SARS-CoV-2 proteases PLpro and 3CLpro cleave IRF3 and critical modulators of inflammatory pathways (NLRP12 and TAB1): implications for disease presentation across species

References

• Acter T, Uddin N, Das J, et al. Evolution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) as coronavirus disease 2019 (COVID-19) pandemic: A global health emergency. Sci Total Environ. 2020;730:138996.
   PubMed Web of Science ®Google Scholar
• Bahadur S, Long W, Shuaib M. Human coronaviruses with emphasis on the COVID-19 outbreak. Virus Disease. 2020;31(2):80–84.
   Google Scholar
• Qiu Y, Xu K. Functional studies of the coronavirus nonstructural proteins. STE Med. 2020;1(2):e39. https://doi.org/https://doi.org/10.37175/stemedecine.v1i2.39
   Google Scholar
• Klemm T, Ebert G, Calleja DJ, et al. Mechanism and inhibition of the papain-like protease, PLpro, of SARS-CoV-2. Embo J. 2020;39(18):e106275.
   PubMed Web of Science ®Google Scholar
• Zhang L, Lin D, Sun X, et al. Crystal structure of SARS-CoV-2 main protease provides a basis for design of improved α-ketoamide inhibitors. Science. 2020;368(6489):409–412.
   PubMed Web of Science ®Google Scholar
• Dai W, Zhang B, Jiang X-M, et al. Structure-based design of antiviral drug candidates targeting the SARS-CoV-2 main protease. Science. 2020;368(6497):1331–1335.
   PubMed Web of Science ®Google Scholar
• Macchiagodena M, Pagliai M, Procacci P. Identification of potential binders of the main protease 3CLpro of the COVID-19 via structure-based ligand design and molecular modeling. Chem Phys Lett. 2020;750:137489.
   PubMed Web of Science ®Google Scholar
• ul Qamar MT, Alqahtani SM, Alamri MA, et al. Structural basis of SARS-CoV-2 3CLpro and anti-COVID-19 drug discovery from medicinal plants. J Pharm Anal. 2020;10(4):313–319.
   PubMed Web of Science ®Google Scholar
• Chen YW, Yiu CB, Wong KY. Prediction of the SARS-CoV-2 (2019-nCoV) 3C-like protease (3CL (pro)) structure: virtual screening reveals velpatasvir, ledipasvir, and other drug repurposing candidates. F1000Res. 2020;9:129.
   PubMedGoogle Scholar
• Kandeel M, Al-Nazawi M. Virtual screening and repurposing of FDA approved drugs against COVID-19 main protease. Life Sci. 2020;251:117627.
   PubMed Web of Science ®Google Scholar
• Ke YY, Peng TT, Yeh TK, et al. Artificial intelligence approach fighting COVID-19 with repurposing drugs. Biomed J. 2020;43(4):355–362.
   PubMed Web of Science ®Google Scholar
• Frieman M, Heise M, Baric R. SARS coronavirus and innate immunity. Virus Res. 2008;133(1):101–112.
   PubMed Web of Science ®Google Scholar
• Lei J, Hilgenfeld R. RNA-virus proteases counteracting host innate immunity. FEBS Lett. 2017;591(20):3190–3210.
   Web of Science ®Google Scholar
• Niemeyer D, Mösbauer K, Klein EM, et al. The papain-like protease determines a virulence trait that varies among members of the SARS-coronavirus species. PLoS Pathog. 2018;14(9):e1007296.
   Web of Science ®Google Scholar
• Chen X, Yang X, Zheng Y, et al. SARS coronavirus papain-like protease inhibits the type I interferon signaling pathway through interaction with the STING-TRAF3-TBK1 complex. Protein Cell. 2014;5(5):369–381.
   PubMed Web of Science ®Google Scholar
• Frieman M, Ratia K, Johnston RE, et al. Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-κB signaling. J Virol. 2009;83(13):6689–6705.
   PubMed Web of Science ®Google Scholar
• Yang X, Chen X, Bian G, et al. Proteolytic processing, deubiquitinase and interferon antagonist activities of Middle East respiratory syndrome coronavirus papain-like protease. J Gen Virol. 2014;95(Pt 3):614–626.
