Application of B cell immortalization for the isolation of antibodies and B cell clones from vaccine and infection settings

The isolation and characterization of neutralizing antibodies from infection and vaccine settings informs future vaccine design, and methodologies that streamline the isolation of antibodies and the generation of B cell clones are of great interest. Retroviral transduction to express Bcl-6 and Bcl-x...

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Vydáno v:	Frontiers in immunology Ročník 13; s. 1087018
Hlavní autoři:	Boswell, Kristin L., Watkins, Timothy A., Cale, Evan M., Samsel, Jakob, Andrews, Sarah F., Ambrozak, David R., Driscoll, Jefferson I., Messina, Michael A., Narpala, Sandeep, Hopp, Christine S., Cagigi, Alberto, Casazza, Joseph P., Yamamoto, Takuya, Zhou, Tongqing, Schief, William R., Crompton, Peter D., Ledgerwood, Julie E., Connors, Mark, Gama, Lucio, Kwong, Peter D., McDermott, Adrian, Mascola, John R., Koup, Richard A.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	Switzerland Frontiers Media S.A 13.12.2022
Témata:	Antibodies, Neutralizing B cell B-Lymphocytes Cell Line chronic infection Clone Cells HIV Seropositivity HIV-1 Humans immortalization Immunology malaria vaccination Vaccines HIV-1 influenza B cell antibody chronic infection immortalization malaria vaccination
ISSN:	1664-3224, 1664-3224
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Abstract	The isolation and characterization of neutralizing antibodies from infection and vaccine settings informs future vaccine design, and methodologies that streamline the isolation of antibodies and the generation of B cell clones are of great interest. Retroviral transduction to express Bcl-6 and Bcl-xL and transform primary B cells has been shown to promote long-term B cell survival and antibody secretion in vitro , and can be used to isolate antibodies from memory B cells. However, application of this methodology to B cell subsets from different tissues and B cells from chronically infected individuals has not been well characterized. Here, we characterize Bcl-6/Bcl-xL B cell immortalization across multiple tissue types and B cell subsets in healthy and HIV-1 infected individuals, as well as individuals recovering from malaria. In healthy individuals, naïve and memory B cell subsets from PBMCs and tonsil tissue transformed with similar efficiencies, and displayed similar characteristics with respect to their longevity and immunoglobulin secretion. In HIV-1-viremic individuals or in individuals with recent malaria infections, the exhausted CD27 - CD21 - memory B cells transformed with lower efficiency, but the transformed B cells expanded and secreted IgG with similar efficiency. Importantly, we show that this methodology can be used to isolate broadly neutralizing antibodies from HIV-infected individuals. Overall, we demonstrate that Bcl-6/Bcl-xL B cell immortalization can be used to isolate antibodies and generate B cell clones from different B cell populations, albeit with varying efficiencies.
AbstractList	The isolation and characterization of neutralizing antibodies from infection and vaccine settings informs future vaccine design, and methodologies that streamline the isolation of antibodies and the generation of B cell clones are of great interest. Retroviral transduction to express Bcl-6 and Bcl-xL and transform primary B cells has been shown to promote long-term B cell survival and antibody secretion in vitro , and can be used to isolate antibodies from memory B cells. However, application of this methodology to B cell subsets from different tissues and B cells from chronically infected individuals has not been well characterized. Here, we characterize Bcl-6/Bcl-xL B cell immortalization across multiple tissue types and B cell subsets in healthy and HIV-1 infected individuals, as well as individuals recovering from malaria. In healthy individuals, naïve and memory B cell subsets from PBMCs and tonsil tissue transformed with similar efficiencies, and displayed similar characteristics with respect to their longevity and immunoglobulin secretion. In HIV-1-viremic individuals or in individuals with recent malaria infections, the exhausted CD27 - CD21 - memory B cells transformed with lower efficiency, but the transformed B cells expanded and secreted IgG with similar efficiency. Importantly, we show that this methodology can be used to isolate broadly neutralizing antibodies from HIV-infected individuals. Overall, we demonstrate that Bcl-6/Bcl-xL B cell immortalization can be used to isolate antibodies and generate B cell clones from different B cell populations, albeit with varying efficiencies. The isolation and characterization of neutralizing antibodies from infection and vaccine settings informs future vaccine design, and methodologies that streamline the isolation of antibodies and the generation of B cell clones are of great interest. Retroviral transduction to express Bcl-6 and Bcl-xL and transform primary B cells has been shown to promote long-term B cell survival and antibody secretion in vitro, and can be used to isolate antibodies from memory B cells. However, application of this methodology to B cell subsets from different tissues and B cells from chronically infected individuals has not been well characterized. Here, we characterize Bcl-6/Bcl-xL B cell immortalization across multiple tissue types and B cell subsets in healthy and HIV-1 infected individuals, as well as individuals recovering from malaria. In healthy individuals, naïve and memory B cell