The Wnt/β-catenin pathway is important for replication of SARS-CoV-2 and other pathogenic RNA viruses

DOI record: { "DOI": "10.1038/s44298-024-00018-4", "ISSN": [ "2948-1767" ], "URL": "http://dx.doi.org/10.1038/s44298-024-00018-4", "abstract": "<jats:title>Abstract</jats:title><jats:p>Understanding how viruses affect cellular pathways during infection may facilitate development of host cell-targeted therapeutics with broad-spectrum antiviral activity. The interferon (IFN) response is critical for reducing replication and pathogenesis of many viruses including Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), the causative agent of COVID-19. Mounting evidence indicates that peroxisomes which are best known as metabolic organelles, function in the IFN response. Recently, we reported that the Wnt/β-catenin signaling pathway strongly suppresses peroxisome biogenesis. Here, we show that SARS-CoV-2 infection activates Wnt/β-catenin signaling and hypothesized that pharmacological inhibition of this pathway would result in increased peroxisome formation and enhanced IFN production. Indeed, Wnt/β-catenin signaling potently inhibits replication of SARS-CoV-2 and other pathogenic RNA viruses in vitro and reduces viral load, inflammation and clinical symptoms in a mouse model of COVID-19. As such, targeting this cellular pathway may have prophylactic and/or therapeutic value in reducing the disease burden caused by emerging viral pathogens.</jats:p>", "alternative-id": [ "18" ], "article-number": "6", "assertion": [ { "group": { "label": "Article History", "name": "ArticleHistory" }, "label": "Received", "name": "received", "order": 1, "value": "26 September 2023" }, { "group": { "label": "Article History", "name": "ArticleHistory" }, "label": "Accepted", "name": "accepted", "order": 2, "value": "10 January 2024" }, { "group": { "label": "Article History", "name": "ArticleHistory" }, "label": "First Online", "name": "first_online", "order": 3, "value": "21 February 2024" }, { "group": { "label": "Competing interests", "name": "EthicsHeading" }, "name": "Ethics", "order": 1, "value": "T.C.H., Z.X. and C.P.W. are co-inventors on US patent application (PCT/CA2021/051077) entitled: Use of WNT/BETA-Catenin Pathway Inhibitors to Block Replication of SARS-COV-2 and other pathogenic viruses tonix pharmaceuticals had no role in design or interpretation of the experiments described in this study." } ], "author": [ { "affiliation": [], "family": "Xu", "given": "Zaikun", "sequence": "first" }, { "affiliation": [], "family": "Elaish", "given": "Mohamed", "sequence": "additional" }, { "affiliation": [], "family": "Wong", "given": "Cheung Pang", "sequence": "additional" }, { "affiliation": [], "family": "Hassan", "given": "Bardes B.", "sequence": "additional" }, { "affiliation": [], "family": "Lopez-Orozco", "given": "Joaquin", "sequence": "additional" }, { "affiliation": [], "family": "Felix-Lopez", "given": "Alberto", "sequence": "additional" }, { "affiliation": [], "family": "Ogando", "given": "Natacha S.", "sequence": "additional" }, { "affiliation": [], "family": "Nagata", "given": "Les", "sequence": "additional" }, { "affiliation": [], "family": "Mahal", "given": "Lara K.", "sequence": "additional" }, { "affiliation": [], "family": "Kumar", "given": "Anil", "sequence": "additional" }, { "affiliation": [], "family": "Wilson", "given": "Joyce A.", "sequence": "additional" }, { "affiliation": [], "family": "Noyce", "given": "Ryan", "sequence": "additional" }, { "affiliation": [], "family": "Mayers", "given": "Irv", "sequence": "additional" }, { "affiliation": [], "family": "Power", "given": "Christopher", "sequence": "additional" }, { "affiliation": [], "family": "Evans", "given": "David", "sequence": "additional" }, { "affiliation": [], "family": "Hobman", "given": "Tom C.", "sequence": "additional" } ], "container-title": "npj Viruses", "container-title-short": "npj Viruses", "content-domain": { "crossmark-restriction": false, "domain": [ "link.springer.com" ] }, "created": { "date-parts": [ [ 2024, 2, 21 ] ], "date-time": "2024-02-21T11:03:49Z", "timestamp": 1708513429000 }, "deposited": { "date-parts": [ [ 2024, 2, 21 ] ], "date-time": "2024-02-21T11:05:21Z", "timestamp": 1708513521000 }, "indexed": { "date-parts": [ [ 2024, 8, 8 ] ], "date-time": "2024-08-08T05:55:45Z", "timestamp": 1723096545780 }, "is-referenced-by-count": 1, "issue": "1", "issued": { "date-parts": [ [ 2024, 2, 21 ] ] }, "journal-issue": { "issue": "1", "published-online": { "date-parts": [ [ 2024, 12 ] ] } }, "language": "en", "license": [ { "URL": "https://creativecommons.org/licenses/by/4.0", "content-version": "tdm", "delay-in-days": 0, "start": { "date-parts": [ [ 2024, 2, 21 ] ], "date-time": "2024-02-21T00:00:00Z", "timestamp": 1708473600000 } }, { "URL": "https://creativecommons.org/licenses/by/4.0", "content-version": "vor", "delay-in-days": 0, "start": { "date-parts": [ [ 2024, 2, 21 ] ], "date-time": "2024-02-21T00:00:00Z", "timestamp": 1708473600000 } } ], "link": [ { "URL": "https://www.nature.com/articles/s44298-024-00018-4.pdf", "content-type": "application/pdf", "content-version": "vor", "intended-application": "text-mining" }, { "URL": "https://www.nature.com/articles/s44298-024-00018-4", "content-type": "text/html", "content-version": "vor", "intended-application": "text-mining" }, { "URL": "https://www.nature.com/articles/s44298-024-00018-4.pdf", "content-type": "application/pdf", "content-version": "vor", "intended-application": "similarity-checking" } ], "member": "297", "original-title": [], "prefix": "10.1038", "published": { "date-parts": [ [ 2024, 2, 21 ] ] }, "published-online": { "date-parts": [ [ 2024, 2, 21 ] ] }, "publisher": "Springer Science and Business Media LLC", "reference": [ { "DOI": "10.1056/NEJMoa2119451", "author": "N Andrews", "doi-asserted-by": "publisher", "first-page": "1532", "journal-title": "N. Engl. J. Med.", "key": "18_CR1", "unstructured": "Andrews, N. et al. Covid-19 vaccine effectiveness against the omicron (B.1.1.529) Variant. N. Engl. J. Med. 386, 1532–1546 (2022).", "volume": "386", "year": "2022" }, { "DOI": "10.1016/S0140-6736(22)00152-0", "author": "DR Feikin", "doi-asserted-by": "publisher", "first-page": "924", "journal-title": "Lancet", "key": "18_CR2", "unstructured": "Feikin, D. R. et al. Duration of effectiveness of vaccines against SARS-CoV-2 infection and COVID-19 disease: results of a systematic review and meta-regression. Lancet 399, 924–944 (2022).", "volume": "399", "year": "2022" }, { "DOI": "10.1038/s41579-021-00573-0", "author": "WT Harvey", "doi-asserted-by": "publisher", "first-page": "409", "journal-title": "Nat. Rev. Microbiol.", "key": "18_CR3", "unstructured": "Harvey, W. T. et al. SARS-CoV-2 variants, spike mutations and immune escape. Nat. Rev. Microbiol. 19, 409–424 (2021).", "volume": "19", "year": "2021" }, { "DOI": "10.1038/s41586-022-04980-y", "author": "Y Cao", "doi-asserted-by": "publisher", "first-page": "593", "journal-title": "Nature", "key": "18_CR4", "unstructured": "Cao, Y. et al. BA.2.12.1, BA.4 and BA.5 escape antibodies elicited by Omicron infection. Nature 608, 593–602 (2022).", "volume": "608", "year": "2022" }, { "DOI": "10.1002/rmv.2381", "author": "LB Shrestha", "doi-asserted-by": "publisher", "first-page": "e2381", "journal-title": "Rev. Med. Virol.", "key": "18_CR5", "unstructured": "Shrestha, L. B., Foster, C., Rawlinson, W., Tedla, N. & Bull, R. A. Evolution of the SARS-CoV-2 omicron variants BA.1 to BA.5: Implications for immune escape and transmission. Rev. Med. Virol. 32, e2381 (2022).", "volume": "32", "year": "2022" }, { "DOI": "10.1038/s41591-021-01678-y", "author": "LA VanBlargan", "doi-asserted-by": "publisher", "first-page": "490", "journal-title": "Nat. Med.", "key": "18_CR6", "unstructured": "VanBlargan, L. A. et al. An infectious SARS-CoV-2 B.1.1.529 Omicron virus escapes neutralization by therapeutic monoclonal antibodies. Nat. Med. 28, 490–495 (2022).", "volume": "28", "year": "2022" }, { "DOI": "10.1126/sciadv.ade8778", "author": "SA Moghadasi", "doi-asserted-by": "publisher", "first-page": "eade8778", "journal-title": "Sci. Adv.", "key": "18_CR7", "unstructured": "Moghadasi, S. A. et al. Transmissible SARS-CoV-2 variants with resistance to clinical protease inhibitors. Sci. Adv. 9, eade8778 (2023).", "volume": "9", "year": "2023" }, { "DOI": "10.1371/journal.ppat.1009929", "author": "AM Szemiel", "doi-asserted-by": "publisher", "first-page": "e1009929", "journal-title": "PLoS Pathog.", "key": "18_CR8", "unstructured": "Szemiel, A. M. et al. In vitro selection of Remdesivir resistance suggests evolutionary predictability of SARS-CoV-2. PLoS Pathog. 