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Title: Modeling Latently Infected Cell Activation: Viral and Latent Reservoir Persistence, and Viral Blips in HIV-infected Patients on Potent Therapy

Journal Article · · PLoS Computational Biology (Online)
 [1];  [2];  [2]
  1. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics; DOE/OSTI
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics
+ Show Author Affiliations

Although potent combination therapy is usually able to suppress plasma viral loads in HIV-1 patients to below the detection limit of conventional clinical assays, a low level of viremia frequently can be detected in plasma by more sensitive assays. Additionally, many patients experience transient episodes of viremia above the detection limit, termed viral blips, even after being on highly suppressive therapy for many years. An obstacle to viral eradication is the persistence of a latent reservoir for HIV-1 in resting memory CD4+ T cells. The mechanisms underlying low viral load persistence, slow decay of the latent reservoir, and intermittent viral blips are not fully characterized. The quantitative contributions of residual viral replication to viral and the latent reservoir persistence remain unclear. In this paper, we probe these issues by developing a mathematical model that considers latently infected cell activation in response to stochastic antigenic stimulation. We demonstrate that programmed expansion and contraction of latently infected cells upon immune activation can generate both low-level persistent viremia and intermittent viral blips. Also, a small fraction of activated T cells revert to latency, providing a potential to replenish the latent reservoir. By this means, occasional activation of latently infected cells can explain the variable decay characteristics of the latent reservoir observed in different clinical studies. Finally, we propose a phenomenological model that includes a logistic term representing homeostatic proliferation of latently infected cells. The model is simple but can robustly generate the multiphasic viral decline seen after initiation of therapy, as well as low-level persistent viremia and intermittent HIV-1 blips. Using these models, we provide a quantitative and integrated prospective into the long-term dynamics of HIV-1 and the latent reservoir in the setting of potent antiretroviral therapy.

Research Organization:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC52-06NA25396
OSTI ID:
1627194
Journal Information:
PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 10 Vol. 5; ISSN 1553-7358
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy journal May 1999
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Modeling the Effects of Vaccination on Chronically Infected HIV-Positive Patients journal January 2002
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Evolution of Envelope Sequences of Human Immunodeficiency Virus Type 1 in Cellular Reservoirs in the Setting of Potent Antiviral Therapy journal November 1999
Recruitment Times, Proliferation, and Apoptosis Rates during the CD8+ T-Cell Response to Lymphocytic Choriomeningitis Virus journal November 2001
Decelerating Decay of Latently Infected Cells during Prolonged Therapy for Human Immunodeficiency Virus Type 1 Infection journal September 2002
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 journal September 2002
In a Subset of Subjects on Highly Active Antiretroviral Therapy, Human Immunodeficiency Virus Type 1 RNA in Plasma Decays from 50 to <5 Copies per Milliliter, with a Half-Life of 6 Months journal February 2003
A Novel Antiviral Intervention Results in More Accurate Assessment of Human Immunodeficiency Virus Type 1 Replication Dynamics and T-Cell Decay In Vivo journal April 2003
Reservoirs for HIV-1: Mechanisms for Viral Persistence in the Presence of Antiviral Immune Responses and Antiretroviral Therapy journal April 2000
The Challenge of Viral Reservoirs in HIV-1 Infection journal February 2002
Transient Rebounds of Low-Level Viraemia among HIV-Infected Patients under Haart are Not Associated with Virological or Immunological Failure journal May 2001
Viral and Latent Reservoir Persistence in HIV-1–Infected Patients on Therapy journal January 2006
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Different Dynamics of CD4 + and CD8 + T Cell Responses During and After Acute Lymphocytic Choriomeningitis Virus Infection journal October 2003
Cellular and Anatomical Reservoirs of HIV-1 in Patients Receiving Potent Antiretroviral Combination Therapy journal July 1998
Residual HIV-1 RNA in Blood Plasma of Patients Taking Suppressive Highly Active Antiretroviral Therapy journal November 1999
Prevalence and Predictive Value of Intermittent Viremia With Combination HIV Therapy journal July 2001
HIV-1 Drug Resistance Profiles in Children and Adults With Viral Load of <50 Copies/mL Receiving Combination Therapy journal July 2001
Intermittent HIV-1 Viremia (Blips) and Drug Resistance in Patients Receiving HAART journal February 2005
HIV-1 Infection and Low Steady State Viral Loads journal January 2002
Dynamics of HIV infection of CD4+ T cells journal March 1993
Viral Dynamics in HIV-1 Infection journal May 1998
Rapid production and clearance of HIV-1 and hepatitis C virus assessed by large volume plasma apheresis journal November 1999
Treatment Implications of the Latent Reservoir for HIV‐1 book January 2007
