{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T07:40:01Z","timestamp":1740123601375,"version":"3.37.3"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2020,5,8]],"date-time":"2020-05-08T00:00:00Z","timestamp":1588896000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,5,8]],"date-time":"2020-05-08T00:00:00Z","timestamp":1588896000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Fundamental Research Funds for Central Universities","award":["XDJK2020D009"],"award-info":[{"award-number":["XDJK2020D009"]}]},{"name":"Fundamental Research Funds for Central Universities","award":["XDJK2019B045"],"award-info":[{"award-number":["XDJK2019B045"]}]},{"name":"Chongqing Social Undertakings and the People\u2019s Livelihood Security Program","award":["cstc2018jscx-msybX0315"],"award-info":[{"award-number":["cstc2018jscx-msybX0315"]}]},{"name":"Doctoral Fund of Southwest University","award":["swu117040"],"award-info":[{"award-number":["swu117040"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Virus Genes"],"published-print":{"date-parts":[[2020,8]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Pseudorabies virus (PRV) belongs to the Alphaherpesvirinae subfamily of Herpesviridae. PRV-induced pseudorabies is a highly contagious disease that has caused huge economic losses to the global swine industry. The PRV gE\/gI gene deletion vaccine strain (Fa \u0394gE\/gI strain) constructed from the PRV Fa wild-type strain was shown to have a protective effect against infection. However, the interaction between PRV gE\/gI genes and host miRNA needs further exploration, and little is known about the regulatory mechanisms of non-coding RNAs during PRV infection. miRNAs play a key regulatory role in viral infection and immune responses, so we analyzed the differential expression of miRNAs induced by the PRV Fa \u0394gE\/gI strain and Fa wild-type strain in the PK15 cell line. High-throughput sequencing reads were aligned to known <jats:italic>Sus scrofa<\/jats:italic> pre-miRNAs in the miRBase database. Target genes of differentially expressed miRNAs were predicted using the miRGen 3.0 database, then filtered miRNA target genes were subjected to Gene Ontology (GO) analysis and Search Tool for the Retrieval of Interacting Genes\/ Proteins (STRING) analysis. Stem-loop quantitative real-time PCR was performed to confirm the accuracy of high-throughput sequencing data. In total, 387, 472, and 490 annotated and novel mature miRNAs were identified from PRV Fa \u0394gE\/gI strain-infected, Fa wild-type strain-infected, and non-infected PK-15 cells, respectively. Five PRV-encoded miRNAs were also identified. GO analysis showed that target genes of differentially expressed miRNAs in PRV Fa \u0394gE\/gI strain-infected and Fa wild-type strain-infected PK-15 cells were mainly involved in biological regulation and metabolic processes. STRING analysis showed that immune-related target genes of differentially expressed miRNAs in the Toll-like receptor signaling pathway, B cell receptor signaling pathway, T cell receptor signaling pathway, nuclear factor-\u03baB signaling pathway, and transforming growth factor-\u03b2 signaling pathway were interrelated. This is the first report of the small RNA transcriptome in PRV mutant wild-type strain-infected and Fa \u0394gE\/gI strain-infected porcine cell lines. Our findings will contribute to the prevention and treatment of PRV mutant strains.