.A.; Rosains, J.; Rowe, D.C.; Golenbock, D.T.; Maniatis, T. IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. USA 2004, 101, 233–238. [Google Scholar] [CrossRef] [Green Version]
- Tanaka, Y.; Chen, Z.J. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 2012, 5, ra20. [Google Scholar] [CrossRef] [Green Version]
- Takeuchi, O.; Akira, S. Innate immunity to virus infection. Immunol. Rev. 2009, 227, 75–86. [Google Scholar] [CrossRef]
- Gack, M.U.; Shin, Y.C.; Joo, C.H.; Urano, T.; Liang, C.; Sun, L.; Takeuchi, O.; Akira, S.; Chen, Z.; Inoue, S.; et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007, 446, 916–920. [Google Scholar] [CrossRef]
- Kuniyoshi, K.; Takeuchi, O.; Pandey, S.; Satoh, T.; Iwasaki, H.; Akira, S.; Kawai, T. Pivotal role of RNA-binding E3 ubiquitin ligase MEX3C in RIG-I-mediated antiviral innate immunity. Proc. Natl. Acad. Sci. USA 2014, 111, 5646–5651. [Google Scholar] [CrossRef] [Green Version]
- Yan, J.; Li, Q.; Mao, A.P.; Hu, M.M.; Shu, H.B. TRIM4 modulates type I interferon induction and cellular antiviral response by targeting RIG-I for K63-linked ubiquitination. J. Mol. Cell Biol. 2014, 6, 154–163. [Google Scholar] [CrossRef] [PubMed]
- Cadena, C.; Ahmad, S.; Xavier, A.; Willemsen, J.; Park, S.; Park, J.W.; Oh, S.W.; Fujita, T.; Hou, F.; Binder, M.; et al. Ubiquitin-Dependent and -Independent Roles of E3 Ligase RIPLET in Innate Immunity. Cell 2019, 177, 1187–1200.e1116. [Google Scholar] [CrossRef] [PubMed]
- Oshiumi, H.; Miyashita, M.; Inoue, N.; Okabe, M.; Matsumoto, M.; Seya, T. The Ubiquitin Ligase Riplet Is Essential for RIG-I-Dependent Innate Immune Responses to RNA Virus Infection. Cell Host Microbe 2010, 8, 496–509. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hayman, T.J.; Hsu, A.C.; Kolesnik, T.B.; Dagley, L.F.; Willemsen, J.; Tate, M.D.; Baker, P.J.; Kershaw, N.J.; Kedzierski, L.; Webb, A.I.; et al. RIPLET, and not TRIM25, is required for endogenous RIG-I-dependent antiviral responses. Immunol. Cell Biol. 2019, 97, 840–852. [Google Scholar] [CrossRef] [PubMed]
- Oshiumi, H.; Matsumoto, M.; Hatakeyama, S.; Seya, T. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J. Biol Chem 2009, 284, 807–817. [Google Scholar] [CrossRef] [Green Version]
- Jiang, X.; Kinch, L.N.; Brautigam, C.A.; Chen, X.; Du, F.; Grishin, N.V.; Chen, Z.J. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 2012, 36, 959–973. [Google Scholar] [CrossRef] [Green Version]
- Cui, J.; Song, Y.; Li, Y.; Zhu, Q.; Tan, P.; Qin, Y.; Wang, H.Y.; Wang, R.F. USP3 inhibits type I interferon signaling by deubiquitinating RIG-I-like receptors. Cell Res. 2014, 24, 400–416. [Google Scholar] [CrossRef] [Green Version]
- Fan, Y.; Mao, R.; Yu, Y.; Liu, S.; Shi, Z.; Cheng, J.; Zhang, H.; An, L.; Zhao, Y.; Xu, X.; et al. USP21 negatively regulates antiviral response by acting as a RIG-I deubiquitinase. J. Exp. Med. 2014, 211, 313–328. [Google Scholar] [CrossRef] [Green Version]
- Friedman, C.S.; O’Donnell, M.A.; Legarda-Addison, D.; Ng, A.; Cardenas, W.B.; Yount, J.S.; Moran, T.M.; Basler, C.F.; Komuro, A.; Horvath, C.M.; et al. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. Embo Rep. 2008, 9, 930–936. [Google Scholar] [CrossRef]
