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Title: Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients

Abstract

In a study of 114 epidemiologically linked Zambian transmission pairs, we evaluated the impact of human leukocyte antigen class I (HLA-I)–associated amino acid polymorphisms, presumed to reflect cytotoxic T lymphocyte (CTL) escape in Gag and Nef of the virus transmitted from the chronically infected donor, on the plasma viral load (VL) in matched recipients 6 mo after infection. CTL escape mutations in Gag and Nef were seen in the donors, which were subsequently transmitted to recipients, largely unchanged soon after infection. We observed a significant correlation between the number of Gag escape mutations targeted by specific HLA-B allele–restricted CTLs and reduced VLs in the recipients. This negative correlation was most evident in newly infected individuals, whose HLA alleles were unable to effectively target Gag and select for CTL escape mutations in this gene. Nef mutations in the donor had no impact on VL in the recipient. Thus, broad Gag-specific CTL responses capable of driving virus escape in the donor may be of clinical benefit to both the donor and recipient. In addition to their direct implications for HIV-1 vaccine design, these data suggest that CTL-induced viral polymorphisms and their associated in vivo viral fitness costs could have a significant impactmore » on HIV-1 pathogenesis.« less

Authors:
 [1];  [2];  [2];  [3];  [3];  [4];  [2];  [2];  [1];  [1];  [5];  [4];  [6];  [2];  [7];  [2]
+ Show Author Affiliations
  1. University of Alabama, Birmingham, AL (United States)
  2. Emory University, Atlanta, GA (United States)
  3. University of Oxford (United Kingdom)
  4. Microsoft Research, Redmond, WA (United States)
  5. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  6. Zambia-Emory HIV Research Group, Lusaka (Zambia)
  7. Emory University, Atlanta, GA (United States); University of KwaZulu-Natal, Durban (South Africa); Massachusetts General Hospital, Charlestown, MA (United States)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH); International AIDS Vaccine Initiative; Wellcome Trust; Medical Research Fund UK; Microsoft Research
OSTI Identifier:
1625193
Grant/Contract Number:  
AC52-06NA25396; AI-64060; AI-46995; P30 AI050409
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Experimental Medicine
Additional Journal Information:
Journal Volume: 205; Journal Issue: 5; Journal ID: ISSN 0022-1007
Publisher:
Rockefeller University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; immunology; research and experimental medicine

Citation Formats

Goepfert, Paul A., Lumm, Wendy, Farmer, Paul, Matthews, Philippa, Prendergast, Andrew, Carlson, Jonathan M., Derdeyn, Cynthia A., Tang, Jianming, Kaslow, Richard A., Bansal, Anju, Yusim, Karina, Heckerman, David, Mulenga, Joseph, Allen, Susan, Goulder, Philip J. R., and Hunter, Eric. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. United States: N. p., 2008. Web. doi:10.1084/jem.20072457.
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Goepfert, Paul A., Lumm, Wendy, Farmer, Paul, Matthews, Philippa, Prendergast, Andrew, Carlson, Jonathan M., Derdeyn, Cynthia A., Tang, Jianming, Kaslow, Richard A., Bansal, Anju, Yusim, Karina, Heckerman, David, Mulenga, Joseph, Allen, Susan, Goulder, Philip J. R., & Hunter, Eric. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. United States. https://doi.org/10.1084/jem.20072457
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Goepfert, Paul A., Lumm, Wendy, Farmer, Paul, Matthews, Philippa, Prendergast, Andrew, Carlson, Jonathan M., Derdeyn, Cynthia A., Tang, Jianming, Kaslow, Richard A., Bansal, Anju, Yusim, Karina, Heckerman, David, Mulenga, Joseph, Allen, Susan, Goulder, Philip J. R., and Hunter, Eric. Mon . "Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients". United States. https://doi.org/10.1084/jem.20072457. https://www.osti.gov/servlets/purl/1625193.
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@article{osti_1625193,
title = {Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients},
author = {Goepfert, Paul A. and Lumm, Wendy and Farmer, Paul and Matthews, Philippa and Prendergast, Andrew and Carlson, Jonathan M. and Derdeyn, Cynthia A. and Tang, Jianming and Kaslow, Richard A. and Bansal, Anju and Yusim, Karina and Heckerman, David and Mulenga, Joseph and Allen, Susan and Goulder, Philip J. R. and Hunter, Eric},
abstractNote = {In a study of 114 epidemiologically linked Zambian transmission pairs, we evaluated the impact of human leukocyte antigen class I (HLA-I)–associated amino acid polymorphisms, presumed to reflect cytotoxic T lymphocyte (CTL) escape in Gag and Nef of the virus transmitted from the chronically infected donor, on the plasma viral load (VL) in matched recipients 6 mo after infection. CTL escape mutations in Gag and Nef were seen in the donors, which were subsequently transmitted to recipients, largely unchanged soon after infection. We observed a significant correlation between the number of Gag escape mutations targeted by specific HLA-B allele–restricted CTLs and reduced VLs in the recipients. This negative correlation was most evident in newly infected individuals, whose HLA alleles were unable to effectively target Gag and select for CTL escape mutations in this gene. Nef mutations in the donor had no impact on VL in the recipient. Thus, broad Gag-specific CTL responses capable of driving virus escape in the donor may be of clinical benefit to both the donor and recipient. In addition to their direct implications for HIV-1 vaccine design, these data suggest that CTL-induced viral polymorphisms and their associated in vivo viral fitness costs could have a significant impact on HIV-1 pathogenesis.},
doi = {10.1084/jem.20072457},
journal = {Journal of Experimental Medicine},
number = 5,
volume = 205,
place = {United States},
year = {Mon Apr 21 00:00:00 EDT 2008},
month = {Mon Apr 21 00:00:00 EDT 2008}
}
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    • Journal of Translational Medicine, Vol. 9, Issue 1
    • DOI: 10.1186/1479-5876-9-212

