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Antoine Chaillon, … , Bram Vrancken, Davey M. Smith
Published January 7, 2020
Citation Information: J Clin Invest. 2020;130(4):1699-1712. https://doi.org/10.1172/JCI134815.
Citation Information: J Clin Invest. 2020;130(4):1699-1712. https://doi.org/10.1172/JCI134815.
Abstract
BACKGROUND Understanding HIV dynamics across the human body is important for cure efforts. This goal has been hampered by technical difficulties and the challenge of obtaining fresh tissues.METHODS This observational study evaluated 6 individuals with HIV (n = 4 with viral suppression using antiretroviral [ART] therapy; n = 2 with rebound viremia after stopping ART), who provided serial blood samples before death and their bodies for rapid autopsy. HIV reservoirs were characterized by digital droplet PCR, single-genome amplification, and sequencing of full-length (FL) envelope HIV. Phylogeographic methods were used to reconstruct HIV spread, and generalized linear models were tested for viral factors associated with dispersal.RESULTS Across participants, HIV DNA levels varied from approximately 0 to 659 copies/106 cells (IQR: 22.9–126.5). A total of 605 intact FL env sequences were recovered in antemortem blood cells and across 28 tissues (IQR: 5–9). Sequence analysis showed (a) the emergence of large, identical, intact HIV RNA populations in blood after cessation of therapy, which repopulated tissues throughout the body; (b) that multiple sites acted as hubs for HIV dissemination but that blood and lymphoid tissues were the main source; (c) that viral exchanges occurred within brain areas and across the blood-brain barrier; and (d) that migration was associated with low HIV divergence between sites and greater diversity at the recipient site.CONCLUSION HIV reservoirs persisted in all deep tissues, and blood was the main source of dispersal. This may explain why eliminating HIV susceptibility in circulating T cells via bone marrow transplants allowed some individuals with HIV to experience therapy-free remission, even though deeper tissue reservoirs were not targeted.TRIAL REGISTRATION Not applicable.FUNDING NIH grants P01 AI31385, P30 AI036214, AI131971-01, AI120009AI036214, HD094646, AI027763, AI134295, and AI68636.
Authors
Antoine Chaillon, Sara Gianella, Simon Dellicour, Stephen A. Rawlings, Timothy E. Schlub, Michelli Faria De Oliveira, Caroline Ignacio, Magali Porrachia, Bram Vrancken, Davey M. Smith
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Citations to this article (137)
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Veronica Obregon-Perko, Katherine M. Bricker, Gloria Mensah, Ferzan Uddin, Laura Rotolo, Daryll Vanover, Yesha Desai, Philip J. Santangelo, Sherrie Jean, Jennifer S. Wood, Fawn C. Connor-Stroud, Stephanie Ehnert, Stella J. Berendam, Shan Liang, Thomas H. Vanderford, Katharine Bar, George M. Shaw, Guido Silvestri, Amit Kumar, Genevieve Fouda, Sallie Permar, Ann Chahroudi |
JCI Insight | 2021 |
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Gut Innate Immunity and HIV Pathogenesis
SM Dillon, CC Wilson |
Current HIV/AIDS Reports | 2021 |
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Quantitative Imaging Analysis of the Spatial Relationship between Antiretrovirals, Reverse Transcriptase Simian-Human Immunodeficiency Virus RNA, and Collagen in the Mesenteric Lymph Nodes of Nonhuman Primates
EM Scholz, JN Mwangi, GD la Cruz, M Nekorchuk, CN Chan, K Busman-Sahay, L Adamson, P Luciw, Y Fedoriw, JD Estes, EP Rosen, AD Kashuba |
Antimicrobial agents and chemotherapy | 2021 |
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Eliminating HIV reservoirs for a cure: the issue is in the tissue
K Busman-Sahay, CE Starke, MD Nekorchuk, JD Estes |
Current Opinion in HIV and AIDS | 2021 |
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Predator-Prey Dynamics of Intra-Host Simian Immunodeficiency Virus Evolution Within the Untreated Host
BR Magalis, P Autissier, KC Williams, X Chen, C Browne, M Salemi |
