{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T03:22:49Z","timestamp":1790738569987,"version":"4.1.0"},"reference-count":61,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2021,5,25]],"date-time":"2021-05-25T00:00:00Z","timestamp":1621900800000},"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>Arenaviruses cause chronic and asymptomatic infections in their natural host, rodents, and several arenaviruses cause severe hemorrhagic fever that has a high mortality in infected humans, seriously threatening public health. There are currently no FDA-licensed drugs available against arenaviruses; therefore, it is important to develop novel antiviral strategies to combat them, which would be facilitated by a detailed understanding of the interactions between the viruses and their hosts. To this end, we performed a transcriptomic analysis on cells infected with arenavirus lymphocytic choriomeningitis virus (LCMV), a neglected human pathogen with clinical significance, and found that the signal transducer and activator of transcription 3 (STAT3) signaling pathway was activated. A further investigation indicated that STAT3 could be activated by the RNA-dependent RNA polymerase L protein (Lp) of LCMV. Our functional analysis found that STAT3 cannot affect LCMV multiplication in A549 cells. We also found that STAT3 was activated by the Lp of Mopeia virus and Junin virus, suggesting that this activation may be conserved across certain arenaviruses. Our study explored the interactions between arenaviruses and STAT3, which may help us to better understand the molecular and cell biology of arenaviruses.<\/jats:p>","DOI":"10.3390\/v13060976","type":"journal-article","created":{"date-parts":[[2021,5,25]],"date-time":"2021-05-25T22:02:23Z","timestamp":1621980143000},"page":"976","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Activation of the STAT3 Signaling Pathway by the RNA-Dependent RNA Polymerase Protein of Arenavirus"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1028-1267","authenticated-orcid":false,"given":"Qingxing","family":"Wang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, Hubei, China"},{"name":"University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1087-2422","authenticated-orcid":false,"given":"Qilin","family":"Xin","sequence":"additional","affiliation":[{"name":"UMR754, Viral Infections and Comparative Pathology, 50 Avenue Tony Garnier, CEDEX 07, 69366 Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weijuan","family":"Shang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, Hubei, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weiwei","family":"Wan","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, Hubei, China"},{"name":"University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gengfu","family":"Xiao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, Hubei, China"},{"name":"University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2593-2571","authenticated-orcid":false,"given":"Lei-Ke","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, Hubei, China"},{"name":"University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,25]]},"reference":[{"key":"ref_1","unstructured":"Buchmeier, M.J., Peters, C.J., and de la Torre, J.C. Arenaviridae: The Virus and Their Replication, Lippincott, Williams and Wilkins. [5th ed.]. Fields Virology, 2."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1126\/science.aam7260","article-title":"Structural basis for antibody-mediated neutralization of Lassa virus","volume":"356","author":"Hastie","year":"2017","journal-title":"Science"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1038\/nature09605","article-title":"Cap binding and immune evasion revealed by Lassa nucleoprotein structure","volume":"468","author":"Qi","year":"2010","journal-title":"Nature"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"12978","DOI":"10.1073\/pnas.2133782100","article-title":"The small RING finger protein Z drives arenavirus budding: Implications for antiviral strategies","volume":"100","author":"Perez","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"9415","DOI":"10.1128\/JVI.75.19.9415-9426.2001","article-title":"RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome","volume":"75","author":"Cornu","year":"2001","journal-title":"J. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1038\/s41586-020-2114-2","article-title":"Structural insight into arenavirus replication machinery","volume":"579","author":"Peng","year":"2020","journal-title":"Nature"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3470","DOI":"10.1128\/JVI.74.8.3470-3477.2000","article-title":"NP and L proteins of lymphocytic choriomeningitis virus (LCMV) are sufficient for efficient transcription and replication of LCMV genomic RNA analogs","volume":"74","author":"Lee","year":"2000","journal-title":"J. Virol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2295","DOI":"10.1007\/s00705-018-3843-5","article-title":"Taxonomy of the family Arenaviridae and the order Bunyavirales: Update 2018","volume":"163","author":"Maes","year":"2018","journal-title":"Arch. