Natural Killer Cell Receptors and Ligands Are Associated With Markers of HIV-1 Persistence in Chronically Infected ART Suppressed Patients

The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer (NK) cells are innate immune cells that play a critical role in controlling viral infections and have been shown to be involved in preventing H...

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Veröffentlicht in:	Frontiers in cellular and infection microbiology Jg. 12; S. 757846
Hauptverfasser:	Ivison, Geoffrey T., Vendrame, Elena, Martínez-Colón, Giovanny J., Ranganath, Thanmayi, Vergara, Rosemary, Zhao, Nancy Q., Martin, Maureen P., Bendall, Sean C., Carrington, Mary, Cyktor, Joshua C., McMahon, Deborah K., Eron, Joseph, Jones, R. Brad, Mellors, John W., Bosch, Ronald J., Gandhi, Rajesh T., Holmes, Susan, Blish, Catherine A.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	Switzerland Frontiers Media SA 10.02.2022 Frontiers Media S.A
Schlagworte:	Acquired immune deficiency syndrome AIDS Antibodies Antiretroviral therapy CD16 antigen CD58 antigen Cellular and Infection Microbiology Chronic infection Genetic analysis Heterozygotes Histocompatibility antigen HLA HIV HIV cure HIV Infections - drug therapy HIV latency HIV-1 Human immunodeficiency virus human immunodeficiency virus (HIV) Humans Immunoglobulin-like receptors Infections Killer cell immunoglobulin-like receptors Ligands natural killer cell receptor ligands Natural killer cells NKG2 antigen Peptides Peripheral blood Phenotypes Plasma Potassium channels (inwardly-rectifying) Receptors, Natural Killer Cell - metabolism Receptors, Natural Killer Cell - therapeutic use Remission Tumor necrosis factor-TNF Virus Latency United States > US natural killer cell receptor ligands natural killer cells human immunodeficiency virus (HIV) HIV latency HIV cure
ISSN:	2235-2988, 2235-2988
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Abstract	The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer (NK) cells are innate immune cells that play a critical role in controlling viral infections and have been shown to be involved in preventing HIV-1 infection and, in those who are infected, delaying time to progression to AIDS. However, their role in limiting HIV-1 persistence on long term ART is still uncharacterized. To identify associations between markers of HIV-1 persistence and the NK cell receptor-ligand repertoire, we used twin mass cytometry panels to characterize the peripheral blood NK receptor-ligand repertoire in individuals with long-term antiretroviral suppression enrolled in the AIDS Clinical Trial Group A5321 study. At the time of testing, participants had been on ART for a median of 7 years, with virological suppression <50 copies/mL since at most 48 weeks on ART. We found that the NK cell receptor and ligand repertoires did not change across three longitudinal samples over one year—a median of 25 weeks and 50 weeks after the initial sampling. To determine the features of the receptor-ligand repertoire that associate with markers of HIV-1 persistence, we performed a LASSO normalized regression. This analysis revealed that the NK cell ligands CD58, HLA-B, and CRACC, as well as the killer cell immunoglobulin-like receptors (KIRs) KIR2DL1, KIR2DL3, and KIR2DS4 were robustly predictive of markers of HIV-1 persistence, as measured by total HIV-1 cell-associated DNA, HIV-1 cell-associated RNA, and single copy HIV-RNA assays. To characterize the roles of cell populations defined by multiple markers, we augmented the LASSO analysis with FlowSOM clustering. This analysis found that a less mature NK cell phenotype (CD16 + CD56 dim CD57 - LILRB1 - NKG2C - ) was associated with lower HIV-1 cell associated DNA. Finally, we found that surface expression of HLA-Bw6 measured by CyTOF was associated with lower HIV-1 persistence. Genetic analysis revealed that this was driven by lower HIV-1 persistence in HLA-Bw4/6 heterozygotes. These findings suggest that there may be a role for NK cells in controlling HIV-1 persistence in individuals on long-term ART, which must be corroborated by future studies.