Frontiers in immunology | 2021 |
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In Situ Characterization of Human Lymphoid Tissue Immune Cells by Multispectral Confocal Imaging and Quantitative Image Analysis; Implications for HIV Reservoir Characterization
E Moysi, PM Estrada, F Torres-Ruiz, G Reyes-Terán, RA Koup, C Petrovas |
Frontiers in immunology | 2021 |
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Visualization of HIV-1 reservoir: an imaging perspective
C Chapon, E Moysi, T Naninck, C Mayet, C Petrovas |
Current Opinion in HIV and AIDS | 2021 |
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Antibodies for Human Immunodeficiency Virus-1 Cure Strategies
E Rossignol, G Alter, B Julg |
The Journal of Infectious Diseases | 2021 |
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Challenges and Promise of Human Immunodeficiency Virus Remission
Y Li, A Mohammadi, JZ Li |
The Journal of Infectious Diseases | 2021 |
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Residual Proviral Reservoirs: A High Risk for HIV Persistence and Driving Forces for Viral Rebound after Analytical Treatment Interruption
X Wang, H Xu |
Viruses | 2021 |
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Why the HIV Reservoir Never Runs Dry: Clonal Expansion and the Characteristics of HIV-Infected Cells Challenge Strategies to Cure and Control HIV Infection
CY Lau, MA Adan, F Maldarelli |
Viruses | 2021 |
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The Effect of JAK1/2 Inhibitors on HIV Reservoir Using Primary Lymphoid Cell Model of HIV Latency
LR de Armas, C Gavegnano, S Pallikkuth, S Rinaldi, L Pan, E Battivelli, E Verdin, RT Younis, R Pahwa, SL Williams, RF Schinazi, S Pahwa |
Frontiers in immunology | 2021 |
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A highly multiplexed droplet digital PCR assay to measure the intact HIV-1 proviral reservoir
CN Levy, SM Hughes, P Roychoudhury, DB Reeves, C Amstuz, H Zhu, ML Huang, Y Wei, ME Bull, NA Cassidy, J McClure, LM Frenkel, M Stone, S Bakkour, ER Wonderlich, MP Busch, SG Deeks, JT Schiffer, RW Coombs, DA Lehman, KR Jerome, F Hladik |
Reproduction | 2021 |
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Addressing an HIV cure in LMIC
SD Ismail, J Pankrac, E Ndashimye, JL Prodger, MR Abrahams, JF Mann, AD Redd, EJ Arts |
Retrovirology | 2021 |
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Predicting Post-treatment HIV Remission: Does Size of the Viral Reservoir Matter?
AO Pasternak, CK Psomas, B Berkhout |
Frontiers in microbiology | 2021 |
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Emerging Single-cell Approaches to Understand HIV in the Central Nervous System
MJ Corley, SF Farhadian |
Current HIV/AIDS Reports | 2021 |
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Persistence of viral RNA in lymph nodes in ART-suppressed SIV/SHIV-infected Rhesus Macaques
AM Cadena, JD Ventura, P Abbink, EN Borducchi, H Tuyishime, NB Mercado, V Walker-Sperling, M Siamatu, PT Liu, A Chandrashekar, JP Nkolola, K McMahan, N Kordana, V Hamza, EA Bondzie, E Fray, M Kumar, S Fischinger, SA Shin, MG Lewis, RF Siliciano, G Alter, DH Barouch |
Nature Communications | 2021 |
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HIV-1 viral blips are associated with repeated and increasingly high levels of cell-associated HIV-1 RNA transcriptional activity
K Suzuki, A Levert, J Yeung, M Starr, J Cameron, R Williams, N Rismanto, T Stark, D Druery, S Prasad, C Ferrarini, I Hanafi, LP McNally, P Cunningham, Z Liu, T Ishida, CS Huang, V Oswald, L Evans, G Symonds, BJ Brew, J Zaunders |
AIDS | 2021 |
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Astrocytes are HIV reservoirs in the brain: A cell type with poor HIV infectivity and replication but efficient cell‐to‐cell viral transfer
S Valdebenito, P Castellano, D Ajasin, EA Eugenin |
Journal of Neurochemistry | 2021 |
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A Small Molecule, ACAi-028, with Anti-HIV-1 Activity Targets a Novel Hydrophobic Pocket on HIV-1 Capsid
