Redefining the Viral Reservoirs that Prevent HIV-1 Eradication

Eisele, Evelyn; Siliciano, Robert F.

doi:10.1016/j.immuni.2012.08.010

Cited by 474HIV Research and TreatmentVirus-based gene therapy researchHIV/AIDS drug development and treatment

Redefining the Viral Reservoirs that Prevent HIV-1 Eradication

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Eisele, Evelyn, Siliciano, Robert F.·2012·Immunity

DOI 10.1016/j.immuni.2012.08.010PMC PMC3963158

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Abstract

This Perspective proposes definitions for key terms in the field of HIV-1 latency and eradication. In the context of eradication, a reservoir is a cell type that allows persistence of replication-competent HIV-1 on a timescale of years in patients on optimal antiretroviral therapy. Reservoirs act as a barrier to eradication in the patient population in which cure attempts will likely be made. Halting viral replication is essential to eradication, and definitions and criteria for assessing whether this goal has been achieved are proposed. The cell types that may serve as reservoirs for HIV-1 are discussed. Currently, only latently infected resting CD4(+) T cells fit the proposed definition of a reservoir, and more evidence is necessary to demonstrate that other cell types, including hematopoietic stem cells and macrophages, fit this definition. Further research is urgently required on potential reservoirs in the gut-associated lymphoid tissue and the central nervous system.

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There is currently no effective strategy to target the latent form of HIV-1 proviruses.
“While highly active anti-retroviral therapy (HARRT) has dramatically decreased mortality from HIV-1 infection, there is currently no effective strategy to target the latent form of HIV-1 proviruses 5 .”
From Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus (2013) · cites this paper as [5]
The Introduction describes the latent reservoir as a major barrier to HIV-1 eradication. In “The latent reservoir in resting CD4+ T cells,” the paper says reactivation alone may not purge that reservoir, but it also reports that SAHA can perturb it in vivo. Thus, the paper supports the lack of an established strategy to eliminate latent infection, not the categorical claim that no strategy effectively targets it. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Highly active anti-retroviral therapy (HAART) has dramatically decreased mortality from HIV-1 infection.
“While highly active anti-retroviral therapy (HARRT) has dramatically decreased mortality from HIV-1 infection, there is currently no effective strategy to target the latent form of HIV-1 proviruses 5 .”
From Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus (2013) · cites this paper as [5]
HAART profoundly reduces HIV-1 replication and plasma viremia but does not suppress low-level viral genome expression and replication in tissues or target the latently infected cells that serve as an HIV-1 reservoir.
“HAART profoundly reduces viral replication in cells that support HIV-1 infection and reduces plasma viremia to a minimal level but neither suppresses low-level viral genome expression and replication in tissues nor targets the latently infected cells that serve as a reservoir for HIV-1”
From RNA-directed gene editing specifically eradicates latent and prevents new HIV-1 infection (2014) · cites this paper as [3]