subsets from PBMCs and tonsil tissue transformed with similar efficiencies, and displayed similar characteristics with respect to their longevity and immunoglobulin secretion. In HIV-1-viremic individuals or in individuals with recent malaria infections, the exhausted CD27-CD21- memory B cells transformed with lower efficiency, but the transformed B cells expanded and secreted IgG with similar efficiency. Importantly, we show that this methodology can be used to isolate broadly neutralizing antibodies from HIV-infected individuals. Overall, we demonstrate that Bcl-6/Bcl-xL B cell immortalization can be used to isolate antibodies and generate B cell clones from different B cell populations, albeit with varying efficiencies. The isolation and characterization of neutralizing antibodies from infection and vaccine settings informs future vaccine design, and methodologies that streamline the isolation of antibodies and the generation of B cell clones are of great interest. Retroviral transduction to express Bcl-6 and Bcl-xL and transform primary B cells has been shown to promote long-term B cell survival and antibody secretion in vitro, and can be used to isolate antibodies from memory B cells. However, application of this methodology to B cell subsets from different tissues and B cells from chronically infected individuals has not been well characterized. Here, we characterize Bcl-6/Bcl-xL B cell immortalization across multiple tissue types and B cell subsets in healthy and HIV-1 infected individuals, as well as individuals recovering from malaria. In healthy individuals, naïve and memory B cell subsets from PBMCs and tonsil tissue transformed with similar efficiencies, and displayed similar characteristics with respect to their longevity and immunoglobulin secretion. In HIV-1-viremic individuals or in individuals with recent malaria infections, the exhausted CD27-CD21- memory B cells transformed with lower efficiency, but the transformed B cells expanded and secreted IgG with similar efficiency. Importantly, we show that this methodology can be used to isolate broadly neutralizing antibodies from HIV-infected individuals. Overall, we demonstrate that Bcl-6/Bcl-xL B cell immortalization can be used to isolate antibodies and generate B cell clones from different B cell populations, albeit with varying efficiencies.The isolation and characterization of neutralizing antibodies from infection and vaccine settings informs future vaccine design, and methodologies that streamline the isolation of antibodies and the generation of B cell clones are of great interest. Retroviral transduction to express Bcl-6 and Bcl-xL and transform primary B cells has been shown to promote long-term B cell survival and antibody secretion in vitro, and can be used to isolate antibodies from memory B cells. However, application of this methodology to B cell subsets from different tissues and B cells from chronically infected individuals has not been well characterized. Here, we characterize Bcl-6/Bcl-xL B cell immortalization across multiple tissue types and B cell subsets in healthy and HIV-1 infected individuals, as well as individuals recovering from malaria. In healthy individuals, naïve and memory B cell subsets from PBMCs and tonsil tissue transformed with similar efficiencies, and displayed similar characteristics with respect to their longevity and immunoglobulin secretion. In HIV-1-viremic individuals or in individuals with recent malaria infections, the exhausted CD27-CD21- memory B cells transformed with lower efficiency, but the transformed B cells expanded and secreted IgG with similar efficiency. Importantly, we show that this methodology can be used to isolate broadly neutralizing antibodies from HIV-infected individuals. Overall, we demonstrate that Bcl-6/Bcl-xL B cell immortalization can be used to isolate antibodies and generate B cell clones from different B cell populations, albeit with varying efficiencies. The isolation and characterization of neutralizing antibodies from infection and vaccine settings informs future vaccine design, and methodologies that streamline the isolation of antibodies and the generation of B cell clones are of great interest. Retroviral transduction to express Bcl-6 and Bcl-xL and transform primary B cells has been shown to promote long-term B cell survival and antibody secretion , and can be used to isolate antibodies from memory B cells. However, application of this methodology to B cell subsets from different tissues and B cells from chronically infected individuals has not been well characterized. Here, we characterize Bcl-6/Bcl-xL B cell immortalization across multiple tissue types and B cell subsets in healthy and HIV-1 infected individuals, as well as individuals recovering from malaria. In healthy individuals, naïve and memory B cell subsets from PBMCs and tonsil tissue transformed with similar efficiencies, and displayed similar characteristics with respect to their longevity and immunoglobulin secretion. In HIV-1-viremic individuals or in individuals with recent malaria infections, the exhausted CD27 CD21 memory B cells transformed with lower efficiency, but the transformed B cells expanded and secreted IgG with similar efficiency. Importantly, we show that this methodology can be used to isolate broadly neutralizing antibodies from HIV-infected individuals. Overall, we demonstrate that Bcl-6/Bcl-xL B cell immortalization can be used to isolate antibodies and generate B cell clones from different B cell populations, albeit with varying efficiencies.
