Determinants of vaccine immunogenicity in HIV-infected pregnant women: analysis of B and T cell responses to pandemic H1N1 monovalent vaccine
Influenza infections have high frequency and morbidity in HIV-infected pregnant women, underscoring the importance of vaccine-conferred protection. To identify the factors that determine vaccine immunogenicity in this group, we characterized the relationship of B- and T-cell responses to pandemic H1...
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| Veröffentlicht in: | PloS one 2015-04, Vol.10 (4), p.e0122431-e0122431 |
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| creator | Weinberg, Adriana Muresan, Petronella Richardson, Kelly M Fenton, Terence Dominguez, Teresa Bloom, Anthony Watts, D Heather Abzug, Mark J Nachman, Sharon A Levin, Myron J |
| description | Influenza infections have high frequency and morbidity in HIV-infected pregnant women, underscoring the importance of vaccine-conferred protection. To identify the factors that determine vaccine immunogenicity in this group, we characterized the relationship of B- and T-cell responses to pandemic H1N1 (pH1N1) vaccine with HIV-associated immunologic and virologic characteristics. pH1N1 and seasonal-H1N1 (sH1N1) antibodies were measured in 119 HIV-infected pregnant women after two double-strength pH1N1 vaccine doses. pH1N1-IgG and IgA B-cell FluoroSpot, pH1N1- and sH1N1-interferon γ (IFNγ) and granzyme B (GrB) T-cell FluoroSpot, and flow cytometric characterization of B- and T-cell subsets were performed in 57 subjects. pH1N1-antibodies increased after vaccination, but less than previously described in healthy adults. pH1N1-IgG memory B cells (Bmem) increased, IFNγ-effector T-cells (Teff) decreased, and IgA Bmem and GrB Teff did not change. pH1N1-antibodies and Teff were significantly correlated with each other and with sH1N1-HAI and Teff, respectively, before and after vaccination. pH1N1-antibody responses to the vaccine significantly increased with high proportions of CD4+, low CD8+ and low CD8+HLADR+CD38+ activated (Tact) cells. pH1N1-IgG Bmem responses increased with high proportions of CD19+CD27+CD21- activated B cells (Bact), high CD8+CD39+ regulatory T cells (Treg), and low CD19+CD27-CD21- exhausted B cells (Bexhaust). IFNγ-Teff responses increased with low HIV plasma RNA, CD8+HLADR+CD38+ Tact, CD4+FoxP3+ Treg and CD19+IL10+ Breg. In conclusion, pre-existing antibody and Teff responses to sH1N1 were associated with increased responses to pH1N1 vaccination in HIV-infected pregnant women suggesting an important role for heterosubtypic immunologic memory. High CD4+% T cells were associated with increased, whereas high HIV replication, Tact and Bexhaust were associated with decreased vaccine immunogenicity. High Treg increased antibody responses but decreased Teff responses to the vaccine. The proportions of immature and transitional B cells did not affect the responses to vaccine. Increased Bact were associated with high Bmem responses to the vaccine. |
| doi_str_mv | 10.1371/journal.pone.0122431 |
| format | Article |
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To identify the factors that determine vaccine immunogenicity in this group, we characterized the relationship of B- and T-cell responses to pandemic H1N1 (pH1N1) vaccine with HIV-associated immunologic and virologic characteristics. pH1N1 and seasonal-H1N1 (sH1N1) antibodies were measured in 119 HIV-infected pregnant women after two double-strength pH1N1 vaccine doses. pH1N1-IgG and IgA B-cell FluoroSpot, pH1N1- and sH1N1-interferon γ (IFNγ) and granzyme B (GrB) T-cell FluoroSpot, and flow cytometric characterization of B- and T-cell subsets were performed in 57 subjects. pH1N1-antibodies increased after vaccination, but less than previously described in healthy adults. pH1N1-IgG memory B cells (Bmem) increased, IFNγ-effector T-cells (Teff) decreased, and IgA Bmem and GrB Teff did not change. pH1N1-antibodies and Teff were significantly correlated with each other and with sH1N1-HAI and Teff, respectively, before and after vaccination. pH1N1-antibody responses to the vaccine significantly increased with high proportions of CD4+, low CD8+ and low CD8+HLADR+CD38+ activated (Tact) cells. pH1N1-IgG