{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T21:13:28Z","timestamp":1792790008750,"version":"4.5.0"},"reference-count":51,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2025,6,30]],"date-time":"2025-06-30T00:00:00Z","timestamp":1751241600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2023YFD2402400"],"award-info":[{"award-number":["2023YFD2402400"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2023AFB393"],"award-info":[{"award-number":["2023AFB393"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2023M731234"],"award-info":[{"award-number":["2023M731234"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["31972824"],"award-info":[{"award-number":["31972824"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["32303048"],"award-info":[{"award-number":["32303048"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2023BBA001"],"award-info":[{"award-number":["2023BBA001"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["SZYJY2023006"],"award-info":[{"award-number":["SZYJY2023006"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Hubei Provincial Natural Science Foundation of China","award":["2023YFD2402400"],"award-info":[{"award-number":["2023YFD2402400"]}]},{"name":"Hubei Provincial Natural Science Foundation of China","award":["2023AFB393"],"award-info":[{"award-number":["2023AFB393"]}]},{"name":"Hubei Provincial Natural Science Foundation of China","award":["2023M731234"],"award-info":[{"award-number":["2023M731234"]}]},{"name":"Hubei Provincial Natural Science Foundation of China","award":["31972824"],"award-info":[{"award-number":["31972824"]}]},{"name":"Hubei Provincial Natural Science Foundation of China","award":["32303048"],"award-info":[{"award-number":["32303048"]}]},{"name":"Hubei Provincial Natural Science Foundation of China","award":["2023BBA001"],"award-info":[{"award-number":["2023BBA001"]}]},{"name":"Hubei Provincial Natural Science Foundation of China","award":["SZYJY2023006"],"award-info":[{"award-number":["SZYJY2023006"]}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2023YFD2402400"],"award-info":[{"award-number":["2023YFD2402400"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2023AFB393"],"award-info":[{"award-number":["2023AFB393"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2023M731234"],"award-info":[{"award-number":["2023M731234"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["31972824"],"award-info":[{"award-number":["31972824"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["32303048"],"award-info":[{"award-number":["32303048"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2023BBA001"],"award-info":[{"award-number":["2023BBA001"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["SZYJY2023006"],"award-info":[{"award-number":["SZYJY2023006"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2023YFD2402400"],"award-info":[{"award-number":["2023YFD2402400"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2023AFB393"],"award-info":[{"award-number":["2023AFB393"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2023M731234"],"award-info":[{"award-number":["2023M731234"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31972824"],"award-info":[{"award-number":["31972824"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32303048"],"award-info":[{"award-number":["32303048"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2023BBA001"],"award-info":[{"award-number":["2023BBA001"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["SZYJY2023006"],"award-info":[{"award-number":["SZYJY2023006"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Major Science and Technology Project of Hubei Province","award":["2023YFD2402400"],"award-info":[{"award-number":["2023YFD2402400"]}]},{"name":"Major Science and Technology Project of Hubei Province","award":["2023AFB393"],"award-info":[{"award-number":["2023AFB393"]}]},{"name":"Major Science and Technology Project of Hubei Province","award":["2023M731234"],"award-info":[{"award-number":["2023M731234"]}]},{"name":"Major Science and Technology Project of Hubei Province","award":["31972824"],"award-info":[{"award-number":["31972824"]}]},{"name":"Major Science and Technology Project of Hubei Province","award":["32303048"],"award-info":[{"award-number":["32303048"]}]},{"name":"Major Science and Technology Project of Hubei Province","award":["2023BBA001"],"award-info":[{"award-number":["2023BBA001"]}]},{"name":"Major Science and