Specificity in Ubiquitination Triggered by Virus Infection
Abstract
1. Introduction
2. Enzymes in the Ubiquitin System
3. Biochemical Diversity of Ubiquitin Code
4. Functional Specificity and Complexity of Ubiquitin Code
5. Ubiquitination in Every Step of Viral Infection
5.1. Role of Ubiquitination in Virus Entry
5.2. Role of Ubiquitination in Virus Uncoating
5.3. Role of Ubiquitination in Virus Replication
5.3.1. Ubiquitin Specificity in DNA Induced IFN Production and Viral Counteractions
5.3.2. Ubiquitin Specificity in RNA Induced IFN Production and Viral Counteractions
5.3.3. Ubiquitin Specificity of Transcription Factors Promoting IFN Production and Viral Counteractions
5.3.4. Ubiquitin in IFN Responses and Viral Counteractions
5.3.5. Ubiquitin Specificity in Intrinsic Responses and Viral Counteractions
5.3.6. Ubiquitin Specificity in Viral Replication Enzymes
5.4. Role of Ubiquitination in Virus Egress
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
AdV | Adenovirus |
AMFR | Autocrine motility factor receptor |
APC/C | Cullin-containing anaphase-promoting complex |
APOBEC | Apolipoprotein B mRNA editing enzyme catalytic polypeptide |
CARD | Caspase recruitment domains |
cGAS | Cyclic GMP-AMP synthase |
DUB | Deubiquitinase |
EBOV | Ebola virus |
EBV | Epstein Barr virus |
ESCRT | Endosomal sorting complex required for transport |
HBV | Hepatitis B virus |
HCMV | Human cytomegalovirus |
HECT | Homologous to the E6AP carboxyl terminus |
HPV | Human papillomavirus |
HSV-1 | Herpes simplex virus 1 |
HTLV-1 | Human T lymphotropic virus 1 |
IAV | Influenza A virus |
IFN | Interferon |
INSIG1 | Insulin-induced gene 1 |
IKK | Inhibitor of nuclear factor kappa-B kinase |
ISG | Interferon stimulated genes |
JAK | Janus kinase |
KSHV | Kaposi’s sarcoma herpesvirus |
LUBAC | Linear ubiquitin chain assembly complex |
MAVS | Mitochondrial antiviral signaling proteins |
ND10 | Nuclear domain 10 |
PAMPs | Pathogen associated molecular patterns |
PML | Promyelocytic leukemia |
P-TEFb | Positive transcription elongation factor b |
PTM | Post-translational modification |
RIG-I | Retinoic acid-inducible gene I |
RING | Really interesting new gene |
RBR | RING-between-RING |
SARS-CoV | Severe acute respiratory syndrome coronavirus |
STAT | Signal transducers and activators of transcription |
STING | Stimulator of interferon genes |
TBK1 | TANK-binding kinase 1 |
TIM | Immunoglobulin and mucin |
TOSV | Toscana virus |
TRIM | Tripartite motif |
UBD | Ubiquitin binding domain |
ZIKV | Zika virus |
References
- Goldknopf, I.L.; Busch, H. Isopeptide linkage between nonhistone and histone 2A polypeptides of chromosomal conjugate-protein A24. Proc. Natl. Acad. Sci. USA 1977, 74, 864–868. [Google Scholar] [CrossRef] [PubMed]
- Hunt, L.T.; Dayhoff, M.O. Amino-terminal sequence identity of ubiquitin and the nonhistone component of nuclear protein A24. Biochem. Biophys. Res. Commun. 1977, 74, 650–655. [Google Scholar] [CrossRef]
- Hershko, A.; Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67, 425–479. [Google Scholar] [CrossRef]
- Swatek, K.N.; Komander, D. Ubiquitin modifications. Cell Res. 2016, 26, 399–422. [Google Scholar] [CrossRef]
- Haakonsen, D.L.; Rape, M. Branching Out: Improved Signaling by Heterotypic Ubiquitin Chains. Trends Cell Biol. 2019, 29, 704–716. [Google Scholar] [CrossRef]
- Pohl, C.; Dikic, I. Cellular quality control by the ubiquitin-proteasome system and autophagy. Science 2019, 366, 818–822. [Google Scholar] [CrossRef]
- Zheng, N.; Shabek, N. Ubiquitin Ligases: Structure, Function, and Regulation. Annu. Rev. Biochem. 2017, 86, 129–157. [Google Scholar] [CrossRef]
- Schulman, B.A.; Harper, J.W. Ubiquitin-like protein activation by E1 enzymes: The apex for downstream signalling pathways. Nat. Rev.. Mol. Cell Biol. 2009, 10, 319–331. [Google Scholar] [CrossRef]