- Lin, W.; Zhang, J.; Lin, H.Y.; Li, Z.X.; Sun, X.F.; Xin, D.; Yang, M.; Sun, L.W.; Li, L.; Wang, H.M.; et al. Syndecan-4 negatively regulates antiviral signalling by mediating RIG-I deubiquitination via CYLD. Nat. Commun. 2016, 7. [Google Scholar] [CrossRef] [Green Version]
- Wang, W.D.; Jiang, M.H.; Liu, S.; Zhang, S.K.; Liu, W.; Ma, Y.W.; Zhang, L.F.; Zhang, J.Y.; Cao, X.T. RNF122 suppresses antiviral type I interferon production by targeting RIG-I CARDs to mediate RIG-I degradation. Proc. Natl. Acad. Sci. USA 2016, 113, 9581–9586. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arimoto, K.I.; Takahashi, H.; Hishiki, T.; Konishi, H.; Fujita, T.; Shimotohno, K. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. USA 2007, 104, 7500–7505. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, K.; Zhang, Q.; Li, X.; Zhao, D.; Liu, Y.; Shen, Q.; Yang, M.; Wang, C.; Li, N.; Cao, X. Cytoplasmic STAT4 Promotes Antiviral Type I IFN Production by Blocking CHIP-Mediated Degradation of RIG-I. J. Immunol. 2016, 196, 1209–1217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, W.; Han, C.; Xie, B.; Hu, X.; Yu, Q.; Shi, L.; Wang, Q.; Li, D.; Wang, J.; Zheng, P.; et al. Induction of Siglec-G by RNA viruses inhibits the innate immune response by promoting RIG-I degradation. Cell 2013, 152, 467–478. [Google Scholar] [CrossRef] [Green Version]
- Zhao, C.; Jia, M.; Song, H.; Yu, Z.; Wang, W.; Li, Q.; Zhang, L.; Zhao, W.; Cao, X. The E3 Ubiquitin Ligase TRIM40 Attenuates Antiviral Immune Responses by Targeting MDA5 and RIG-I. Cell Rep. 2017, 21, 1613–1623. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.J.; Zhao, W.; Zhang, M.; Wang, P.; Zhao, K.; Zhao, X.Y.; Yang, S.R.; Gao, C.J. USP4 Positively Regulates RIG-I-Mediated Antiviral Response through Deubiquitination and Stabilization of RIG-I. J. Virol. 2013, 87, 4507–4515. [Google Scholar] [CrossRef] [Green Version]
- Pauli, E.K.; Chan, Y.K.; Davis, M.E.; Gableske, S.; Wang, M.K.; Feister, K.F.; Gack, M.U. The ubiquitin-specific protease USP15 promotes RIG-I-mediated antiviral signaling by deubiquitylating TRIM25. Sci. Signal. 2014, 7, ra3. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Tong, X.; Ye, X. Ndfip1 negatively regulates RIG-I-dependent immune signaling by enhancing E3 ligase Smurf1-mediated MAVS degradation. J. Immunol. 2012, 189, 5304–5313. [Google Scholar] [CrossRef] [Green Version]
- Pan, Y.; Li, R.; Meng, J.L.; Mao, H.T.; Zhang, Y.; Zhang, J. Smurf2 negatively modulates RIG-I-dependent antiviral response by targeting VISA/MAVS for ubiquitination and degradation. J. Immunol. 2014, 192, 4758–4764. [Google Scholar] [CrossRef] [Green Version]
- Yoo, Y.S.; Park, Y.Y.; Kim, J.H.; Cho, H.; Kim, S.H.; Lee, H.S.; Kim, T.H.; Sun Kim, Y.; Lee, Y.; Kim, C.J.; et al. The mitochondrial ubiquitin ligase MARCH5 resolves MAVS aggregates during antiviral signalling. Nat. Commun. 2015, 6, 7910. [Google Scholar] [CrossRef] [Green Version]
- Castanier, C.; Zemirli, N.; Portier, A.; Garcin, D.; Bidere, N.; Vazquez, A.; Arnoult, D. MAVS ubiquitination by the E3 ligase TRIM25 and degradation by the proteasome is involved in type I interferon production after activation of the antiviral RIG-I-like receptors. BMC Biol. 2012, 10, 44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- You, F.; Sun, H.; Zhou, X.; Sun, W.; Liang, S.; Zhai, Z.; Jiang, Z. PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat. Immunol. 2009, 10, 1300–1308. [Google Scholar] [CrossRef] [PubMed]