   PubMed Web of Science ®Google Scholar
• Sun L, Xing Y, Chen X, et al. Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS One. 2012;7(2):e30802.
   PubMed Web of Science ®Google Scholar
• Wang G, Chen G, Zheng D, et al. PLP2 of mouse hepatitis virus A59 (MHV-A59) targets TBK1 to negatively regulate cellular type I interferon signaling pathway. PLoS One. 2011;6(2):e17192.
   PubMed Web of Science ®Google Scholar
• Li SW, Wang CY, Jou YJ, et al. 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(5):678.
   Web of Science ®Google Scholar
• Matthews K, Schäfer A, Pham A, et al. The SARS coronavirus papain like protease can inhibit IRF3 at a post activation step that requires deubiquitination activity. Virol J. 2014;11(1):209.
   Web of Science ®Google Scholar
• Devaraj SG, Wang N, Chen Z, et al. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J Biol Chem. 2007;282(44):32208–32221.
   PubMed Web of Science ®Google Scholar
• Mielech AM, Kilianski A, Baez-Santos YM, et al. MERS-CoV papain-like protease has deISGylating and deubiquitinating activities. Virology. 2014;450-451:64–70.
   PubMed Web of Science ®Google Scholar
• Lei J, Kusov Y, Hilgenfeld R. Nsp3 of coronaviruses: structures and functions of a large multi-domain protein. Antiviral Res. 2018;149:58–74.
   PubMed Web of Science ®Google Scholar
• Békés M, van der Heden van Noort G, Ekkebus R, et al. Recognition of Lys48-linked Di-ubiquitin and deubiquitinating activities of the SARS coronavirus papain-like protease. Mol Cell. 2016;62(4):572–585.
   PubMed Web of Science ®Google Scholar
• Wang C-Y, Lu C-Y, Li S-W, et al. SARS coronavirus papain-like protease up-regulates the collagen expression through non-Samd TGF-β1 signaling. Virus Res. 2017;235:58–66.
   Web of Science ®Google Scholar
• Ma-Lauer Y, Carbajo-Lozoya J, Hein MY, et al. P53 down-regulates SARS coronavirus replication and is targeted by the SARS-unique domain and PLpro via E3 ubiquitin ligase RCHY1. Proc Natl Acad Sci U S A. 2016;113(35):E5192–E5201.
   PubMed Web of Science ®Google Scholar
• Chen S, Tian J, Li Z, et al. Feline infectious peritonitis virus Nsp5 inhibits type I interferon production by cleaving NEMO at multiple sites. Viruses. 2019;12(1):43.
   Web of Science ®Google Scholar
• Zhu X, Chen J, Tian L, et al. Porcine deltacoronavirus nsp5 cleaves DCP1A To decrease Its antiviral activity. J Virol. 2020;94(15):e02162–19.
   Web of Science ®Google Scholar
• Lin C-W, Lin K-H, Hsieh T-H, et al. Severe acute respiratory syndrome coronavirus 3C-like protease-induced apoptosis. FEMS Immunol Med Microbiol. 2006;46(3):375–380.
   PubMedGoogle Scholar
• Shin D, Mukherjee R, Grewe D, et al. Papain-like protease regulates SARS-CoV-2 viral spread and innate immunity. Nature. 2020;587:657–662.
   PubMed Web of Science ®Google Scholar
• Chen G, Wu D, Guo W, et al. Clinical and immunological features of severe and moderate coronavirus disease 2019. J Clin Invest. 2020;130(5):2620–2629.
   PubMed Web of Science ®Google Scholar
• Giamarellos-Bourboulis EJ, Netea MG, Rovina N, et al. Complex immune Dysregulation in COVID-19 patients with severe respiratory Failure. Cell Host Microbe. 2020;27(6):992–1000.e3.
   PubMed Web of Science ®Google Scholar
• Breuer K, Foroushani AK, Laird MR, et al. InnateDB: systems biology of innate immunity and beyond–recent updates and continuing curation. Nucleic Acids Res. 2013;41:D1228–D1233.