Duration of TCR Stimulation Determines Costimulatory Requirement of T Cells journal July 1996
The Duration of Antigenic Stimulation Determines the Fate of Naive and Effector T Cells journal January 1998
Duration of an intermittent episode of viremia journal July 2005
Opportunistic infection as a cause of transient viremia in chronically infected HIV patients under treatment with HAART journal November 2005
Transient rebounds of HIV plasma viremia are associated with the emergence of drug resistance mutations in patients on highly active antiretroviral therapy journal October 2005
Modeling HIV persistence, the latent reservoir, and viral blips journal September 2009
Asymmetric division of activated latently infected cells may explain the decay kinetics of the HIV-1 latent reservoir and intermittent viral blips journal January 2009
Residual HIV-1 RNA in blood plasma of patients taking suppressive highly active antiretroviral therapy journal February 2001
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Decay characteristics of HIV-1-infected compartments during combination therapy journal May 1997
The decay of the latent reservoir of replication-competent HIV-1 is inversely correlated with the extent of residual viral replication during prolonged anti-retroviral therapy journal January 2000
Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy journal May 1999
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Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4+ T cells journal May 2003
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Determination of virus burst size in vivo using a single-cycle SIV in rhesus macaques journal November 2007
Heterogeneous clearance rates of long-lived lymphocytes infected with HIV: Intrinsic stability predicts lifelong persistence journal April 2003
Low-level viremia persists for at least 7 years in patients on suppressive antiretroviral therapy journal March 2008
HIV rebounds from latently infected cells, rather than from continuing low-level replication journal October 2008
Treatment intensification does not reduce residual HIV-1 viremia in patients on highly active antiretroviral therapy journal May 2009
Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy journal November 1997
Drug concentration heterogeneity facilitates the evolution of drug resistance journal September 1998
Latent reservoirs of HIV: Obstacles to the eradication of virus journal September 1999
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Residual Human Immunodeficiency Virus (HIV) Type 1 RNA and DNA in Lymph Nodes and HIV RNA in Genital Secretions and in Cerebrospinal Fluid after Suppression of Viremia for 2 Years journal May 2001
Genotypic Analysis of HIV‐1 Drug Resistance at the Limit of Detection: Virus Production without Evolution in Treated Adults with Undetectable HIV Loads journal April 2004
Effect of Treatment, during Primary Infection, on Establishment and Clearance of Cellular Reservoirs of HIV-1 journal May 2005
Decay of the HIV Reservoir in Patients Receiving Antiretroviral Therapy for Extended Periods: Implications for Eradication of Virus journal June 2007
Long‐Term Persistence of Transmitted HIV Drug Resistance in Male Genital Tract Secretions: Implications for Secondary Transmission journal August 2007
A long-term latent reservoir for HIV-1: discovery and clinical implications journal June 2004
Immuno-activation with anti-CD3 and recombinant human IL-2 in HIV-1-infected patients on potent antiretroviral therapy journal January 1999
The natural history and clinical significance of intermittent viraemia in patients with initial viral suppression to < 400 copies/ml journal January 2002
Consecutive rebounds in plasma viral load are associated with virological failure at 52 weeks among HIV-infected patients journal January 2002
Intermittent and sustained low-level HIV viral rebound in patients receiving potent antiretroviral therapy journal January 2002
Prevalence and clinical correlates of HIV viremia (`blips') in patients with previous suppression below the limits of quantification journal January 2002
Prevalence and Predictive Value of Intermittent Viremia with Combination HIV Therapy journal August 2001
Transient Relapses (“Blips”) of Plasma HIV RNA Levels During HAART Are Associated With Drug Resistance journal January 2001
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Intensification of Antiretroviral Therapy Accelerates the Decay of the HIV-1 Latent Reservoir and Decreases, But Does Not Eliminate, Ongoing Virus Replication journal January 2004
Density-Dependent Decay in HIV-1 Dynamics journal January 2006
Transient Viremia, Plasma Viral Load, and Reservoir Replenishment in HIV-Infected Patients on Antiretroviral Therapy journal January 2007
The role of antigenic stimulation and cytotoxic T cell activity in regulating the long–term immunopathogenesis of HIV: mechanisms and clinical implications
  • Frazer, Christophe; Ferguson, Neil M.; Wolf, Frank de
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 268, Issue 1481 https://doi.org/10.1098/rspb.2001.1777
journal October 2001
The Challenge of Finding a Cure for HIV Infection journal March 2009
Immunological Memory and Protective Immunity: Understanding Their Relation journal April 1996
Recovery of Replication-Competent HIV Despite Prolonged Suppression of Plasma Viremia journal November 1997