Bmem responses increased with high proportions of CD19+CD27+CD21- activated B cells (Bact), high CD8+CD39+ regulatory T cells (Treg), and low CD19+CD27-CD21- exhausted B cells (Bexhaust). IFNγ-Teff responses increased with low HIV plasma RNA, CD8+HLADR+CD38+ Tact, CD4+FoxP3+ Treg and CD19+IL10+ Breg. In conclusion, pre-existing antibody and Teff responses to sH1N1 were associated with increased responses to pH1N1 vaccination in HIV-infected pregnant women suggesting an important role for heterosubtypic immunologic memory. High CD4+% T cells were associated with increased, whereas high HIV replication, Tact and Bexhaust were associated with decreased vaccine immunogenicity. High Treg increased antibody responses but decreased Teff responses to the vaccine. The proportions of immature and transitional B cells did not affect the responses to vaccine. Increased Bact were associated with high Bmem responses to the vaccine.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0122431</identifier><identifier>PMID: 25874544</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Adults ; Antibodies ; Antibodies, Viral - immunology ; CD19 antigen ; CD27 antigen ; CD38 antigen ; CD4 antigen ; CD8 antigen ; Effector cells ; Female ; Flow cytometry ; Foxp3 protein ; Granzyme B ; Histocompatibility antigen HLA ; HIV ; HIV Infections - complications ; HIV Infections - immunology ; HIV Infections - pathology ; Human immunodeficiency virus ; Humans ; Immunogenicity ; Immunoglobulin A ; Immunoglobulin G ; Immunological memory ; Influenza ; Influenza A Virus, H1N1 Subtype - immunology ; Influenza A Virus, H1N1 Subtype - pathogenicity ; Influenza Vaccines - administration & dosage ; Influenza Vaccines - immunology ; Influenza, Human - complications ; Influenza, Human - immunology ; Influenza, Human - pathology ; Interferon ; Interleukin 1 ; Interleukin 10 ; Lymphocyte Activation - immunology ; Lymphocytes ; Lymphocytes B ; Lymphocytes T ; Male ; Morbidity ; Pandemics ; Pregnancy ; Pregnancy Complications, Infectious - immunology ; Pregnancy Complications, Infectious - prevention & control ; Ribonucleic acid ; RNA ; T-Lymphocyte Subsets - immunology ; Vaccination ; Vaccines ; γ-Interferon</subject><ispartof>PloS one, 2015-04, Vol.10 (4), p.e0122431-e0122431</ispartof><rights>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (the “License”) Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-c296458010c3121afb48c43267c39437723f77cc82881c5407c9b050025c36813</citedby><cites>FETCH-LOGICAL-c526t-c296458010c3121afb48c43267c39437723f77cc82881c5407c9b050025c36813</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4395240/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4395240/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23871,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25874544$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Apetrei, Cristian</contributor><creatorcontrib>Weinberg, Adriana</creatorcontrib><creatorcontrib>Muresan, Petronella</creatorcontrib><creatorcontrib>Richardson, Kelly M</creatorcontrib><creatorcontrib>Fenton, Terence</creatorcontrib><creatorcontrib>Dominguez, Teresa</creatorcontrib><creatorcontrib>Bloom, Anthony</creatorcontrib><creatorcontrib>Watts, D Heather</creatorcontrib><creatorcontrib>Abzug, Mark J</creatorcontrib><creatorcontrib>Nachman, Sharon A</creatorcontrib><creatorcontrib>Levin, Myron J</creatorcontrib><creatorcontrib>P1086 team</creatorcontrib><creatorcontrib>for the P1086 team</creatorcontrib><title>Determinants of vaccine immunogenicity in HIV-infected pregnant women: analysis of B and T cell responses to pandemic H1N1 monovalent vaccine</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Influenza infections have high frequency and morbidity in HIV-infected pregnant women, underscoring the importance of vaccine-conferred protection. To identify the factors that determine vaccine immunogenicity in this group, we characterized the relationship of B- and T-cell responses to pandemic H1N1 (pH1N1) vaccine with HIV-associated immunologic and virologic characteristics. pH1N1 and seasonal-H1N1 (sH1N1) antibodies were measured in 119 HIV-infected pregnant women after two double-strength pH1N1 vaccine doses. pH1N1-IgG and IgA B-cell