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1146\/annurev-pathol-020712-164041","article-title":"Pathogenesis of the viral hemorrhagic fevers","volume":"8","author":"Paessler","year":"2013","journal-title":"Annu. Rev. Pathol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1271","DOI":"10.1136\/bmj.327.7426.1271","article-title":"Lassa fever: Epidemiology, clinical features, and social consequences","volume":"327","author":"Richmond","year":"2003","journal-title":"BMJ"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.antiviral.2007.10.010","article-title":"Treatment of Argentine hemorrhagic fever","volume":"78","author":"Enria","year":"2008","journal-title":"Antivir. Res."},{"key":"ref_12","first-page":"486","article-title":"Lymphocytic choriomeningitis virus. A neglected pathogen of man","volume":"116","author":"Jahrling","year":"1992","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"E35","DOI":"10.1542\/peds.105.3.e35","article-title":"Lymphocytic choriomeningitis virus: Reemerging central nervous system pathogen","volume":"105","author":"Barton","year":"2000","journal-title":"Pediatrics"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2235","DOI":"10.1056\/NEJMoa053240","article-title":"Transmission of lymphocytic choriomeningitis virus by organ transplantation","volume":"354","author":"Fischer","year":"2006","journal-title":"N. Engl. J. Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2208","DOI":"10.1056\/NEJMp068021","article-title":"Lymphocytic choriomeningitis virus--an old enemy up to new tricks","volume":"354","author":"Peters","year":"2006","journal-title":"N. Engl. J. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1128\/JVI.02110-13","article-title":"Sodium hydrogen exchangers contribute to arenavirus cell entry","volume":"88","author":"Iwasaki","year":"2014","journal-title":"J. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1038\/nrm909","article-title":"Stats: Transcriptional control and biological impact","volume":"3","author":"Levy","year":"2002","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"557","DOI":"10.2217\/fvl-2018-0033","article-title":"STAT3 roles in viral infection: Antiviral or proviral?","volume":"13","author":"Chang","year":"2018","journal-title":"Future Virol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1038\/nrc1275","article-title":"The STATs of cancer--new molecular targets come of age","volume":"4","author":"Yu","year":"2004","journal-title":"Nat. Rev. Cancer"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Roca Suarez, A.A., Van Renne, N., Baumert, T.F., and Lupberger, J. (2018). Viral manipulation of STAT3: Evade, exploit, and injure. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1006839"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Morgan, E.L., Wasson, C.W., Hanson, L., Kealy, D., Pentland, I., McGuire, V., Scarpini, C., Coleman, N., Arthur, J.S.C., and Parish, J.L. (2018). STAT3 activation by E6 is essential for the differentiation-dependent HPV18 life cycle. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1006975"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1084\/jem.20012127","article-title":"Activation of STAT3 by the hepatitis C virus core protein leads to cellular transformation","volume":"196","author":"Yoshida","year":"2002","journal-title":"J. Exp. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1093\/jmcb\/mjw005","article-title":"PASD1 promotes STAT3 activity and tumor growth by inhibiting TC45-mediated dephosphorylation of STAT3 in the nucleus","volume":"8","author":"Xu","year":"2016","journal-title":"J. Mol. Cell Biol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Zhu, S., Wan, W., Zhang, Y., Shang, W., Pan, X., Zhang, L.K., and Xiao, G. (2019). Comprehensive Interactome Analysis Reveals that STT3B is Required for the N-Glycosylation of Lassa Virus Glycoprotein. J. Virol., 93.","DOI":"10.1128\/JVI.01443-19"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"10259","DOI":"10.1128\/JVI.01292-16","article-title":"Activation of the RLR\/MAVS Signaling Pathway by the L Protein of Mopeia Virus","volume":"90","author":"Zhang","year":"2016","journal-title":"J. Virol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"5961","DOI":"10.1074\/jbc.271.11.5961","article-title":"Dominant negative stat3 mutant inhibits interleukin-6-induced Jak-STAT signal transduction","volume":"271","author":"Kaptein","year":"1996","journal-title":"J. Biol. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/0092-8674(94)90235-6","article-title":"Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway","volume":"77","author":"Akira","year":"1994","journal-title":"Cell"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3441","DOI":"10.1038\/s41467-018-05796-z","article-title":"TRIM27 mediates STAT3 activation at retromer-positive structures to promote colitis and colitis-associated carcinogenesis","volume":"9","author":"Zhang","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"8261","DOI":"10.1128\/JVI.00989-13","article-title":"The rabies virus interferon antagonist P protein interacts with activated STAT3 and inhibits Gp130 receptor signaling","volume":"87","author":"Lieu","year":"2013","journal-title":"J. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Morgan, E.L., and Macdonald, A. (2019). Autocrine STAT3 activation in HPV positive cervical cancer through a virus-driven Rac1-NFkappaB-IL-6 signalling axis. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1007835"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"7100","DOI":"10.1128\/JVI.00403-08","article-title":"The hepatitis E virus ORF3 protein modulates epidermal growth factor receptor trafficking, STAT3 translocation, and the acute-phase response","volume":"82","author":"Chandra","year":"2008","journal-title":"J. Virol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.bbrc.2008.11.053","article-title":"Epstein-Barr virus-derived EBNA2 regulates STAT3 activation","volume":"378","author":"Muromoto","year":"2009","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4399","DOI":"10.1128\/JVI.01703-10","article-title":"Epstein-Barr virus LMP1 activates EGFR, STAT3, and ERK through effects on PKCdelta","volume":"85","author":"Kung","year":"2011","journal-title":"J. Virol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"10847","DOI":"10.1074\/jbc.M110.217653","article-title":"Extracellular hepatitis C virus core protein activates STAT3 in human monocytes\/macrophages\/dendritic cells via an IL-6 autocrine pathway","volume":"286","author":"Tacke","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2149","DOI":"10.1007\/s00705-016-2892-x","article-title":"Hepatitis C virus and its protein NS4B activate the cancer-related STAT3 pathway via the endoplasmic reticulum overload response","volume":"161","author":"Kong","year":"2016","journal-title":"Arch. Virol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.virol.2016.10.015","article-title":"Epstein-Barr Virus Latent Membrane Protein 2A (LMP2A) enhances IL-10 production through the activation of Bruton\u2019s tyrosine kinase and STAT3","volume":"500","author":"Incrocci","year":"2017","journal-title":"Virology"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Yang, L., Wang, R., Ma, Z., Xiao, Y., Nan, Y., Wang, Y., Lin, S., and Zhang, Y.J. (2017). Porcine Reproductive and Respiratory Syndrome Virus Antagonizes JAK\/STAT3 Signaling via nsp5, Which Induces STAT3 Degradation. J. Virol., 91.","DOI":"10.1128\/JVI.02087-16"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Wu, C.C., Jiang, X., Wang, X.Z., Liu, X.J., Li, X.J., Yang, B., Ye, H.Q., Harwardt, T., Jiang, M., and Xia, H.M. (2018). Human Cytomegalovirus Immediate Early 1 Protein Causes Loss of SOX2 from Neural Progenitor Cells by Trapping Unphosphorylated STAT3 in the Nucleus. J. Virol., 92.","DOI":"10.1128\/JVI.00340-18"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Iwasaki, M., and de la Torre, J.C. (2018). A Highly Conserved Leucine in Mammarenavirus Matrix Z Protein Is Required for Z Interaction with the Virus L Polymerase and Z Stability in Cells Harboring an Active Viral Ribonucleoprotein. J. Virol., 92.","DOI":"10.1128\/JVI.02256-17"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1934","DOI":"10.1128\/JVI.01657-09","article-title":"An N-terminal region of Lassa virus L protein plays a critical role in transcription but not replication of the virus genome","volume":"84","author":"Lelke","year":"2010","journal-title":"J. Virol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"10207","DOI":"10.1128\/JVI.00220-08","article-title":"Mutational evidence for a structural model of the Lassa virus RNA polymerase domain and identification of two residues, Gly1394 and Asp1395, that are critical for transcription but not replication of the genome","volume":"82","author":"Hass","year":"2008","journal-title":"J. Virol."},{"key":"ref_42","first-page":"2057","article-title":"Two novel protein-tyrosine kinases, each with a second phosphotransferase-related catalytic domain, define a new class of protein kinase","volume":"11","author":"Wilks","year":"1991","journal-title":"Mol. Cell. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1248\/bpb.32.45","article-title":"Pyridone 6, a pan-Janus-activated kinase inhibitor, suppresses osteoclast formation and bone resorption through down-regulation of receptor activator of nuclear factor-kappaB (NF-kappaB) ligand (RANKL)-induced c-Fos and nuclear factor of activated T cells (NFAT) c1 expression","volume":"32","author":"Kwak","year":"2009","journal-title":"Biol. Pharm. Bull."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/S1074-7613(00)80011-4","article-title":"Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells","volume":"10","author":"Landowski","year":"1999","journal-title":"Immunity"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5887","DOI":"10.1158\/1078-0432.CCR-05-2501","article-title":"MLN120B, a novel IkappaB kinase beta inhibitor, blocks multiple myeloma cell growth in vitro and in vivo","volume":"12","author":"Hideshima","year":"2006","journal-title":"Clin. Cancer Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1038\/nm.3082","article-title":"An inhibitor of the protein kinases TBK1 and IKK-varepsilon improves obesity-related metabolic dysfunctions in mice","volume":"19","author":"Reilly","year":"2013","journal-title":"Nat. Med."