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CpG Methylation Controls Reactivation of HIV from Latency
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Prostratin: activation of latent HIV-1 expression suggests a potential inductive adjuvant therapy for HAART
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Resting CD4+T Cells from Human Immunodeficiency Virus Type 1 (HIV-1)-Infected Individuals Carry Integrated HIV-1 Genomes within Actively Transcribed Host Genes
Han, Y., Lassen, K. G., Monie, D., Sedaghat, A. R., Shimoji, S., Liu, X., Pierson, T. C., Margolick, J. B., Siliciano, R. F., & Siliciano, J. D. (2004) · Journal of Virology · doi:10.1128/jvi.78.12.6122-6133.2004 · Cited by 328 · see citing works
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HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs
Carter, C. C., Onafuwa-Nuga, A., McNamara, L. A., et al. (2010) · Nature Medicine · doi:10.1038/nm.2109 · Cited by 318 · see citing works
Prostratin Antagonizes HIV Latency by Activating NF-κB
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The Effect of Raltegravir Intensification on Low-level Residual Viremia in HIV-Infected Patients on Antiretroviral Therapy: A Randomized Controlled Trial
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Evidence for Human Immunodeficiency Virus Type 1 Replication In Vivo in CD14 + Monocytes and Its Potential Role as a Source of Virus in Patients on Highly Active Antiretroviral Therapy
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Differences in HIV Burden and Immune Activation within the Gut of HIV‐Positive Patients Receiving Suppressive Antiretroviral Therapy
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HIV rebounds from latently infected cells, rather than from continuing low-level replication
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Lack of Mucosal Immune Reconstitution during Prolonged Treatment of Acute and Early HIV-1 Infection
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Isolation and Characterization of Replication-Competent Human Immunodeficiency Virus Type 1 from a Subset of Elite Suppressors
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Maintenance of viral suppression in HIV-1–infected HLA-B*57+ elite suppressors despite CTL escape mutations
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Suberoylanilide Hydroxamic Acid Reactivates HIV from Latently Infected Cells
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Heterogeneous clearance rates of long-lived lymphocytes infected with HIV: Intrinsic stability predicts lifelong persistence
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Coaxing HIV-1 from resting CD4 T cells
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HIV-1 Replication in the Central Nervous System Occurs in Two Distinct Cell Types
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Human Immunodeficiency Virus cDNA Metabolism: Notable Stability of Two-Long Terminal Repeat Circles
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Effect of raltegravir-containing intensification on HIV burden and T-cell activation in multiple gut sites of HIV-positive adults on suppressive antiretroviral therapy
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Molecular Characterization of Preintegration Latency in Human Immunodeficiency Virus Type 1 Infection
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CCR7 ligands CCL19 and CCL21 increase permissiveness of resting memory CD4+ T cells to HIV-1 infection: a novel model of HIV-1 latency
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Bryostatin Modulates Latent HIV-1 Infection via PKC and AMPK Signaling but Inhibits Acute Infection in a Receptor Independent Manner
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Effects of Prostratin on T-Cell Activation and Human Immunodeficiency Virus Latency
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A Sensitive, Quantitative Assay for Human Immunodeficiency Virus Type 1 Integration
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The transport of anti-HIV drugs across blood–CNS interfaces: Summary of current knowledge and recommendations for further research
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HMBA Releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and Activates HIV Transcription
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Persistent Low‐Level Viremia in HIV‐1 Elite Controllers and Relationship to Immunologic Parameters
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Thirty Years of HIV and AIDS: Future Challenges and Opportunities
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Genotypic Analysis of HIV‐1 Drug Resistance at the Limit of Detection: Virus Production without Evolution in Treated Adults with Undetectable HIV Loads
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Kinetics of Human Immunodeficiency Virus Type 1 Decay following Entry into Resting CD4 + T Cells
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A stable latent reservoir for HIV-1 in resting CD4+ T lymphocytes in infected children
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The molecular biology of HIV latency: breaking and restoring the Tat-dependent transcriptional circuit
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Intrinsic Stability of Episomal Circles Formed during Human Immunodeficiency Virus Type 1 Replication
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HIV Evolution in Early Infection: Selection Pressures, Patterns of Insertion and Deletion, and the Impact of APOBEC
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Majority of CD4 + T cells from peripheral blood of HIV-1–infected individuals contain only one HIV DNA molecule
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G→A Hypermutation in Protease and Reverse Transcriptase Regions of Human Immunodeficiency Virus Type 1 Residing in Resting CD4 + T Cells In Vivo
Kieffer, T. L., Kwon, P., Nettles, R. E., Han, Y., Ray, S. C., & Siliciano, R. F. (2005) · Journal of Virology · doi:10.1128/jvi.79.3.1975-1980.2005 · Cited by 171 · see citing works
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A quantitative basis for antiretroviral therapy for HIV-1 infection
Jilek, B. L., Zarr, M. A., Sampah, M. E., Rabi, S. A., Bullen, C. K., Lai, J., Shen, L., & Siliciano, R. F. (2012) · Nature Medicine · doi:10.1038/nm.2649 · Cited by 166 · see citing works
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Intracellular Pharmacokinetics of Antiretroviral Drugs in HIV-Infected Patients, and their Correlation with Drug Action
