In Vitro Measles Virus Infection of Human Lymphocyte Subsets Demonstrates High Susceptibility and Permissiveness of both Naive and Memory B Cells

Measles is characterized by a transient immune suppression, leading to an increased risk of opportunistic infections. Measles virus (MV) infection of immune cells is mediated by the cellular receptor CD150, expressed by subsets of lymphocytes, dendritic cells, macrophages, and thymocytes. Previous s...

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Veröffentlicht in:Journal of virology 2018-04, Vol.92 (8)
Hauptverfasser: Laksono, Brigitta M, Grosserichter-Wagener, Christina, de Vries, Rory D, Langeveld, Simone A G, Brem, Maarten D, van Dongen, Jacques J M, Katsikis, Peter D, Koopmans, Marion P G, van Zelm, Menno C, de Swart, Rik L
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container_title Journal of virology
container_volume 92
creator Laksono, Brigitta M
Grosserichter-Wagener, Christina
de Vries, Rory D
Langeveld, Simone A G
Brem, Maarten D
van Dongen, Jacques J M
Katsikis, Peter D
Koopmans, Marion P G
van Zelm, Menno C
de Swart, Rik L
description Measles is characterized by a transient immune suppression, leading to an increased risk of opportunistic infections. Measles virus (MV) infection of immune cells is mediated by the cellular receptor CD150, expressed by subsets of lymphocytes, dendritic cells, macrophages, and thymocytes. Previous studies showed that human and nonhuman primate memory T cells express higher levels of CD150 than naive cells and are more susceptible to MV infection. However, limited information is available about the CD150 expression and relative susceptibility to MV infection of B-cell subsets. In this study, we assessed the susceptibility and permissiveness of naive and memory T- and B-cell subsets from human peripheral blood or tonsils to MV infection. Our study demonstrates that naive and memory B cells express CD150, but at lower frequencies than memory T cells. Nevertheless, both naive and memory B cells proved to be highly permissive to MV infection. Furthermore, we assessed the susceptibility and permissiveness of various functionally distinct T and B cells, such as helper T (T ) cell subsets and IgG- and IgA-positive memory B cells, in peripheral blood and tonsils. We demonstrated that T 1T 17 cells and plasma and germinal center B cells were the subsets most susceptible and permissive to MV infection. Our study suggests that both naive and memory B cells, along with several other antigen-experienced lymphocytes, are important target cells of MV infection. Depletion of these cells potentially contributes to the pathogenesis of measles immune suppression. Measles is associated with immune suppression and is often complicated by bacterial pneumonia, otitis media, or gastroenteritis. Measles virus infects antigen-presenting cells and T and B cells, and depletion of these cells may contribute to lymphopenia and immune suppression. Measles has been associated with follicular exhaustion in lymphoid tissues in humans and nonhuman primates, emphasizing the importance of MV infection of B cells However, information on the relative susceptibility of B-cell subsets is scarce. Here, we compared the susceptibility and permissiveness to MV infection of human naive and memory T- and B-cell subsets isolated from peripheral blood or tonsils. Our results demonstrate that both naive and memory B cells are more permissive to MV infection than T cells. The highest infection levels were detected in plasma cells and germinal center B cells, suggesting that infection and depletion of these
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Measles virus (MV) infection of immune cells is mediated by the cellular receptor CD150, expressed by subsets of lymphocytes, dendritic cells, macrophages, and thymocytes. Previous studies showed that human and nonhuman primate memory T cells express higher levels of CD150 than naive cells and are more susceptible to MV infection. However, limited information is available about the CD150 expression and relative susceptibility to MV infection of B-cell subsets. In this study, we assessed the susceptibility and permissiveness of naive and memory T- and B-cell subsets from human peripheral blood or tonsils to MV infection. Our study demonstrates that naive and memory B cells express CD150, but at lower frequencies than memory T cells. Nevertheless, both naive and memory B cells proved to be highly permissive to MV infection. Furthermore, we assessed the susceptibility and permissiveness of various