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Title: Recombination enhances HIV-1 envelope diversity by facilitating the survival of latent genomic fragments in the plasma virus population

Abstract

HIV-1 is subject to immune pressure exerted by the host, giving variants that escape the immune response an advantage. Virus released from activated latent cells competes against variants that have continually evolved and adapted to host immune pressure. Nevertheless, there is increasing evidence that virus displaying a signal of latency survives in patient plasma despite having reduced fitness due to long-term immune memory. We investigated the survival of virus with latent envelope genomic fragments by simulating within-host HIV-1 sequence evolution and the cycling of viral lineages in and out of the latent reservoir. Our model incorporates a detailed mutation process including nucleotide substitution, recombination, latent reservoir dynamics, diversifying selection pressure driven by the immune response, and purifying selection pressure asserted by deleterious mutations. We evaluated the ability of our model to capture sequence evolution in vivo by comparing our simulated sequences to HIV-1 envelope sequence data from 16 HIV-infected untreated patients. Empirical sequence divergence and diversity measures were qualitatively and quantitatively similar to those of our simulated HIV-1 populations, suggesting that our model invokes realistic trends of HIV-1 genetic evolution. Moreover, reconstructed phylogenies of simulated and patient HIV-1 populations showed similar topological structures. Our simulation results suggest that recombination ismore » a key mechanism facilitating the persistence of virus with latent envelope genomic fragments in the productively infected cell population. Recombination increased the survival probability of latent virus forms approximately 13-fold. Prevalence of virus with latent fragments in productively infected cells was observed in only 2% of simulations when we ignored recombination, while the proportion increased to 27% of simulations when we allowed recombination. We also found that the selection pressures exerted by different fitness landscapes influenced the shape of phylogenies, diversity trends, and survival of virus with latent genomic fragments. Furthermore, our model predicts that the persistence of latent genomic fragments from multiple different ancestral origins increases sequence diversity in plasma for reasonable fitness landscapes.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [3]
+ Show Author Affiliations
  1. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  2. The Pennsylvania State Univ., University Park, PA (United States)
  3. Univ. of Zurich (Switzerland)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1235898
Report Number(s):
LA-UR-15-21253
Journal ID: ISSN 1553-7358
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Computational Biology (Online)
Additional Journal Information:
Journal Name: PLoS Computational Biology (Online); Journal Volume: 11; Journal Issue: 12; Journal ID: ISSN 1553-7358
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 97 MATHEMATICS AND COMPUTING; HIV-1; immune response; viral genomics; viral persistence and latency; viral evolution; viral replication; evolutionary immunology; phylogenetics