Identification of a Reservoir for HIV-1 in Patients on Highly Active Antiretroviral Therapy journal November 1997
Rapid Turnover of T Lymphocytes in SIV-Infected Rhesus Macaques journal February 1998
New Real-Time Reverse Transcriptase-Initiated PCR Assay with Single-Copy Sensitivity for Human Immunodeficiency Virus Type 1 RNA in Plasma journal October 2003
Residual Human Immunodeficiency Virus Type 1 Viremia in Some Patients on Antiretroviral Therapy Is Dominated by a Small Number of Invariant Clones Rarely Found in Circulating CD4+ T Cells journal June 2006
Monotypic Human Immunodeficiency Virus Type 1 Genotypes across the Uterine Cervix and in Blood Suggest Proliferation of Cells with Provirus journal April 2009
Evolution of Envelope Sequences of Human Immunodeficiency Virus Type 1 in Cellular Reservoirs in the Setting of Potent Antiviral Therapy journal November 1999
Recruitment Times, Proliferation, and Apoptosis Rates during the CD8+ T-Cell Response to Lymphocytic Choriomeningitis Virus journal November 2001
Decelerating Decay of Latently Infected Cells during Prolonged Therapy for Human Immunodeficiency Virus Type 1 Infection journal September 2002
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 journal September 2002
Viral Blip Dynamics during Highly Active Antiretroviral Therapy journal November 2003
In a Subset of Subjects on Highly Active Antiretroviral Therapy, Human Immunodeficiency Virus Type 1 RNA in Plasma Decays from 50 to <5 Copies per Milliliter, with a Half-Life of 6 Months journal February 2003
A Novel Antiviral Intervention Results in More Accurate Assessment of Human Immunodeficiency Virus Type 1 Replication Dynamics and T-Cell Decay In Vivo journal April 2003
Continued Production of Drug-Sensitive Human Immunodeficiency Virus Type 1 in Children on Combination Antiretroviral Therapy Who Have Undetectable Viral Loads journal January 2004
Evidence that Low-Level Viremias during Effective Highly Active Antiretroviral Therapy Result from Two Processes: Expression of Archival Virus and Replication of Virus journal July 2005
A Novel Assay Allows Genotyping of the Latent Reservoir for Human Immunodeficiency Virus Type 1 in the Resting CD4+ T Cells of Viremic Patients journal April 2005
Deep Gene Sequence Cluster Analyses of Multi-Virus-Infected Mucosal Tissue Reveal Enhanced Transmission of Acute HIV-1 journal January 2021
Reservoirs for HIV-1: Mechanisms for Viral Persistence in the Presence of Antiviral Immune Responses and Antiretroviral Therapy journal April 2000
The Challenge of Viral Reservoirs in HIV-1 Infection journal February 2002
HIV-infected individuals receiving effective antiviral therapy for extended periods of time continually replenish their viral reservoir journal November 2005
Transient Rebounds of Low-Level Viraemia among HIV-Infected Patients under Haart are Not Associated with Virological or Immunological Failure journal May 2001
Low-level HIV-1 replication and the dynamics of the resting CD4+T cell reservoir for HIV-1 in the setting of HAART journal January 2008
Viral and Latent Reservoir Persistence in HIV-1–Infected Patients on Therapy journal January 2006
Viral and Latent Reservoir Persistence in HIV-1 Infected Patients on Therapy journal January 2005
ART Suppresses Plasma HIV-1 RNA to a Stable Set Point Predicted by Pretherapy Viremia journal January 2007
Limits on Replenishment of the Resting CD4+ T Cell Reservoir for HIV in Patients on HAART journal August 2007
HIV-Infected Individuals Receiving Effective Antiviral Therapy for Extended Periods of Time Continually Replenish Their Viral Reservoir journal August 2006
Treatment with indinavir, zidovudine, and lamivudine in adults with human immunodeficiency virus infection and prior antiretroviral therapy text January 1997
Two Distinct Stages in the Transition from Naive CD4 T Cells to Effectors, Early Antigen-Dependent and Late Cytokine-Driven Expansion and Differentiation journal November 2000
Different Dynamics of CD4 + and CD8 + T Cell Responses During and After Acute Lymphocytic Choriomeningitis Virus Infection journal October 2003
Opportunistic infection as a cause of transient viremia in chronically infected HIV patients under treatment with HAART text January 2004
Effect of Influenza Vaccination on Viral Replication and Immune Response in Persons Infected with Human Immunodeficiency Virus Receiving Potent Antiretroviral Therapy text January 2000
Residual Human Immunodeficiency Virus (HIV) Type 1 RNA and DNA in Lymph Nodes and HIV RNA in Genital Secretions and in Cerebrospinal Fluid after Suppression of Viremia for 2 Years text January 2001
Effect of treatment, during primary infection, on establishment and clearance of cellular reservoirs of HIV-1 text January 2005
HIV rebounds from latently infected cells, rather than from continuing low-level replication text January 2008

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Modelling HIV and MTB Co-Infection Including Combined Treatment Strategies journal November 2012
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Modeling the Effects of Vorinostat In Vivo Reveals both Transient and Delayed HIV Transcriptional Activation and Minimal Killing of Latently Infected Cells journal October 2015
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Precise Quantitation of the Latent HIV-1 Reservoir: Implications for Eradication Strategies text January 2015
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