T Chia, T Nakamura, M Amano, N Takamune, M Matsuoka, H Nakata |
Antimicrobial agents and chemotherapy | 2021 |
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Diminished Peripheral CD29hi Cytotoxic CD4+ T Cells Are Associated With Deleterious Effects During SIV Infection
OA Olwenyi, SD Johnson, K Pandey, M Thurman, A Acharya, SJ Buch, HS Fox, AT Podany, CV Fletcher, SN Byrareddy |
Frontiers in immunology | 2021 |
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Recovery of Latent HIV-1 from Brain Tissue by Adoptive Cell Transfer in Virally Suppressed Humanized Mice
H Su, S Sravanam, B Sillman, E Waight, E Makarov, S Mathews, LY Poluektova, S Gorantla, HE Gendelman, PK Dash |
Journal of Neuroimmune Pharmacology | 2021 |
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Tissue‐specific differences in HIV DNA levels and mechanisms that govern HIV transcription in blood, gut, genital tract and liver in ART‐treated women
S MoronLopez, G Xie, P Kim, DA Siegel, S Lee, JK Wong, JC Price, N Elnachef, RM Greenblatt, PC Tien, NR Roan, SA Yukl |
Journal of the International AIDS Society | 2021 |
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Ethics of HIV cure research: an unfinished agenda
K Dubé, J Kanazawa, J Taylor, L Dee, N Jones, C Roebuck, L Sylla, M Louella, J Kosmyna, D Kelly, O Clanton, D Palm, DM Campbell, MG Onaiwu, H Patel, S Ndukwe, L Henley, MO Johnson, P Saberi, B Brown, JA Sauceda, J Sugarman |
BMC Medical Ethics | 2021 |
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Pharmacology of HIV Cure: Site of Action
AS Devanathan, ML Cottrell |
Clinical Pharmacology & Therapeutics | 2021 |
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Prevalence and risk of residual viremia after ART in low- and middle-income countries: A cross-sectional study
S Gatechompol, L Zheng, Y Bao, A Avihingsanon, SJ Kerr, N Kumarasamy, JG Hakim, F Maldarelli, RJ Gorelick, JL Welker, JD Lifson, MC Hosseinipour, JJ Eron, K Ruxrungtham |
Medicine | 2021 |
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Attitudes and perceptions of next-of-kin/loved ones toward end-of-life HIV cure-related research: A qualitative focus group study in Southern California
SS Javadi, K Mathur, S Concha-Garcia, H Patel, KE Perry, M Lo, J Taylor, A Kaytes, S Little, S Gianella, D Smith, K Dubé, A Todd |
PloS one | 2021 |
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Editing out HIV: application of gene editing technology to achieve functional cure
J Xun, X Zhang, S Guo, H Lu, J Chen |
Retrovirology | 2021 |
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The Gift of a Lifetime: Analysis of HIV at Autopsy
Frank Maldarelli |
Journal of Clinical Investigation | 2020 |
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The multifaceted nature of HIV latency
Caroline Dufour, Pierre Gantner, Rémi Fromentin, Nicolas Chomont |
Journal of Clinical Investigation | 2020 |
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Therapeutic Vaccines for the Treatment of HIV
Z Chen, B Julg |
Translational research : the journal of laboratory and clinical medicine | 2020 |
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Reduce and Control: A Combinatorial Strategy for Achieving Sustained HIV Remissions in the Absence of Antiretroviral Therapy
R Schwarzer, A Gramatica, WC Greene |
Viruses | 2020 |
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The Biology of the HIV-1 Latent Reservoir and Implications for Cure Strategies
LB Cohn, N Chomont, SG Deeks |
Cell Host & Microbe | 2020 |
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HIV RNA Rebound in Seminal Plasma after Antiretroviral Treatment Interruption
S Gianella, A Chaillon, TW Chun, MC Sneller, C Ignacio, MV Vargas-Meneses, G Caballero, RJ Ellis, C Kovacs, E Benko, S Huibner, R Kaul, G Silvestri |
Journal of virology | 2020 |
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Recommendations for measuring HIV reservoir size in cure-directed clinical trials