<\/jats:p>","DOI":"10.1007\/s11262-020-01760-6","type":"journal-article","created":{"date-parts":[[2020,5,8]],"date-time":"2020-05-08T11:02:58Z","timestamp":1588935778000},"page":"461-471","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Effects of gE\/gI deletions on the miRNA expression of PRV-infected PK-15 cells"],"prefix":"10.1007","volume":"56","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8400-7052","authenticated-orcid":false,"given":"Xiao","family":"Liu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuancheng","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuan","family":"Luo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yanxi","family":"Chen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2020,5,8]]},"reference":[{"key":"1760_CR1","doi-asserted-by":"publisher","first-page":"9431","DOI":"10.1128\/JVI.01317-13","volume":"87","author":"R Kratchmarov","year":"2013","unstructured":"Kratchmarov R, Kramer T, Greco TM, Taylor MP, Chang TH, Cristea IM, Enquist LW (2013) Glycoproteins gE and gI are required for efficient KIF1A-dependent anterograde axonal transport of alphaherpesvirus particles in neurons. J Virol 87:9431","journal-title":"J Virol"},{"key":"1760_CR2","doi-asserted-by":"publisher","first-page":"948","DOI":"10.1099\/vir.0.059253-0","volume":"95","author":"K Klingbeil","year":"2014","unstructured":"Klingbeil K, Lange E, Teifke JP, Mettenleiter TC, Fuchs W (2014) Immunization of pigs with an attenuated pseudorabies virus recombinant expressing the haemagglutinin of pandemic swine origin H1N1 influenza A virus. J Gen Virol 95:948\u2013959","journal-title":"J Gen Virol"},{"key":"1760_CR3","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.expneurol.2013.10.016","volume":"251","author":"K-Z Lee","year":"2014","unstructured":"Lee K-Z, Lane MA, Dougherty BJ, Mercier LM, Sandhu MS, Sanchez JC, Reier PJ, Fuller DD (2014) Intraspinal transplantation and modulation of donor neuron electrophysiological activity. Exp Neurol 251:47\u201357","journal-title":"Exp Neurol"},{"key":"1760_CR4","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.vetmic.2016.11.019","volume":"206","author":"CM Freuling","year":"2017","unstructured":"Freuling CM, M\u00fcller TF, Mettenleiter TC (2017) Vaccines against pseudorabies virus (PrV). Vet Microbiol 206:3\u20139","journal-title":"Vet Microbiol"},{"key":"1760_CR5","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1016\/j.chom.2013.03.010","volume":"13","author":"O Koyuncu Orkide","year":"2013","unstructured":"Koyuncu Orkide O, Hogue Ian B, Enquist Lynn W (2013) Virus infections in the nervous system. Cell Host Microbe 13:379\u2013393","journal-title":"Cell Host Microbe"},{"key":"1760_CR6","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.virusres.2014.09.003","volume":"195","author":"Z Gu","year":"2015","unstructured":"Gu Z, Dong J, Wang J, Hou C, Sun H, Yang W, Bai J, Jiang P (2015) A novel inactivated gE\/gI deleted pseudorabies virus (PRV) vaccine completely protects pigs from an emerged variant PRV challenge. Virus Res 195:57\u201363","journal-title":"Virus Res"},{"key":"1760_CR7","first-page":"e00440","volume":"4","author":"E Mathijs","year":"2016","unstructured":"Mathijs E, Vandenbussche F, Verpoest S, De Regge N, Van Borm S (2016) Complete genome sequence of pseudorabies virus reference strain NIA3 using single-molecule real-time sequencing. Genome Announc 4:e00440\u2013e516","journal-title":"Genome Announc"},{"key":"1760_CR8","doi-asserted-by":"publisher","first-page":"e00566","DOI":"10.1128\/JVI.00566-18","volume":"92","author":"BG Klupp","year":"2018","unstructured":"Klupp BG, Hellberg T, R\u00f6nfeldt S, Franzke K, Fuchs W, Mettenleiter TC (2018) Function of the nonconserved N-terminal domain of pseudorabies virus pUL31 in nuclear egress. J Virol 92:e00566\u2013e618","journal-title":"J Virol"},{"key":"1760_CR9","first-page":"e00084","volume":"92","author":"M Vallbracht","year":"2018","unstructured":"Vallbracht M, Rehwaldt S, Klupp BG, Mettenleiter TC, Fuchs W (2018) Functional role of N-Linked glycosylation in pseudorabies virus glycoprotein gH. J Virol 92:e00084\u2013e118","journal-title":"J Virol"},{"key":"1760_CR10","first-page":"e00050","volume":"91","author":"G DuRaine","year":"2017","unstructured":"DuRaine