functionally distinct T and B cells, such as helper T (T ) cell subsets and IgG- and IgA-positive memory B cells, in peripheral blood and tonsils. We demonstrated that T 1T 17 cells and plasma and germinal center B cells were the subsets most susceptible and permissive to MV infection. Our study suggests that both naive and memory B cells, along with several other antigen-experienced lymphocytes, are important target cells of MV infection. Depletion of these cells potentially contributes to the pathogenesis of measles immune suppression. Measles is associated with immune suppression and is often complicated by bacterial pneumonia, otitis media, or gastroenteritis. Measles virus infects antigen-presenting cells and T and B cells, and depletion of these cells may contribute to lymphopenia and immune suppression. Measles has been associated with follicular exhaustion in lymphoid tissues in humans and nonhuman primates, emphasizing the importance of MV infection of B cells However, information on the relative susceptibility of B-cell subsets is scarce. Here, we compared the susceptibility and permissiveness to MV infection of human naive and memory T- and B-cell subsets isolated from peripheral blood or tonsils. Our results demonstrate that both naive and memory B cells are more permissive to MV infection than T cells. The highest infection levels were detected in plasma cells and germinal center B cells, suggesting that infection and depletion of these populations contribute to reduced host resistance.</description><identifier>ISSN: 0022-538X</identifier><identifier>EISSN: 1098-5514</identifier><identifier>DOI: 10.1128/JVI.00131-18</identifier><identifier>PMID: 29437964</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Adult ; B-Lymphocytes - immunology ; B-Lymphocytes - pathology ; B-Lymphocytes - virology ; Child ; Female ; Humans ; Immunologic Memory ; Male ; Measles - immunology ; Measles - pathology ; Measles virus - immunology ; Pathogenesis and Immunity ; Th1 Cells - immunology ; Th1 Cells - pathology ; Th1 Cells - virology ; Th17 Cells - immunology ; Th17 Cells - pathology ; Th17 Cells - virology</subject><ispartof>Journal of virology, 2018-04, Vol.92 (8)</ispartof><rights>Copyright © 2018 Laksono et al.</rights><rights>Copyright © 2018 Laksono et al. 2018 Laksono et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c346t-da5070d3ef7ec18abe1985604caebdd3af0be839d560e2e6c0cdedadc4008c843</citedby><cites>FETCH-LOGICAL-c346t-da5070d3ef7ec18abe1985604caebdd3af0be839d560e2e6c0cdedadc4008c843</cites><orcidid>0000-0003-4161-1919 ; 0000-0001-7690-5218 ; 0000-0003-3599-8969</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5874404/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5874404/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29437964$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Dutch, Rebecca Ellis</contributor><creatorcontrib>Laksono, Brigitta M</creatorcontrib><creatorcontrib>Grosserichter-Wagener, Christina</creatorcontrib><creatorcontrib>de Vries, Rory D</creatorcontrib><creatorcontrib>Langeveld, Simone A G</creatorcontrib><creatorcontrib>Brem, Maarten D</creatorcontrib><creatorcontrib>van Dongen, Jacques J M</creatorcontrib><creatorcontrib>Katsikis, Peter D</creatorcontrib><creatorcontrib>Koopmans, Marion P G</creatorcontrib><creatorcontrib>van Zelm, Menno C</creatorcontrib><creatorcontrib>de Swart, Rik L</creatorcontrib><title>In Vitro Measles Virus Infection of Human Lymphocyte Subsets Demonstrates High Susceptibility and Permissiveness of both Naive and Memory B Cells</title><title>Journal of virology</title><addtitle>J Virol</addtitle><description>Measles is characterized by a transient immune suppression, leading to an increased risk of opportunistic infections. Measles virus (MV) infection of immune cells is mediated by the cellular receptor CD150, expressed by subsets of lymphocytes, dendritic cells, macrophages, and thymocytes. Previous studies showed that human and nonhuman primate memory T cells express higher levels of CD150 than naive cells and are more susceptible to MV infection. However, limited information is available about the CD150 expression and relative susceptibility to MV infection of B-cell subsets. In this study, we assessed the susceptibility and permissiveness of naive and memory T- and B-cell subsets from human peripheral blood or tonsils to MV infection. Our study demonstrates that naive and memory B cells express CD150, but at lower frequencies than memory T cells. Nevertheless, both naive and memory B cells proved to be highly permissive to MV