Footprints of innate immune activity during HIV-1 reservoir cell evolution in early-treated infection
Antiretroviral treatment (ART) initiation during the early stages of HIV-1 infection is associated with a higher probability of maintaining drug-free viral control during subsequent treatment interruptions, for reasons that remain unclear. Using samples from a randomized-controlled human clinical tr...
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| Published in | The Journal of experimental medicine Vol. 221; no. 11 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
04.11.2024
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0022-1007 1540-9538 1540-9538 |
| DOI | 10.1084/jem.20241091 |
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| Abstract | Antiretroviral treatment (ART) initiation during the early stages of HIV-1 infection is associated with a higher probability of maintaining drug-free viral control during subsequent treatment interruptions, for reasons that remain unclear. Using samples from a randomized-controlled human clinical trial evaluating therapeutic HIV-1 vaccines, we here show that early ART commencement is frequently associated with accelerated and efficient selection of genome-intact HIV-1 proviruses in repressive chromatin locations during the first year after treatment initiation. This selection process was unaffected by vaccine-induced HIV-1-specific T cell responses. Single-cell proteogenomic profiling demonstrated that cells harboring intact HIV-1 displayed a discrete phenotypic signature of immune selection by innate immune responses, characterized by a slight but significant upregulation of HLA-C, HLA-G, the IL-10 receptor, and other markers involved in innate immune regulation. Together, these results suggest an accelerated immune selection of viral reservoir cells during early-treated HIV-1 infection that seems at least partially driven by innate immune responses. |
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| AbstractList | Antiretroviral treatment (ART) initiation during the early stages of HIV-1 infection is associated with a higher probability of maintaining drug-free viral control during subsequent treatment interruptions, for reasons that remain unclear. Using samples from a randomized-controlled human clinical trial evaluating therapeutic HIV-1 vaccines, we here show that early ART commencement is frequently associated with accelerated and efficient selection of genome-intact HIV-1 proviruses in repressive chromatin locations during the first year after treatment initiation. This selection process was unaffected by vaccine-induced HIV-1-specific T cell responses. Single-cell proteogenomic profiling demonstrated that cells harboring intact HIV-1 displayed a discrete phenotypic signature of immune selection by innate immune responses, characterized by a slight but significant upregulation of HLA-C, HLA-G, the IL-10 receptor, and other markers involved in innate immune regulation. Together, these results suggest an accelerated immune selection of viral reservoir cells during early-treated HIV-1 infection that seems at least partially driven by innate immune responses. Antiretroviral treatment (ART) initiation during the early stages of HIV-1 infection is associated with a higher probability of maintaining drug-free viral control during subsequent treatment interruptions, for reasons that remain unclear. Using samples from a randomized-controlled human clinical trial evaluating therapeutic HIV-1 vaccines, we here show that early ART commencement is frequently associated with accelerated and efficient selection of genome-intact HIV-1 proviruses in repressive chromatin locations during the first year after treatment initiation. This selection process was unaffected by vaccine-induced HIV-1-specific T cell responses. Single-cell proteogenomic profiling demonstrated that cells harboring intact HIV-1 displayed a discrete phenotypic signature of immune selection by innate immune responses, characterized by a slight but significant upregulation of HLA-C, HLA-G, the IL-10 receptor, and other markers involved in innate immune regulation. Together, these results suggest an accelerated immune selection of viral reservoir cells during early-treated HIV-1 infection that seems at least partially driven by innate immune responses.Antiretroviral treatment (ART) initiation during the early stages of HIV-1 infection is associated with a higher probability of maintaining drug-free viral control during subsequent treatment interruptions, for reasons that remain unclear. Using samples from a randomized-controlled human clinical trial evaluating therapeutic HIV-1 vaccines, we here show that early ART commencement is frequently associated with accelerated and efficient selection of genome-intact HIV-1 proviruses in repressive chromatin locations during the first year after treatment initiation. This selection process was unaffected by vaccine-induced HIV-1-specific T cell responses. Single-cell proteogenomic profiling demonstrated that cells harboring intact HIV-1 displayed a discrete phenotypic signature of immune selection by innate immune responses, characterized by a slight but significant upregulation of HLA-C, HLA-G, the IL-10 receptor, and other markers involved in innate immune regulation. Together, these results suggest an accelerated immune selection of viral reservoir cells during early-treated HIV-1 infection that seems at least partially driven by innate immune responses. This study demonstrates that early initiation of ART enhances immune selection pressure on HIV-1 reservoir cells and accelerates the accumulation of intact proviruses in heterochromatin