AbstractList	The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer (NK) cells are innate immune cells that play a critical role in controlling viral infections and have been shown to be involved in preventing HIV-1 infection and, in those who are infected, delaying time to progression to AIDS. However, their role in limiting HIV-1 persistence on long term ART is still uncharacterized. To identify associations between markers of HIV-1 persistence and the NK cell receptor-ligand repertoire, we used twin mass cytometry panels to characterize the peripheral blood NK receptor-ligand repertoire in individuals with long-term antiretroviral suppression enrolled in the AIDS Clinical Trial Group A5321 study. At the time of testing, participants had been on ART for a median of 7 years, with virological suppression <50 copies/mL since at most 48 weeks on ART. We found that the NK cell receptor and ligand repertoires did not change across three longitudinal samples over one year—a median of 25 weeks and 50 weeks after the initial sampling. To determine the features of the receptor-ligand repertoire that associate with markers of HIV-1 persistence, we performed a LASSO normalized regression. This analysis revealed that the NK cell ligands CD58, HLA-B, and CRACC, as well as the killer cell immunoglobulin-like receptors (KIRs) KIR2DL1, KIR2DL3, and KIR2DS4 were robustly predictive of markers of HIV-1 persistence, as measured by total HIV-1 cell-associated DNA, HIV-1 cell-associated RNA, and single copy HIV-RNA assays. To characterize the roles of cell populations defined by multiple markers, we augmented the LASSO analysis with FlowSOM clustering. This analysis found that a less mature NK cell phenotype (CD16 + CD56 dim CD57 - LILRB1 - NKG2C - ) was associated with lower HIV-1 cell associated DNA. Finally, we found that surface expression of HLA-Bw6 measured by CyTOF was associated with lower HIV-1 persistence. Genetic analysis revealed that this was driven by lower HIV-1 persistence in HLA-Bw4/6 heterozygotes. These findings suggest that there may be a role for NK cells in controlling HIV-1 persistence in individuals on long-term ART, which must be corroborated by future studies. The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer (NK) cells are innate immune cells that play a critical role in controlling viral infections and have been shown to be involved in preventing HIV-1 infection and, in those who are infected, delaying time to progression to AIDS. However, their role in limiting HIV-1 persistence on long term ART is still uncharacterized. To identify associations between markers of HIV-1 persistence and the NK cell receptor-ligand repertoire, we used twin mass cytometry panels to characterize the peripheral blood NK receptor-ligand repertoire in individuals with long-term antiretroviral suppression enrolled in the AIDS Clinical Trial Group A5321 study. At the time of testing, participants had been on ART for a median of 7 years, with virological suppression <50 copies/mL since at most 48 weeks on ART. We found that the NK cell receptor and ligand repertoires did not change across three longitudinal samples over one year-a median of 25 weeks and 50 weeks after the initial sampling. To determine the features of the receptor-ligand repertoire that associate with markers of HIV-1 persistence, we performed a LASSO normalized regression. This analysis revealed that the NK cell ligands CD58, HLA-B, and CRACC, as well as the killer cell immunoglobulin-like receptors (KIRs) KIR2DL1, KIR2DL3, and KIR2DS4 were robustly predictive of markers of HIV-1 persistence, as measured by total HIV-1 cell-associated DNA, HIV-1 cell-associated RNA, and single copy HIV-RNA assays. To characterize the roles of cell populations defined by multiple markers, we augmented the LASSO analysis with FlowSOM clustering. This analysis found that a less mature NK cell phenotype (CD16 CD56 CD57 LILRB1 NKG2C ) was associated with lower HIV-1 cell associated DNA. Finally, we found that surface expression of HLA-Bw6 measured by CyTOF was associated with lower HIV-1 persistence. Genetic analysis revealed that this was driven by lower HIV-1 persistence in HLA-Bw4/6 heterozygotes. These findings