{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T05:13:38Z","timestamp":1787030018263,"version":"build-2736575974"},"reference-count":58,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T00:00:00Z","timestamp":1682380800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Mx proteins are key factors of the innate intracellular defense mechanisms that act against viruses induced by type I\/III interferons. The family Peribunyaviridae includes many viruses of veterinary importance, either because infection results in clinical disease or because animals serve as reservoirs for arthropod vectors. According to the evolutionary arms race hypothesis, evolutionary pressures should have led to the selection of the most appropriate Mx1 antiviral isoforms to resist these infections. Although human, mouse, bat, rat, and cotton rat Mx isoforms have been shown to inhibit different members of the Peribunyaviridae, the possible antiviral function of the Mx isoforms from domestic animals against bunyaviral infections has, to our knowledge, never been studied. Herein, we investigated the anti-Schmallenberg virus activity of bovine, canine, equine, and porcine Mx1 proteins. We concluded that Mx1 has a strong, dose-dependent anti-Schmallenberg activity in these four mammalian species.<\/jats:p>","DOI":"10.3390\/v15051055","type":"journal-article","created":{"date-parts":[[2023,4,26]],"date-time":"2023-04-26T01:16:25Z","timestamp":1682471785000},"page":"1055","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Anti-Schmallenberg Virus Activities of Type I\/III Interferons-Induced Mx1 GTPases from Different Mammalian Species"],"prefix":"10.3390","volume":"15","author":[{"given":"Calixte","family":"Bayrou","sequence":"first","affiliation":[{"name":"Animal Pathology, FARAH Research Center, Faculty of Veterinary Medicine, University of Li\u00e8ge, Sart-Tilman B43, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2919-7658","authenticated-orcid":false,"given":"Anne-Sophie","family":"Van Laere","sequence":"additional","affiliation":[{"name":"Animal Pathology, FARAH Research Center, Faculty of Veterinary Medicine, University of Li\u00e8ge, Sart-Tilman B43, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Phai","family":"Dam Van","sequence":"additional","affiliation":[{"name":"Animal Pathology, FARAH Research Center, Faculty of Veterinary Medicine, University of Li\u00e8ge, Sart-Tilman B43, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4438-8759","authenticated-orcid":false,"given":"Nassim","family":"Moula","sequence":"additional","affiliation":[{"name":"Animal Productions, FARAH Research Center, Faculty of Veterinary Medicine, University of Li\u00e8ge, Sart-Tilman B43, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mutien-Marie","family":"Garigliany","sequence":"additional","affiliation":[{"name":"Animal Pathology, FARAH Research Center, Faculty of Veterinary Medicine, University of Li\u00e8ge, Sart-Tilman B43, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9440-0993","authenticated-orcid":false,"given":"Daniel","family":"Desmecht","sequence":"additional","affiliation":[{"name":"Animal Pathology, FARAH Research Center, Faculty of Veterinary Medicine, University of Li\u00e8ge, Sart-Tilman B43, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1016\/j.immuni.2019.03.025","article-title":"Shared and Distinct Functions of Type I and Type III Interferons","volume":"50","author":"Lazear","year":"2019","journal-title":"Immunity"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1016\/j.immuni.2011.07.012","article-title":"Structure of myxovirus resistance protein a reveals intra- and intermolecular domain interactions required for the antiviral function","volume":"35","author":"Gao","year":"2011","journal-title":"Immunity"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/0042-6822(62)90297-0","article-title":"Resistance of mice to mouse-adapted influenza A virus","volume":"16","author":"Lindenmann","year":"1962","journal-title":"Virology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1128\/MMBR.00024-13","article-title":"Mx proteins: Antiviral gatekeepers that restrain the uninvited","volume":"77","author":"Verhelst","year":"2013","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1373\/clinchem.2018.292391","article-title":"Interferon-Inducible Myxovirus Resistance Proteins: Potential Biomarkers for Differentiating Viral from Bacterial Infections","volume":"65","author":"Korpela","year":"2019","journal-title":"Clin. Chem."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Elliott, R.M. (1996). The Bunyaviridae. The Viruses, Springer.","DOI":"10.1007\/978-1-4899-1364-7"},{"key":"ref_7","unstructured":"King, A., Adams, M., Carstens, E., and Lefkowitz, E. (2012). Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier Academic Press."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1949","DOI":"10.1007\/s00705-019-04253-6","article-title":"Taxonomy of the order Bunyavirales: Update 2019","volume":"164","author":"Abudurexiti","year":"2019","journal-title":"Arch. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e050122199975","DOI":"10.2174\/1871526522666220105110819","article-title":"Global Comprehensive Outlook of Hantavirus Contagion on Humans: A Review","volume":"22","author":"Ashique","year":"2022","journal-title":"Infect. Disord. Drug Targets"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Odendaal, L., Davis, S., and Venter, E. (2021). Insights into the Pathogenesis of Viral Haemorrhagic Fever Based on Virus Tropism and Tissue Lesions of Natural Rift Valley Fever. Viruses, 13.","DOI":"10.3390\/v13040709"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1016\/j.cmi.2019.12.015","article-title":"An update on Toscana virus distribution, genetics, medical and diagnostic aspects","volume":"26","author":"Ayhan","year":"2020","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1080\/13550280591002496","article-title":"Emerging infectious diseases: The Bunyaviridae","volume":"11","author":"Soldan","year":"2005","journal-title":"J. Neurovirol."},{"key":"ref_13","first-page":"1","article-title":"Crimean-Congo haemorrhagic fever virus","volume":"14","author":"Hawman","year":"2023","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"4323","DOI":"10.1128\/JVI.78.8.4323-4329.2004","article-title":"Human MxA protein inhibits the replication of Crimean-Congo hemorrhagic fever virus","volume":"78","author":"Andersson","year":"2004","journal-title":"J. Virol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.virusres.2003.10.002","article-title":"Inhibition of Dugbe nairovirus replication by human MxA protein","volume":"99","author":"Bridgen","year":"2004","journal-title":"Virus Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1128\/jvi.70.2.915-923.1996","article-title":"Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein","volume":"70","author":"Frese","year":"1996","journal-title":"J. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1006\/viro.1996.0506","article-title":"Inhibition of puumala and tula hantaviruses in Vero cells by MxA protein","volume":"224","author":"Kanerva","year":"1996","journal-title":"Virology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3153","DOI":"10.1073\/pnas.052430399","article-title":"Antivirally active MxA protein sequesters La Crosse virus nucleocapsid protein into perinuclear complexes","volume":"99","author":"Kochs","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"6984","DOI":"10.1128\/JVI.73.8.6984-6991.1999","article-title":"Human MxA protein protects mice lacking a functional alpha\/beta interferon system against La crosse virus and other lethal viral infections","volume":"73","author":"Hefti","year":"1999","journal-title":"J. Virol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1007\/s007050170189","article-title":"Mouse Mx2 protein inhibits hantavirus but not influenza virus replication","volume":"146","author":"Jin","year":"2001","journal-title":"Arch. Virol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1089\/107999001753124390","article-title":"Interferon-induced rat Mx proteins confer resistance to Rift Valley fever virus and other arthropod-borne viruses","volume":"21","author":"Sandrock","year":"2001","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1089\/jir.2006.0176","article-title":"The antiviral potential of interferon-induced cotton rat Mx proteins against orthomyxovirus (influenza), rhabdovirus, and bunyavirus","volume":"27","author":"Stertz","year":"2007","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e00361-17","DOI":"10.1128\/JVI.00361-17","article-title":"Evolution and Antiviral Specificities of Interferon-Induced Mx Proteins of Bats against Ebola, Influenza, and Other RNA Viruses","volume":"91","author":"Fuchs","year":"2017","journal-title":"J. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s42522-022-00069-8","article-title":"Vaccine development against Schmallenberg virus: From classical inactivated to modified-live to scaffold particle vaccines","volume":"4","author":"Wernike","year":"2022","journal-title":"One Health Outlook"},{"key":"ref_25","first-page":"443","article-title":"First detection of Schmallenberg virus antibody in cattle population of eastern Iran","volume":"13","author":"Rasekh","year":"2022","journal-title":"Vet. Res. Forum Int. Q. J."