- Morreale, F.E.; Walden, H. Types of Ubiquitin Ligases. Cell 2016, 165, 248. [Google Scholar] [CrossRef]
- Clague, M.J.; Urbe, S.; Komander, D. Breaking the chains: Deubiquitylating enzyme specificity begets function. Nat. Rev.. Mol. Cell Biol. 2019, 20, 338–352. [Google Scholar] [CrossRef]
- Mevissen, T.E.T.; Komander, D. Mechanisms of Deubiquitinase Specificity and Regulation. Annu. Rev. Biochem. 2017, 86, 159–192. [Google Scholar] [CrossRef] [PubMed]
- Komander, D.; Rape, M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81, 203–229. [Google Scholar] [CrossRef] [PubMed]
- George, A.J.; Hoffiz, Y.C.; Charles, A.J.; Zhu, Y.; Mabb, A.M. A Comprehensive Atlas of E3 Ubiquitin Ligase Mutations in Neurological Disorders. Front. Genet. 2018, 9, 29. [Google Scholar] [CrossRef] [PubMed]
- Pinto-Fernandez, A.; Kessler, B.M. DUBbing Cancer: Deubiquitylating Enzymes Involved in Epigenetics, DNA Damage and the Cell Cycle As Therapeutic Targets. Front. Genet. 2016, 7, 133. [Google Scholar] [CrossRef] [PubMed]
- Akutsu, M.; Dikic, I.; Bremm, A. Ubiquitin chain diversity at a glance. J. Cell Sci. 2016, 129, 875–880. [Google Scholar] [CrossRef] [PubMed]
- Kliza, K.; Husnjak, K. Resolving the Complexity of Ubiquitin Networks. Front. Mol. Biosci. 2020, 7, 21. [Google Scholar] [CrossRef] [PubMed]
- Ohtake, F.; Tsuchiya, H. The emerging complexity of ubiquitin architecture. J. Biochem. 2017, 161, 125–133. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Husnjak, K.; Dikic, I. Ubiquitin-binding proteins: Decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 2012, 81, 291–322. [Google Scholar] [CrossRef]
- Xu, P.; Duong, D.M.; Seyfried, N.T.; Cheng, D.; Xie, Y.; Robert, J.; Rush, J.; Hochstrasser, M.; Finley, D.; Peng, J. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009, 137, 133–145. [Google Scholar] [CrossRef]
- Kim, W.; Bennett, E.J.; Huttlin, E.L.; Guo, A.; Li, J.; Possemato, A.; Sowa, M.E.; Rad, R.; Rush, J.; Comb, M.J.; et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44, 325–340. [Google Scholar] [CrossRef] [PubMed]
- Thrower, J.S.; Hoffman, L.; Rechsteiner, M.; Pickart, C.M. Recognition of the polyubiquitin proteolytic signal. Embo, J. 2000, 19, 94–102. [Google Scholar] [CrossRef] [PubMed]
- Jacobson, A.D.; Zhang, N.Y.; Xu, P.; Han, K.J.; Noone, S.; Peng, J.; Liu, C.W. The lysine 48 and lysine 63 ubiquitin conjugates are processed differently by the 26 s proteasome. J. Biol. Chem. 2009, 284, 35485–35494. [Google Scholar] [CrossRef] [PubMed]
- Ohtake, F.; Tsuchiya, H.; Saeki, Y.; Tanaka, K. K63 ubiquitylation triggers proteasomal degradation by seeding branched ubiquitin chains. Proc. Natl. Acad. Sci. USA 2018, 115, E1401–e1408. [Google Scholar] [CrossRef] [PubMed]
- Rajsbaum, R.; Versteeg, G.A.; Schmid, S.; Maestre, A.M.; Belicha-Villanueva, A.; Martínez-Romero, C.; Patel, J.R.; Morrison, J.; Pisanelli, G.; Miorin, L.; et al. Unanchored K48-linked polyubiquitin synthesized by the E3-ubiquitin ligase TRIM6 stimulates the interferon-IKKε kinase-mediated antiviral response. Immunity 2014, 40, 880–895. [Google Scholar] [CrossRef]
- 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]
- Pertel, T.; Hausmann, S.; Morger, D.; Zuger, S.; Guerra, J.; Lascano, J.; Reinhard, C.; Santoni, F.A.; Uchil, P.D.; Chatel, L.; et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472, 361–365. [Google Scholar] [CrossRef]
- Hao, R.; Nanduri, P.; Rao, Y.; Panichelli, R.S.; Ito, A.; Yoshida, M.; Yao, T.P. Proteasomes activate aggresome disassembly and clearance by producing unanchored ubiquitin chains. Mol. Cell 2013, 51, 819–828. [Google Scholar] [CrossRef]
- Matsumoto, M.L.; Wickliffe, K.E.; Dong, K.C.; Yu, C.; Bosanac, I.; Bustos, D.; Phu, L.; Kirkpatrick, D.S.; Hymowitz, S.G.; Rape, M.; et al. K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 2010, 39, 477–484. [Google Scholar] [CrossRef] [PubMed]