infection. Furthermore, we assessed the susceptibility and permissiveness of various functionally distinct T and B cells, such as helper T (T ) cell subsets and IgG- and IgA-positive memory B cells, in peripheral blood and tonsils. We demonstrated that T 1T 17 cells and plasma and germinal center B cells were the subsets most susceptible and permissive to MV infection. Our study suggests that both naive and memory B cells, along with several other antigen-experienced lymphocytes, are important target cells of MV infection. Depletion of these cells potentially contributes to the pathogenesis of measles immune suppression. Measles is associated with immune suppression and is often complicated by bacterial pneumonia, otitis media, or gastroenteritis. Measles virus infects antigen-presenting cells and T and B cells, and depletion of these cells may contribute to lymphopenia and immune suppression. Measles has been associated with follicular exhaustion in lymphoid tissues in humans and nonhuman primates, emphasizing the importance of MV infection of B cells However, information on the relative susceptibility of B-cell subsets is scarce. Here, we compared the susceptibility and permissiveness to MV infection of human naive and memory T- and B-cell subsets isolated from peripheral blood or tonsils. Our results demonstrate that both naive and memory B cells are more permissive to MV infection than T cells. The highest infection levels were detected in plasma cells and germinal center B cells, suggesting that infection and depletion of these populations contribute to reduced host resistance.</description><subject>Adult</subject><subject>B-Lymphocytes - immunology</subject><subject>B-Lymphocytes - pathology</subject><subject>B-Lymphocytes - virology</subject><subject>Child</subject><subject>Female</subject><subject>Humans</subject><subject>Immunologic Memory</subject><subject>Male</subject><subject>Measles - immunology</subject><subject>Measles - pathology</subject><subject>Measles virus - immunology</subject><subject>Pathogenesis and Immunity</subject><subject>Th1 Cells - immunology</subject><subject>Th1 Cells - pathology</subject><subject>Th1 Cells - virology</subject><subject>Th17 Cells - immunology</subject><subject>Th17 Cells - pathology</subject><subject>Th17 Cells - virology</subject><issn>0022-538X</issn><issn>1098-5514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUFv1DAQhS0Eokvhxhn5yKEpduJknQsSbIFdtAUkoOJmOfaka5TYi8eplJ_Rf4y3LVU5WTPz-dlvHiEvOTvlvJRvPl9sThnjFS-4fEQWnLWyqGsuHpMFY2VZ1JX8dUSeIf7OlBCNeEqOylZUy7YRC3K98fTCpRjoOWgcAHMVJ6Qb34NJLngaerqeRu3pdh73u2DmBPT71CEkpGcwBo8p6pQvrt3lLk_QwD65zg0uzVR7S79BHB2iuwIPiAe9LqQd_aJz5wY4zypxpu_pCoYBn5MnvR4QXtydx-Tnxw8_Vuti-_XTZvVuW5hKNKmwumZLZivol2C41B3wVtYNE0ZDZ22le9aBrFqbe1BCY5ixYLU1gjFppKiOydtb3f3UjWAN-OxjUPvoRh1nFbRT_0-826nLcKVquRSCHQRe3wnE8GcCTCrbNNmC9hAmVOVh_axlbZnRk1vUxIAYob9_hjN1SFHlFNVNiorLjL96-LV7-F9s1V8_MJyv</recordid><startdate>20180415</startdate><enddate>20180415</enddate><creator>Laksono, Brigitta M</creator><creator>Grosserichter-Wagener, Christina</creator><creator>de Vries, Rory D</creator><creator>Langeveld, Simone A G</creator><creator>Brem, Maarten D</creator><creator>van Dongen, Jacques J M</creator><creator>Katsikis, Peter D</creator><creator>Koopmans, Marion P G</creator><creator>van Zelm, Menno C</creator><creator>de Swart, Rik L</creator><general>American Society for Microbiology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4161-1919</orcidid><orcidid>https://orcid.org/0000-0001-7690-5218</orcidid><orcidid>https://orcid.org/0000-0003-3599-8969</orcidid></search><sort><creationdate>20180415</creationdate><title>In Vitro Measles Virus Infection of Human Lymphocyte Subsets Demonstrates High Susceptibility and Permissiveness of both Naive and Memory B Cells</title><author>Laksono, Brigitta M ; Grosserichter-Wagener, Christina ; de Vries, Rory D ; Langeveld, Simone A G ; Brem, Maarten D ; van Dongen, Jacques J M ; Katsikis, Peter D ; Koopmans, Marion P G ; van Zelm, Menno C ; de Swart, Rik L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c346t-da5070d3ef7ec18abe1985604caebdd3af0be839d560e2e6c0cdedadc4008c843</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adult</topic><topic>B-Lymphocytes - immunology</topic><topic>B-Lymphocytes - pathology</topic><topic>B-Lymphocytes - virology</topic><topic>Child</topic><topic>Female</topic><topic>Humans</topic><topic>Immunologic Memory</topic><topic>Male</topic><topic>Measles - immunology</topic><topic>Measles - pathology</topic><topic>Measles virus - immunology</topic><topic>Pathogenesis and