M Abdel-Mohsen, D Richman, RF Siliciano, MC Nussenzweig, BJ Howell, J Martinez-Picado, N Chomont, KJ Bar, XG Yu, M Lichterfeld, J Alcami, D Hazuda, F Bushman, JD Siliciano, MR Betts, AM Spivak, V Planelles, BH Hahn, DM Smith, YC Ho, MJ Buzon, C Gaebler, M Paiardini, Q Li, JD Estes, TJ Hope, J Kostman, K Mounzer, M Caskey, L Fox, I Frank, JL Riley, P Tebas, LJ Montaner |
Nature Medicine | 2020 |
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Phenotypic analysis of the unstimulated in vivo HIV CD4 T cell reservoir
J Neidleman, X Luo, J Frouard, G Xie, F Hsiao, T Ma, V Morcilla, A Lee, S Telwatte, R Thomas, W Tamaki, B Wheeler, R Hoh, M Somsouk, P Vohra, J Milush, KS James, NM Archin, PW Hunt, SG Deeks, SA Yukl, S Palmer, WC Greene, NR Roan |
eLife | 2020 |
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Simian-Human Immunodeficiency Virus SHIV.C.CH505 Persistence in ART-Suppressed Infant Macaques Is Characterized by Elevated SHIV RNA in the Gut and a High Abundance of Intact SHIV DNA in Naive CD4 + T Cells
V Obregon-Perko, KM Bricker, G Mensah, F Uddin, MR Kumar, EJ Fray, RF Siliciano, N Schoof, A Horner, M Mavigner, S Liang, T Vanderford, J Sass, C Chan, SJ Berendam, KJ Bar, GM Shaw, G Silvestri, GG Fouda, SR Permar, A Chahroudi, V Simon |
Journal of virology | 2020 |
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“My Death Will Not [Be] in Vain”: Testimonials from Last Gift Rapid Research Autopsy Study Participants Living with HIV at the End of Life
KE Perry, K Dube, S Concha-Garcia, H Patel, A Kaytes, J Taylor, SS Javadi, K Mathur, M Lo, B Brown, J Sauceda, DA Wohl, SJ Little, S Hendrickx, S Rawlings, DM Smith, S Gianella |
AIDS Research and Human Retroviruses | 2020 |
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Performing rapid autopsy for the interrogation of HIV reservoirs:
SA Rawlings, L Layman, D Smith, B Scott, C Ignacio, M Porrachia, S Concha-Garcia, S Hendrickx, A Kaytes, J Taylor, S Gianella |
AIDS | 2020 |
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Tissue is the issue: how altruistic people with HIV are changing the HIV tissue reservoir landscape
SA Rawlings, S Gianella |
Future Virology | 2020 |
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Role of Tunneling Nanotube–like Structures during the Early Events of HIV Infection: Novel Features of Tissue Compartmentalization and Mechanism of HIV Spread
G Okafo, S Valdebenito, M Donoso, R Luu, D Ajasin, B Prideaux, S Gorantla, EA Eugenin |
Journal of immunology (Baltimore, Md. : 1950) | 2020 |
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Dynamics and Dispersal of Local Human Immunodeficiency Virus Epidemics Within San Diego and Across the San Diego–Tijuana Border
B Vrancken, SR Mehta, S Ávila-Ríos, C García-Morales, D Tapia-Trejo, G Reyes-Terán, S Navarro-Álvarez, SJ Little, M Hoenigl, HA Pines, T Patterson, SA Strathdee, DM Smith, S Dellicour, A Chaillon |
Clinical Infectious Diseases | 2020 |
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Comparative Circulation Dynamics of the Five Main HIV Types in China
B Vrancken, B Zhao, X Li, X Han, H Liu, J Zhao, P Zhong, Y Lin, J Zai, M Liu, DM Smith, S Dellicour, A Chaillon, G Silvestri |
Journal of virology | 2020 |
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Perceptions of Next-of-Kin/Loved Ones About Last Gift Rapid Research Autopsy Study Enrolling People with HIV/AIDS at the End of Life: A Qualitative Interview Study
K Dubé, H Patel, S Concha-Garcia, KE Perry, K Mathur, SS Javadi, J Taylor, A Kaytes, B Brown, JA Sauceda, S Little, S Hendrickx, SA Rawlings, DM Smith, S Gianella |
AIDS Research and Human Retroviruses | 2020 |
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Willingness to risk death endpoint in HIV cure-related research with otherwise healthy volunteers is misleading
Dubé K, Dee L |
Journal of Virus Eradication | 2020 |
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Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd |
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology | 2009 |
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