- Brown, N.G.; VanderLinden, R.; Watson, E.R.; Weissmann, F.; Ordureau, A.; Wu, K.P.; Zhang, W.; Yu, S.; Mercredi, P.Y.; Harrison, J.S.; et al. Dual RING E3 Architectures Regulate Multiubiquitination and Ubiquitin Chain Elongation by APC/C. Cell 2016, 165, 1440–1453. [Google Scholar] [CrossRef]
- Li, Z.; Wang, Y.; Li, Y.; Yin, W.; Mo, L.; Qian, X.; Zhang, Y.; Wang, G.; Bu, F.; Zhang, Z.; et al. Ube2s stabilizes beta-Catenin through K11-linked polyubiquitination to promote mesendoderm specification and colorectal cancer development. Cell Death Dis. 2018, 9, 456. [Google Scholar] [CrossRef] [PubMed]
- Michel, M.A.; Swatek, K.N.; Hospenthal, M.K.; Komander, D. Ubiquitin Linkage-Specific Affimers Reveal Insights into K6-Linked Ubiquitin Signaling. Mol. Cell 2017, 68, 233–246. [Google Scholar] [CrossRef]
- Ordureau, A.; Heo, J.M.; Duda, D.M.; Paulo, J.A.; Olszewski, J.L.; Yanishevski, D.; Rinehart, J.; Schulman, B.A.; Harper, J.W. Defining roles of PARKIN and ubiquitin phosphorylation by PINK1 in mitochondrial quality control using a ubiquitin replacement strategy. Proc. Natl. Acad. Sci. USA 2015, 112, 6637–6642. [Google Scholar] [CrossRef] [PubMed]
- Kirisako, T.; Kamei, K.; Murata, S.; Kato, M.; Fukumoto, H.; Kanie, M.; Sano, S.; Tokunaga, F.; Tanaka, K.; Iwai, K. A ubiquitin ligase complex assembles linear polyubiquitin chains. Embo J. 2006, 25, 4877–4887. [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] [PubMed]
- 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]
- Spit, M.; Rieser, E.; Walczak, H. Linear ubiquitination at a glance. J. Cell Sci. 2019, 132. [Google Scholar] [CrossRef]
- Dittmar, G.; Winklhofer, K.F. Linear Ubiquitin Chains: Cellular Functions and Strategies for Detection and Quantification. Front. Chem. 2019, 7, 915. [Google Scholar] [CrossRef]
- Helenius, A. Virus Entry: Looking Back and Moving Forward. J. Mol. Biol. 2018, 430, 1853–1862. [Google Scholar] [CrossRef]
- Yamauchi, Y.; Helenius, A. Virus entry at a glance. J. Cell Sci. 2013, 126, 1289–1295. [Google Scholar] [CrossRef]
- Foot, N.; Henshall, T.; Kumar, S. Ubiquitination and the Regulation of Membrane Proteins. Physiol. Rev. 2017, 97, 253–281. [Google Scholar] [CrossRef] [PubMed]
- Simhadri, V.R.; Andersen, J.F.; Calvo, E.; Choi, S.C.; Coligan, J.E.; Borrego, F. Human CD300a binds to phosphatidylethanolamine and phosphatidylserine, and modulates the phagocytosis of dead cells. Blood 2012, 119, 2799–2809. [Google Scholar] [CrossRef] [PubMed]
- Freeman, G.J.; Casasnovas, J.M.; Umetsu, D.T.; DeKruyff, R.H. TIM genes: A family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol. Rev. 2010, 235, 172–189. [Google Scholar] [CrossRef]
- Brouillette, R.B.; Phillips, E.K.; Patel, R.; Mahauad-Fernandez, W.; Moller-Tank, S.; Rogers, K.J.; Dillard, J.A.; Cooney, A.L.; Martinez-Sobrido, L.; Okeoma, C.; et al. TIM-1 Mediates Dystroglycan-Independent Entry of Lassa Virus. J. Virol. 2018, 92. [Google Scholar] [CrossRef]
- Niu, J.; Jiang, Y.; Xu, H.; Zhao, C.; Zhou, G.; Chen, P.; Cao, R. TIM-1 Promotes Japanese Encephalitis Virus Entry and Infection. Viruses 2018, 10. [Google Scholar] [CrossRef] [PubMed]
- Hu, M.; Wang, F.; Li, W.; Zhang, X.; Zhang, Z.; Zhang, X.E.; Cui, Z. Ebola Virus Uptake into Polarized Cells from the Apical Surface. Viruses 2019, 11. [Google Scholar] [CrossRef]
- Dejarnac, O.; Hafirassou, M.L.; Chazal, M.; Versapuech, M.; Gaillard, J.; Perera-Lecoin, M.; Umana-Diaz, C.; Bonnet-Madin, L.; Carnec, X.; Tinevez, J.Y.; et al. TIM-1 Ubiquitination Mediates Dengue Virus Entry. Cell Rep. 2018, 23, 1779–1793. [Google Scholar] [CrossRef]
- Levkowitz, G.; Waterman, H.; Zamir, E.; Kam, Z.; Oved, S.; Langdon, W.Y.; Beguinot, L.; Geiger, B.; Yarden, Y. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 1998, 12, 3663–3674. [Google Scholar] [CrossRef]