FluoroSpot, pH1N1- and sH1N1-interferon γ (IFNγ) and granzyme B (GrB) T-cell FluoroSpot, and flow cytometric characterization of B- and T-cell subsets were performed in 57 subjects. pH1N1-antibodies increased after vaccination, but less than previously described in healthy adults. pH1N1-IgG memory B cells (Bmem) increased, IFNγ-effector T-cells (Teff) decreased, and IgA Bmem and GrB Teff did not change. pH1N1-antibodies and Teff were significantly correlated with each other and with sH1N1-HAI and Teff, respectively, before and after vaccination. pH1N1-antibody responses to the vaccine significantly increased with high proportions of CD4+, low CD8+ and low CD8+HLADR+CD38+ activated (Tact) cells. pH1N1-IgG Bmem responses increased with high proportions of CD19+CD27+CD21- activated B cells (Bact), high CD8+CD39+ regulatory T cells (Treg), and low CD19+CD27-CD21- exhausted B cells (Bexhaust). IFNγ-Teff responses increased with low HIV plasma RNA, CD8+HLADR+CD38+ Tact, CD4+FoxP3+ Treg and CD19+IL10+ Breg. In conclusion, pre-existing antibody and Teff responses to sH1N1 were associated with increased responses to pH1N1 vaccination in HIV-infected pregnant women suggesting an important role for heterosubtypic immunologic memory. High CD4+% T cells were associated with increased, whereas high HIV replication, Tact and Bexhaust were associated with decreased vaccine immunogenicity. High Treg increased antibody responses but decreased Teff responses to the vaccine. The proportions of immature and transitional B cells did not affect the responses to vaccine. Increased Bact were associated with high Bmem responses to the vaccine.</description><subject>Adult</subject><subject>Adults</subject><subject>Antibodies</subject><subject>Antibodies, Viral - immunology</subject><subject>CD19 antigen</subject><subject>CD27 antigen</subject><subject>CD38 antigen</subject><subject>CD4 antigen</subject><subject>CD8 antigen</subject><subject>Effector cells</subject><subject>Female</subject><subject>Flow cytometry</subject><subject>Foxp3 protein</subject><subject>Granzyme B</subject><subject>Histocompatibility antigen HLA</subject><subject>HIV</subject><subject>HIV Infections - complications</subject><subject>HIV Infections - immunology</subject><subject>HIV Infections - pathology</subject><subject>Human immunodeficiency virus</subject><subject>Humans</subject><subject>Immunogenicity</subject><subject>Immunoglobulin A</subject><subject>Immunoglobulin G</subject><subject>Immunological memory</subject><subject>Influenza</subject><subject>Influenza A Virus, H1N1 Subtype - 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pathology</topic><topic>Interferon</topic><topic>Interleukin 1</topic><topic>Interleukin 10</topic><topic>Lymphocyte Activation - immunology</topic><topic>Lymphocytes</topic><topic>Lymphocytes B</topic><topic>Lymphocytes T</topic><topic>Male</topic><topic>Morbidity</topic><topic>Pandemics</topic><topic>Pregnancy</topic><topic>Pregnancy Complications, Infectious - immunology</topic><topic>Pregnancy Complications, Infectious - prevention & control</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>T-Lymphocyte Subsets - immunology</topic><topic>Vaccination</topic><topic>Vaccines</topic><topic>γ-Interferon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Weinberg, Adriana</creatorcontrib><creatorcontrib>Muresan, Petronella</creatorcontrib><creatorcontrib>Richardson, Kelly M</creatorcontrib><creatorcontrib>Fenton, Terence</creatorcontrib><creatorcontrib>Dominguez, Teresa</creatorcontrib><creatorcontrib>Bloom, Anthony</creatorcontrib><creatorcontrib>Watts, D Heather</creatorcontrib><creatorcontrib>Abzug, Mark J</creatorcontrib><creatorcontrib>Nachman, Sharon A</creatorcontrib><creatorcontrib>Levin, Myron J</creatorcontrib><creatorcontrib>P1086 team</creatorcontrib><creatorcontrib>for the P1086 team</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Weinberg, Adriana</au><au>Muresan, Petronella</au><au>Richardson, Kelly M</au><au>Fenton, Terence</au><au>Dominguez, Teresa</au><au>Bloom, Anthony</au><au>Watts, D Heather</au><au>Abzug, Mark J</au><au>Nachman, Sharon A</au><au>Levin, Myron J</au><au>Apetrei, Cristian</au><aucorp>P1086 team</aucorp><aucorp>for the P1086 