    Impact of immune escape mutations on HIV-1 fitness in the context of the cognate transmitted/founder genome
    journal, January 2012

    • Song, Hongshuo; Pavlicek, Jeffrey W.; Cai, Fangping
    • Retrovirology, Vol. 9, Issue 1
    • DOI: 10.1186/1742-4690-9-89

    Antenatal HIV-1 RNA load and timing of mother to child transmission; a nested case-control study in a resource poor setting
    journal, August 2010

    • Duri, Kerina; Gumbo, Felicity Z.; Kristiansen, Knut I.
    • Virology Journal, Vol. 7, Issue 1
    • DOI: 10.1186/1743-422x-7-176

    A strongly selected mutation in the HIV-1 genome is independent of T cell responses and neutralizing antibodies
    journal, October 2017

    Rapid HIV disease progression following superinfection in an HLA-B*27:05/B*57:01-positive transmission recipient
    journal, January 2018

    Quantifying the Impact of Human Immunodeficiency Virus-1 Escape From Cytotoxic T-Lymphocytes
    journal, November 2010

    The Fitness Landscape of HIV-1 Gag: Advanced Modeling Approaches and Validation of Model Predictions by In Vitro Testing
    journal, August 2014

    Timing Constraints of In Vivo Gag Mutations during Primary HIV-1 Subtype C Infection
    journal, November 2009

    HLA-Associated Immune Pressure on Gag Protein in CRF01_AE-Infected Individuals and Its Association with Plasma Viral Load
    journal, June 2010

    Timing of Immune Escape Linked to Success or Failure of Vaccination
    journal, September 2010

    Progression to AIDS in South Africa Is Associated with both Reverting and Compensatory Viral Mutations
    journal, April 2011

    Influence of HAART on Alternative Reading Frame Immune Responses over the Course of HIV-1 Infection
    journal, June 2012

    Co-Operative Additive Effects between HLA Alleles in Control of HIV-1
    journal, October 2012

    HIV-1 Replication Fitness of HLA-B*57/58:01 CTL Escape Variants Is Restored by the Accumulation of Compensatory Mutations in Gag
    journal, December 2013

    Complexity of the Inoculum Determines the Rate of Reversion of SIV Gag CD8 T Cell Mutant Virus and Outcome of Infection
    journal, April 2009

    Modelling the Evolution and Spread of HIV Immune Escape Mutants
    journal, November 2010

    The Antiviral Efficacy of HIV-Specific CD8+ T-Cells to a Conserved Epitope Is Heavily Dependent on the Infecting HIV-1 Isolate
    journal, May 2011

    Whole Genome Deep Sequencing of HIV-1 Reveals the Impact of Early Minor Variants Upon Immune Recognition During Acute Infection
    journal, March 2012

    Role of Transmitted Gag CTL Polymorphisms in Defining Replicative Capacity and Early HIV-1 Pathogenesis
    journal, November 2012

    Transmitted Virus Fitness and Host T Cell Responses Collectively Define Divergent Infection Outcomes in Two HIV-1 Recipients
    journal, January 2015

    Discordant Impact of HLA on Viral Replicative Capacity and Disease Progression in Pediatric and Adult HIV Infection
    journal, June 2015

    Broadly Neutralizing Antibody Responses in a Large Longitudinal Sub-Saharan HIV Primary Infection Cohort
    journal, January 2016

    Deep sequence analysis of HIV adaptation following vertical transmission reveals the impact of immune pressure on the evolution of HIV
    journal, December 2019

    Immune Activation and Collateral Damage in AIDS Pathogenesis
    journal, January 2013

    Immunity to HIV in Early Life
    journal, August 2014

    • Muenchhoff, Maximilian; Prendergast, Andrew J.; Goulder, Philip Jeremy Renshaw
    • Frontiers in Immunology, Vol. 5
    • DOI: 10.3389/fimmu.2014.00391

    Role of HLA Adaptation in HIV Evolution
    journal, January 2016

    • Kløverpris, Henrik N.; Leslie, Alasdair; Goulder, Philip
    • Frontiers in Immunology, Vol. 6
    • DOI: 10.3389/fimmu.2015.00665

    A Strong Case for Viral Genetic Factors in HIV Virulence
    journal, March 2011

    • Müller, Viktor; Fraser, Christophe; Herbeck, Joshua T.
    • Viruses, Vol. 3, Issue 3
    • DOI: 10.3390/v3030204

    Mechanisms of HIV Protein Degradation into Epitopes: Implications for Vaccine Design
    journal, August 2014

    • Rucevic, Marijana; Boucau, Julie; Dinter, Jens
    • Viruses, Vol. 6, Issue 8
    • DOI: 10.3390/v6083271

    A transmission-virulence evolutionary trade-off explains attenuation of HIV-1 in Uganda
    journal, November 2016

    • Blanquart, François; Grabowski, Mary Kate; Herbeck, Joshua
    • eLife, Vol. 5
    • DOI: 10.7554/elife.20492
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