suggest that there may be a role for NK cells in controlling HIV-1 persistence in individuals on long-term ART, which must be corroborated by future studies. The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer (NK) cells are innate immune cells that play a critical role in controlling viral infections and have been shown to be involved in preventing HIV-1 infection and, in those who are infected, delaying time to progression to AIDS. However, their role in limiting HIV-1 persistence on long term ART is still uncharacterized. To identify associations between markers of HIV-1 persistence and the NK cell receptor-ligand repertoire, we used twin mass cytometry panels to characterize the peripheral blood NK receptor-ligand repertoire in individuals with long-term antiretroviral suppression enrolled in the AIDS Clinical Trial Group A5321 study. At the time of testing, participants had been on ART for a median of 7 years, with virological suppression <50 copies/mL since at most 48 weeks on ART. We found that the NK cell receptor and ligand repertoires did not change across three longitudinal samples over one year—a median of 25 weeks and 50 weeks after the initial sampling. To determine the features of the receptor-ligand repertoire that associate with markers of HIV-1 persistence, we performed a LASSO normalized regression. This analysis revealed that the NK cell ligands CD58, HLA-B, and CRACC, as well as the killer cell immunoglobulin-like receptors (KIRs) KIR2DL1, KIR2DL3, and KIR2DS4 were robustly predictive of markers of HIV-1 persistence, as measured by total HIV-1 cell-associated DNA, HIV-1 cell-associated RNA, and single copy HIV-RNA assays. To characterize the roles of cell populations defined by multiple markers, we augmented the LASSO analysis with FlowSOM clustering. This analysis found that a less mature NK cell phenotype (CD16+CD56dimCD57-LILRB1-NKG2C-) was associated with lower HIV-1 cell associated DNA. Finally, we found that surface expression of HLA-Bw6 measured by CyTOF was associated with lower HIV-1 persistence. Genetic analysis revealed that this was driven by lower HIV-1 persistence in HLA-Bw4/6 heterozygotes. These findings suggest that there may be a role for NK cells in controlling HIV-1 persistence in individuals on long-term ART, which must be corroborated by future studies. The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer (NK) cells are innate immune cells that play a critical role in controlling viral infections and have been shown to be involved in preventing HIV-1 infection and, in those who are infected, delaying time to progression to AIDS. However, their role in limiting HIV-1 persistence on long term ART is still uncharacterized. To identify associations between markers of HIV-1 persistence and the NK cell receptor-ligand repertoire, we used twin mass cytometry panels to characterize the peripheral blood NK receptor-ligand repertoire in individuals with long-term antiretroviral suppression enrolled in the AIDS Clinical Trial Group A5321 study. At the time of testing, participants had been on ART for a median of 7 years, with virological suppression <50 copies/mL since at most 48 weeks on ART. We found that the NK cell receptor and ligand repertoires did not change across three longitudinal samples over one year-a median of 25 weeks and 50 weeks after the initial sampling. To determine the features of the receptor-ligand repertoire that associate with markers of HIV-1 persistence, we performed a LASSO normalized regression. This analysis revealed that the NK cell ligands CD58, HLA-B, and CRACC, as well as the killer cell immunoglobulin-like receptors (KIRs) KIR2DL1, KIR2DL3, and KIR2DS4 were robustly predictive of markers of HIV-1 persistence, as measured by total HIV-1 cell-associated DNA, HIV-1 cell-associated RNA, and single copy HIV-RNA assays. To characterize the roles of cell populations defined by multiple markers, we augmented the LASSO analysis with FlowSOM clustering. This analysis found that a less mature NK cell phenotype (CD16+CD56dimCD57-LILRB1-NKG2C-) was associated with lower HIV-1 cell associated DNA. Finally, we found that surface expression of HLA-Bw6 measured by CyTOF was associated with lower HIV-1 