Unanchored ubiquitin chain sustains RIG-I-induced interferon-I activation and controls selective gene expression

Loo, 2011, Immune signaling by RIG-I-like receptors, Immunity, 34, 680, 10.1016/j.immuni.2011.05.003 Goubau, 2013, Cytosolic sensing of viruses, Immunity, 38, 855, 10.1016/j.immuni.2013.05.007 Wies, 2013, Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling, Immunity, 38, 437, 10.1016/j.immuni.2012.11.018 Wallach, 2013, Phosphorylation and dephosphorylation of the RIG-I-like receptors: a safety latch on a fateful pathway, Immunity, 38, 402, 10.1016/j.immuni.2013.02.014 Peisley, 2014, Structural basis for ubiquitin-mediated antiviral signal activation by RIG-I, Nature, 509, 110, 10.1038/nature13140 Gack, 2007, TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity, Nature, 446, 916, 10.1038/nature05732 Yan, 2014, TRIM4 modulates type I interferon induction and cellular antiviral response by targeting RIG-I for K63-linked ubiquitination, J Mol Cell Biol, 6, 154, 10.1093/jmcb/mju005 Kuniyoshi, 2014, Pivotal role of RNA-binding E3 ubiquitin ligase MEX3C in RIG-I-mediated antiviral innate immunity, Proc Natl Acad Sci USA, 111, 5646, 10.1073/pnas.1401674111 Xian, 2017, Stratified ubiquitination of RIG-I creates robust immune response and induces selective gene expression, Sci Adv, 3, e1701764, 10.1126/sciadv.1701764 Cui, 2014, USP3 inhibits type I interferon signaling by deubiquitinating RIG-I-like receptors, Cell Res, 24, 400, 10.1038/cr.2013.170 Fan, 2014, USP21 negatively regulates antiviral response by acting as a RIG-I deubiquitinase, J Exp Med, 211, 313, 10.1084/jem.20122844 Malynn, 2010, Ubiquitin makes its mark on immune regulation, Immunity, 33, 843, 10.1016/j.immuni.2010.12.007 Zeng, 2010, Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity, Cell, 141, 315, 10.1016/j.cell.2010.03.029 Sun, 2016, A hierarchical mechanism of RIG-I ubiquitination provides sensitivity, robustness and synergy in antiviral immune responses, Sci Rep, 6, 29263, 10.1038/srep29263 Di Rienzo, 2019, Autophagy induction in atrophic muscle cells requires ULK1 activation by TRIM32 through unanchored K63-linked polyubiquitin chains, Sci Adv, 5, eaau8857, 10.1126/sciadv.aau8857 Xia, 2009, Direct activation of protein kinases by unanchored polyubiquitin chains, Nature, 461, 114, 10.1038/nature08247 Reyes-Turcu, 2006, The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin, Cell, 124, 1197, 10.1016/j.cell.2006.02.038 Maelfait, 2012, Emerging role of ubiquitination in antiviral RIG-I signaling, Microbiol Mol Biol Rev, 76, 33, 10.1128/MMBR.05012-11 van Huizen, 2019, The role of atypical ubiquitin chains in the regulation of the antiviral innate immune response, Front Cell Dev Biol, 7, 392, 10.3389/fcell.2019.00392 Hoffmann, 2002, The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation, Science, 298, 1241, 10.1126/science.1071914 Lee, 2014, Fold change of nuclear NF-KB determines TNF-induced transcription in single cells, Mol Cell, 53, 867, 10.1016/j.molcel.2014.01.026 Krump, 2018, Molecular mechanisms of viral oncogenesis in humans, Nat Rev Microbiol, 16, 684, 10.1038/s41579-018-0064-6 Yu, 2011, Viral effects on metabolism: changes in glucose and glutamine utilization during human cytomegalovirus infection, Trends Microbiol, 19, 360, 10.1016/j.tim.2011.04.002 Heaton, 2011, Multifaceted roles for lipids in viral infection, Trends Microbiol, 19, 368, 10.1016/j.tim.2011.03.007 Saka, 2012, Emerging roles for lipid droplets in immunity and host-pathogen interactions, Annu Rev Cell