- Duval, M.; Bedard-Goulet, S.; Delisle, C.; Gratton, J.P. Vascular endothelial growth factor-dependent down-regulation of Flk-1/KDR involves Cbl-mediated ubiquitination. Consequences on nitric oxide production from endothelial cells. J. Biol. Chem. 2003, 278, 20091–20097. [Google Scholar] [CrossRef]
- Cooper, J.A.; Kaneko, T.; Li, S.S. Cell regulation by phosphotyrosine-targeted ubiquitin ligases. Mol. Cell. Biol. 2015, 35, 1886–1897. [Google Scholar] [CrossRef]
- Chakraborty, S.; ValiyaVeettil, M.; Sadagopan, S.; Paudel, N.; Chandran, B. c-Cbl-mediated selective virus-receptor translocations into lipid rafts regulate productive Kaposi’s sarcoma-associated herpesvirus infection in endothelial cells. J. Virol. 2011, 85, 12410–12430. [Google Scholar] [CrossRef]
- Valiya Veettil, M.; Sadagopan, S.; Kerur, N.; Chakraborty, S.; Chandran, B. Interaction of c-Cbl with myosin IIA regulates Bleb associated macropinocytosis of Kaposi’s sarcoma-associated herpesvirus. Plos Pathog. 2010, 6, e1001238. [Google Scholar] [CrossRef]
- Deschamps, T.; Dogrammatzis, C.; Mullick, R.; Kalamvoki, M. Cbl E3 Ligase Mediates the Removal of Nectin-1 from the Surface of Herpes Simplex Virus 1-Infected Cells. J. Virol. 2017, 91. [Google Scholar] [CrossRef] [PubMed]
- Liang, Y.; Kurakin, A.; Roizman, B. Herpes simplex virus 1 infected cell protein 0 forms a complex with CIN85 and Cbl and mediates the degradation of EGF receptor from cell surfaces. Proc. Natl. Acad. Sci. USA 2005, 102, 5838–5843. [Google Scholar] [CrossRef] [PubMed]
- Gu, H. Infected cell protein 0 functional domains and their coordination in herpes simplex virus replication. World J. Virol. 2016, 5, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Greber, U.F.; Willetts, M.; Webster, P.; Helenius, A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993, 75, 477–486. [Google Scholar] [CrossRef]
- Wiethoff, C.M.; Wodrich, H.; Gerace, L.; Nemerow, G.R. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol. 2005, 79, 1992–2000. [Google Scholar] [CrossRef]
- Wodrich, H.; Henaff, D.; Jammart, B.; Segura-Morales, C.; Seelmeir, S.; Coux, O.; Ruzsics, Z.; Wiethoff, C.M.; Kremer, E.J. A capsid-encoded PPxY-motif facilitates adenovirus entry. PLoS Pathog. 2010, 6, e1000808. [Google Scholar] [CrossRef]
- Montespan, C.; Marvin, S.A.; Austin, S.; Burrage, A.M.; Roger, B.; Rayne, F.; Faure, M.; Campell, E.M.; Schneider, C.; Reimer, R.; et al. Multi-layered control of Galectin-8 mediated autophagy during adenovirus cell entry through a conserved PPxY motif in the viral capsid. PLoS Pathog. 2017, 13, e1006217. [Google Scholar] [CrossRef]
- Bauer, M.; Flatt, J.W.; Seiler, D.; Cardel, B.; Emmenlauer, M.; Boucke, K.; Suomalainen, M.; Hemmi, S.; Greber, U.F. The E3 Ubiquitin Ligase Mind Bomb 1 Controls Adenovirus Genome Release at the Nuclear Pore Complex. Cell Rep. 2019, 29, 3785–3795. [Google Scholar] [CrossRef]
- Banerjee, I.; Miyake, Y.; Nobs, S.P.; Schneider, C.; Horvath, P.; Kopf, M.; Matthias, P.; Helenius, A.; Yamauchi, Y. Influenza A virus uses the aggresome processing machinery for host cell entry. Science 2014, 346, 473–477. [Google Scholar] [CrossRef] [PubMed]
- Yan, J. Interplay between HDAC6 and its interacting partners: Essential roles in the aggresome-autophagy pathway and neurodegenerative diseases. DNA Cell Biol. 2014, 33, 567–580. [Google Scholar] [CrossRef] [PubMed]
- Kattenhorn, L.M.; Korbel, G.A.; Kessler, B.M.; Spooner, E.; Ploegh, H.L. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol. Cell 2005, 19, 547–557. [Google Scholar] [CrossRef] [PubMed]
- Schipke, J.; Pohlmann, A.; Diestel, R.; Binz, A.; Rudolph, K.; Nagel, C.H.; Bauerfeind, R.; Sodeik, B. The C terminus of the large tegument protein pUL36 contains multiple capsid binding sites that function differently during assembly and cell entry of herpes simplex virus. J. Virol. 2012, 86, 3682–3700. [Google Scholar] [CrossRef]