G, Wisner TW, Howard P, Williams M, Johnson DC (2017) Herpes simplex virus gE\/gI and US9 promote both envelopment and sorting of virus particles in the cytoplasm of neurons, two processes that precede anterograde transport in axons. J Virol 91:e00050\u2013e117","journal-title":"J Virol"},{"key":"1760_CR11","doi-asserted-by":"publisher","first-page":"462","DOI":"10.1128\/MMBR.69.3.462-500.2005","volume":"69","author":"LE Pomeranz","year":"2005","unstructured":"Pomeranz LE, Reynolds AE, Hengartner CJ (2005) Molecular biology of pseudorabies virus: impact on neurovirology and veterinary medicine. Microbiol Mol Biol Rev 69:462","journal-title":"Microbiol Mol Biol Rev"},{"key":"1760_CR12","doi-asserted-by":"publisher","first-page":"e02276","DOI":"10.1128\/JVI.02276-16","volume":"91","author":"JAS Lamote","year":"2017","unstructured":"Lamote JAS, Kestens M, Van Waesberghe C, Delva J, De Pelsmaeker S, Devriendt B, Favoreel HW (2017) The pseudorabies virus glycoprotein gE\/gI complex suppresses type I interferon production by plasmacytoid dendritic cells. J Virol 91:e02276\u2013e2316","journal-title":"J Virol"},{"key":"1760_CR13","doi-asserted-by":"publisher","first-page":"90","DOI":"10.3390\/v8040090","volume":"8","author":"Y Tang","year":"2016","unstructured":"Tang Y, Liu J, Fang Q, Wang T, Sun M, An T, Tian Z, Cai X (2016) Recombinant pseudorabies virus (PRV) expressing firefly luciferase effectively screened for CRISPR\/Cas9 single guide RNAs and antiviral compounds. Viruses 8:90","journal-title":"Viruses"},{"key":"1760_CR14","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1186\/1743-422X-8-272","volume":"8","author":"L Zhu","year":"2011","unstructured":"Zhu L, Yi Y, Xu Z, Cheng L, Tang S, Guo W (2011) Growth, physicochemical properties, and morphogenesis of Chinese wild-type PRV Fa and its gene-deleted mutant strain PRV SA215. Virol J 8:272","journal-title":"Virol J"},{"key":"1760_CR15","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.antiviral.2016.03.002","volume":"130","author":"W Tong","year":"2016","unstructured":"Tong W, Li G, Liang C, Liu F, Tian Q, Cao Y, Li L, Zheng X, Zheng H, Tong G (2016) A live, attenuated pseudorabies virus strain JS-2012 deleted for gE\/gI protects against both classical and emerging strains. Antivir Res 130:110\u2013117","journal-title":"Antivir Res"},{"key":"1760_CR16","doi-asserted-by":"publisher","first-page":"3379","DOI":"10.1016\/j.vaccine.2014.04.035","volume":"32","author":"C Wang","year":"2014","unstructured":"Wang C, Yuan J, Qin H, Luo Y, Cong X, Li Y, Chen J, Li S, Sun Y, Qiu H (2014) A novel gE-deleted pseudorabies virus (PRV) provides rapid and complete protection from lethal challenge with the PRV variant emerging in Bartha-K61-vaccinated swine population in China. Vaccine 32:3379\u20133385","journal-title":"Vaccine"},{"key":"1760_CR17","doi-asserted-by":"publisher","first-page":"9301","DOI":"10.1128\/JVI.79.14.9301-9305.2005","volume":"79","author":"MA Samols","year":"2005","unstructured":"Samols MA, Hu J, Skalsky RL, Renne R (2005) Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi\u2019s sarcoma-associated herpesvirus. J Virol 79:9301","journal-title":"J Virol"},{"key":"1760_CR18","doi-asserted-by":"publisher","first-page":"2684","DOI":"10.1128\/JVI.03189-14","volume":"89","author":"T Kanda","year":"2015","unstructured":"Kanda T, Miyata M, Kano M, Kondo S, Yoshizaki T, Iizasa H (2015) Clustered microRNAs of the epstein-barr virus cooperatively downregulate an epithelial cell-specific metastasis suppressor. J Virol 89:2684","journal-title":"J Virol"},{"key":"1760_CR19","doi-asserted-by":"publisher","first-page":"734","DOI":"10.1126\/science.1096781","volume":"304","author":"S Pfeffer","year":"2004","unstructured":"Pfeffer S, Zavolan M, Gr\u00e4sser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T (2004) Identification of virus-encoded microRNAs. Science 304:734","journal-title":"Science"},{"key":"1760_CR20","doi-asserted-by":"publisher","first-page":"e1007156","DOI":"10.1371\/journal.ppat.1007156","volume":"14","author":"R Chirayil","year":"2018","unstructured":"Chirayil R, Kincaid RP, Dahlke C, Kuny CV, D\u00e4lken N, Spohn M, Lawson B, Grundhoff A, Sullivan CS (2018) Identification of virus-encoded microRNAs in divergent Papillomaviruses. PLOS Pathog 14:e1007156","journal-title":"PLOS Pathog"},{"key":"1760_CR21","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.jviromet.2015.07.021","volume":"225","author":"J Fan","year":"2015","unstructured":"Fan J, Zuo Y, Shen X, Gu W, Di J (2015) Development of an enzyme-linked immunosorbent assay for the monitoring and surveillance of antibodies to porcine epidemic diarrhea virus based on a recombinant membrane protein. J Virol Methods 225:90\u201394","journal-title":"J Virol Methods"},{"key":"1760_CR22","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1128\/JVI.75.1.469-479.2001","volume":"75","author":"N Alema\u00f1","year":"2001","unstructured":"Alema\u00f1 N, MaI Q, L\u00f3pez-Pe\u00f1a M, V\u00e1zquez S, Guerrero FH, Nieto JM (2001) Induction and inhibition of apoptosis by pseudorabies virus in the trigeminal ganglion during acute infection of swine. J Virol 75:469","journal-title":"J Virol"},{"key":"1760_CR23","doi-asserted-by":"publisher","first-page":"580","DOI":"10.1016\/j.molmed.2006.10.006","volume":"12","author":"R Garzon","year":"2006","unstructured":"Garzon R, Fabbri M, Cimmino A, Calin GA, Croce CM (2006) MicroRNA expression and function in cancer. Trends Mol Med 12:580\u2013587","journal-title":"Trends Mol Med"},{"key":"1760_CR24","doi-asserted-by":"publisher","first-page":"e0120377","DOI":"10.1371\/journal.pone.0120377","volume":"10","author":"X Liu","year":"2015","unstructured":"Liu X, Zhu L, Liao S, Xu Z, Zhou Y (2015) The porcine microRNA transcriptome response to transmissible gastroenteritis virus infection. PLoS ONE 10:e0120377","journal-title":"PLoS ONE"},{"key":"1760_CR25","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1016\/j.gene.2013.06.012","volume":"527","author":"J Zhang","year":"2013","unstructured":"Zhang J, Liu Y, Zhang X, Pan J, Nie Z, Zhang W, Yu W, Chen J, Liu L, Li J et al (2013) The identification of microRNAs in the whitespotted bamboo shark (Chiloscyllium plagiosum) liver by Illumina sequencing. Gene 527:259\u2013265","journal-title":"Gene"},{"key":"1760_CR26","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1186\/s12985-018-0922-x","volume":"15","author":"X Liu","year":"2018","unstructured":"Liu X, Wei H, Liao S, Ye J, Zhu L, Xu Z (2018) MicroRNA transcriptome analysis of porcine vital organ responses to immunosuppressive porcine cytomegalovirus infection. Virol J 15:16","journal-title":"Virol J"},{"key":"1760_CR27","doi-asserted-by":"publisher","first-page":"624","DOI":"10.1099\/jgv.0.000708","volume":"98","author":"G Zhao","year":"2017","unstructured":"Zhao G, Hou J, Xu G, Xiang A, Kang Y, Yan Y, Zhang X, Yang G, Xiao S, Sun S (2017) Cellular microRNA miR-10a-5p inhibits replication of porcine reproductive and respiratory syndrome virus by targeting the host factor signal recognition particle 14. J Gen Virol 98:624\u2013632","journal-title":"J Gen Virol"},{"key":"1760_CR28","doi-asserted-by":"publisher","first-page":"5879","DOI":"10.4049\/jimmunol.1100535","volume":"187","author":"X Xue","year":"2011","unstructured":"Xue X, Feng T, Yao S, Wolf KJ, Liu C-G, Liu X, Elson CO, Cong Y (2011) Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12\/IL-23p40. J Immunol 187:5879","journal-title":"J Immunol"},{"key":"1760_CR29","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1016\/j.jinf.2013.05.003","volume":"67","author":"S Wu","year":"2013","unstructured":"Wu S, He L, Li Y, Wang