   PubMed Web of Science ®Google Scholar
• Wishart DS, Li C, Marcu A, et al. Pathbank: a comprehensive pathway database for model organisms. Nucleic Acids Res. 2019;48(D1):D470–D478.
   Web of Science ®Google Scholar
• Hunter DJB, Bhumkar A, Giles N, et al. Unexpected instabilities explain batch-to-batch variability in cell-free protein expression systems. Biotechnol Bioeng. 2018;115(8):1904–1914.
   Web of Science ®Google Scholar
• Gambin Y, Giles N, O'Carroll A, et al. Single-Molecule fluorescence reveals the oligomerization and folding steps driving the Prion-like Behavior of ASC. J Mol Biol. 2018;430(4):491–508.
   PubMed Web of Science ®Google Scholar
• O’Carroll A, Chauvin B, Brown JWP, et al. Pathological mutations differentially affect the self-assembly and polymerisation of the innate immune system signalling adaptor molecule MyD88. BMC Biol. 2018;16(1):149.
   Web of Science ®Google Scholar
• Ve T, Vajjhala PR, Hedger A, et al. Structural basis of TIR-domain-assembly formation in MAL- and MyD88-dependent TLR4 signaling. Nat Struct Mol Biol. 2017;24(9):743–751.
   PubMed Web of Science ®Google Scholar
• Sierecki E, Giles N, Polinkovsky M, et al. A cell-free approach to accelerate the study of protein-protein interactions in vitro. Interface Focus. 2013;3(5):20130018.
   Web of Science ®Google Scholar
• Xie X, Muruato A, Lokugamage KG, et al. An infectious cDNA clone of SARS-CoV-2. Cell Host Microbe. 2020;27(5):841–848. e3.
   PubMed Web of Science ®Google Scholar
• Steinbeck J, Ross IL, Rothnagel R, et al. Structure of a PSI-LHCI-cyt b(6)f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions. Proc Natl Acad Sci USA. 2018;115(41):10517–10522.
   Web of Science ®Google Scholar
• Jefferies CA. Regulating IRFs in IFN driven disease. Front Immunol. 2019;10(325).
   Google Scholar
• Zhao B, Shu C, Gao X, et al. Structural basis for concerted recruitment and activation of IRF-3 by innate immune adaptor proteins. Proc Natl Acad Sci USA. 2016;113(24):E3403–E3412.
   PubMed Web of Science ®Google Scholar
• Lin R, Heylbroeck C, Pitha PM, et al. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol Cell Biol. 1998;18(5):2986–2996.
   PubMed Web of Science ®Google Scholar
• Shi H-X, Yang K, Liu X, et al. Positive regulation of interferon regulatory factor 3 activation by Herc5 via ISG15 modification. Mol Cell Biol. 2010;30(10):2424–2436.
   PubMed Web of Science ®Google Scholar
• Antonczyk A, Krist B, Sajek M, et al. Direct inhibition of IRF-dependent transcriptional regulatory mechanisms associated with disease. Front Immunol. 2019;10:1176. https://doi.org/https://doi.org/10.3389/fimmu.2019.01176
   PubMed Web of Science ®Google Scholar
• Blanco-Melo D, Nilsson-Payant BE, Liu WC, et al. Imbalanced host response to SARS-CoV-2 drives development of COVID-19. Cell. 2020;181(5):1036–1045.e9.
   PubMed Web of Science ®Google Scholar
• Rut W, Groborz K, Zhang L, et al. Substrate specificity profiling of SARS-CoV-2 Mpro protease provides basis for anti-COVID-19 drug design. BioRxiv. 2020. https://doi.org/https://doi.org/10.1101/2020.03.07.981928
   Google Scholar
• Zhong Y, Kinio A, Saleh M. Functions of NOD-like receptors in human Diseases. Front Immunol. 2013;4:333.
   PubMed Web of Science ®Google Scholar
• Wang L, Manji GA, Grenier JM, et al. PYPAF7, a novel PYRIN-containing Apaf1-like protein that regulates activation of NF-kappa B and caspase-1-dependent cytokine processing. J Biol Chem. 2002;277(33):29874–29880.