Dev Biol, 28, 411, 10.1146/annurev-cellbio-092910-153958 Agnello, 1999, Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor, Proc Natl Acad Sci USA, 96, 12766, 10.1073/pnas.96.22.12766 Zaitseva, 2010, Dengue virus ensures its fusion in late endosomes using compartment-specific lipids, PLoS Pathog, 6, e1001131, 10.1371/journal.ppat.1001131 York, 2015, Limiting cholesterol biosynthetic flux spontaneously engages Type I IFN signaling, Cell, 163, 1716, 10.1016/j.cell.2015.11.045 O’Neill, 2015, How low cholesterol is good for anti-viral immunity, Cell, 163, 1572, 10.1016/j.cell.2015.12.004 MacMicking, 2012, Interferon-inducible effector mechanisms in cell-autonomous immunity, Nat Rev Immunol, 12, 367, 10.1038/nri3210 Schneider, 2014, Interferon-stimulated genes: a complex web of host defenses, Annu Rev Immunol, 32, 513, 10.1146/annurev-immunol-032713-120231 Gu, 2019, Loss of EZH2 reprograms BCAA metabolism to drive leukemic transformation, Cancer Discov, 9, 1228, 10.1158/2159-8290.CD-19-0152 Tarazona-Santos, 2013, Evolutionary dynamics of the human NADPH oxidase genes CYBB, CYBA, NCF2, and NCF4: functional implications, Mol Biol Evol, 30, 2157, 10.1093/molbev/mst119 Jacob, 2012, Lupus-associated causal mutation in neutrophil cytosolic factor 2 (NCF2) brings unique insights to the structure and function of NADPH oxidase, Proc Natl Acad Sci USA, 109, E59, 10.1073/pnas.1113251108 Chun, 2019, Recruitment of APOL1 kidney disease risk variants to lipid droplets attenuates cell toxicity, Proc Natl Acad Sci USA, 116, 3712, 10.1073/pnas.1820414116 Guemez-Gamboa, 2015, Inactivating mutations in MFSD2A, required for omega-3 fatty acid transport in brain, cause a lethal microcephaly syndrome, Nat Genet, 47, 809, 10.1038/ng.3311 Ungaro, 2017, MFSD2A promotes endothelial generation of inflammation-resolving lipid mediators and reduces colitis in mice, Gastroenterology, 153, 1363, 10.1053/j.gastro.2017.07.048 Munger, 2008, Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy, Nat Biotechnol, 26, 1179, 10.1038/nbt.1500 Balzarini, 2007, Targeting the glycans of glycoproteins: a novel paradigm for antiviral therapy, Nat Rev Microbiol, 5, 583, 10.1038/nrmicro1707 Fritsch, 2019, Caspase-8 is the molecular switch for apoptosis, necroptosis and pyroptosis, Nature, 575, 683, 10.1038/s41586-019-1770-6 Wang, 2016, Association of SLCO2B1 genotypes with time to progression and overall survival in patients receiving androgen-deprivation therapy for prostate cancer, JCO, 34, 352, 10.1200/JCO.2015.62.5988 Jackson, 2000, Cytohesins and centaurins: mediators of PI 3-kinase-regulated Arf signaling, Trends Biochem Sci, 25, 489, 10.1016/S0968-0004(00)01644-3 Yin, 2019, Pharmacological targeting of STK19 inhibits oncogenic NRAS-driven melanomagenesis, Cell, 176, 1113, 10.1016/j.cell.2019.01.002 Suzuki, 2014, Exposure of phosphatidylserine by Xk-related protein family members during apoptosis, J Biol Chem, 289, 30257, 10.1074/jbc.M114.583419 Laukoter, 2020, Imprinted Cdkn1c genomic locus cell-autonomously promotes cell survival in cerebral cortex development, Nat Commun, 11, 195, 10.1038/s41467-019-14077-2 Hu, 2016, Liver-enriched gene 1, a glycosylated secretory protein, binds to FGFR and mediates an anti-stress pathway to protect liver development in zebrafish, PLoS Genet, 12, e1005881, 10.1371/journal.pgen.1005881 Wei, 2019, Bioinformatics-based analysis reveals elevated MFSD12 as a key promoter of cell proliferation and a potential therapeutic target in melanoma, Oncogene, 38, 1876, 10.1038/s41388-018-0531-6