persistence. Genetic analysis revealed that this was driven by lower HIV-1 persistence in HLA-Bw4/6 heterozygotes. These findings suggest that there may be a role for NK cells in controlling HIV-1 persistence in individuals on long-term ART, which must be corroborated by future studies.The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer (NK) cells are innate immune cells that play a critical role in controlling viral infections and have been shown to be involved in preventing HIV-1 infection and, in those who are infected, delaying time to progression to AIDS. However, their role in limiting HIV-1 persistence on long term ART is still uncharacterized. To identify associations between markers of HIV-1 persistence and the NK cell receptor-ligand repertoire, we used twin mass cytometry panels to characterize the peripheral blood NK receptor-ligand repertoire in individuals with long-term antiretroviral suppression enrolled in the AIDS Clinical Trial Group A5321 study. At the time of testing, participants had been on ART for a median of 7 years, with virological suppression <50 copies/mL since at most 48 weeks on ART. We found that the NK cell receptor and ligand repertoires did not change across three longitudinal samples over one year-a median of 25 weeks and 50 weeks after the initial sampling. To determine the features of the receptor-ligand repertoire that associate with markers of HIV-1 persistence, we performed a LASSO normalized regression. This analysis revealed that the NK cell ligands CD58, HLA-B, and CRACC, as well as the killer cell immunoglobulin-like receptors (KIRs) KIR2DL1, KIR2DL3, and KIR2DS4 were robustly predictive of markers of HIV-1 persistence, as measured by total HIV-1 cell-associated DNA, HIV-1 cell-associated RNA, and single copy HIV-RNA assays. To characterize the roles of cell populations defined by multiple markers, we augmented the LASSO analysis with FlowSOM clustering. This analysis found that a less mature NK cell phenotype (CD16+CD56dimCD57-LILRB1-NKG2C-) was associated with lower HIV-1 cell associated DNA. Finally, we found that surface expression of HLA-Bw6 measured by CyTOF was associated with lower HIV-1 persistence. Genetic analysis revealed that this was driven by lower HIV-1 persistence in HLA-Bw4/6 heterozygotes. These findings suggest that there may be a role for NK cells in controlling HIV-1 persistence in individuals on long-term ART, which must be corroborated by future studies.
Author	Martin, Maureen P. Eron, Joseph Gandhi, Rajesh T. Vendrame, Elena Bosch, Ronald J. Holmes, Susan Zhao, Nancy Q. Bendall, Sean C. Jones, R. Brad Martínez-Colón, Giovanny J. Mellors, John W. Vergara, Rosemary Carrington, Mary Ranganath, Thanmayi Blish, Catherine A. Ivison, Geoffrey T. McMahon, Deborah K. Cyktor, Joshua C.
AuthorAffiliation	1 Department of Medicine, Division of Infectious Diseases and Geographic Medicine, Stanford University School of Medicine , Stanford, CA , United States 14 Department of Statistics, School of Humanities and Sciences, Stanford University , Stanford, CA , United States 8 Department of Infectious Diseases and Microbiology, University of Pittsburgh Graduate School of Public Health , Pittsburgh, PA , United States 9 Division of Infectious Diseases, University of North Carolina , Chapel Hill, NC , United States 5 Laboratory of Integrative Cancer, Immunology, Center for Cancer Research, National Cancer Institute , Bethesda, MD , United States 6 Ragon Institute of Massachusetts General Hospital (MGH), Massachusetts Institute of Technology (MIT), and Harvard , Boston, MA , United States 3 Program in Immunology, Stanford University School of Medicine , Stanford, CA , United States 4 Basic Science Program, Frederick National Laboratory for Cancer Research, National, Cancer Institute , Frederick, MD , Un