17, e1009929 (2021).", "volume": "17", "year": "2021" }, { "DOI": "10.1038/s41586-021-03312-w", "author": "A Wahl", "doi-asserted-by": "publisher", "first-page": "451", "journal-title": "Nature", "key": "18_CR9", "unstructured": "Wahl, A. et al. SARS-CoV-2 infection is effectively treated and prevented by EIDD-2801. Nature 591, 451–457 (2021).", "volume": "591", "year": "2021" }, { "DOI": "10.1126/scitranslmed.abb5883", "author": "TP Sheahan", "doi-asserted-by": "publisher", "first-page": "eabb5883", "journal-title": "Sci. Transl. Med.", "key": "18_CR10", "unstructured": "Sheahan, T. P. et al. An orally bioavailable broad-spectrum antiviral inhibits SARS-CoV-2 in human airway epithelial cell cultures and multiple coronaviruses in mice. Sci. Transl. Med. 12, eabb5883 (2020).", "volume": "12", "year": "2020" }, { "DOI": "10.1074/jbc.RA120.013679", "author": "CJ Gordon", "doi-asserted-by": "publisher", "first-page": "6785", "journal-title": "J. Biol. Chem.", "key": "18_CR11", "unstructured": "Gordon, C. J. et al. Remdesivir is a direct-acting antiviral that inhibits RNA-dependent RNA polymerase from severe acute respiratory syndrome coronavirus 2 with high potency. J. Biol. Chem. 295, 6785–6797 (2020).", "volume": "295", "year": "2020" }, { "DOI": "10.1038/s41467-021-22580-8", "author": "K Rosenke", "doi-asserted-by": "publisher", "journal-title": "Nat. Commun.", "key": "18_CR12", "unstructured": "Rosenke, K. et al. Orally delivered MK-4482 inhibits SARS-CoV-2 replication in the Syrian hamster model. Nat. Commun. 12, 2295 (2021).", "volume": "12", "year": "2021" }, { "DOI": "10.1038/s41467-020-18096-2", "author": "W Vuong", "doi-asserted-by": "publisher", "journal-title": "Nat. Commun.", "key": "18_CR13", "unstructured": "Vuong, W. et al. Feline coronavirus drug inhibits the main protease of SARS-CoV-2 and blocks virus replication. Nat. Commun. 11, 4282 (2020).", "volume": "11", "year": "2020" }, { "DOI": "10.1126/science.abg5827", "author": "N Drayman", "doi-asserted-by": "publisher", "first-page": "931", "journal-title": "Science", "key": "18_CR14", "unstructured": "Drayman, N. et al. Masitinib is a broad coronavirus 3CL inhibitor that blocks replication of SARS-CoV-2. Science 373, 931–936 (2021).", "volume": "373", "year": "2021" }, { "DOI": "10.1038/s41586-021-03720-y", "author": "RE Chen", "doi-asserted-by": "publisher", "first-page": "103", "journal-title": "Nature", "key": "18_CR15", "unstructured": "Chen, R. E. et al. In vivo monoclonal antibody efficacy against SARS-CoV-2 variant strains. Nature 596, 103–108 (2021).", "volume": "596", "year": "2021" }, { "DOI": "10.1126/science.abe2402", "author": "A Baum", "doi-asserted-by": "publisher", "first-page": "1110", "journal-title": "Science", "key": "18_CR16", "unstructured": "Baum, A. et al. REGN-COV2 antibodies prevent and treat SARS-CoV-2 infection in rhesus macaques and hamsters. Science 370, 1110–1115 (2020).", "volume": "370", "year": "2020" }, { "DOI": "10.1056/NEJMoa2033130", "author": "A-TL-CS Group", "doi-asserted-by": "publisher", "first-page": "905", "journal-title": "N. Engl. J. Med.", "key": "18_CR17", "unstructured": "Group, A.-T. L.-C. S. et al. A neutralizing monoclonal antibody for hospitalized patients with Covid-19. N. Engl. J. Med. 384, 905–914 (2021).", "volume": "384", "year": "2021" }, { "DOI": "10.1073/pnas.2016093117", "author": "A Glasgow", "doi-asserted-by": "publisher", "first-page": "28046", "journal-title": "Proc. Natl. Acad. Sci. USA", "key": "18_CR18", "unstructured": "Glasgow, A. et al. Engineered ACE2 receptor traps potently neutralize SARS-CoV-2. Proc. Natl. Acad. Sci. USA 117, 28046–28055 (2020).", "volume": "117", "year": "2020" }, { "DOI": "10.1128/AAC.00491-21", "author": "D Limonta", "doi-asserted-by": "publisher", "first-page": "e0049121", "journal-title": "Antimicrob. Agents Chemother.", "key": "18_CR19", "unstructured": "Limonta, D. et al. Nodosome inhibition as a novel broad-spectrum antiviral strategy against arboviruses, enteroviruses and SARS-CoV-2. Antimicrob. Agents Chemother. 