team</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Determinants of vaccine immunogenicity in HIV-infected pregnant women: analysis of B and T cell responses to pandemic H1N1 monovalent vaccine</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-04-13</date><risdate>2015</risdate><volume>10</volume><issue>4</issue><spage>e0122431</spage><epage>e0122431</epage><pages>e0122431-e0122431</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Influenza infections have high frequency and morbidity in HIV-infected pregnant women, underscoring the importance of vaccine-conferred protection. To identify the factors that determine vaccine immunogenicity in this group, we characterized the relationship of B- and T-cell responses to pandemic H1N1 (pH1N1) vaccine with HIV-associated immunologic and virologic characteristics. pH1N1 and seasonal-H1N1 (sH1N1) antibodies were measured in 119 HIV-infected pregnant women after two double-strength pH1N1 vaccine doses. pH1N1-IgG and IgA B-cell FluoroSpot, pH1N1- and sH1N1-interferon γ (IFNγ) and granzyme B (GrB) T-cell FluoroSpot, and flow cytometric characterization of B- and T-cell subsets were performed in 57 subjects. pH1N1-antibodies increased after vaccination, but less than previously described in healthy adults. pH1N1-IgG memory B cells (Bmem) increased, IFNγ-effector T-cells (Teff) decreased, and IgA Bmem and GrB Teff did not change. pH1N1-antibodies and Teff were significantly correlated with each other and with sH1N1-HAI and Teff, respectively, before and after vaccination. pH1N1-antibody responses to the vaccine significantly increased with high proportions of CD4+, low CD8+ and low CD8+HLADR+CD38+ activated (Tact) cells. pH1N1-IgG Bmem responses increased with high proportions of CD19+CD27+CD21- activated B cells (Bact), high CD8+CD39+ regulatory T cells (Treg), and low CD19+CD27-CD21- exhausted B cells (Bexhaust). IFNγ-Teff responses increased with low HIV plasma RNA, CD8+HLADR+CD38+ Tact, CD4+FoxP3+ Treg and CD19+IL10+ Breg. In conclusion, pre-existing antibody and Teff responses to sH1N1 were associated with increased responses to pH1N1 vaccination in HIV-infected pregnant women suggesting an important role for heterosubtypic immunologic memory. High CD4+% T cells were associated with increased, whereas high HIV replication, Tact and Bexhaust were associated with decreased vaccine immunogenicity. High Treg increased antibody responses but decreased Teff responses to the vaccine. The proportions of immature and transitional B cells did not affect the responses to vaccine. Increased Bact were associated with high Bmem responses to the vaccine.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25874544</pmid><doi>10.1371/journal.pone.0122431</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-04, Vol.10 (4), p.e0122431-e0122431 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1673121870 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS) Journals Open Access; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adult Adults Antibodies Antibodies, Viral - immunology CD19 antigen CD27 antigen CD38 antigen CD4 antigen CD8 antigen Effector cells Female Flow cytometry Foxp3 protein Granzyme B Histocompatibility antigen HLA HIV HIV Infections - complications HIV Infections - immunology HIV Infections - pathology Human immunodeficiency virus Humans Immunogenicity Immunoglobulin A Immunoglobulin G Immunological memory Influenza Influenza A Virus, H1N1 Subtype - immunology Influenza A Virus, H1N1 Subtype - pathogenicity Influenza Vaccines - administration & dosage Influenza Vaccines - immunology Influenza, Human - complications Influenza, Human - immunology Influenza, Human - pathology Interferon Interleukin 1 Interleukin 10 Lymphocyte Activation - immunology Lymphocytes Lymphocytes B Lymphocytes T Male Morbidity Pandemics Pregnancy Pregnancy Complications, Infectious - immunology Pregnancy Complications, Infectious - prevention & control Ribonucleic acid RNA T-Lymphocyte Subsets - immunology Vaccination Vaccines γ-Interferon |
| title | Determinants of vaccine immunogenicity in HIV-infected pregnant women: analysis of B and T cell responses to pandemic H1N1 monovalent vaccine |
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