   Web of Science ®Google Scholar
• Coulon P-G, Dhanushkodi N, Prakash S, et al. NLRP3, NLRP12, and IFI16 inflammasomes induction and caspase-1 activation triggered by Virulent HSV-1 strains are associated with severe corneal inflammatory herpetic disease. Front Immunol. 2019;10:1631.
   PubMed Web of Science ®Google Scholar
• Coutermarsh-Ott S, Eden K, Allen IC. Beyond the inflammasome: regulatory NOD-like receptor modulation of the host immune response following virus exposure. J Gen Virol. 2016;97(4):825–838.
   Web of Science ®Google Scholar
• Chen S-T, Chen L, Lin DS-C, et al. NLRP12 regulates anti-viral RIG-I activation via interaction with TRIM25. Cell Host Microbe. 2019;25(4):602–616.e7.
   Web of Science ®Google Scholar
• Williams KL, Taxman DJ, Linhoff MW, et al. Cutting edge: Monarch-1: a pyrin/nucleotide-binding domain/leucine-rich repeat protein that controls classical and nonclassical MHC class I genes. J Immunol. 2003;170(11):5354–5358.
   Web of Science ®Google Scholar
• Mogensen TH. IRF and STAT transcription factors - from Basic biology to Roles in infection, Protective immunity, and primary Immunodeficiencies. Front Immunol. 2019;9:3047.
   PubMed Web of Science ®Google Scholar
• Chiang H-S, Liu HM. The molecular basis of viral inhibition of IRF- and STAT-dependent immune responses. Front Immunol. 2019;9:3086.
   Web of Science ®Google Scholar
• Lei X, Han N, Xiao X, et al. Enterovirus 71 3C inhibits cytokine expression through cleavage of the TAK1/TAB1/TAB2/TAB3 complex. J Virol. 2014;88(17):9830–9841.
   PubMed Web of Science ®Google Scholar
• Xiang Z, Liu L, Lei X, et al. 3C protease of enterovirus D68 inhibits cellular Defense mediated by interferon regulatory factor 7. J Virol. 2016;90(3):1613–1621.
   PubMed Web of Science ®Google Scholar
• Nelemans T, Kikkert M. Viral innate immune Evasion and the Pathogenesis of Emerging RNA virus infections. Viruses. 2019;11(10):961.
   PubMed Web of Science ®Google Scholar
• Zheng D, Chen G, Guo B, et al. PLP2, a potent deubiquitinase from murine hepatitis virus, strongly inhibits cellular type I interferon production. Cell Res. 2008;18(11):1105–1113.
   PubMed Web of Science ®Google Scholar
• Trouillet-Assant S, Viel S, Gaymard A, et al. Type I IFN immunoprofiling in COVID-19 patients. J Allergy Clin Immunol. 2020;146(1):206–208.
   PubMed Web of Science ®Google Scholar
• Hirata Y, Takahashi M, Morishita T, et al. Post-Translational modifications of the TAK1-TAB complex. Int J Mol Sci. 2017;18(1):205.
   Web of Science ®Google Scholar
• Dai L, Aye Thu C, Liu X-Y, et al. TAK1, more than just innate immunity. IUBMB Life. 2012;64(10):825–834.
   Web of Science ®Google Scholar
• Malireddi RKS, Kesavardhana S, Kanneganti T-D. ZBP1 and TAK1: master regulators of NLRP3 inflammasome/pyroptosis, apoptosis, and Necroptosis (PAN-optosis). Front Cell Infect Microbiol. 2019;9:406–406.
   PubMed Web of Science ®Google Scholar
• Ninomiya-Tsuji J, Kishimoto K, Hiyama A, et al. The kinase TAK1 can activate the NIK-IκB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature. 1999;398(6724):252–256.
   PubMed Web of Science ®Google Scholar
• Wald D, Commane M, Stark GR, et al. IRAK and TAK1 are required for IL-18-mediated signaling. Eur J Immunol. 2001;31(12):3747–3754.
   Web of Science ®Google Scholar
• Ge B, Xiong X, Jing Q, et al. TAB1β (Transforming growth factor-β-activated protein kinase 1-binding protein 1β), a novel Splicing Variant of TAB1 that Interacts with p38α but Not TAK1. J Biol Chem. 2003;278(4):2286–2293.