65, e0049121 (2021).", "volume": "65", "year": "2021" }, { "DOI": "10.1016/j.molcel.2021.05.023", "author": "W Kamel", "doi-asserted-by": "publisher", "first-page": "2851", "journal-title": "Mol. Cell", "key": "18_CR20", "unstructured": "Kamel, W. et al. Global analysis of protein-RNA interactions in SARS-CoV-2-infected cells reveals key regulators of infection. Mol. Cell 81, 2851–2867.e2857 (2021).", "volume": "81", "year": "2021" }, { "DOI": "10.1016/j.cell.2020.10.028", "author": "J Wei", "doi-asserted-by": "publisher", "first-page": "76", "journal-title": "Cell", "key": "18_CR21", "unstructured": "Wei, J. et al. Genome-wide CRISPR screens reveal host factors critical for SARS-CoV-2 infection. Cell 184, 76–91.e13 (2021).", "volume": "184", "year": "2021" }, { "DOI": "10.1073/pnas.2012939117", "author": "S Weston", "doi-asserted-by": "publisher", "first-page": "30687", "journal-title": "Proc. Natl. Acad. Sci. USA", "key": "18_CR22", "unstructured": "Weston, S. et al. The SKI complex is a broad-spectrum, host-directed antiviral drug target for coronaviruses, influenza, and filoviruses. Proc. Natl. Acad. Sci. USA 117, 30687–30698 (2020).", "volume": "117", "year": "2020" }, { "DOI": "10.1016/j.cell.2020.12.004", "author": "R Wang", "doi-asserted-by": "publisher", "first-page": "106", "journal-title": "Cell", "key": "18_CR23", "unstructured": "Wang, R. et al. Genetic screens identify host factors for SARS-CoV-2 and common cold coronaviruses. Cell 184, 106–119.e114 (2021).", "volume": "184", "year": "2021" }, { "DOI": "10.1016/j.cell.2021.02.008", "author": "L Sun", "doi-asserted-by": "publisher", "first-page": "1865", "journal-title": "Cell", "key": "18_CR24", "unstructured": "Sun, L. et al. In vivo structural characterization of the SARS-CoV-2 RNA genome identifies host proteins vulnerable to repurposed drugs. Cell 184, 1865–1883.e1820 (2021).", "volume": "184", "year": "2021" }, { "DOI": "10.1021/acsinfecdis.1c00017", "author": "SB Biering", "doi-asserted-by": "publisher", "first-page": "2337", "journal-title": "ACS Infect. Dis.", "key": "18_CR25", "unstructured": "Biering, S. B. et al. Screening a library of FDA-approved and bioactive compounds for antiviral activity against SARS-CoV-2. ACS Infect. Dis. 7, 2337–2351 (2021).", "volume": "7", "year": "2021" }, { "DOI": "10.1073/pnas.2105815118", "author": "C Mirabelli", "doi-asserted-by": "publisher", "first-page": "e2105815118", "journal-title": "Proc. Natl. Acad. Sci. USA", "key": "18_CR26", "unstructured": "Mirabelli, C. et al. Morphological cell profiling of SARS-CoV-2 infection identifies drug repurposing candidates for COVID-19. Proc. Natl. Acad. Sci. USA 118, e2105815118 (2021).", "volume": "118", "year": "2021" }, { "DOI": "10.1038/s41586-021-03491-6", "author": "L Braga", "doi-asserted-by": "publisher", "first-page": "88", "journal-title": "Nature", "key": "18_CR27", "unstructured": "Braga, L. et al. Drugs that inhibit TMEM16 proteins block SARS-CoV-2 spike-induced syncytia. Nature 594, 88–93 (2021).", "volume": "594", "year": "2021" }, { "DOI": "10.1016/j.celrep.2021.108959", "author": "M Dittmar", "doi-asserted-by": "publisher", "first-page": "108959", "journal-title": "Cell Rep.", "key": "18_CR28", "unstructured": "Dittmar, M. et al. Drug repurposing screens reveal cell-type-specific entry pathways and FDA-approved drugs active against SARS-Cov-2. Cell Rep. 35, 108959 (2021).", "volume": "35", "year": "2021" }, { "DOI": "10.1002/med.21664", "author": "X Ji", "doi-asserted-by": "publisher", "first-page": "1519", "journal-title": "Med. Res. Rev.", "key": "18_CR29", "unstructured": "Ji, X. & Li, Z. Medicinal chemistry strategies toward host targeting antiviral agents. Med. Res. Rev. 40, 1519–1557 (2020).", "volume": "40", "year": "2020" }, { "DOI": "10.2174/1874467210902010032", "author": "JD Burke", "doi-asserted-by": "publisher", "first-page": "32", "journal-title": "Curr. Mol. Pharmacol.", "key": "18_CR30", "unstructured": "Burke, J. D. & Fish, E. N. Antiviral strategies: the present and beyond. Curr. Mol. Pharmacol. 