Immunity</topic><topic>Th1 Cells - immunology</topic><topic>Th1 Cells - pathology</topic><topic>Th1 Cells - virology</topic><topic>Th17 Cells - immunology</topic><topic>Th17 Cells - pathology</topic><topic>Th17 Cells - virology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Laksono, Brigitta M</creatorcontrib><creatorcontrib>Grosserichter-Wagener, Christina</creatorcontrib><creatorcontrib>de Vries, Rory D</creatorcontrib><creatorcontrib>Langeveld, Simone A G</creatorcontrib><creatorcontrib>Brem, Maarten D</creatorcontrib><creatorcontrib>van Dongen, Jacques J M</creatorcontrib><creatorcontrib>Katsikis, Peter D</creatorcontrib><creatorcontrib>Koopmans, Marion P G</creatorcontrib><creatorcontrib>van Zelm, Menno C</creatorcontrib><creatorcontrib>de Swart, Rik L</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of virology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Laksono, Brigitta M</au><au>Grosserichter-Wagener, Christina</au><au>de Vries, Rory D</au><au>Langeveld, Simone A G</au><au>Brem, Maarten D</au><au>van Dongen, Jacques J M</au><au>Katsikis, Peter D</au><au>Koopmans, Marion P G</au><au>van Zelm, Menno C</au><au>de Swart, Rik L</au><au>Dutch, Rebecca Ellis</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>In Vitro Measles Virus Infection of Human Lymphocyte Subsets Demonstrates High Susceptibility and Permissiveness of both Naive and Memory B Cells</atitle><jtitle>Journal of virology</jtitle><addtitle>J Virol</addtitle><date>2018-04-15</date><risdate>2018</risdate><volume>92</volume><issue>8</issue><issn>0022-538X</issn><eissn>1098-5514</eissn><abstract>Measles is characterized by a transient immune suppression, leading to an increased risk of opportunistic infections. Measles virus (MV) infection of immune cells is mediated by the cellular receptor CD150, expressed by subsets of lymphocytes, dendritic cells, macrophages, and thymocytes. Previous studies showed that human and nonhuman primate memory T cells express higher levels of CD150 than naive cells and are more susceptible to MV infection. However, limited information is available about the CD150 expression and relative susceptibility to MV infection of B-cell subsets. In this study, we assessed the susceptibility and permissiveness of naive and memory T- and B-cell subsets from human peripheral blood or tonsils to MV infection. Our study demonstrates that naive and memory B cells express CD150, but at lower frequencies than memory T cells. Nevertheless, both naive and memory B cells proved to be highly permissive to MV infection. Furthermore, we assessed the susceptibility and permissiveness of various functionally distinct T and B cells, such as helper T (T ) cell subsets and IgG- and IgA-positive memory B cells, in peripheral blood and tonsils. We demonstrated that T 1T 17 cells and plasma and germinal center B cells were the subsets most susceptible and permissive to MV infection. Our study suggests that both naive and memory B cells, along with several other antigen-experienced lymphocytes, are important target cells of MV infection. Depletion of these cells potentially contributes to the pathogenesis of measles immune suppression. Measles is associated with immune suppression and is often complicated by bacterial pneumonia, otitis media, or gastroenteritis. Measles virus infects antigen-presenting cells and T and B cells, and depletion of these cells may contribute to lymphopenia and immune suppression. Measles has been associated with follicular exhaustion in lymphoid tissues in humans and nonhuman primates, emphasizing the importance of MV infection of B cells However, information on the relative susceptibility of B-cell subsets is scarce. Here, we compared the susceptibility and permissiveness to MV infection of human naive and memory T- and B-cell subsets isolated from peripheral blood or tonsils. Our results demonstrate that both naive and memory B cells are more permissive to MV infection than T cells. 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subjects Adult
B-Lymphocytes - immunology
B-Lymphocytes - pathology
B-Lymphocytes - virology
Child
Female
Humans
Immunologic Memory
Male
Measles - immunology
Measles - pathology
Measles virus - immunology
Pathogenesis and Immunity
Th1 Cells - immunology
Th1 Cells - pathology
Th1 Cells - virology
Th17 Cells - immunology
Th17 Cells - pathology
Th17 Cells - virology
title In Vitro Measles Virus Infection of Human Lymphocyte Subsets Demonstrates High Susceptibility and Permissiveness of both Naive and Memory B Cells
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