regions; phenotypic profiling of reservoir cells suggests that these effects are primarily driven by innate immunity. Antiretroviral treatment (ART) initiation during the early stages of HIV-1 infection is associated with a higher probability of maintaining drug-free viral control during subsequent treatment interruptions, for reasons that remain unclear. Using samples from a randomized-controlled human clinical trial evaluating therapeutic HIV-1 vaccines, we here show that early ART commencement is frequently associated with accelerated and efficient selection of genome-intact HIV-1 proviruses in repressive chromatin locations during the first year after treatment initiation. This selection process was unaffected by vaccine-induced HIV-1-specific T cell responses. Single-cell proteogenomic profiling demonstrated that cells harboring intact HIV-1 displayed a discrete phenotypic signature of immune selection by innate immune responses, characterized by a slight but significant upregulation of HLA-C, HLA-G, the IL-10 receptor, and other markers involved in innate immune regulation. Together, these results suggest an accelerated immune selection of viral reservoir cells during early-treated HIV-1 infection that seems at least partially driven by innate immune responses. |
| Author | Shidfar, Shaadi Fisher, M. Dorrell, Lucy Lewis, Heather Sowunmi, Yinka Yu, Xu G. Lever, Andrew Gabriel, Michelle Kingsley, Cherry Robinson, Nicola Cerrone, Maddalena Roseto, Isabelle Fedele, Serge Lee, Ming Russell, Charlotte Sun, Weiwei Clarke, Aamanda Frater, John Rowlands, Jane Johnson, Margaret Byrne, Patrick Lwanga, Julianne Darbyshire, Janet Erlwein, Otto Fitzpatrick, Colin Nelson, Mark Rauchenberger, Mary Bandara, Mikaila Gregory, Andrew Gasca-Capote, Carmen Olejniczak, Natalia Bennett, Rachel Fun, Alex Conlon, Christopher Castrillo Martinez, Nadia Nwokolo, Nneka Hudson, Fleur Lichterfeld, Mathias Jones, Martin Pett, Sarah Fidler, Sarah Pace, Matthew Higgs, Christopher Weller, Ian Brown, Helen Hanke, Tomáš Parsons, Elizabeth M. Bracchi, Margherita Uzu, Hiromi Thornhill, John Wills, Mark Fox, Julie Kinloch, Sabine Ngwu, Nnenna Yang, Hongbing Anderson, Jane Box, Hanna Lawrenson, Gaynor Maini, Mala Markham, Alex Finnerty, Fiounnouala Sandström, Eric Thunder, Orla Fernandez, Tina Topping, Katie Collins, Simon McClure, Myra Kopycinski, Jakub Stöhr, W |
| AuthorAffiliation | 1 https://ror.org/053r20n13 Ragon Institute of MGH, MIT and Harvard , Cambridge, MA, USA 2 Infectious Disease Division, https://ror.org/04b6nzv94 Brigham and Women’s Hospital , Boston, MA, USA 3 Nuffield Department of Medicine, https://ror.org/052gg0110 University of Oxford , Oxford, UK 4 Department of Infectious Disease, https://ror.org/041kmwe10 Imperial College and Imperial College NIHR Biomedical Research Centre , London, UK |
| AuthorAffiliation_xml | – name: 1 https://ror.org/053r20n13 Ragon Institute of MGH, MIT and Harvard , Cambridge, MA, USA – name: 4 Department of Infectious Disease, https://ror.org/041kmwe10 Imperial College and Imperial College NIHR Biomedical Research Centre , London, UK – name: 3 Nuffield Department of Medicine, https://ror.org/052gg0110 University of Oxford , Oxford, UK – name: 2 Infectious Disease Division, https://ror.org/04b6nzv94 Brigham and Women’s Hospital , Boston, MA, USA |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39466203$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Contributor | Murray, Tammy Shidfar, Shaadi Kinloch, Sabine Ngwu, Nnenna Yang, Hongbing Anderson, Jane Box, Hanna Dorrell, Lucy Lewis, Heather Sowunmi, Yinka Lawrenson, Gaynor Maini, Mala Lever, Andrew Gabriel, Michelle Markham, Alex Finnerty, Fiounnouala Sandström, Eric Kingsley, Cherry Thunder, Orla Fernandez, Tina Robinson, Nicola Topping, Katie Collins, Simon McClure, Myra Cerrone, Maddalena Fedele, Serge Lee, Ming Russell, Charlotte Fisher, M Clarke, Aamanda Frater, John Rowlands, Jane Johnson, Margaret Kopycinski, Jakub Byrne, Patrick Lwanga, Julianne Darbyshire, Janet Stöhr, Wolfgang Erlwein, Otto Adams, Tanya Fitzpatrick, Colin Peto, Timothy O'Rourke, Patrick Jendrulek, Isabel Nelson, Mark Schoolmeesters, Alexandra Rauchenberger, Mary Lukha, Hinal Hague, Dominic Bandara, Mikaila Taylor, Mark Gregory, Andrew Merle, Simon Babiker, Abdel Thomas, Lervina Olejniczak, Natalia Kelly, Damian Weaver, Christine Lovell, Andrew Bennett, Rachel Wood, Gemma Fun, Alex Gleig, Rebecca Khan, Maryam Miller, Veronica ZarkoFlynn, Taras Conlon, Christopher Castrillo Martinez, Na |
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| Copyright | 2024 Sun et al. 2024 Sun et al. 2024 Sun et al. |
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| CorporateAuthor | the RIVER Trial Study Group RIVER Trial Study Group |
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| DOI | 10.1084/jem.20241091 |
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| Snippet | Antiretroviral treatment (ART) initiation during the early stages of HIV-1 infection is associated with a higher probability of maintaining drug-free viral... This study demonstrates that early initiation of ART enhances immune selection pressure on HIV-1 reservoir cells and accelerates the accumulation of intact... |
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| SubjectTerms | AIDS Vaccines - immunology HIV Infections - drug therapy HIV Infections - immunology HIV Infections - virology HIV-1 - immunology Humans Immunity, Innate - drug effects Male Proviruses - genetics Randomized Controlled Trials as Topic Virology |
| Title | Footprints of innate immune activity during HIV-1 reservoir cell evolution in early-treated infection |
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