2, 32–39 (2009).", "volume": "2", "year": "2009" }, { "DOI": "10.1128/JVI.01410-20", "doi-asserted-by": "publisher", "key": "18_CR31", "unstructured": "Lokugamage, K. G. et al. Type I interferon susceptibility distinguishes SARS-CoV-2 from SARS-CoV. J. Virol. 94. https://doi.org/10.1128/JVI.01410-20 (2020)." }, { "DOI": "10.1007/s00430-022-00734-9", "author": "JH Lee", "doi-asserted-by": "publisher", "first-page": "125", "journal-title": "Med. Microbiol. Immunol.", "key": "18_CR32", "unstructured": "Lee, J. H., Koepke, L., Kirchhoff, F. & Sparrer, K. M. J. Interferon antagonists encoded by SARS-CoV-2 at a glance. Med. Microbiol. Immunol. 212, 125–131 (2023).", "volume": "212", "year": "2023" }, { "DOI": "10.1016/j.chom.2021.05.004", "author": "SA Lowery", "doi-asserted-by": "publisher", "first-page": "1052", "journal-title": "Cell Host Microbe", "key": "18_CR33", "unstructured": "Lowery, S. A., Sariol, A. & Perlman, S. Innate immune and inflammatory responses to SARS-CoV-2: Implications for COVID-19. Cell Host Microbe 29, 1052–1062 (2021).", "volume": "29", "year": "2021" }, { "DOI": "10.1016/j.antiviral.2020.104791", "author": "E Sallard", "doi-asserted-by": "publisher", "first-page": "104791", "journal-title": "Antiviral Res.", "key": "18_CR34", "unstructured": "Sallard, E., Lescure, F. X., Yazdanpanah, Y., Mentre, F. & Peiffer-Smadja, N. Type 1 interferons as a potential treatment against COVID-19. Antiviral Res. 178, 104791 (2020).", "volume": "178", "year": "2020" }, { "DOI": "10.1371/journal.ppat.1005264", "author": "S Bender", "doi-asserted-by": "publisher", "first-page": "e1005264", "journal-title": "PLoS Pathog.", "key": "18_CR35", "unstructured": "Bender, S. et al. Activation of type I and III interferon response by mitochondrial and peroxisomal MAVS and inhibition by hepatitis C virus. PLoS Pathog. 11, e1005264 (2015).", "volume": "11", "year": "2015" }, { "DOI": "10.1091/mbc.E21-02-0074", "author": "B Knoblach", "doi-asserted-by": "publisher", "first-page": "1273", "journal-title": "Mol. Biol. Cell", "key": "18_CR36", "unstructured": "Knoblach, B., Ishida, R., Hobman, T. C. & Rachubinski, R. A. Peroxisomes exhibit compromised structure and matrix protein content in SARS-CoV-2-infected cells. Mol. Biol. Cell 32, 1273–1282 (2021).", "volume": "32", "year": "2021" }, { "DOI": "10.1002/ana.26679", "author": "A Roczkowsky", "doi-asserted-by": "publisher", "first-page": "531", "journal-title": "Ann. Neurol.", "key": "18_CR37", "unstructured": "Roczkowsky, A. et al. COVID-19 induces neuroinflammation and suppresses peroxisomes in the brain. Ann. Neurol. 94, 531–546 (2023).", "volume": "94", "year": "2023" }, { "DOI": "10.1128/JVI.01677-17", "doi-asserted-by": "publisher", "key": "18_CR38", "unstructured": "Zhang, Q., Ke, H., Blikslager, A., Fujita, T. & Yoo, D. Type III interferon restriction by porcine epidemic diarrhea virus and the role of viral protein nsp1 in IRF1 signaling. J. Virol. 92, https://doi.org/10.1128/JVI.01677-17 (2018).." }, { "DOI": "10.1128/JVI.01365-15", "author": "J You", "doi-asserted-by": "publisher", "first-page": "12349", "journal-title": "J. Virol.", "key": "18_CR39", "unstructured": "You, J. et al. Flavivirus infection impairs peroxisome biogenesis and early antiviral signaling. J. Virol. 89, 12349–12361 (2015).", "volume": "89", "year": "2015" }, { "DOI": "10.1371/journal.ppat.1006360", "author": "Z Xu", "doi-asserted-by": "publisher", "first-page": "e1006360", "journal-title": "PLoS Pathog.", "key": "18_CR40", "unstructured": "Xu, Z. et al. MicroRNAs upregulated during HIV infection target peroxisome biogenesis factors: Implications for virus biology, disease mechanisms and neuropathology. PLoS Pathog. 