- Schneider, S.M.; Pritchard, S.M.; Wudiri, G.A.; Trammell, C.E.; Nicola, A.V. Early Steps in Herpes Simplex Virus Infection Blocked by a Proteasome Inhibitor. mBio 2019, 10. [Google Scholar] [CrossRef]
- Isaacs, A.; Lindenmann, J.; Valentine, R.C. Virus interference. II. Some properties of interferon. Proc. R. Soc. Lond.. Ser. BBiol. Sci. 1957, 147, 268–273. [Google Scholar] [CrossRef]
- Isaacs, A.; Lindenmann, J. Virus interference. I. The interferon. Proc. R. Soc. Lond. 1957, 147, 258–267. [Google Scholar] [CrossRef]
- Samuel, C.E. Antiviral actions of interferons. Clin. Microbiol. Rev. 2001, 14, 778–809. [Google Scholar] [CrossRef]
- Cao, X. Self-regulation and cross-regulation of pattern-recognition receptor signalling in health and disease. Nat. Rev. Immunol. 2016, 16, 35–50. [Google Scholar] [CrossRef]
- Ablasser, A.; Hur, S. Regulation of cGAS- and RLR-mediated immunity to nucleic acids. Nat. Immunol. 2020, 21, 17–29. [Google Scholar] [CrossRef]
- Sun, L.; Wu, J.; Du, F.; Chen, X.; Chen, Z.J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339, 786–791. [Google Scholar] [CrossRef] [PubMed]
- Van Gent, M.; Sparrer, K.M.J.; Gack, M.U. TRIM Proteins and Their Roles in Antiviral Host Defenses. Annu. Rev. Virol. 2018, 5, 385–405. [Google Scholar] [CrossRef] [PubMed]
- Seo, G.J.; Kim, C.; Shin, W.J.; Sklan, E.H.; Eoh, H.; Jung, J.U. TRIM56-mediated monoubiquitination of cGAS for cytosolic DNA sensing. Nat. Commun. 2018, 9, 613. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Huang, L.; Hong, Z.; Lv, Z.; Mao, Z.; Tang, Y.; Kong, X.; Li, S.; Cui, Y.; Liu, H.; et al. The E3 ubiquitin ligase RNF185 facilitates the cGAS-mediated innate immune response. Plos Pathog. 2017, 13, e10006264. [Google Scholar] [CrossRef] [PubMed]
- Tsuchida, T.; Zou, J.; Saitoh, T.; Kumar, H.; Abe, T.; Matsuura, Y.; Kawai, T.; Akira, S. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 2010, 33, 765–776. [Google Scholar] [CrossRef]
- Zhang, J.; Hu, M.M.; Wang, Y.Y.; Shu, H.B. TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J. Biol. Chem. 2012, 287, 28646–28655. [Google Scholar] [CrossRef]
- Ni, G.; Konno, H.; Barber, G.N. Ubiquitination of STING at lysine 224 controls IRF3 activation. Sci. Immunol. 2017, 2. [Google Scholar] [CrossRef]
- Wang, Q.; Liu, X.; Cui, Y.; Tang, Y.; Chen, W.; Li, S.; Yu, H.; Pan, Y.; Wang, C. The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 2014, 41, 919–933. [Google Scholar] [CrossRef]
- Zhong, B.; Zhang, L.; Lei, C.; Li, Y.; Mao, A.P.; Yang, Y.; Wang, Y.Y.; Zhang, X.L.; Shu, H.B. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 2009, 30, 397–407. [Google Scholar] [CrossRef]
- Qin, Y.; Zhou, M.T.; Hu, M.M.; Hu, Y.H.; Zhang, J.; Guo, L.; Zhong, B.; Shu, H.B. RNF26 temporally regulates virus-triggered type I interferon induction by two distinct mechanisms. PLoS Pathog. 2014, 10, e1004358. [Google Scholar] [CrossRef]
- Wang, J.; Yang, S.; Liu, L.; Wang, H.; Yang, B. HTLV-1 Tax impairs K63-linked ubiquitination of STING to evade host innate immunity. Virus Res. 2017, 232, 13–21. [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]
- 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]
- 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] [PubMed]
- Okamoto, M.; Kouwaki, T.; Fukushima, Y.; Oshiumi, H. Regulation of RIG-I Activation by K63-Linked Polyubiquitination. Front. Immunol. 2017, 8, 1942. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Zhang, H.L.; Ye, H.Q.; Liu, S.Q.; Deng, C.L.; Li, X.D.; Shi, P.Y.; Zhang, B. West Nile Virus NS1 Antagonizes Interferon Beta Production by Targeting RIG-I and MDA5. J. Virol. 2017, 91. [Google Scholar] [CrossRef] [PubMed]
- Ban, J.; Lee, N.R.; Lee, N.J.; Lee, J.K.; Quan, F.S.; Inn, K.S. Human Respiratory Syncytial Virus NS 1 Targets TRIM25 to Suppress RIG-I Ubiquitination and Subsequent RIG-I-Mediated Antiviral Signaling. Viruses 2018, 10. [Google Scholar] [CrossRef]