- Du, J.; Zhang, D.; Zhang, W.; Ouyang, G.; Wang, J.; Liu, X.; Li, S.; Ji, W.; Liu, W.; Xiao, W. pVHL Negatively Regulates Antiviral Signaling by Targeting MAVS for Proteasomal Degradation. J. Immunol. 2015, 195, 1782–1790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, B.; Zhang, M.; Chu, H.; Zhang, H.; Wu, H.; Song, G.; Wang, P.; Zhao, K.; Hou, J.; Wang, X.; et al. The ubiquitin E3 ligase TRIM31 promotes aggregation and activation of the signaling adaptor MAVS through Lys63-linked polyubiquitination. Nat. Immunol. 2017, 18, 214–224. [Google Scholar] [CrossRef] [PubMed]
- Xue, B.; Li, H.; Guo, M.; Wang, J.; Xu, Y.; Zou, X.; Deng, R.; Li, G.; Zhu, H. TRIM21 Promotes Innate Immune Response to RNA Viral Infection through Lys27-Linked Polyubiquitination of MAVS. J. Virol. 2018, 92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liuyu, T.; Yu, K.; Ye, L.; Zhang, Z.; Zhang, M.; Ren, Y.; Cai, Z.; Zhu, Q.; Lin, D.; Zhong, B. Induction of OTUD4 by viral infection promotes antiviral responses through deubiquitinating and stabilizing MAVS. Cell Res. 2019, 29, 67–79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, C.; Huang, S.; Wang, X.; Wen, M.; Zheng, J.; Wang, W.; Fu, Y.; Tian, S.; Li, L.; Li, Z.; et al. The Otubain YOD1 Suppresses Aggregation and Activation of the Signaling Adaptor MAVS through Lys63-Linked Deubiquitination. J. Immunol. 2019, 202, 2957–2970. [Google Scholar] [CrossRef]
- Yang, B.; Wang, J.; Wang, Y.; Zhou, H.; Wu, X.; Tian, Z.; Sun, B. Novel function of Trim44 promotes an antiviral response by stabilizing VISA. J. Immunol. 2013, 190, 3613–3619. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Z.; Jia, X.; Xue, Q.; Dou, Z.; Ma, Y.; Zhao, Z.; Jiang, Z.; He, B.; Jin, Q.; Wang, J. TRIM14 is a mitochondrial adaptor that facilitates retinoic acid-inducible gene-I-like receptor-mediated innate immune response. Proc. Natl. Acad. Sci. USA 2014, 111, E245. [Google Scholar] [CrossRef] [Green Version]
- Jin, S.; Tian, S.; Luo, M.; Xie, W.; Liu, T.; Duan, T.; Wu, Y.; Cui, J. Tetherin Suppresses Type I Interferon Signaling by Targeting MAVS for NDP52-Mediated Selective Autophagic Degradation in Human Cells. Mol. Cell 2017, 68, 308–322 e304. [Google Scholar] [CrossRef] [Green Version]
- He, X.; Zhu, Y.; Zhang, Y.; Geng, Y.; Gong, J.; Geng, J.; Zhang, P.; Zhang, X.; Liu, N.; Peng, Y.; et al. RNF34 functions in immunity and selective mitophagy by targeting MAVS for autophagic degradation. EMBO J. 2019, 38, e100978. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Wang, L.; Berman, M.; Kong, Y.Y.; Dorf, M.E. Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 2011, 35, 426–440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, G.; Liu, B.; Li, Z.; Wu, H.; Wang, P.; Zhao, K.; Jiang, G.; Zhang, L.; Gao, C. E3 ubiquitin ligase RNF128 promotes innate antiviral immunity through K63-linked ubiquitination of TBK1. Nat. Immunol. 2016, 17, 1342–1351. [Google Scholar] [CrossRef] [PubMed]