13, e1006360 (2017).", "volume": "13", "year": "2017" }, { "DOI": "10.3390/cells8070725", "author": "CP Wong", "doi-asserted-by": "publisher", "first-page": "725", "journal-title": "Cells", "key": "18_CR41", "unstructured": "Wong, C. P. et al. Interplay between Zika Virus and Peroxisomes during Infection. Cells 8, 725 (2019).", "volume": "8", "year": "2019" }, { "DOI": "10.1128/mBio.03395-19", "author": "Z Xu", "doi-asserted-by": "publisher", "first-page": "e03395", "journal-title": "mBio", "key": "18_CR42", "unstructured": "Xu, Z., Lodge, R., Power, C., Cohen, E. A. & Hobman, T. C. The HIV-1 accessory protein VPU downregulates peroxisome biogenesis. mBio 11, e03395–19 (2020).", "volume": "11", "year": "2020" }, { "DOI": "10.1183/13993003.01531-2020", "author": "EY Choi", "doi-asserted-by": "publisher", "first-page": "2001531", "journal-title": "Eur. Respir. J.", "key": "18_CR43", "unstructured": "Choi, E. Y. et al. Wnt5a and Wnt11 as acute respiratory distress syndrome biomarkers for severe acute respiratory syndrome coronavirus 2 patients. Eur. Respir. J. 56, 2001531 (2020).", "volume": "56", "year": "2020" }, { "DOI": "10.3390/cancers12123638", "author": "MJ Kim", "doi-asserted-by": "publisher", "first-page": "3638", "journal-title": "Cancers", "key": "18_CR44", "unstructured": "Kim, M. J., Huang, Y. & Park, J. I. Targeting Wnt signaling for gastrointestinal cancer therapy: present and evolving views. Cancers 12, 3638 (2020).", "volume": "12", "year": "2020" }, { "DOI": "10.1038/cr.2011.127", "author": "J Gwak", "doi-asserted-by": "publisher", "first-page": "237", "journal-title": "Cell Res.", "key": "18_CR45", "unstructured": "Gwak, J. et al. Small molecule-based disruption of the Axin/beta-catenin protein complex regulates mesenchymal stem cell differentiation. Cell Res. 22, 237–247 (2012).", "volume": "22", "year": "2012" }, { "DOI": "10.1242/jcs.236943", "author": "Y Fujiki", "doi-asserted-by": "publisher", "first-page": "jcs236943", "journal-title": "J. Cell Sci.", "key": "18_CR46", "unstructured": "Fujiki, Y. et al. Recent insights into peroxisome biogenesis and associated diseases. J. Cell Sci. 133, jcs236943 (2020).", "volume": "133", "year": "2020" }, { "DOI": "10.1016/S0196-0709(83)80019-2", "author": "WJ Richtsmeier", "doi-asserted-by": "publisher", "first-page": "325", "journal-title": "Am. J. Otolaryngol.", "key": "18_CR47", "unstructured": "Richtsmeier, W. J. Human interferon production in tonsil and adenoid tissue cultures. Am. J. Otolaryngol. 4, 325–333 (1983).", "volume": "4", "year": "1983" }, { "DOI": "10.1128/jvi.2.10.955-961.1968", "author": "J Desmyter", "doi-asserted-by": "publisher", "first-page": "955", "journal-title": "J. Virol.", "key": "18_CR48", "unstructured": "Desmyter, J., Melnick, J. L. & Rawls, W. E. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J. Virol. 2, 955–961 (1968).", "volume": "2", "year": "1968" }, { "DOI": "10.1146/annurev-cellbio-120319-023657", "author": "LV Albrecht", "doi-asserted-by": "publisher", "first-page": "369", "journal-title": "Annu. Rev. Cell Dev. Biol.", "key": "18_CR49", "unstructured": "Albrecht, L. V., Tejeda-Munoz, N. & De Robertis, E. M. Cell biology of canonical Wnt signaling. Annu. Rev. Cell Dev. Biol. 37, 369–389 (2021).", "volume": "37", "year": "2021" }, { "DOI": "10.1016/j.cell.2020.09.050", "author": "SR Leist", "doi-asserted-by": "publisher", "first-page": "1070", "journal-title": "Cell", "key": "18_CR50", "unstructured": "Leist, S. R. et al. A mouse-adapted SARS-CoV-2 induces acute lung injury and mortality in standard laboratory mice. Cell 183, 1070–1085.e1012 (2020).", "volume": "183", "year": "2020" }, { "DOI": "10.1038/s41416-020-0916-5", "author": "R Plummer", "doi-asserted-by": "publisher", "first-page": "525", "journal-title": "Br. J. Cancer", "key": "18_CR51", "unstructured": "Plummer, R. et al. First-in-human study of the PARP/tankyrase inhibitor E7449 in patients with advanced solid tumours and evaluation of a novel drug-response predictor. Br. J. Cancer 123, 525–533 (2020).", "volume": "123", "year": "2020" }, { "author": "S Ramasamy", "first-page": "e00299", "journal-title": "Clin. Microbiol. Rev.", "key": "18_CR52", "unstructured": "Ramasamy, S. & Subbian, S. Critical determinants of cytokine storm and type I interferon response in COVID-19 pathogenesis. Clin. Microbiol. Rev. 34, e00299–20 (2021).", "volume": "34", "year": "2021" }, { "DOI": "10.1016/j.cell.2010.04.018", "author": "E Dixit", "doi-asserted-by": "publisher", "first-page": "668", "journal-title": "Cell", "key": "18_CR53", "unstructured": "Dixit, E. et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141, 668–681 (2010).", "volume": "141", "year": "2010" }, { "DOI": "10.1089/dna.2018.4153", "author": "CP Wong", "doi-asserted-by": "publisher", "first-page": "417", "journal-title": "DNA Cell Biol", "key": "18_CR54", "unstructured": "Wong, C. P., Xu, Z., Power, C. & Hobman, T. C. Targeted elimination of peroxisomes during viral infection: lessons from HIV and other viruses. DNA Cell Biol 37, 417–421 (2018).", "volume": "37", "year": "2018" }, { "DOI": "10.1038/ni.2915", "author": "C Odendall", "doi-asserted-by": "publisher", "first-page": "717", "journal-title": "Nat. Immunol.", "key": "18_CR55", "unstructured": "Odendall, C. et al. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 15, 717–726 (2014).", "volume": "15", "year": "2014" }, { "DOI": "10.1371/journal.ppat.1008636", "author": "F Di Cara", "doi-asserted-by": "publisher", "first-page": "e1008636", "journal-title": "PLoS Pathog.", "key": "18_CR56", "unstructured": "Di Cara, F. Peroxisomes in host defense. PLoS Pathog. 16, e1008636 (2020).", "volume": "16", "year": "2020" }, { "DOI": "10.1091/mbc.E18-07-0434", "author": "F Di Cara", "doi-asserted-by": "publisher", "first-page": "2766", "journal-title": "Mol. Biol. Cell", "key": "18_CR57", "unstructured": "Di Cara, F., Bulow, M. H., Simmonds, A. J. & Rachubinski, R. A. Dysfunctional peroxisomes compromise gut structure and host defense by increased cell death and Tor-dependent autophagy. Mol. Biol. Cell 29, 2766–2783 (2018).", "volume": "29", "year": "2018" }, { "DOI": "10.1016/j.immuni.2017.06.016", "author": "F Di Cara", "doi-asserted-by": "publisher", "first-page": "93", "journal-title": "Immunity", "key": "18_CR58", "unstructured": "Di Cara, F., Sheshachalam, A., Braverman, N. E., Rachubinski, R. A. & Simmonds, A. J. Peroxisome-mediated metabolism is required for immune response to microbial infection. Immunity 47, 93–106.e107 (2017).", "volume": "47", "year": "2017" }, { "DOI": "10.1074/jbc.AC120.013788", "author": "U Felgenhauer", "doi-asserted-by": "publisher", "first-page": "13958", "journal-title": "J. Biol. Chem.", "key": "18_CR59", "unstructured": "Felgenhauer, U. et al. Inhibition of SARS-CoV-2 by type I and type III interferons. J. Biol. Chem. 295, 13958–13964 (2020).", "volume": "295", "year": "2020" }, { "DOI": "10.1128/JVI.00985-20", "author": "A Vanderheiden", "doi-asserted-by": "publisher", "first-page": "e00985", "journal-title": "J. Virol.", "key": "18_CR60", "unstructured": "Vanderheiden, A. et al. Type I and type III interferons restrict SARS-CoV-2 infection of human airway epithelial cultures. J. Virol. 94, e00985–20 (2020).", "volume": "94", "year": "2020" }, { "DOI": "10.1016/S0140-6736(03)13973-6", "author": "J Cinatl", "doi-asserted-by": "publisher", "first-page": "293", "journal-title": "Lancet", "key": "18_CR61", "unstructured": "Cinatl, J. et al. Treatment of SARS with human interferons. Lancet 362, 293–294 (2003).", "volume": "362", "year": "2003" }, { "DOI": "10.1016/j.chom.2016.01.007", "author": "R Channappanavar", "doi-asserted-by": "publisher", "first-page": "181", "journal-title": "Cell Host Microbe", "key": "18_CR62", "unstructured": "Channappanavar, R. et al. Dysregulated type I interferon and inflammatory monocyte-macrophage responses cause lethal pneumonia in SARS-CoV-infected mice. Cell Host Microbe 19, 181–193 (2016).", "volume": "19", "year": "2016" }, { "DOI": "10.1099/vir.0.046284-0", "author": "T Mahlakoiv", "doi-asserted-by": "publisher", "first-page": "2601", "journal-title": "J. Gen. Virol.", "key": "18_CR63", "unstructured": "Mahlakoiv, T. et al. Combined action of type I and type III interferon restricts initial replication of severe acute respiratory syndrome coronavirus in the lung but fails to inhibit systemic virus spread. J. Gen. Virol. 93, 2601–2605 (2012).", "volume": "93", "year": "2012" }, { "DOI": "10.1128/JVI.00009-13", "author": "RW Chan", "doi-asserted-by": "publisher", "first-page": "6604", "journal-title": "J. Virol.", "key": "18_CR64", "unstructured": "Chan, R. W. et al. Tropism of and innate immune responses to the novel human betacoronavirus lineage C virus in human ex vivo respiratory organ cultures. J. Virol. 