- Sun, L.; Xing, Y.; Chen, X.; Zheng, Y.; Yang, Y.; Nichols, D.B.; Clementz, M.A.; Banach, B.S.; Li, K.; Baker, S.C.; et al. Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS ONE 2012, 7, e30802. [Google Scholar] [CrossRef]
- Gori Savellini, G.; Anichini, G.; Gandolfo, C.; Prathyumnan, S.; Cusi, M.G. Toscana virus non-structural protein NSs acts as E3 ubiquitin ligase promoting RIG-I degradation. Plos Pathog. 2019, 15, e1008186. [Google Scholar] [CrossRef]
- Gupta, S.; Yla-Anttila, P.; Callegari, S.; Tsai, M.H.; Delecluse, H.J.; Masucci, M.G. Herpesvirus deconjugases inhibit the IFN response by promoting TRIM25 autoubiquitination and functional inactivation of the RIG-I signalosome. Plos Pathog. 2018, 14, e1006852. [Google Scholar] [CrossRef] [PubMed]
- Chiang, C.; Pauli, E.K.; Biryukov, J.; Feister, K.F.; Meng, M.; White, E.A.; Munger, K.; Howley, P.M.; Meyers, C.; Gack, M.U. The Human Papillomavirus E6 Oncoprotein Targets USP15 and TRIM25 To Suppress RIG-I-Mediated Innate Immune Signaling. J. Virol. 2018, 92. [Google Scholar] [CrossRef] [PubMed]
- 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]
- 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]
- Li, W.; Li, N.; Dai, S.; Hou, G.; Guo, K.; Chen, X.; Yi, C.; Liu, W.; Deng, F.; Wu, Y.; et al. Zika virus circumvents host innate immunity by targeting the adaptor proteins MAVS and MITA. Faseb J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2019, 33, 9929–9944. [Google Scholar] [CrossRef]
- Yu, Y.; Hayward, G.S. The ubiquitin E3 ligase RAUL negatively regulates type i interferon through ubiquitination of the transcription factors IRF7 and IRF3. Immunity 2010, 33, 863–877. [Google Scholar] [CrossRef] [PubMed]
- Wang, P.; Zhao, W.; Zhao, K.; Zhang, L.; Gao, C. TRIM26 negatively regulates interferon-beta production and antiviral response through polyubiquitination and degradation of nuclear IRF3. Plos Pathog. 2015, 11, e1004726. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, S.; Dass, J.F.P. Study of pathway cross-talk interactions with NF-kappaB leading to its activation via ubiquitination or phosphorylation: A brief review. Gene 2016, 584, 97–109. [Google Scholar] [CrossRef] [PubMed]
- Courtois, G.; Fauvarque, M.O. The Many Roles of Ubiquitin in NF-kappaB Signaling. Biomedicines 2018, 6. [Google Scholar] [CrossRef]
- Davis, K.A.; Morelli, M.; Patton, J.T. Rotavirus NSP1 Requires Casein Kinase II-Mediated Phosphorylation for Hijacking of Cullin-RING Ligases. mBio 2017, 8. [Google Scholar] [CrossRef] [PubMed]
- Whitmer, T.; Malouli, D.; Uebelhoer, L.S.; DeFilippis, V.R.; Fruh, K.; Verweij, M.C. The ORF61 Protein Encoded by Simian Varicella Virus and Varicella-Zoster Virus Inhibits NF-kappaB Signaling by Interfering with IkappaBalpha Degradation. J. Virol. 2015, 89, 8687–8700. [Google Scholar] [CrossRef] [PubMed]
- 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]
- 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]
- Morris, R.; Kershaw, N.J.; Babon, J.J. The molecular details of cytokine signaling via the JAK/STAT pathway. Protein Sci. A Publ. Protein Soc. 2018, 27, 1984–2009. [Google Scholar] [CrossRef]
- Goraya, M.U.; Zaighum, F.; Sajjad, N.; Anjum, F.R.; Sakhawat, I.; Rahman, S.U. Web of interferon stimulated antiviral factors to control the influenza A viruses replication. Microb. Pathog. 2020, 139, 103919. [Google Scholar] [CrossRef]
- Xia, C.; Vijayan, M.; Pritzl, C.J.; Fuchs, S.Y.; McDermott, A.B.; Hahm, B. Hemagglutinin of Influenza A Virus Antagonizes Type I Interferon (IFN) Responses by Inducing Degradation of Type I IFN Receptor 1. J. Virol. 2015, 90, 2403–2417. [Google Scholar] [CrossRef]
- Chen, J.; Xu, W.; Chen, Y.; Xie, X.; Zhang, Y.; Ma, C.; Yang, Q.; Han, Y.; Zhu, C.; Xiong, Y.; et al. Matrix Metalloproteinase 9 Facilitates Hepatitis B Virus Replication through Binding with Type I Interferon (IFN) Receptor 1 To Repress IFN/JAK/STAT Signaling. J. Virol. 2017, 91. [Google Scholar] [CrossRef]