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CD8+ Lymphocytes Control Viral Replication in SIVmac239-Infected Rhesus Macaques without Decreasing the Lifespan of Productively Infected Cells
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Compartmentalization and Clonal Amplification of HIV-1 Variants in the Cerebrospinal Fluid during Primary Infection
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Circularization of human immunodeficiency virus type 1 DNA in vitro
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Characterization of Chemokine Receptor Utilization of Viruses in the Latent Reservoir for Human Immunodeficiency Virus Type 1
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Potential Effect of the Plasma Proteins on Drug Distribution
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Towards an Understanding of the Herpes Simplex Virus Type 1 Latency-Reactivation Cycle
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In Vivo CD8+ T-Cell Suppression of SIV Viremia Is Not Mediated by CTL Clearance of Productively Infected Cells
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Antiretroviral Therapy and Central Nervous System HIV Type 1 Infection
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Control of HIV-1 in Elite Suppressors despite Ongoing Replication and Evolution in Plasma Virus
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Persistence of Wild-Type Virus and Lack of Temporal Structure in the Latent Reservoir for Human Immunodeficiency Virus Type 1 in Pediatric Patients with Extensive Antiretroviral Exposure
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Absence of HIV-1 Evolution in the Gut-Associated Lymphoid Tissue from Patients on Combination Antiviral Therapy Initiated during Primary Infection
Evering, T. H., Mehandru, S., Rácz, P., Tenner‐Racz, K., Poles, M. A., Figueroa, A., Mohri, H., & Markowitz, M. H. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002506 · Cited by 124 · see citing works
HIV-1 DNA Is Detected in Bone Marrow Populations Containing CD4+ T Cells but Is not Found in Purified CD34+ Hematopoietic Progenitor Cells in Most Patients on Antiretroviral Therapy
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HIV-1 Utilizes the CXCR4 Chemokine Receptor to Infect Multipotent Hematopoietic Stem and Progenitor Cells
Carter, C. C., McNamara, L. A., Onafuwa-Nuga, A., Shackleton, M. J., Riddell, J., Bixby, D. L., Savona, M. R., Morrison, S. J., & Collins, K. L. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.02.005 · Cited by 115 · see citing works
Influence of Host Gene Transcription Level and Orientation on HIV-1 Latency in a Primary-Cell Model
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Simian Immunodeficiency Virus–Infected Macaques Treated with Highly Active Antiretroviral Therapy Have Reduced Central Nervous System Viral Replication and Inflammation but Persistence of Viral DNA
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In Vivo Evidence for Instability of Episomal Human Immunodeficiency Virus Type 1 cDNA
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Continued Production of Drug-Sensitive Human Immunodeficiency Virus Type 1 in Children on Combination Antiretroviral Therapy Who Have Undetectable Viral Loads
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Evolutionary Indicators of Human Immunodeficiency Virus Type 1 Reservoirs and Compartments
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Multiple Viral Genetic Analyses Detect Low-Level Human Immunodeficiency Virus Type 1 Replication during Effective Highly Active Antiretroviral Therapy
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Developing strategies for HIV-1 eradication
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Human Kupffer cells infected with HIV-1 in vivo.
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Clonal Sequences Recovered from Plasma from Patients with Residual HIV-1 Viremia and on Intensified Antiretroviral Therapy Are Identical to Replicating Viral RNAs Recovered from Circulating Resting CD4 + T Cells
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The latent HIV-1 reservoir in patients undergoing HAART: an archive of pre-HAART drug resistance
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Hematopoietic stem/precursor cells as HIV reservoirs
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A Novel Simian Immunodeficiency Virus Model that Provides Insight into Mechanisms of Human Immunodeficiency Virus Central Nervous System Disease
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Characterization of the Early Steps of Infection of Primary Blood Monocytes by Human Immunodeficiency Virus Type 1
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Human immunodeficiency virus type 1 2-LTR circles reside in a nucleoprotein complex which is different from the preintegration complex
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Low‐level plasma HIVs in patients on prolonged suppressive highly active antiretroviral therapy are produced mostly by cells other than CD4 T‐cells
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Role of Low CD4 Levels in the Influence of Human Immunodeficiency Virus Type 1 Envelope V1 and V2 Regions on Entry and Spread in Macrophages
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HIV Compartmentalization: A Review on a Clinically Important Phenomenon
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Neuropathogenesis of AIDS
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The Male Genital Tract Is Not a Pharmacological Sanctuary From Efavirenz
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Human memory T cells: generation, compartmentalization and homeostasis
Farber, D. L., Yudanin, N. A., & Restifo, N. P. (2014) · Nature Reviews Immunology · doi:10.1038/nri3567 · Cited by 897 · see citing works
Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus
Ebina, H., Misawa, N., Kanemura, Y., & Koyanagi, Y. (2013) · Scientific Reports · doi:10.1038/srep02510 · Cited by 565 · see citing works
RNA-directed gene editing specifically eradicates latent and prevents new HIV-1 infection
Hu, W., Kaminski, R., Yang, F., Zhang, Y., Cosentino, L., Li, F., Luo, B., Alvarez-Carbonell, D., Garcia-Mesa, Y., Karn, J., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1405186111 · Cited by 527 · see citing works
Extracellular ATP induces the rapid release of HIV-1 from virus containing compartments of human macrophages
Graziano, F., Desdouits, M., Garzetti, L., Podini, P., Alfano, M., Rubartelli, A., Furlan, R., Benaroch, P., & Poli, G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500656112 · Cited by 77 · see citing works