87, 6604–6614 (2013).", "volume": "87", "year": "2013" }, { "DOI": "10.1016/j.jcv.2003.11.013", "author": "M Spiegel", "doi-asserted-by": "publisher", "first-page": "211", "journal-title": "J. Clin. Virol.", "key": "18_CR65", "unstructured": "Spiegel, M., Pichlmair, A., Mühlberger, E., Haller, O. & Weber, F. The antiviral effect of interferon-beta against SARS-coronavirus is not mediated by MxA protein. J. Clin. Virol. 30, 211–213 (2004).", "volume": "30", "year": "2004" }, { "DOI": "10.1128/JVI.03496-12", "author": "F Zielecki", "doi-asserted-by": "publisher", "first-page": "5300", "journal-title": "J. Virol.", "key": "18_CR66", "unstructured": "Zielecki, F. et al. Human cell tropism and innate immune system interactions of human respiratory coronavirus EMC compared to those of severe acute respiratory syndrome coronavirus. J. Virol. 87, 5300–5304 (2013).", "volume": "87", "year": "2013" }, { "DOI": "10.1007/s11096-005-1319-7", "author": "S Sleijfer", "doi-asserted-by": "publisher", "first-page": "423", "journal-title": "Pharm. World Sci.", "key": "18_CR67", "unstructured": "Sleijfer, S., Bannink, M., Van Gool, A. R., Kruit, W. H. & Stoter, G. Side effects of interferon-alpha therapy. Pharm. World Sci. 27, 423–431 (2005).", "volume": "27", "year": "2005" }, { "DOI": "10.1038/nchembio.2103", "author": "PH Cha", "doi-asserted-by": "publisher", "first-page": "593", "journal-title": "Nat. Chem. Biol.", "key": "18_CR68", "unstructured": "Cha, P. H. et al. Small-molecule binding of the axin RGS domain promotes beta-catenin and Ras degradation. Nat. Chem. Biol. 12, 593–600 (2016).", "volume": "12", "year": "2016" }, { "DOI": "10.18632/oncotarget.5846", "author": "S McGonigle", "doi-asserted-by": "publisher", "first-page": "41307", "journal-title": "Oncotarget", "key": "18_CR69", "unstructured": "McGonigle, S. et al. E7449: a dual inhibitor of PARP1/2 and tankyrase1/2 inhibits growth of DNA repair deficient tumors and antagonizes Wnt signaling. Oncotarget 6, 41307–41323 (2015).", "volume": "6", "year": "2015" }, { "DOI": "10.1016/j.jmb.2023.168170", "author": "J Lopez-Orozco", "doi-asserted-by": "publisher", "first-page": "168170", "journal-title": "J. Mol. Biol.", "key": "18_CR70", "unstructured": "Lopez-Orozco, J. et al. The RNA interference effector protein argonaute 2 functions as a restriction factor against SARS-CoV-2. J. Mol. Biol. 435, 168170 (2023).", "volume": "435", "year": "2023" }, { "DOI": "10.1038/s41596-021-00491-8", "author": "X Xie", "doi-asserted-by": "publisher", "first-page": "1761", "journal-title": "Nat. Protoc.", "key": "18_CR71", "unstructured": "Xie, X. et al. Engineering SARS-CoV-2 using a reverse genetic system. Nat. Protoc. 16, 1761–1784 (2021).", "volume": "16", "year": "2021" }, { "DOI": "10.1128/JVI.00266-21", "author": "A Kumar", "doi-asserted-by": "publisher", "first-page": "e0026621", "journal-title": "J. Virol.", "key": "18_CR72", "unstructured": "Kumar, A. et al. SARS-CoV-2 nonstructural protein 1 inhibits the interferon response by causing depletion of key host signaling factors. J. Virol. 95, e0026621 (2021).", "volume": "95", "year": "2021" }, { "DOI": "10.1006/meth.2001.1262", "author": "KJ Livak", "doi-asserted-by": "publisher", "first-page": "402", "journal-title": "Methods", "key": "18_CR73", "unstructured": "Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408 (2001).", "volume": "25", "year": "2001" }, { "DOI": "10.1038/s41598-018-32420-3", "author": "F Wang", "doi-asserted-by": "publisher", "journal-title": "Sci. Rep.", "key": "18_CR74", "unstructured": "Wang, F. et al. Histopathological changes caused by inflammation and oxidative stress in diet-induced-obese mouse following experimental lung injury. Sci. Rep. 8, 14250 (2018).", "volume": "8", "year": "2018" } ], "reference-count": 74, "references-count": 74, "relation": {}, "resource": { "primary": { "URL": "https://www.nature.com/articles/s44298-024-00018-4" } }, "score": 1, "short-title": [], "source": "Crossref", "subject": [], "subtitle": [], "title": "The Wnt/β-catenin pathway is important for replication of SARS-CoV-2 and other pathogenic RNA viruses", "type": "journal-article", "update-policy": "http://dx.doi.org/10.1007/springer_crossmark_policy", "volume": "2" }