AuthorAffiliation_xml	– name: 7 Division of Infectious Diseases, University of Pittsburgh , Pittsburgh, PA , United States – name: 8 Department of Infectious Diseases and Microbiology, University of Pittsburgh Graduate School of Public Health , Pittsburgh, PA , United States – name: 13 Center for AIDS Research, Harvard University , Boston, MA , United States – name: 1 Department of Medicine, Division of Infectious Diseases and Geographic Medicine, Stanford University School of Medicine , Stanford, CA , United States – name: 11 Center for Biostatistics in AIDS Research, Harvard TH Chan School of Public Health , Boston, MA , United States – name: 6 Ragon Institute of Massachusetts General Hospital (MGH), Massachusetts Institute of Technology (MIT), and Harvard , Boston, MA , United States – name: 3 Program in Immunology, Stanford University School of Medicine , Stanford, CA , United States – name: 5 Laboratory of Integrative Cancer, Immunology, Center for Cancer Research, National Cancer Institute , Bethesda, MD , United States – name: 12 Division of Infectious Diseases, Massachusetts General Hospital, Harvard Medical School , Boston, MA , United States – name: 14 Department of Statistics, School of Humanities and Sciences, Stanford University , Stanford, CA , United States – name: 15 Chan Zuckerberg Biohub , San Francisco, CA , United States – name: 4 Basic Science Program, Frederick National Laboratory for Cancer Research, National, Cancer Institute , Frederick, MD , United States – name: 9 Division of Infectious Diseases, University of North Carolina , Chapel Hill, NC , United States – name: 10 Division of Infectious Diseases, Department of Medicine, Weill Cornell Medicine , New York, NY , United States – name: 2 Department of Pathology, Stanford University School of Medicine , Stanford, CA , United States
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Copyright	Copyright © 2022 Ivison, Vendrame, Martínez-Colón, Ranganath, Vergara, Zhao, Martin, Bendall, Carrington, Cyktor, McMahon, Eron, Jones, Mellors, Bosch, Gandhi, Holmes, Blish and The ACTG 5321 Team. 2022. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2022 Ivison, Vendrame, Martínez-Colón, Ranganath, Vergara, Zhao, Martin, Bendall, Carrington, Cyktor, McMahon, Eron, Jones, Mellors, Bosch, Gandhi, Holmes, Blish and The ACTG 5321 Team 2022 Ivison, Vendrame, Martínez-Colón, Ranganath, Vergara, Zhao, Martin, Bendall, Carrington, Cyktor, McMahon, Eron, Jones, Mellors, Bosch, Gandhi, Holmes, Blish and The ACTG 5321 Team
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Keywords	natural killer cell receptor ligands natural killer cells human immunodeficiency virus (HIV) HIV latency HIV cure
Language	English
License	Copyright © 2022 Ivison, Vendrame, Martínez-Colón, Ranganath, Vergara, Zhao, Martin, Bendall, Carrington, Cyktor, McMahon, Eron, Jones, Mellors, Bosch, Gandhi, Holmes, Blish and The ACTG 5321 Team. 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 14 content type line 23 Edited by: Sonia Navas-Martin, Drexel University, United States Reviewed by: Kun Zhang, Virginia Commonwealth University, United States; Michael A. Eller, Division of AIDS (NIAID), United States These authors have contributed equally to this work This article was submitted to Virus and Host, a section of the journal Frontiers in Cellular and Infection Microbiology
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Snippet	The latent HIV-1 reservoir represents a major barrier to achieving a long-term antiretroviral therapy (ART)-free remission or cure for HIV-1. Natural Killer...
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SubjectTerms	Acquired immune deficiency syndrome AIDS Antibodies Antiretroviral therapy CD16 antigen CD58 antigen Cellular and Infection Microbiology Chronic infection Genetic analysis Heterozygotes Histocompatibility antigen HLA HIV HIV cure HIV Infections - drug therapy HIV latency HIV-1 Human immunodeficiency virus human immunodeficiency virus (HIV) Humans Immunoglobulin-like receptors Infections Killer cell immunoglobulin-like receptors Ligands natural killer cell receptor ligands Natural killer cells NKG2 antigen Peptides Peripheral blood Phenotypes Plasma Potassium channels (inwardly-rectifying) Receptors, Natural Killer Cell - metabolism Receptors, Natural Killer Cell - therapeutic use Remission Tumor necrosis factor-TNF Virus Latency
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Title	Natural Killer Cell Receptors and Ligands Are Associated With Markers of HIV-1 Persistence in Chronically Infected ART Suppressed Patients
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