- Boutell, C.; Sadis, S.; Everett, R.D. Herpes simplex virus type 1 immediate-early protein ICP0 and is isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 2002, 76, 841–850. [Google Scholar] [CrossRef] [Green Version]
- Zhang, J.; Wang, K.; Wang, S.; Zheng, C. Herpes simplex virus 1 E3 ubiquitin ligase ICP0 protein inhibits tumor necrosis factor alpha-induced NF-kappaB activation by interacting with p65/RelA and p50/NF-kappaB1. J. Virol. 2013, 87, 12935–12948. [Google Scholar] [CrossRef] [Green Version]
- van Lint, A.L.; Murawski, M.R.; Goodbody, R.E.; Severa, M.; Fitzgerald, K.A.; Finberg, R.W.; Knipe, D.M.; Kurt-Jones, E.A. Herpes simplex virus immediate-early ICP0 protein inhibits Toll-like receptor 2-dependent inflammatory responses and NF-kappaB signaling. J. Virol. 2010, 84, 10802–10811. [Google Scholar] [CrossRef] [Green Version]
- Di Fiore, I.J.; Pane, J.A.; Holloway, G.; Coulson, B.S. NSP1 of human rotaviruses commonly inhibits NF-kappaB signalling by inducing beta-TrCP degradation. J. Gen. Virol. 2015, 96, 1768–1776. [Google Scholar] [CrossRef]
- Morelli, M.; Dennis, A.F.; Patton, J.T. Putative E3 ubiquitin ligase of human rotavirus inhibits NF-kappaB activation by using molecular mimicry to target beta-TrCP. mBio 2015, 6. [Google Scholar] [CrossRef] [Green Version]
- Li, S.W.; Wang, C.Y.; Jou, Y.J.; Huang, S.H.; Hsiao, L.H.; Wan, L.; Lin, Y.J.; Kung, S.H.; Lin, C.W. SARS Coronavirus Papain-Like Protease Inhibits the TLR7 Signaling Pathway through Removing Lys63-Linked Polyubiquitination of TRAF3 and TRAF6. Int. J. Mol. Sci. 2016, 17, 678. [Google Scholar] [CrossRef] [Green Version]
- Clementz, M.A.; Chen, Z.; Banach, B.S.; Wang, Y.; Sun, L.; Ratia, K.; Baez-Santos, Y.M.; Wang, J.; Takayama, J.; Ghosh, A.K.; et al. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J. Virol. 2010, 84, 4619–4629. [Google Scholar] [CrossRef] [Green Version]
- Frieman, M.; Ratia, K.; Johnston, R.E.; Mesecar, A.D.; Baric, R.S. Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-kappaB signaling. J. Virol. 2009, 83, 6689–6705. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, D.; Fang, L.; Li, P.; Sun, L.; Fan, J.; Zhang, Q.; Luo, R.; Liu, X.; Li, K.; Chen, H.; et al. The leader proteinase of foot-and-mouth disease virus negatively regulates the type I interferon pathway by acting as a viral deubiquitinase. J. Virol. 2011, 85, 3758–3766. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Inn, K.S.; Lee, S.H.; Rathbun, J.Y.; Wong, L.Y.; Toth, Z.; Machida, K.; Ou, J.H.; Jung, J.U. Inhibition of RIG-I-mediated signaling by Kaposi’s sarcoma-associated herpesvirus-encoded deubiquitinase ORF64. J. Virol. 2011, 85, 10899–10904. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, C.; Schattgen, S.A.; Pisitkun, P.; Jorgensen, J.P.; Hilterbrand, A.T.; Wang, L.J.; West, J.A.; Hansen, K.; Horan, K.A.; Jakobsen, M.R.; et al. Evasion of innate cytosolic DNA sensing by a gammaherpesvirus facilitates establishment of latent infection. J. Immunol. 2015, 194, 1819–1831. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kwon, K.M.; Oh, S.E.; Kim, Y.E.; Han, T.H.; Ahn, J.H. Cooperative inhibition of RIP1-mediated NF-kappaB signaling by cytomegalovirus-encoded deubiquitinase and inactive homolog of cellular ribonucleotide reductase large subunit. PLoS Pathog. 2017, 13, e1006423. [Google Scholar] [CrossRef] [Green Version]