   Web of Science ®Google Scholar
• Makeeva N, Roomans GM, Myers JW, et al. Transforming growth factor-β-activated protein kinase 1-binding protein (TΑΒ)-1α, But Not ΤΑΒ1β, mediates cytokine-induced p38 Mitogen-activated protein kinase phosphorylation and cell death in Insulin-Producing cells. Endocrinology. 2008;149(1):302–309.
   Web of Science ®Google Scholar
• Wolf A, Beuerlein K, Eckart C, et al. Identification and functional Characterization of novel phosphorylation sites in TAK1-binding protein (TAB) 1. PLoS ONE. 2011;6(12):e29256.
   Web of Science ®Google Scholar
• Wilmanski JM, Petnicki-Ocwieja T, Kobayashi KS. NLR proteins: integral members of innate immunity and mediators of inflammatory diseases. J Leukoc Biol. 2008;83(1):13–30.
   Web of Science ®Google Scholar
• Schroder K, Tschopp J. The inflammasomes. Cell. 2010;140(6):821–832.
   PubMed Web of Science ®Google Scholar
• Ye Z, Lich JD, Moore CB, et al. ATP binding by monarch-1/NLRP12 is critical for its inhibitory function. Mol Cell Biol. 2008;28(5):1841–1850.
   PubMed Web of Science ®Google Scholar
• Duncan JA, Bergstralh DT, Wang Y, et al. Cryopyrin/NALP3 binds ATP/dATP, is an ATPase, and requires ATP binding to mediate inflammatory signaling. Proc Natl Acad Sci U S A. 2007;104(19):8041–8046.
   PubMed Web of Science ®Google Scholar
• Lu A, Magupalli V, Ruan J, et al. Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell. 2014;156(6):1193–1206.
   PubMed Web of Science ®Google Scholar
• Tuncer S, Fiorillo MT, Sorrentino R. The multifaceted nature of NLRP12. J Leukoc Biol. 2014;96(6):991–1000.
   Web of Science ®Google Scholar
• Tay MZ, Poh CM, Rénia L, et al. The trinity of COVID-19: immunity, inflammation and intervention. Nat Rev Immunol. 2020;20(6):363–374.
   PubMed Web of Science ®Google Scholar
• Gurung P, Kanneganti TD. NLRP12 in autoimmune diseases. Oncotarget. 2015;6(24):19950–1.
   Google Scholar
• Jeru I, Duquesnoy P, Fernandes-Alnemri T, et al. Mutations in NALP12 cause hereditary periodic fever syndromes. Proc Natl Acad Sci U S A. 2008;105(5):1614–1619.
   PubMed Web of Science ®Google Scholar
• Huang Y-H, Lo M-H, Cai X-Y, et al. Epigenetic hypomethylation and upregulation of NLRC4 and NLRP12 in Kawasaki disease. Oncotarget. 2018;9(27):18939–18948.
   PubMedGoogle Scholar
• Verdoni L, Mazza A, Gervasoni A, et al. An outbreak of severe Kawasaki-like disease at the Italian epicentre of the SARS-CoV-2 epidemic: an observational cohort study. Lancet. 2020;395(10239):1171–1178.
   Web of Science ®Google Scholar
• Licciardi F, Pruccoli G, Denina M, et al. SARS-CoV-2-Induced Kawasaki-like hyperinflammatory syndrome: a novel COVID phenotype in children. Pediatrics. 2020;146(2):e20201711.
   Web of Science ®Google Scholar
• Shang J, Ye G, Shi K, et al. Structural basis of receptor recognition by SARS-CoV-2. Nature. 2020;581(7807):221–224.
   PubMed Web of Science ®Google Scholar
• Shi J, Wen Z, Zhong G, et al. Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. Science. 2020;368(6494):1016–1020.
   PubMed Web of Science ®Google Scholar
• Olival KJ, Cryan PM, Amman BR, et al. Possibility for reverse zoonotic transmission of SARS-CoV-2 to free-ranging wildlife: A case study of bats. PLoS Pathog. 2020;16(9):e1008758.
   Web of Science ®Google Scholar