Technology Project of Hubei Province","award":["SZYJY2023006"],"award-info":[{"award-number":["SZYJY2023006"]}]},{"name":"HZAU-AGIS Cooperation Fund","award":["2023YFD2402400"],"award-info":[{"award-number":["2023YFD2402400"]}]},{"name":"HZAU-AGIS Cooperation Fund","award":["2023AFB393"],"award-info":[{"award-number":["2023AFB393"]}]},{"name":"HZAU-AGIS Cooperation Fund","award":["2023M731234"],"award-info":[{"award-number":["2023M731234"]}]},{"name":"HZAU-AGIS Cooperation Fund","award":["31972824"],"award-info":[{"award-number":["31972824"]}]},{"name":"HZAU-AGIS Cooperation Fund","award":["32303048"],"award-info":[{"award-number":["32303048"]}]},{"name":"HZAU-AGIS Cooperation Fund","award":["2023BBA001"],"award-info":[{"award-number":["2023BBA001"]}]},{"name":"HZAU-AGIS Cooperation Fund","award":["SZYJY2023006"],"award-info":[{"award-number":["SZYJY2023006"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Grass carp reovirus (GCRV), particularly the highly prevalent genotype II (GCRV-II), is known to infect peripheral blood leukocytes (PBLs) of grass carp. However, it is unclear whether GCRV-II can induce apoptosis in bystander lymphocytes within infected PBLs. Here, we have shown that GCRV-II infection induces apoptosis via the mitochondria-dependent caspase-3 pathway in infected PBLs. GCRV-II infection was also found to induce a significant increase in reactive oxygen species (ROS) accumulation in leukocytes and lymphocytes, accompanied by increased apoptosis in IgM+ B and CD4+ T lymphocyte subsets. Further studies have demonstrated that the targeted inhibition of mitochondrial ROS production can effectively attenuate apoptosis in neighboring B and T lymphocytes within infected PBLs, suggesting that GCRV-II-induced pro-apoptotic effects on bystander lymphocytes largely require the involvement of the mitochondrial-dependent ROS pathway. Taken together, our study reveals the underlying mechanism by which GCRV-II induces apoptosis in bystander B and T lymphocytes through ROS production, providing new insights into understanding the virus-induced pro-apoptotic mechanism in specific immune cells and a potential strategy for viral immune escape.<\/jats:p>","DOI":"10.3390\/v17070930","type":"journal-article","created":{"date-parts":[[2025,7,2]],"date-time":"2025-07-02T07:55:43Z","timestamp":1751442943000},"page":"930","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["GCRV-II Triggers B and T Lymphocyte Apoptosis via Mitochondrial ROS Pathway"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0009-0001-1008-2236","authenticated-orcid":false,"given":"Jie","family":"Wang","sequence":"first","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Jing","family":"Dong","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chang-Song","family":"Wu","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tian-Tian","family":"Tian","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xu-Jie","family":"Zhang","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China"},{"name":"Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan 430070, China"},{"name":"Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9956-3879","authenticated-orcid":false,"given":"Yong-An","family":"Zhang","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,6,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1111\/raq.12844","article-title":"Structure, function and immune evasion strategies of aquareoviruses, with focus on grass carp reovirus","volume":"16","author":"Li","year":"2023","journal-title":"Rev. Aquac."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1016\/j.virs.2023.04.006","article-title":"Temperature-regulated type II grass carp reovirus establishes latent infection in Ctenopharyngodon idella brain","volume":"38","author":"Jiang","year":"2023","journal-title":"Virol. Sin."