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Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism

Previous studies imply that peripheral blood leukocytes (PBLs) may play an important role in systemic lymphocystis disease virus (LCDV) dissemination, but whether the PBLs are susceptible and permissive to LCDV infection and the dissemination mechanism need to be clarified. In this study, LCDV was f...

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Autores principales: Sheng, Xiuzhen, Zeng, Jing, Zhong, Ying, Tang, Xiaoqian, Xing, Jing, Chi, Heng, Zhan, Wenbin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9409355/
https://www.ncbi.nlm.nih.gov/pubmed/36012490
http://dx.doi.org/10.3390/ijms23169225
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author Sheng, Xiuzhen
Zeng, Jing
Zhong, Ying
Tang, Xiaoqian
Xing, Jing
Chi, Heng
Zhan, Wenbin
author_facet Sheng, Xiuzhen
Zeng, Jing
Zhong, Ying
Tang, Xiaoqian
Xing, Jing
Chi, Heng
Zhan, Wenbin
author_sort Sheng, Xiuzhen
collection PubMed
description Previous studies imply that peripheral blood leukocytes (PBLs) may play an important role in systemic lymphocystis disease virus (LCDV) dissemination, but whether the PBLs are susceptible and permissive to LCDV infection and the dissemination mechanism need to be clarified. In this study, LCDV was firstly confirmed to infect the PBLs in flounder (Paralichthys olivaceus) in vivo, and to replicate in PBLs in vitro. Subsequently, the 27.8 kDa receptor protein (27.8R), a functional receptor mediating LCDV infection in flounder gill cells, was shown to locate on the cell membrane of PBLs and co-localize with LCDV in PBLs, while blocking of the 27.8R via pre-incubation of anti-27.8R MAb with the PBLs could obviously inhibit LCDV infection, revealing the 27.8R as a receptor for LCDV entry into PBLs. Multicolor fluorescence imaging studies verified that IgM(+) and IgD(+) B-lymphocyte were involved in LCDV infection. In the sorted IgM(+) B-cells, 27.8R(+) and LCDV(+) signals were simultaneously observed, and LCDV copy numbers increased with time, indicating that IgM(+) B-cells expressed the 27.8R and were permissive to LCDV infection. Furthermore, the dynamic changes of IgM(+), 27.8R(+), LCDV(+) and LCDV(+)/IgM(+) PBLs were monitored during the early phase of LCDV infection. It was found that the percentage of IgM(+) B-cells in PBLs clearly declined first and then increased, suggesting LCDV infection facilitated damage to B-cells, whereas the amounts of 27.8R(+) and LCDV(+) PBLs, as well as LCDV-infected IgM(+) B-cells, showed an opposite trend. These results proved that IgM(+) B-lymphocytes could be infected by LCDV via a receptor-mediated mechanism and support viral replication, which provided novel insights for the first time into the role of B-lymphocytes in LCDV dissemination and pathogenesis in teleost fish.
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spelling pubmed-94093552022-08-26 Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism Sheng, Xiuzhen Zeng, Jing Zhong, Ying Tang, Xiaoqian Xing, Jing Chi, Heng Zhan, Wenbin Int J Mol Sci Article Previous studies imply that peripheral blood leukocytes (PBLs) may play an important role in systemic lymphocystis disease virus (LCDV) dissemination, but whether the PBLs are susceptible and permissive to LCDV infection and the dissemination mechanism need to be clarified. In this study, LCDV was firstly confirmed to infect the PBLs in flounder (Paralichthys olivaceus) in vivo, and to replicate in PBLs in vitro. Subsequently, the 27.8 kDa receptor protein (27.8R), a functional receptor mediating LCDV infection in flounder gill cells, was shown to locate on the cell membrane of PBLs and co-localize with LCDV in PBLs, while blocking of the 27.8R via pre-incubation of anti-27.8R MAb with the PBLs could obviously inhibit LCDV infection, revealing the 27.8R as a receptor for LCDV entry into PBLs. Multicolor fluorescence imaging studies verified that IgM(+) and IgD(+) B-lymphocyte were involved in LCDV infection. In the sorted IgM(+) B-cells, 27.8R(+) and LCDV(+) signals were simultaneously observed, and LCDV copy numbers increased with time, indicating that IgM(+) B-cells expressed the 27.8R and were permissive to LCDV infection. Furthermore, the dynamic changes of IgM(+), 27.8R(+), LCDV(+) and LCDV(+)/IgM(+) PBLs were monitored during the early phase of LCDV infection. It was found that the percentage of IgM(+) B-cells in PBLs clearly declined first and then increased, suggesting LCDV infection facilitated damage to B-cells, whereas the amounts of 27.8R(+) and LCDV(+) PBLs, as well as LCDV-infected IgM(+) B-cells, showed an opposite trend. These results proved that IgM(+) B-lymphocytes could be infected by LCDV via a receptor-mediated mechanism and support viral replication, which provided novel insights for the first time into the role of B-lymphocytes in LCDV dissemination and pathogenesis in teleost fish. MDPI 2022-08-17 /pmc/articles/PMC9409355/ /pubmed/36012490 http://dx.doi.org/10.3390/ijms23169225 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Sheng, Xiuzhen
Zeng, Jing
Zhong, Ying
Tang, Xiaoqian
Xing, Jing
Chi, Heng
Zhan, Wenbin
Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism
title Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism
title_full Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism
title_fullStr Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism
title_full_unstemmed Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism
title_short Peripheral Blood B-Lymphocytes Are Involved in Lymphocystis Disease Virus Infection in Flounder (Paralichthys olivaceus) via Cellular Receptor-Mediated Mechanism
title_sort peripheral blood b-lymphocytes are involved in lymphocystis disease virus infection in flounder (paralichthys olivaceus) via cellular receptor-mediated mechanism
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9409355/
https://www.ncbi.nlm.nih.gov/pubmed/36012490
http://dx.doi.org/10.3390/ijms23169225
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