- Sun, Z.; Chen, Z.; Lawson, S.R.; Fang, Y. The cysteine protease domain of porcine reproductive and respiratory syndrome virus nonstructural protein 2 possesses deubiquitinating and interferon antagonism functions. J. Virol. 2010, 84, 7832–7846. [Google Scholar] [CrossRef] [Green Version]
- van Kasteren, P.B.; Bailey-Elkin, B.A.; James, T.W.; Ninaber, D.K.; Beugeling, C.; Khajehpour, M.; Snijder, E.J.; Mark, B.L.; Kikkert, M. Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc. Natl. Acad. Sci. USA 2013, 110, E838–E847. [Google Scholar] [CrossRef] [Green Version]
- Ye, R.; Su, C.; Xu, H.; Zheng, C. Herpes Simplex Virus 1 Ubiquitin-Specific Protease UL36 Abrogates NF-kappaB Activation in DNA Sensing Signal Pathway. J. Virol. 2017, 91. [Google Scholar] [CrossRef] [Green Version]
- van Gent, M.; Braem, S.G.; de Jong, A.; Delagic, N.; Peeters, J.G.; Boer, I.G.; Moynagh, P.N.; Kremmer, E.; Wiertz, E.J.; Ovaa, H.; et al. Epstein-Barr virus large tegument protein BPLF1 contributes to innate immune evasion through interference with toll-like receptor signaling. PLoS Pathog. 2014, 10, e1003960. [Google Scholar] [CrossRef]
- Brady, G.; Haas, D.A.; Farrell, P.J.; Pichlmair, A.; Bowie, A.G. Poxvirus Protein MC132 from Molluscum Contagiosum Virus Inhibits NF-B Activation by Targeting p65 for Degradation. J. Virol. 2015, 89, 8406–8415. [Google Scholar] [CrossRef] [Green Version]
- Li, X.; Liang, D.; Lin, X.; Robertson, E.S.; Lan, K. Kaposi’s sarcoma-associated herpesvirus-encoded latency-associated nuclear antigen reduces interleukin-8 expression in endothelial cells and impairs neutrophil chemotaxis by degrading nuclear p65. J. Virol. 2011, 85, 8606–8615. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodrigues, L.; Filipe, J.; Seldon, M.P.; Fonseca, L.; Anrather, J.; Soares, M.P.; Simas, J.P. Termination of NF-kappaB activity through a gammaherpesvirus protein that assembles an EC5S ubiquitin-ligase. EMBO J. 2009, 28, 1283–1295. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shi, C.S.; Qi, H.Y.; Boularan, C.; Huang, N.N.; Abu-Asab, M.; Shelhamer, J.H.; Kehrl, J.H. SARS-coronavirus open reading frame-9b suppresses innate immunity by targeting mitochondria and the MAVS/TRAF3/TRAF6 signalosome. J. Immunol. 2014, 193, 3080–3089. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boutell, C.; Canning, M.; Orr, A.; Everett, R.D. Reciprocal activities between herpes simplex virus type 1 regulatory protein ICP0, a ubiquitin E3 ligase, and ubiquitin-specific protease USP7. J. Virol. 2005, 79, 12342–12354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wei, C.; Ni, C.; Song, T.; Liu, Y.; Yang, X.; Zheng, Z.; Jia, Y.; Yuan, Y.; Guan, K.; Xu, Y.; et al. The hepatitis B virus X protein disrupts innate immunity by downregulating mitochondrial antiviral signaling protein. J. Immunol. 2010, 185, 1158–1168. [Google Scholar] [CrossRef] [PubMed]
- Goswami, R.; Majumdar, T.; Dhar, J.; Chattopadhyay, S.; Bandyopadhyay, S.K.; Verbovetskaya, V.; Sen, G.C.; Barik, S. Viral degradasome hijacks mitochondria to suppress innate immunity. Cell Res. 2013, 23, 1025–1042. [Google Scholar] [CrossRef] [Green Version]