- Elliott, J.; Lynch, O.T.; Suessmuth, Y.; Qian, P.; Boyd, C.R.; Burrows, J.F.; Buick, R.; Stevenson, N.J.; Touzelet, O.; Gadina, M.; et al. Respiratory syncytial virus NS1 protein degrades STAT2 by using the Elongin-Cullin E3 ligase. J. Virol. 2007, 81, 3428–3436. [Google Scholar] [CrossRef]
- Morrison, J.; Laurent-Rolle, M.; Maestre, A.M.; Rajsbaum, R.; Pisanelli, G.; Simon, V.; Mulder, L.C.; Fernandez-Sesma, A.; Garcia-Sastre, A. Dengue virus co-opts UBR4 to degrade STAT2 and antagonize type I interferon signaling. Plos Pathog. 2013, 9, e1003265. [Google Scholar] [CrossRef]
- Grant, A.; Ponia, S.S.; Tripathi, S.; Balasubramaniam, V.; Miorin, L.; Sourisseau, M.; Schwarz, M.C.; Sanchez-Seco, M.P.; Evans, M.J.; Best, S.M.; et al. Zika Virus Targets Human STAT2 to Inhibit Type I Interferon Signaling. Cell Host Microbe 2016, 19, 882–890. [Google Scholar] [CrossRef] [PubMed]
- Ulane, C.M.; Kentsis, A.; Cruz, C.D.; Parisien, J.P.; Schneider, K.L.; Horvath, C.M. Composition and assembly of STAT-targeting ubiquitin ligase complexes: Paramyxovirus V protein carboxyl terminus is an oligomerization domain. J. Virol. 2005, 79, 10180–10189. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.; Jiang, W.; Liu, Z.; Liu, S.; Liang, X. Virus Infection and Death Receptor-Mediated Apoptosis. Viruses 2017, 9. [Google Scholar] [CrossRef] [PubMed]
- Scheffner, M.; Huibregtse, J.M.; Vierstra, R.D.; Howley, P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75, 495–505. [Google Scholar] [CrossRef]
- Li, S.; Hong, X.; Wei, Z.; Xie, M.; Li, W.; Liu, G.; Guo, H.; Yang, J.; Wei, W.; Zhang, S. Ubiquitination of the HPV Oncoprotein E6 Is Critical for E6/E6AP-Mediated p53 Degradation. Front. Microbiol. 2019, 10, 2483. [Google Scholar] [CrossRef]
- Zhang, H.; Huang, C.; Wang, Y.; Lu, Z.; Zhuang, N.; Zhao, D.; He, J.; Shi, L. Hepatitis B Virus X Protein Sensitizes TRAIL-Induced Hepatocyte Apoptosis by Inhibiting the E3 Ubiquitin Ligase A20. PLoS ONE 2015, 10, e0127329. [Google Scholar] [CrossRef]
- Lallemand-Breitenbach, V.; de The, H. PML nuclear bodies: From architecture to function. Curr. Opin. Cell Biol. 2018, 52, 154–161. [Google Scholar] [CrossRef]
- Gu, H.; Zheng, Y. Role of ND10 nuclear bodies in the chromatin repression of HSV-1. Virol. J. 2016, 13, 62. [Google Scholar] [CrossRef]
- Scherer, M.; Stamminger, T. Emerging Role of PML Nuclear Bodies in Innate Immune Signaling. J. Virol. 2016, 90, 5850–5854. [Google Scholar] [CrossRef]
- Chelbi-Alix, M.K.; de The, H. Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 1999, 18, 935–941. [Google Scholar] [CrossRef]
- Zheng, Y.; Samrat, S.K.; Gu, H. A Tale of Two PMLs: Elements Regulating a Differential Substrate Recognition by the ICP0 E3 Ubiquitin Ligase of Herpes Simplex Virus 1. J. Virol. 2016, 90, 10875–10885. [Google Scholar] [CrossRef] [PubMed]
- Jan Fada, B.; Kaadi, E.; Samrat, S.; Zheng, Y.; Gu, H. Effect of SUMO-SIM interaction on the ICP0-mediated degradation of PML isoform II and its associated proteins in HSV-1 infection. J. Virol. 2020, 94, e00470-20. [Google Scholar] [CrossRef] [PubMed]
- Izumiya, Y.; Kobayashi, K.; Kim, K.Y.; Pochampalli, M.; Izumiya, C.; Shevchenko, B.; Wang, D.H.; Huerta, S.B.; Martinez, A.; Campbell, M.; et al. Kaposi’s sarcoma-associated herpesvirus K-Rta exhibits SUMO-targeting ubiquitin ligase (STUbL) like activity and is essential for viral reactivation. Plos Pathog. 2013, 9, e1003506. [Google Scholar] [CrossRef] [PubMed]
- Harris, R.S.; Dudley, J.P. APOBECs and virus restriction. Virology 2015, 479–480, 131–145. [Google Scholar] [CrossRef] [PubMed]
- Yu, X.; Yu, Y.; Liu, B.; Luo, K.; Kong, W.; Mao, P.; Yu, X.F. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 2003, 302, 1056–1060. [Google Scholar] [CrossRef]