Author	Messina, Michael A. Cagigi, Alberto Watkins, Timothy A. Yamamoto, Takuya Crompton, Peter D. Connors, Mark Boswell, Kristin L. Narpala, Sandeep Ledgerwood, Julie E. Casazza, Joseph P. Mascola, John R. Samsel, Jakob Driscoll, Jefferson I. McDermott, Adrian Kwong, Peter D. Schief, William R. Cale, Evan M. Andrews, Sarah F. Zhou, Tongqing Koup, Richard A. Gama, Lucio Ambrozak, David R. Hopp, Christine S.
AuthorAffiliation	5 HIV-Specific Immunity Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Bethesda, MD , United States 2 Institute for Biomedical Sciences, George Washington University , Washington, DC , United States 3 Malaria Infection Biology and Immunity Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Rockville, MD , United States 1 Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Bethesda, MD , United States 4 Department of Immunology and Microbial Science, IAVI Neutralizing Antibody Center and Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery, The Scripps Research Institute , La Jolla, CA , United States
AuthorAffiliation_xml	– name: 5 HIV-Specific Immunity Section, Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Bethesda, MD , United States – name: 4 Department of Immunology and Microbial Science, IAVI Neutralizing Antibody Center and Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery, The Scripps Research Institute , La Jolla, CA , United States – name: 2 Institute for Biomedical Sciences, George Washington University , Washington, DC , United States – name: 1 Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Bethesda, MD , United States – name: 3 Malaria Infection Biology and Immunity Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health , Rockville, MD , United States
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Copyright	Copyright © 2022 Boswell, Watkins, Cale, Samsel, Andrews, Ambrozak, Driscoll, Messina, Narpala, Hopp, Cagigi, Casazza, Yamamoto, Zhou, Schief, Crompton, Ledgerwood, Connors, Gama, Kwong, McDermott, Mascola and Koup. Copyright © 2022 Boswell, Watkins, Cale, Samsel, Andrews, Ambrozak, Driscoll, Messina, Narpala, Hopp, Cagigi, Casazza, Yamamoto, Zhou, Schief, Crompton, Ledgerwood, Connors, Gama, Kwong, McDermott, Mascola and Koup 2022 Boswell, Watkins, Cale, Samsel, Andrews, Ambrozak, Driscoll, Messina, Narpala, Hopp, Cagigi, Casazza, Yamamoto, Zhou, Schief, Crompton, Ledgerwood, Connors, Gama, Kwong, McDermott, Mascola and Koup
Copyright_xml	– notice: Copyright © 2022 Boswell, Watkins, Cale, Samsel, Andrews, Ambrozak, Driscoll, Messina, Narpala, Hopp, Cagigi, Casazza, Yamamoto, Zhou, Schief, Crompton, Ledgerwood, Connors, Gama, Kwong, McDermott, Mascola and Koup. – notice: Copyright © 2022 Boswell, Watkins, Cale, Samsel, Andrews, Ambrozak, Driscoll, Messina, Narpala, Hopp, Cagigi, Casazza, Yamamoto, Zhou, Schief, Crompton, Ledgerwood, Connors, Gama, Kwong, McDermott, Mascola and Koup 2022 Boswell, Watkins, Cale, Samsel, Andrews, Ambrozak, Driscoll, Messina, Narpala, Hopp, Cagigi, Casazza, Yamamoto, Zhou, Schief, Crompton, Ledgerwood, Connors, Gama, Kwong, McDermott, Mascola and Koup
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Keywords	HIV-1 influenza B cell antibody chronic infection immortalization malaria vaccination
Language	English
License	Copyright © 2022 Boswell, Watkins, Cale, Samsel, Andrews, Ambrozak, Driscoll, Messina, Narpala, Hopp, Cagigi, Casazza, Yamamoto, Zhou, Schief, Crompton, Ledgerwood, Connors, Gama, Kwong, McDermott, Mascola and Koup. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Christopher Sundling, Karolinska Institutet (KI), Sweden; Wataru Ise, Osaka University, Japan; Rajagopal Murugan, Leiden University Medical Center (LUMC), Netherlands Edited by: Annalisa Ciabattini, University of Siena, Italy This article was submitted to B Cell Biology, a section of the journal Frontiers in Immunology
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SubjectTerms	Antibodies, Neutralizing B cell B-Lymphocytes Cell Line chronic infection Clone Cells HIV Seropositivity HIV-1 Humans immortalization Immunology malaria vaccination Vaccines
Title	Application of B cell immortalization for the isolation of antibodies and B cell clones from vaccine and infection settings
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