- Oshiumi, H.; Miyashita, M.; Matsumoto, M.; Seya, T. A distinct role of Riplet-mediated K63-Linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog. 2013, 9, e1003533. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gack, M.U.; Albrecht, R.A.; Urano, T.; Inn, K.S.; Huang, I.C.; Carnero, E.; Farzan, M.; Inoue, S.; Jung, J.U.; Garcia-Sastre, A. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 2009, 5, 439–449. [Google Scholar] [CrossRef] [Green Version]
- Rajsbaum, R.; Albrecht, R.A.; Wang, M.K.; Maharaj, N.P.; Versteeg, G.A.; Nistal-Villan, E.; Garcia-Sastre, A.; Gack, M.U. Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathog. 2012, 8, e1003059. [Google Scholar] [CrossRef]
- Mack, C.; Sickmann, A.; Lembo, D.; Brune, W. Inhibition of proinflammatory and innate immune signaling pathways by a cytomegalovirus RIP1-interacting protein. Proc. Natl. Acad. Sci. USA 2008, 105, 3094–3099. [Google Scholar] [CrossRef] [Green Version]
- Rebsamen, M.; Heinz, L.X.; Meylan, E.; Michallet, M.C.; Schroder, K.; Hofmann, K.; Vazquez, J.; Benedict, C.A.; Tschopp, J. DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-kappaB. EMBO Rep. 2009, 10, 916–922. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Li, J.; Chen, J.; Li, Y.; Wang, W.; Du, X.; Song, W.; Zhang, W.; Lin, L.; Yuan, Z. Hepatitis B virus polymerase disrupts K63-linked ubiquitination of STING to block innate cytosolic DNA-sensing pathways. J. Virol. 2015, 89, 2287–2300. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Y.; Cui, L.; Yang, G.; Zhan, J.; Guo, L.; Chen, Y.; Fan, C.; Liu, D.; Guo, D. Hepatitis B e Antigen Inhibits NF-kappaB Activity by Interrupting K63-Linked Ubiquitination of NEMO. J. Virol. 2019, 93. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; He, L.; Peng, Y.; Shi, X.; Chen, J.; Zhong, J.; Chen, X.; Cheng, G.; Deng, H. The hepatitis C virus protein NS3 suppresses TNF-alpha-stimulated activation of NF-kappaB by targeting LUBAC. Sci. Signal. 2015, 8, ra118. [Google Scholar] [CrossRef]
- Brady, G.; Haas, D.A.; Farrell, P.J.; Pichlmair, A.; Bowie, A.G. Molluscum Contagiosum Virus Protein MC005 Inhibits NF-kappaB Activation by Targeting NEMO-Regulated IkappaB Kinase Activation. J. Virol. 2017, 91. [Google Scholar] [CrossRef] [Green Version]
- Lei, Q.; Li, L.; Cai, J.; Huang, W.; Qin, B.; Zhang, S. ORF3 of Hepatitis E Virus Inhibits the Expression of Proinflammatory Cytokines and Chemotactic Factors in LPS-Stimulated Human PMA-THP1 Cells by Inhibiting NF-kappaB Pathway. Viral Immunol. 2016, 29, 105–111. [Google Scholar] [CrossRef]
- He, M.; Wang, M.; Huang, Y.; Peng, W.; Zheng, Z.; Xia, N.; Xu, J.; Tian, D. The ORF3 Protein of Genotype 1 Hepatitis E Virus Suppresses TLR3-induced NF-kappaB Signaling via TRADD and RIP1. Sci. Rep. 2016, 6, 27597. [Google Scholar] [CrossRef] [Green Version]
- Yokota, S.; Okabayashi, T.; Yokosawa, N.; Fujii, N. Measles virus P protein suppresses Toll-like receptor signal through up-regulation of ubiquitin-modifying enzyme A20. FASEB J. 2008, 22, 74–83. [Google Scholar] [CrossRef] [Green Version]