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"198739","DOI":"10.1016\/j.virusres.2022.198739","article-title":"Identification and molecular characterization of highly divergent RNA viruses in cattle, Uganda","volume":"313","author":"Balinandi","year":"2022","journal-title":"Virus Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.3201\/eid2008.121890","article-title":"Natural intrauterine infection with Schmallenberg virus in malformed newborn calves","volume":"20","author":"Bayrou","year":"2014","journal-title":"Emerg. Infect. Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1111\/tbed.12030","article-title":"Field veterinary survey on clinical and economic impact of Schmallenberg virus in Belgium","volume":"61","author":"Martinelle","year":"2014","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Tilston-Lunel, N.L., Shi, X., Elliott, R.M., and Acrani, G.O. (2017). The Potential for Reassortment between Oropouche and Schmallenberg Orthobunyaviruses. Viruses, 9.","DOI":"10.3390\/v9080220"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1089\/jir.2018.0157","article-title":"Anti-Influenza A Virus Activities of Type I\/III Interferons-Induced Mx1 GTPases from Different Mammalian Species","volume":"39","author":"Desmecht","year":"2019","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1007\/s00251-006-0167-5","article-title":"Bovine and water buffalo Mx2 genes: Polymorphism and antiviral activity","volume":"59","author":"Babiker","year":"2007","journal-title":"Immunogenetics"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1089\/jir.2004.24.513","article-title":"Conditional expression of type I interferon-induced bovine Mx1 GTPase in a stable transgenic vero cell line interferes with replication of vesicular stomatitis virus","volume":"24","author":"Baise","year":"2004","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1089\/vim.2009.0050","article-title":"Specific intracellular localization and antiviral property of genetic and splicing variants in bovine Mx1","volume":"22","author":"Yamada","year":"2009","journal-title":"Viral Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/j.nbd.2005.08.015","article-title":"Expression of the interferon- alpha\/beta-inducible bovine Mx1 dynamin interferes with replication of rabies virus","volume":"21","author":"Leroy","year":"2006","journal-title":"Neurobiol. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1089\/jir.2005.25.192","article-title":"Resistance of paramyxoviridae to type I interferon-induced Bos taurus Mx1 dynamin","volume":"25","author":"Leroy","year":"2005","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1089\/jir.2011.0123","article-title":"In Vivo modulation of the innate response to pneumovirus by type-I and -III interferon-induced Bos taurus Mx1","volume":"32","author":"Dermine","year":"2012","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.virol.2017.06.017","article-title":"Sensitivity to BST-2 restriction correlates with Orthobunyavirus host range","volume":"509","author":"Varela","year":"2017","journal-title":"Virology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1023\/A:1009283126868","article-title":"Cloning and chromosomal localization of MX1 and ETS2 to chromosome 26 of the horse (Equus caballus)","volume":"6","author":"Lear","year":"1998","journal-title":"Chromosome Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/0165-2427(94)90069-8","article-title":"Proteins induced by recombinant equine interferon-beta 1 within equine peripheral blood mononuclear cells and polymorphonuclear neutrophilic granulocytes","volume":"42","author":"Heinz","year":"1994","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Wagner, V., Sabachvili, M., Bendl, E., and Fuchs, J. (2023). The Antiviral Activity of Equine Mx1 against Thogoto Virus Is Determined by the Molecular Structure of Its Viral Specificity Region. J. Virol., ahead of print.","DOI":"10.1128\/jvi.01938-22"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1007\/s00251-006-0109-2","article-title":"Genomic structure, promoter analysis, and expression of the porcine (Sus scrofa) Mx1 gene","volume":"58","author":"Thomas","year":"2006","journal-title":"Immunogenetics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/s10528-006-9045-y","article-title":"A naturally occurring variant of porcine Mx1 associated with increased susceptibility to influenza virus in vitro","volume":"45","author":"Nakajima","year":"2007","journal-title":"Biochem. Genet."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1089\/jir.2006.0119","article-title":"Differential anti-influenza activity among allelic variants at the Sus scrofa Mx1 locus","volume":"27","author":"Palm","year":"2007","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1051\/vetres\/2010001","article-title":"Interferon-induced Sus scrofa Mx1 blocks endocytic traffic of incoming influenza A virus particles","volume":"41","author":"Palm","year":"2010","journal-title":"Vet. Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"109706","DOI":"10.1016\/j.vetmic.2023.109706","article-title":"Porcine Mx proteins inhibit pseudorabies virus replication through interfering with early gene synthesis","volume":"280","author":"Chen","year":"2023","journal-title":"Vet. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Gao, H., Xiang, Z., Ge, X., Zhou, L., Han, J., Guo, X., Chen, Y., Zhang, Y., and Yang, H. (2022). Comparative Proteomic Analysis Reveals Mx1 Inhibits Senecavirus A Replication in PK-15 Cells by Interacting with the Capsid Proteins VP1, VP2 and VP3. Viruses, 14.","DOI":"10.3390\/v14050863"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e02147-17","DOI":"10.1128\/JVI.02147-17","article-title":"Porcine Mx1 Protein Inhibits Classical Swine Fever Virus Replication by Targeting Nonstructural Protein NS5B","volume":"92","author":"Zhou","year":"2018","journal-title":"J. Virol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1080\/10495398.2014.902850","article-title":"Both foot-and-mouth disease virus and bovine viral diarrhea virus replication are inhibited by Mx1 protein originated from porcine","volume":"26","author":"Shi","year":"2015","journal-title":"Anim. Biotechnol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1089\/jir.2005.25.169","article-title":"Intracellular localization and antiviral property of canine Mx proteins","volume":"25","author":"Nakamura","year":"2005","journal-title":"J. Interf. Cytokine Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"7125","DOI":"10.1016\/j.vaccine.2011.05.069","article-title":"Efficient influenza B virus propagation due to deficient interferon-induced antiviral activity in MDCK cells","volume":"29","author":"Frensing","year":"2011","journal-title":"Vaccine"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1099\/vir.0.020370-0","article-title":"High yields of influenza A virus in Madin-Darby canine kidney cells are promoted by an insufficient interferon-induced antiviral state","volume":"91","author":"Seitz","year":"2010","journal-title":"J. Gen. Virol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1023\/A:1026526314875","article-title":"Constitutive expression of interferon-induced human MxA protein in transgenic tobacco plants does not confer resistance to a variety of RNA viruses","volume":"9","author":"Frese","year":"2000","journal-title":"Transgenic Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1111\/j.1600-0854.2004.00219.x","article-title":"Missorting of LaCrosse virus nucleocapsid protein by the interferon-induced MxA GTPase involves smooth ER membranes: Membrane association of antivirally active MxA GTPase","volume":"5","author":"Reichelt","year":"2004","journal-title":"Traffic"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"5166","DOI":"10.1128\/jvi.63.12.5166-5174.1989","article-title":"La Crosse virus nucleocapsid protein controls its own synthesis in mosquito cells by encapsidating its mRNA","volume":"63","author":"Hacker","year":"1989","journal-title":"J. Virol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Schmaljohn, C., and Nichol, S.T. (2001). Hantaviruses, Springer.","DOI":"10.1007\/978-3-642-56753-7"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1016\/j.virol.2008.12.011","article-title":"Efficient production of Rift Valley fever virus-like particles: The antiviral protein MxA can inhibit primary transcription of bunyaviruses","volume":"385","author":"Habjan","year":"2009","journal-title":"Virology"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"7988","DOI":"10.1128\/JVI.00140-12","article-title":"Orthobunyavirus entry into neurons and other mammalian cells occurs via clathrin-mediated endocytosis and requires trafficking into early endosomes","volume":"86","author":"Hollidge","year":"2012","journal-title":"J. Virol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1146\/annurev.cellbio.16.1.483","article-title":"Dynamin and its Role in Membrane Fission","volume":"16","author":"Hinshaw","year":"2000","journal-title":"Annu. Rev. Cell Dev. Biol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/15\/5\/1055\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:23:33Z","timestamp":1760124213000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/15\/5\/1055"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,25]]},"references-count":58,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["v15051055"],"URL":"https:\/\/doi.org\/10.3390\/v15051055","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,25]]}}}