- Sheehy, A.M.; Gaddis, N.C.; Choi, J.D.; Malim, M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418, 646–650. [Google Scholar] [CrossRef]
- Gao, Y.; Feng, J.; Yang, G.; Zhang, S.; Liu, Y.; Bu, Y.; Sun, M.; Zhao, M.; Chen, F.; Zhang, W.; et al. Hepatitis B virus X protein-elevated MSL2 modulates hepatitis B virus covalently closed circular DNA by inducing degradation of APOBEC3B to enhance hepatocarcinogenesis. Hepatology 2017, 66, 1413–1429. [Google Scholar] [CrossRef]
- Kirui, J.; Mondal, A.; Mehle, A. Ubiquitination Upregulates Influenza Virus Polymerase Function. J. Virol. 2016, 90, 10906–10914. [Google Scholar] [CrossRef]
- Karim, M.; Biquand, E.; Declercq, M.; Jacob, Y.; van der Werf, S.; Demeret, C. Nonproteolytic K29-Linked Ubiquitination of the PB2 Replication Protein of Influenza A Viruses by Proviral Cullin 4-Based E3 Ligases. mBio 2020, 11. [Google Scholar] [CrossRef]
- Bharaj, P.; Atkins, C.; Luthra, P.; Giraldo, M.I.; Dawes, B.E.; Miorin, L.; Johnson, J.R.; Krogan, N.J.; Basler, C.F.; Freiberg, A.N.; et al. The Host E3-Ubiquitin Ligase TRIM6 Ubiquitinates the Ebola Virus VP35 Protein and Promotes Virus Replication. J. Virol. 2017, 91. [Google Scholar] [CrossRef]
- Laspia, M.F.; Rice, A.P.; Mathews, M.B. HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 1989, 59, 283–292. [Google Scholar] [CrossRef]
- Faust, T.B.; Li, Y.; Bacon, C.W.; Jang, G.M.; Weiss, A.; Jayaraman, B.; Newton, B.W.; Krogan, N.J.; D’Orso, I.; Frankel, A.D. The HIV-1 Tat protein recruits a ubiquitin ligase to reorganize the 7SK snRNP for transcriptional activation. eLife 2018, 7. [Google Scholar] [CrossRef]
- Ahmed, I.; Akram, Z.; Iqbal, H.M.N.; Munn, A.L. The regulation of Endosomal Sorting Complex Required for Transport and accessory proteins in multivesicular body sorting and enveloped viral budding-An overview. Int. J. Biol. Macromol. 2019, 127, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Strack, B.; Calistri, A.; Accola, M.A.; Palu, G.; Gottlinger, H.G. A role for ubiquitin ligase recruitment in retrovirus release. Proc. Natl. Acad. Sci. USA 2000, 97, 13063–13068. [Google Scholar] [CrossRef]
- Harty, R.N.; Brown, M.E.; Wang, G.; Huibregtse, J.; Hayes, F.P. A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: Implications for filovirus budding. Proc. Natl. Acad. Sci. USA 2000, 97, 13871–13876. [Google Scholar] [CrossRef]
- Kikonyogo, A.; Bouamr, F.; Vana, M.L.; Xiang, Y.; Aiyar, A.; Carter, C.; Leis, J. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. USA 2001, 98, 11199–11204. [Google Scholar] [CrossRef] [PubMed]
- Weiss, E.R.; Popova, E.; Yamanaka, H.; Kim, H.C.; Huibregtse, J.M.; Gottlinger, H. Rescue of HIV-1 release by targeting widely divergent NEDD4-type ubiquitin ligases and isolated catalytic HECT domains to Gag. Plos Pathog. 2010, 6, e1001107. [Google Scholar] [CrossRef]
- Mercenne, G.; Alam, S.L.; Arii, J.; Lalonde, M.S.; Sundquist, W.I. Angiomotin functions in HIV-1 assembly and budding. eLife 2015, 4. [Google Scholar] [CrossRef]
© 2020 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
Gu, H.; Jan Fada, B. Specificity in Ubiquitination Triggered by Virus Infection. Int. J. Mol. Sci. 2020, 21, 4088. https://doi.org/10.3390/ijms21114088
Gu H, Jan Fada B. Specificity in Ubiquitination Triggered by Virus Infection. International Journal of Molecular Sciences. 2020; 21(11):4088. https://doi.org/10.3390/ijms21114088
Chicago/Turabian StyleGu, Haidong, and Behdokht Jan Fada. 2020. "Specificity in Ubiquitination Triggered by Virus Infection" International Journal of Molecular Sciences 21, no. 11: 4088. https://doi.org/10.3390/ijms21114088
APA StyleGu, H., & Jan Fada, B. (2020). Specificity in Ubiquitination Triggered by Virus Infection. International Journal of Molecular Sciences, 21(11), 4088. https://doi.org/10.3390/ijms21114088