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Zhu, W.T., Qiao, M.H., Hu, M.D., Huo, X.C., Zhang, Y.A., and Su, J.G. (2023). Type II grass carp reovirus rapidly invades grass carp (Ctenopharyngodon idella) via nostril\u2013olfactory system\u2013brain axis, gill, and skin on head. Viruses, 15.","DOI":"10.20944\/preprints202306.2070.v1"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Yang, L., and Su, J.G. (2021). Type II grass carp reovirus infects leukocytes but not erythrocytes and thrombocytes in grass carp (Ctenopharyngodon idella). Viruses, 13.","DOI":"10.3390\/v13050870"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Jiang, L., Liu, A.Q., Zhang, C., Zhang, Y.A., and Tu, J.G. (2022). Hsp90 regulates GCRV-II proliferation by interacting with VP35 as its receptor and chaperone. J. Virol., 96.","DOI":"10.1128\/jvi.01175-22"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1016\/j.fsi.2022.06.022","article-title":"Non-pathogenic grass carp reovirus infection leads to both apoptosis and autophagy in a grass carp cell line","volume":"127","author":"Dai","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.virusres.2014.03.021","article-title":"Grass carp reovirus induces apoptosis and oxidative stress in grass carp (Ctenopharyngodon idellus) kidney cell line","volume":"185","author":"Jia","year":"2014","journal-title":"Virus Res."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Liang, B., and Su, J.G. (2019). Inducible nitric oxide synthase (iNOS) mediates vascular endothelial cell apoptosis in grass carp reovirus (GCRV)-induced hemorrhage. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20246335"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Zhao, K.W., Zhang, Y.S., Yin, Z.J., Tan, L.B., Juario, M., Zhang, H.Y., Liu, Y.L., Xu, P.X., Zhang, Q., and Zhao, G.A. (2025). GCRV-II major outer capsid protein VP4 promotes cell apoptosis by VDAC2-mediated calcium pathway facilitation. Int. J. Biol. Macromol., 285.","DOI":"10.1016\/j.ijbiomac.2024.138273"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Xia, N., Zhang, Y.Q., Zhu, W.T., and Su, J.G. (2024). GCRV-II invades monocytes\/macrophages and induces macrophage polarization and apoptosis in tissues to facilitate viral replication and dissemination. J. Virol., 98.","DOI":"10.1128\/jvi.01469-23"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"7369","DOI":"10.1128\/JVI.02310-09","article-title":"Semliki forest virus-induced endoplasmic reticulum stress accelerates apoptotic death of mammalian cells","volume":"84","author":"Barry","year":"2010","journal-title":"J. Virol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Yang, S., Gorshkov, K., Lee, E.M., Xu, M., Cheng, Y.S., Sun, N., Soheilian, F., de Val, N., Ming, G.L., and Song, H.J. (2020). Zika virus-induced neuronal apoptosis via increased mitochondrial fragmentation. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.598203"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2014\/467452","article-title":"RNA viruses: ROS-mediated cell death","volume":"2014","author":"Reshi","year":"2014","journal-title":"Int. J. Cell Biol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Mayank, A.K., Sharma, S., Nailwal, H., and Lal, S.K. (2015). Nucleoprotein of influenza A virus negatively impacts antiapoptotic protein API5 to enhance E2F1-dependent apoptosis and virus replication. Cell Death Dis., 6.","DOI":"10.1038\/cddis.2015.360"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10495-019-01575-3","article-title":"Influenza A virus-induced apoptosis and virus propagation","volume":"25","author":"Ampomah","year":"2020","journal-title":"Apoptosis"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1038\/nri.2016.147","article-title":"Programmed cell death as a defence against infection","volume":"17","author":"Jorgensen","year":"2017","journal-title":"Nat. Rev. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Zhou, X.C., Jiang, W.B., Liu, Z.S., Liu, S., and Liang, X.Z. (2017). Virus infection and death receptor-mediated apoptosis. Viruses, 9.","DOI":"10.3390\/v9110316"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1016\/j.tim.2021.12.011","article-title":"Mitochondria-mediated oxidative stress during viral infection","volume":"30","author":"Foo","year":"2022","journal-title":"Trends Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Finlay, B.B., Galluzzi, L., Brenner, C., Morselli, E., Touat, Z., and Kroemer, G. (2008). Viral control of mitochondrial apoptosis. PLoS Pathog., 4.","DOI":"10.1371\/journal.ppat.1000018"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.cellimm.2015.08.001","article-title":"Epstein-barr virus latent membrane protein 2A (LMP2A)-mediated changes in Fas expression and Fas-dependent apoptosis: Role of Lyn\/Syk activation","volume":"297","author":"Incrocci","year":"2015","journal-title":"Cell Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1182\/blood-2013-03-493718","article-title":"HTLV-1 Tax oncoprotein stimulates ROS production and apoptosis in T cells by interacting with