{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T17:43:49Z","timestamp":1791654229955,"version":"4.3.4"},"reference-count":42,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2022,7,19]],"date-time":"2022-07-19T00:00:00Z","timestamp":1658188800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Laboratory of Lingnan Modern Agriculture Project","award":["NT2021008"],"award-info":[{"award-number":["NT2021008"]}]},{"name":"Laboratory of Lingnan Modern Agriculture Project","award":["2022KJ150"],"award-info":[{"award-number":["2022KJ150"]}]},{"name":"Guangdong Provincial Special Fund for Modern Agriculture Industry Technology Innovation Teams","award":["NT2021008"],"award-info":[{"award-number":["NT2021008"]}]},{"name":"Guangdong Provincial Special Fund for Modern Agriculture Industry Technology Innovation Teams","award":["2022KJ150"],"award-info":[{"award-number":["2022KJ150"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Largemouth bass virus (LMBV), belonging to the genus Ranavirus, causes high mortality and heavy economic losses in largemouth bass aquaculture. In the present study, a novel cell line, designated as MsF, was established from the fin of largemouth bass (Micropterus salmoides), and applied to investigate the characteristics of cell death induced by LMBV. MsF cells showed susceptibility to LMBV, evidenced by the occurrence of a cytopathic effect (CPE), increased viral gene transcription, protein synthesis, and viral titers. In LMBV-infected MsF cells, two or more virus assembly sites were observed around the nucleus. Notably, no apoptotic bodies occurred in LMBV-infected MsF cells after nucleus staining, suggesting that cell death induced by LMBV in host cells was distinct from apoptosis. Consistently, DNA fragmentation was not detected in LMBV-infected MsF cells. Furthermore, only caspase-8 and caspase-3 were significantly activated in LMBV-infected MsF cells, suggesting that caspases were involved in non-apoptotic cell death induced by LMBV in host cells. In addition, the disruption of the mitochondrial membrane potential (\u0394\u03a8m) and reactive oxygen species (ROS) generation were detected in both LMBV-infected MsF cells and fathead minnow (FHM) cells. Combined with our previous study, we propose that cell death induced by LMBV infection was cell type dependent. Although LMBV-infected MsF cells showed the characteristics of non-apoptotic cell death, the signal pathways might crosstalk and interconnect between apoptosis and other PCD during LMBV infection. Together, our results not only established the in vitro LMBV infection model for the study of the interaction between LMBV and host cells but also shed new insights into the mechanisms of ranavirus pathogenesis.<\/jats:p>","DOI":"10.3390\/v14071568","type":"journal-article","created":{"date-parts":[[2022,7,19]],"date-time":"2022-07-19T23:10:22Z","timestamp":1658272222000},"page":"1568","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["Largemouth Bass Virus Infection Induced Non-Apoptotic Cell Death in MsF Cells"],"prefix":"10.3390","volume":"14","author":[{"given":"Jiahui","family":"Yang","sequence":"first","affiliation":[{"name":"Laboratory for Lingnan Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weihua","family":"Xu","sequence":"additional","affiliation":[{"name":"Laboratory for Lingnan Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenji","family":"Wang","sequence":"additional","affiliation":[{"name":"Laboratory for Lingnan Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zanbin","family":"Pan","sequence":"additional","affiliation":[{"name":"Laboratory for Lingnan Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1188-9023","authenticated-orcid":false,"given":"Qiwei","family":"Qin","sequence":"additional","affiliation":[{"name":"Laboratory for Lingnan Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China"},{"name":"University Joint Laboratory of Guangdong Province, Hong Kong and Macao Region on Marine Bioresource Conservation and Exploitation, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohong","family":"Huang","sequence":"additional","affiliation":[{"name":"Laboratory for Lingnan Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Youhua","family":"Huang","sequence":"additional","affiliation":[{"name":"Laboratory for Lingnan Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"167249","DOI":"10.1016\/j.jmb.2021.167249","article-title":"PANoptosis in Viral Infection: The Missing Puzzle Piece in the Cell Death Field","volume":"434","author":"Nguyen","year":"2022","journal-title":"J. Mol. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1146\/annurev-virology-110615-042435","article-title":"Viruses and the Diversity of Cell Death","volume":"3","author":"Danthi","year":"2016","journal-title":"Annu. Rev. Virol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1080\/21505594.2019.1605803","article-title":"The roles of apoptosis, autophagy and unfolded protein response in arbovirus, influenza virus, and HIV infections","volume":"10","author":"Mehrbod","year":"2019","journal-title":"Virulence"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2215","DOI":"10.1099\/vir.0.055277-0","article-title":"Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1\u03b2 secretion and pyroptosis","volume":"94","author":"Tan","year":"2013","journal-title":"J. Gen. Virol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.1164\/rccm.201906-1149OC","article-title":"Respiratory Syncytial Virus Infection Promotes Necroptosis and HMGB1 Release by Airway Epithelial Cells","volume":"201","author":"Simpson","year":"2020","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3181","DOI":"10.3390\/v6083181","article-title":"Human immunodeficiency virus-1 (HIV-1)-mediated apoptosis: New therapeutic targets","volume":"6","author":"Mbita","year":"2014","journal-title":"Viruses"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Silberstein, E., Ulitzky, L., Lima, L.A., Cehan, N., Teixeira-Carvalho, A., Roingeard, P., and Taylor, D.R. (2016). HCV-Mediated Apoptosis of Hepatocytes in Culture and Viral Pathogenesis. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0155708"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.3390\/v4091509","article-title":"Does apoptosis play a role in varicella zoster virus latency and reactivation?","volume":"4","author":"James","year":"2012","journal-title":"Viruses"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1080\/08830180305216","article-title":"Influenza virus induction of apoptosis by intrinsic and extrinsic mechanisms","volume":"22","author":"Lowy","year":"2003","journal-title":"Int. Rev. Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/S0014-5793(01)02573-X","article-title":"West Nile virus-induced bax-dependent apoptosis","volume":"500","author":"Parquet","year":"2001","journal-title":"FEBS Lett."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Zhou, X., Jiang, W., Liu, Z., Liu, S., and Liang, X. (2017). Virus Infection and Death Receptor-Mediated Apoptosis. Viruses, 9.","DOI":"10.3390\/v9110316"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.mib.2020.07.012","article-title":"PANoptosis in microbial infection","volume":"59","author":"Place","year":"2021","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"4641","DOI":"10.1016\/j.csbj.2021.07.038","article-title":"From pyroptosis, apoptosis and necroptosis to PANoptosis: A mechanistic compendium of programmed cell death pathways","volume":"19","author":"Wang","year":"2021","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1408","DOI":"10.1002\/ijc.33698","article-title":"Caspase-8: A key protein of cross-talk signal way in \u201cPANoptosis\u201d in cancer","volume":"149","author":"Jiang","year":"2021","journal-title":"Int. J. Cancer"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1111\/j.1365-2761.2009.01110.x","article-title":"Iridovirus infections in finfish\u2014Critical review with emphasis on ranaviruses","volume":"33","author":"Whittington","year":"2010","journal-title":"J. Fish Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2565","DOI":"10.14202\/vetworld.2020.2565-2577","article-title":"Megalocytiviruses in ornamental fish: A review","volume":"13","author":"Johan","year":"2020","journal-title":"Vet. World"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.virol.2017.06.007","article-title":"Ranaviruses and other members of the family Iridoviridae: Their place in the virosphere","volume":"511","author":"Chinchar","year":"2017","journal-title":"Virology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1099\/jgv.0.000818","article-title":"ICTV Virus Taxonomy Profile: Iridoviridae","volume":"98","author":"Chinchar","year":"2017","journal-title":"J. Gen. Virol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1007\/s10495-007-0089-1","article-title":"Mitochondrion-mediated apoptosis induced by Rana grylio virus infection in fish cells","volume":"12","author":"Huang","year":"2007","journal-title":"Apoptosis"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/S0042-6822(02)00039-9","article-title":"Induction of apoptosis in frog virus 3-infected cells","volume":"306","author":"Chinchar","year":"2003","journal-title":"Virology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.virusres.2012.03.014","article-title":"Differential viral propagation and induction of apoptosis by grouper iridovirus (GIV) in cell lines from three nonhost species","volume":"167","author":"Pham","year":"2012","journal-title":"Virus Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1046\/j.1439-0450.2002.00531.x","article-title":"The epizootic haematopoietic necrosis virus (Iridoviridae) induces apoptosis in vitro","volume":"49","author":"Essbauer","year":"2002","journal-title":"J. Vet. Med. B Infect. Dis. Vet. Public Health"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Li, Y., Jiang, N., Fan, Y., Zhou, Y., Liu, W., Xue, M., Meng, Y., and Zeng, L. (2019). Chinese Giant Salamander (Andrias davidianus) Iridovirus Infection Leads to Apoptotic Cell Death through Mitochondrial Damage, Caspases Activation, and Expression of Apoptotic-Related Genes. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20246149"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1007\/s10495-011-0616-y","article-title":"Singapore grouper iridovirus, a large DNA virus, induces nonapoptotic cell death by a cell type dependent fashion and evokes ERK signaling","volume":"16","author":"Huang","year":"2011","journal-title":"Apoptosis"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1111\/j.1365-2761.2008.00957.x","article-title":"Characterization of apoptosis induced by grouper iridovirus in two newly established cell lines from barramundi, Lates calcarifer (Bloch)","volume":"31","author":"Lai","year":"2008","journal-title":"J. Fish Dis."},{"key":"ref_26","first-page":"104","article-title":"Current status and development trend on China largemouth bass industry","volume":"31","author":"Bai","year":"2013","journal-title":"Chin. Fish. Econ."},{"key":"ref_27","first-page":"72","article-title":"Culture techniques of largemouth bass","volume":"4","author":"Li","year":"2016","journal-title":"Ocean Fish."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"107","DOI":"10.3354\/dao037107","article-title":"Molecular characterization of a ranavirus isolated from largemouth bass Micropterus salmoides","volume":"37","author":"Mao","year":"1999","journal-title":"Dis. Aquat. Org."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.aquaculture.2010.12.032","article-title":"Characterization of a ranavirus isolated from cultured largemouth bass (Micropterus salmoides) in China","volume":"312","author":"Deng","year":"2011","journal-title":"Aquaculture"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"735363","DOI":"10.1016\/j.aquaculture.2020.735363","article-title":"A new ranavirus of the Santee-Cooper group invades largemouth bass (Micropterus salmoides) culture in southwest China","volume":"526","author":"Zhao","year":"2020","journal-title":"Aquaculture"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.fsi.2014.09.010","article-title":"Involvement of the PI3K and ERK signaling pathways in largemouth bass virus-induced apoptosis and viral replication","volume":"41","author":"Huang","year":"2014","journal-title":"Fish Shellfish Immunol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/j.fsi.2022.03.026","article-title":"Autophagy induced by largemouth bass virus inhibits virus replication and apoptosis in epithelioma papulosum cyprini cells","volume":"123","author":"Deng","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.aquaculture.2014.04.044","article-title":"Development of a new cell line from the snout of giant grouper, Epinephelus lanceolatus (Bloch), and its application in iridovirus and nodavirus pathogenesis","volume":"432","author":"Huang","year":"2014","journal-title":"Aquaculture"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.1016\/j.immuni.2019.05.020","article-title":"Caspases in Cell Death, Inflammation, and Disease","volume":"50","author":"Lamkanfi","year":"2019","journal-title":"Immunity"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.fsi.2018.03.008","article-title":"Micropterus salmoides rhabdovirus (MSRV) infection induced apoptosis and activated interferon signaling pathway in largemouth bass skin cells","volume":"76","author":"Gao","year":"2018","journal-title":"Fish Shellfish Immunol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.jviromet.2005.10.029","article-title":"Electron microscopic examination of the viromatrix of Rana grylio virus in a fish cell line","volume":"133","author":"Huang","year":"2006","journal-title":"J. Virol. Methods"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1006\/viro.1996.0509","article-title":"Assembly of African Swine fever virus: Quantitative ultrastructural analysis in vitro and in vivo","volume":"224","author":"Brookes","year":"1996","journal-title":"Virology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1146\/annurev-immunol-073119-095439","article-title":"Caspases in Cell Death, Inflammation, and Pyroptosis","volume":"38","author":"Kesavardhana","year":"2020","journal-title":"Annu. Rev. Immunol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"a036400","DOI":"10.1101\/cshperspect.a036400","article-title":"Mechanism and Regulation of Gasdermin-Mediated Cell Death","volume":"12","author":"Xia","year":"2020","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1038\/s41586-019-1770-6","article-title":"Caspase-8 is the molecular switch for apoptosis, necroptosis and pyroptosis","volume":"575","author":"Fritsch","year":"2019","journal-title":"Nature"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3839","DOI":"10.1038\/onc.2015.455","article-title":"Cell type-dependent ROS and mitophagy response leads to apoptosis or necroptosis in neuroblastoma","volume":"35","author":"Radogna","year":"2016","journal-title":"Oncogene"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1038\/s41590-017-0013-y","article-title":"Oxeiptosis, a ROS-induced caspase-independent apoptosis-like cell-death pathway","volume":"19","author":"Holze","year":"2018","journal-title":"Nat. Immunol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/7\/1568\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:53:58Z","timestamp":1760140438000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/7\/1568"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,19]]},"references-count":42,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["v14071568"],"URL":"https:\/\/doi.org\/10.3390\/v14071568","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,19]]}}}