T, Feng L, Jiang L, Zhang P, Huang X (2013) miR-146a facilitates replication of dengue virus by dampening interferon induction by targeting TRAF6. J Infect 67:329\u2013341","journal-title":"J Infect"},{"key":"1760_CR30","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1186\/s12985-015-0359-4","volume":"12","author":"X Li","year":"2015","unstructured":"Li X, Zhu L, Liu X, Sun X, Zhou Y, Lang Q, Li P, Cai Y, Qiao X, Xu Z (2015) Differential expression of microRNAs in porcine parvovirus infected porcine cell line. Virol J 12:128","journal-title":"Virol J"},{"key":"1760_CR31","doi-asserted-by":"publisher","first-page":"2204","DOI":"10.3390\/ijms16012204","volume":"16","author":"Y Cai","year":"2015","unstructured":"Cai Y, Zhu L, Zhou Y, Liu X, Liu X, Li X, Lang Q, Qiao X, Xu Z (2015) Identification and analysis of differentially-expressed microRNAs in Japanese encephalitis virus-infected PK-15 cells with deep sequencing. Int J Mol Sci 16:2204\u20132219","journal-title":"Int J Mol Sci"},{"key":"1760_CR32","doi-asserted-by":"publisher","first-page":"e0150971","DOI":"10.1371\/journal.pone.0150971","volume":"11","author":"X Liu","year":"2016","unstructured":"Liu X, Liao S, Xu Z, Zhu L, Yang F, Guo W (2016) Identification and analysis of the porcine microRNA in porcine cytomegalovirus-infected macrophages using deep sequencing. PLoS ONE 11:e0150971","journal-title":"PLoS ONE"},{"key":"1760_CR33","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1016\/j.yexcr.2018.05.019","volume":"369","author":"X He","year":"2018","unstructured":"He X, Teng J, Cui C, Li D, Wen L (2018) MicroRNA-182 inhibits HCMV replication through activation of type I IFN response by targeting FOXO3 in neural cells. Exp Cell Res 369:197\u2013207","journal-title":"Exp Cell Res"},{"key":"1760_CR34","doi-asserted-by":"publisher","first-page":"4494","DOI":"10.1128\/JVI.02810-14","volume":"89","author":"S Xiao","year":"2015","unstructured":"Xiao S, Wang X, Ni H, Li N, Zhang A, Liu H, Pu F, Xu L, Gao J, Zhao Q, Mu Y, Wang C, Sun Y, Du T, Xu X, Zhang G, Hiscox JA, Goodfellow IG, Zhou E-M (2015) MicroRNA miR-24-3p promotes porcine reproductive and respiratory syndrome virus replication through suppression of heme oxygenase-1 expression. J Virol 89:4494","journal-title":"J Virol"}],"container-title":["Virus Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11262-020-01760-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s11262-020-01760-6\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11262-020-01760-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,8]],"date-time":"2021-05-08T00:48:53Z","timestamp":1620434933000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s11262-020-01760-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,8]]},"references-count":34,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2020,8]]}},"alternative-id":["1760"],"URL":"https:\/\/doi.org\/10.1007\/s11262-020-01760-6","relation":{},"ISSN":["0920-8569","1572-994X"],"issn-type":[{"type":"print","value":"0920-8569"},{"type":"electronic","value":"1572-994X"}],"subject":[],"published":{"date-parts":[[2020,5,8]]},"assertion":[{"value":"29 December 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 April 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 May 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare that they have no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"The animal welfare standards in this study were established on the basis of internationally agreed and science-based principles within the World Organisation for Animal Health. All experiments were carried out in accordance with Chinese animal welfare legislation and were approved by Southwest University Committee on Ethics in the Care and Use of Laboratory Animals.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Informed consent"}}]}}