USP10","volume":"122","author":"Takahashi","year":"2013","journal-title":"Blood"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Schank, M., Zhao, J., Wang, L., Nguyen, L.N.T., Zhang, Y., Wu, X.Y., Zhang, J.Y., Jiang, Y., Ning, S.B., and El Gazzar, M. (2023). ROS-induced mitochondrial dysfunction in CD4 T cells from ART-controlled people living with HIV. Viruses, 15.","DOI":"10.3390\/v15051061"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Stapleford, K., Verburg, S.G., Lelievre, R.M., Westerveld, M.J., Inkol, J.M., Sun, Y.L., and Workenhe, S.T. (2022). Viral-mediated activation and inhibition of programmed cell death. PLoS Pathog., 18.","DOI":"10.1371\/journal.ppat.1010718"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.redox.2017.11.024","article-title":"HIV-1 Tat protein induces DNA damage in human peripheral blood B-lymphocytes via mitochondrial ROS production","volume":"15","author":"Germini","year":"2018","journal-title":"Redox Biol."},{"key":"ref_25","first-page":"1","article-title":"Monocytic reactive oxygen species-induced T cell apoptosis impairs cellular immune response to SARS-CoV-2 mRNA vaccine","volume":"1","author":"Gimenez","year":"2025","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1016\/j.jaci.2022.06.020","article-title":"Angiotensin II induces reactive oxygen species, DNA damage, and T-cell apoptosis in severe COVID-19","volume":"150","author":"Kundura","year":"2022","journal-title":"J. Allergy Clin. Immun."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2840","DOI":"10.1128\/JVI.74.6.2840-2846.2000","article-title":"Hepatitis B virus X protein colocalizes to mitochondria with a human voltage-dependent anion channel, HVDAC3, and alters its transmembrane potential","volume":"74","author":"Rahmani","year":"2000","journal-title":"J. Virol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1002\/hep.21679","article-title":"Hepatitis C virus protein expression causes calcium-mediated mitochondrial bioenergetic dysfunction and nitro-oxidative stress","volume":"46","author":"Piccoli","year":"2007","journal-title":"Hepatology"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Lecoeur, H., Borgne-Sanchez, A., Chaloin, O., El-Khoury, R., Brabant, M., Langonn\u00e9, A., Porceddu, M., Bri\u00e8re, J.J., Buron, N., and Rebouillat, D. (2012). HIV-1 Tat protein directly induces mitochondrial membrane permeabilization and inactivates cytochrome oxidase. Cell Death Dis., 3.","DOI":"10.1038\/cddis.2012.21"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Boonnate, P., Kariya, R., and Okada, S. (2023). Shikonin induces ROS-dependent apoptosis via mitochondria depolarization and ER stress in adult T cell leukemia\/lymphoma. Antioxidants, 12.","DOI":"10.3390\/antiox12040864"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Meuren, L.M., Prestes, E.B., Papa, M.P., de Carvalho, L.R.P., Mustafa, Y.M., da Costa, L.S., Da Poian, A.T., Bozza, M.T., and Arruda, L.B. (2022). Infection of endothelial cells by dengue virus induces ROS production by different sources affecting virus replication, cellular activation, death and vascular permeability. Front. Immunol., 13.","DOI":"10.3389\/fimmu.2022.810376"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1038\/ni.1913","article-title":"IgT, a primitive immunoglobulin class specialized in mucosal immunity","volume":"11","author":"Zhang","year":"2010","journal-title":"Nat. Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Cui, Z.W., Zhang, X.Y., Wu, C.S., Zhang, Y.A., Zhou, Y., and Zhang, X.J. (2020). Membrane IgM+ plasma cells in grass carp (Ctenopharyngodon idella): Insights into the conserved evolution of IgM+ plasma cells in vertebrates. Dev. Comp. Immunol., 106.","DOI":"10.1016\/j.dci.2020.103613"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Lu, T.Z., Liu, X., Wu, C.S., Ma, Z.Y., Wang, Y., Zhang, Y.A., and Zhang, X.J. (2022). Molecular and functional analyses of the primordial costimulatory molecule CD80\/86 and its receptors CD28 and CD152 (CTLA-4) in a teleost fish. Front. Immunol., 13.","DOI":"10.3389\/fimmu.2022.885005"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Han, X.Q., Pan, Y.R., Zhong, Y.Q., Tian, T.T., Liu, X., Zhang, X.J., and Zhang, Y.A. (2024). Identification and functional analyses of CD4-1+ cells in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol., 150.","DOI":"10.1016\/j.fsi.2024.109649"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1016\/j.aquaculture.2024.741784","article-title":"Edwardsiella