The Sexual Behaviours of HIV Positive Patients Receiving Antiretroviral Therapy in HIV Treatment Centre in Nigeria
Igbe, I. (2014) · Journal of AIDS & Clinical Research · doi:10.4172/2155-6113.1000392 · Cited by 6 · see citing works
HIV-1 latency in proliferating T cells
van der Sluis, R. M. (2013) · UvA-DARE (University of Amsterdam)
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Authors: Eisele, E., & Siliciano, R. F.
Affiliations: Johns Hopkins University (US)
Howard Hughes Medical Institute (US)
Corresponding author: Siliciano, Robert F.
ORCID: Siliciano, Robert F.
Venue: Immunity
Publisher: Elsevier BV
Published: 2012-09
Volume: 37
Issue: 3
Pages: 377-388
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2012.08.010
PMC: PMC3963158
OpenAlex: W1965266980
Cited by: 474
References: 142
Citations by year: 2026: 10 · 2025: 17 · 2024: 24 · 2023: 26 · 2022: 33 · 2021: 32 · 2020: 45 · 2019: 27 · 2018: 33 · 2017: 30 · 2016: 42 · 2015: 48 · 2014: 52 · 2013: 52 · 2012: 2
FWCI: 6.12
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 397 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
National Institute of Allergy and Infectious Diseases (AI 43222, R01AI043222, R37AI051178, U19AI096113)
Topics: Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Health Sciences › Medicine › Infectious Diseases › HIV/AIDS drug development and treatment
Keywords: HIV-1 reservoir, HIV-1 latency, HIV-1 eradication, cure, resting CD4+ T cells, hematopoietic stem cells, macrophages, gut-associated lymphoid tissue, central nervous system, antiretroviral therapy, viral persistence
MeSH terms: Antiviral Agents, Hematopoietic Stem Cells, Humans, Macrophages, CD4-Positive T-Lymphocytes, HIV-1, HIV Infections, Virus Latency, Antiretroviral Therapy, Highly Active, Host-Pathogen Interactions

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Redefining the Viral Reservoirs that Prevent HIV-1 Eradication

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