- Xu, C.; He, X.; Zheng, Z.; Zhang, Z.; Wei, C.; Guan, K.; Hou, L.; Zhang, B.; Zhu, L.; Cao, Y.; et al. Downregulation of microRNA miR-526a by enterovirus inhibits RIG-I-dependent innate immune response. J. Virol. 2014, 88, 11356–11368. [Google Scholar] [CrossRef] [Green Version]
- Bottero, V.; Kerur, N.; Sadagopan, S.; Patel, K.; Sharma-Walia, N.; Chandran, B. Phosphorylation and polyubiquitination of transforming growth factor beta-activated kinase 1 are necessary for activation of NF-kappaB by the Kaposi’s sarcoma-associated herpesvirus G protein-coupled receptor. J. Virol. 2011, 85, 1980–1993. [Google Scholar] [CrossRef] [Green Version]
- Liu, R.; Lin, Y.; Jia, R.; Geng, Y.; Liang, C.; Tan, J.; Qiao, W. HIV-1 Vpr stimulates NF-kappaB and AP-1 signaling by activating TAK1. Retrovirology 2014, 11, 45. [Google Scholar] [CrossRef] [Green Version]
- Chung, Y.H.; Jhun, B.H.; Ryu, S.C.; Kim, H.S.; Kim, C.M.; Kim, B.S.; Kim, Y.O.; Lee, S.J. STP-C, an oncoprotein of herpesvirus saimiri augments the activation of NF-kappaB through ubiquitination of TRAF6. J. Biochem. Mol. Biol. 2007, 40, 341–348. [Google Scholar] [CrossRef] [Green Version]
- Greenfeld, H.; Takasaki, K.; Walsh, M.J.; Ersing, I.; Bernhardt, K.; Ma, Y.; Fu, B.; Ashbaugh, C.W.; Cabo, J.; Mollo, S.B.; et al. TRAF1 Coordinates Polyubiquitin Signaling to Enhance Epstein-Barr Virus LMP1-Mediated Growth and Survival Pathway Activation. PLoS Pathog. 2015, 11, e1004890. [Google Scholar] [CrossRef] [Green Version]
- Xu, M.; Katzenellenbogen, R.A.; Grandori, C.; Galloway, D.A. NFX1 plays a role in human papillomavirus type 16 E6 activation of NFkappaB activity. J. Virol. 2010, 84, 11461–11469. [Google Scholar] [CrossRef] [Green Version]
- Ho, Y.K.; Zhi, H.; Bowlin, T.; Dorjbal, B.; Philip, S.; Zahoor, M.A.; Shih, H.M.; Semmes, O.J.; Schaefer, B.; Glover, J.N.; et al. HTLV-1 Tax Stimulates Ubiquitin E3 Ligase, Ring Finger Protein 8, to Assemble Lysine 63-Linked Polyubiquitin Chains for TAK1 and IKK Activation. PLoS Pathog. 2015, 11, e1005102. [Google Scholar] [CrossRef]
- Shibata, Y.; Tokunaga, F.; Goto, E.; Komatsu, G.; Gohda, J.; Saeki, Y.; Tanaka, K.; Takahashi, H.; Sawasaki, T.; Inoue, S.; et al. HTLV-1 Tax Induces Formation of the Active Macromolecular IKK Complex by Generating Lys63- and Met1-Linked Hybrid Polyubiquitin Chains. PLoS Pathog. 2017, 13, e1006162. [Google Scholar] [CrossRef]
- Oikawa, D.; Sato, Y.; Ohtake, F.; Komakura, K.; Hanada, K.; Sugawara, K.; Terawaki, S.; Mizukami, Y.; Phuong, H.T.; Iio, K.; et al. Molecular bases for HOIPINs-mediated inhibition of LUBAC and innate immune responses. Commun. Biol. 2020, 3, 163. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Song, K.; Li, S. The Role of Ubiquitination in NF-κB Signaling during Virus Infection. Viruses 2021, 13, 145. https://doi.org/10.3390/v13020145
Song K, Li S. The Role of Ubiquitination in NF-κB Signaling during Virus Infection. Viruses. 2021; 13(2):145. https://doi.org/10.3390/v13020145
Chicago/Turabian StyleSong, Kun, and Shitao Li. 2021. "The Role of Ubiquitination in NF-κB Signaling during Virus Infection" Viruses 13, no. 2: 145. https://doi.org/10.3390/v13020145
APA StyleSong, K., & Li, S. (2021). The Role of Ubiquitination in NF-κB Signaling during Virus Infection. Viruses, 13(2), 145. https://doi.org/10.3390/v13020145