piscicida promotes mitophagy to escape autophagy-mediated antibacterial defense in teleost monocytes\/macrophages","volume":"596","author":"Liu","year":"2025","journal-title":"Aquaculture"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Lv, M.Y., Wang, Y.W., Yu, J.Z., Kong, Y.Y., Zhou, H., Zhang, A.Y., and Wang, X.Y. (2024). Grass carp IL-2 promotes neutrophil extracellular traps formation via inducing ROS production and autophagy in vitro. Fish Shellfish Immunol., 144.","DOI":"10.1016\/j.fsi.2023.109261"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1038\/ni1389","article-title":"B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities","volume":"7","author":"Li","year":"2006","journal-title":"Nat. Immunol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Wu, C.S., Dai, Y.S., Yuan, G.L., Su, J.G., and Liu, X.L. (2019). Immunomodulatory effects and induction of apoptosis by different molecular weight chitosan oligosaccharides in head kidney macrophages from blunt snout bream (Megalobrama amblycephala). Front. Immunol., 10.","DOI":"10.3389\/fimmu.2019.00869"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15.","DOI":"10.1186\/s13059-014-0550-8"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3804","DOI":"10.1128\/JVI.02959-14","article-title":"Tom70 mediates sendai virus-induced apoptosis on mitochondria","volume":"89","author":"Wei","year":"2015","journal-title":"J. Virol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"17387","DOI":"10.1074\/jbc.RA118.003840","article-title":"ROS-induced HSP70 promotes cytoplasmic translocation of high-mobility group box 1b and stimulates antiviral autophagy in grass carp kidney cells","volume":"293","author":"Rao","year":"2018","journal-title":"J. Biol. Chem."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Xin, L.S., Li, C., Bai, C.M., and Wang, C.M. (2018). Ostreid Herpesvirus-1 Infects Specific Hemocytes in Ark Clam. Scapharca Broughtonii Viruses, 10.","DOI":"10.3390\/v10100529"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"249","DOI":"10.3354\/dao052249","article-title":"White spot syndrome virus (WSSV) infects specific hemocytes of the shrimp","volume":"52","author":"Wang","year":"2002","journal-title":"Dis. Aquat. Organ."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1038\/s41418-021-00870-4","article-title":"The antiviral action of the RIG-I induced pathway of apoptosis (RIPA) is enhanced by its ability to degrade Otulin, which deubiquitinates IRF3","volume":"29","author":"Raja","year":"2022","journal-title":"Cell Death Differ."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Zhu, H.C., Hou, P.L., Chu, F.Y., Li, X.Y., Zhang, W.J., Sun, X.N., Liu, Y., Zhao, G.M., Gao, Y.W., and He, D.C. (2024). PBLD promotes IRF3 mediated the type I interferon (IFN-I) response and apoptosis to inhibit viral replication. Cell Death Dis., 15.","DOI":"10.1038\/s41419-024-07083-w"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1016\/j.immuni.2022.01.003","article-title":"Interferon-\u03b3 primes macrophages for pathogen ligand-induced killing via a caspase-8 and mitochondrial cell death pathway","volume":"55","author":"Simpson","year":"2022","journal-title":"Immunity"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"5921","DOI":"10.1128\/JVI.73.13.5921-5929.2001","article-title":"Human lymphocyte apoptosis after exposure to influenza A virus","volume":"75","author":"Nichols","year":"2001","journal-title":"J. Virol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Roberts, N.J. (2023). The enigma of lymphocyte apoptosis in the response to influenza virus infection. Viruses, 15.","DOI":"10.3390\/v15030759"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.virol.2019.06.001","article-title":"The role of cell surface expression of influenza virus neuraminidase in induction of human lymphocyte apoptosis","volume":"534","author":"Nichols","year":"2019","journal-title":"Virology"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/17\/7\/930\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:02:08Z","timestamp":1760032928000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/17\/7\/930"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,30]]},"references-count":51,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2025,7]]}},"alternative-id":["v17070930"],"URL":"https:\/\/doi.org\/10.3390\/v17070930","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,30]]}}}