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1038\/cr.2016.16","article-title":"The RNA-binding protein Mex3B is a coreceptor of Toll-like receptor 3 in innate antiviral response","volume":"26","author":"Yang","year":"2016","journal-title":"Cell Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1558","DOI":"10.1002\/hep.26496","article-title":"Signal transducer and activator of transcription 3 is a proviral host factor for hepatitis C virus","volume":"58","author":"McCartney","year":"2013","journal-title":"Hepatology"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1073\/pnas.1114232109","article-title":"Signal transducer and activator of transcription 3 (STAT3) and survivin induction by varicella-zoster virus promote replication and skin pathogenesis","volume":"109","author":"Sen","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"10763","DOI":"10.1128\/JVI.01197-13","article-title":"Human cytomegalovirus IE1 protein disrupts interleukin-6 signaling by sequestering STAT3 in the nucleus","volume":"87","author":"Reitsma","year":"2013","journal-title":"J. Virol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"117221","DOI":"10.1016\/j.lfs.2019.117221","article-title":"Dihydroartemisinin inhibits endothelial cell tube formation by suppression of the STAT3 signaling pathway","volume":"242","author":"Gao","year":"2020","journal-title":"Life Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"53","DOI":"10.4049\/jimmunol.1701507","article-title":"Tick-Borne Encephalitis Virus Nonstructural Protein NS5 Induces RANTES Expression Dependent on the RNA-Dependent RNA Polymerase Activity","volume":"201","author":"Zheng","year":"2018","journal-title":"J. Immunol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1016\/j.chom.2016.05.009","article-title":"Zika Virus Targets Human STAT2 to Inhibit Type I Interferon Signaling","volume":"19","author":"Grant","year":"2016","journal-title":"Cell Host Microbe"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1766","DOI":"10.15252\/embr.201642627","article-title":"Zika virus inhibits type-I interferon production and downstream signaling","volume":"17","author":"Kumar","year":"2016","journal-title":"Embo Rep."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Nikonov, A., Molder, T., Sikut, R., Kiiver, K., Mannik, A., Toots, U., Lulla, A., Lulla, V., Utt, A., and Merits, A. (2013). RIG-I and MDA-5 detection of viral RNA-dependent RNA polymerase activity restricts positive-strand RNA virus replication. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003610"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.molcel.2012.07.032","article-title":"Hepatic expression of HCV RNA-dependent RNA polymerase triggers innate immune signaling and cytokine production","volume":"48","author":"Yu","year":"2012","journal-title":"Mol. Cell"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1016\/j.cell.2020.05.035","article-title":"Hybrid Gene Origination Creates Human-Virus Chimeric Proteins during Infection","volume":"181","author":"Ho","year":"2020","journal-title":"Cell"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Morin, B., Coutard, B., Lelke, M., Ferron, F., Kerber, R., Jamal, S., Frangeul, A., Baronti, C., Charrel, R., and de Lamballerie, X. (2010). The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1001038"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Reguera, J., Gerlach, P., Rosenthal, M., Gaudon, S., Coscia, F., Gunther, S., and Cusack, S. (2016). Comparative Structural and Functional Analysis of Bunyavirus and Arenavirus Cap-Snatching Endonucleases. PLoS Pathog., 12.","DOI":"10.1371\/journal.ppat.1005636"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"8713","DOI":"10.1128\/JVI.00652-14","article-title":"Role of the C terminus of Lassa virus L protein in viral mRNA synthesis","volume":"88","author":"Lehmann","year":"2014","journal-title":"J. Virol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.virol.2016.06.004","article-title":"The role of signal transducer and activator of transcription 3 in Rift Valley fever virus infection","volume":"496","author":"Pinkham","year":"2016","journal-title":"Virology"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/6\/976\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:07:14Z","timestamp":1760162834000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/6\/976"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,25]]},"references-count":61,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,6]]}},"alternative-id":["v13060976"],"URL":"https:\/\/doi.org\/10.3390\/v13060976","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,25]]}}}