Citation Formats

Immonen, Taina T., Conway, Jessica M., Romero-Severson, Ethan O., Perelson, Alan S., Leitner, Thomas, and Kouyos, Roger Dimitri. Recombination enhances HIV-1 envelope diversity by facilitating the survival of latent genomic fragments in the plasma virus population. United States: N. p., 2015. Web. doi:10.1371/journal.pcbi.1004625.
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Immonen, Taina T., Conway, Jessica M., Romero-Severson, Ethan O., Perelson, Alan S., Leitner, Thomas, & Kouyos, Roger Dimitri. Recombination enhances HIV-1 envelope diversity by facilitating the survival of latent genomic fragments in the plasma virus population. United States. https://doi.org/10.1371/journal.pcbi.1004625
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Immonen, Taina T., Conway, Jessica M., Romero-Severson, Ethan O., Perelson, Alan S., Leitner, Thomas, and Kouyos, Roger Dimitri. Tue . "Recombination enhances HIV-1 envelope diversity by facilitating the survival of latent genomic fragments in the plasma virus population". United States. https://doi.org/10.1371/journal.pcbi.1004625. https://www.osti.gov/servlets/purl/1235898.
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@article{osti_1235898,
title = {Recombination enhances HIV-1 envelope diversity by facilitating the survival of latent genomic fragments in the plasma virus population},
author = {Immonen, Taina T. and Conway, Jessica M. and Romero-Severson, Ethan O. and Perelson, Alan S. and Leitner, Thomas and Kouyos, Roger Dimitri},
abstractNote = {HIV-1 is subject to immune pressure exerted by the host, giving variants that escape the immune response an advantage. Virus released from activated latent cells competes against variants that have continually evolved and adapted to host immune pressure. Nevertheless, there is increasing evidence that virus displaying a signal of latency survives in patient plasma despite having reduced fitness due to long-term immune memory. We investigated the survival of virus with latent envelope genomic fragments by simulating within-host HIV-1 sequence evolution and the cycling of viral lineages in and out of the latent reservoir. Our model incorporates a detailed mutation process including nucleotide substitution, recombination, latent reservoir dynamics, diversifying selection pressure driven by the immune response, and purifying selection pressure asserted by deleterious mutations. We evaluated the ability of our model to capture sequence evolution in vivo by comparing our simulated sequences to HIV-1 envelope sequence data from 16 HIV-infected untreated patients. Empirical sequence divergence and diversity measures were qualitatively and quantitatively similar to those of our simulated HIV-1 populations, suggesting that our model invokes realistic trends of HIV-1 genetic evolution. Moreover, reconstructed phylogenies of simulated and patient HIV-1 populations showed similar topological structures. Our simulation results suggest that recombination is a key mechanism facilitating the persistence of virus with latent envelope genomic fragments in the productively infected cell population. Recombination increased the survival probability of latent virus forms approximately 13-fold. Prevalence of virus with latent fragments in productively infected cells was observed in only 2% of simulations when we ignored recombination, while the proportion increased to 27% of simulations when we allowed recombination. We also found that the selection pressures exerted by different fitness landscapes influenced the shape of phylogenies, diversity trends, and survival of virus with latent genomic fragments. Furthermore, our model predicts that the persistence of latent genomic fragments from multiple different ancestral origins increases sequence diversity in plasma for reasonable fitness landscapes.},
doi = {10.1371/journal.pcbi.1004625},
journal = {PLoS Computational Biology (Online)},
number = 12,
volume = 11,
place = {United States},
year = {Tue Dec 22 00:00:00 EST 2015},
month = {Tue Dec 22 00:00:00 EST 2015}
}
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https://doi.org/10.1371/journal.pcbi.1004625
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  • Journal of Theoretical Biology, Vol. 203, Issue 3
  • DOI: 10.1006/jtbi.2000.1076

Quantification of infectious HIV-1 plasma viral load using a boosted in vitro infection protocol
journal, August 2004

Estimating the fraction of progeny virions that must incorporate APOBEC3G for suppression of productive HIV-1 infection
journal, January 2014

Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection
journal, May 1997

  • Chun, Tae-Wook; Carruth, Lucy; Finzi, Diana
  • Nature, Vol. 387, Issue 6629
  • DOI: 10.1038/387183a0

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

  • Finzi, Diana; Blankson, Joel; Siliciano, Janet D.
  • Nature Medicine, Vol. 5, Issue 5
  • DOI: 10.1038/8394

Antibody neutralization and escape by HIV-1
journal, March 2003

  • Wei, Xiping; Decker, Julie M.; Wang, Shuyi
  • Nature, Vol. 422, Issue 6929
  • DOI: 10.1038/nature01470

Rapid seeding of the viral reservoir prior to SIV viraemia in rhesus monkeys
journal, July 2014

  • Whitney, James B.; Hill, Alison L.; Sanisetty, Srisowmya
  • Nature, Vol. 512, Issue 7512
  • DOI: 10.1038/nature13594

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journal, February 1997

  • Goulder, Philip J. R.; Phillips, Rodney E.; Colbert, Robert A.
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journal, March 2003

  • Richman, D. D.; Wrin, T.; Little, S. J.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 7
  • DOI: 10.1073/pnas.0630530100

Determination of virus burst size in vivo using a single-cycle SIV in rhesus macaques
journal, November 2007

  • Chen, H. Y.; Di Mascio, M.; Perelson, A. S.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 48
  • DOI: 10.1073/pnas.0707449104

Immediate antiviral therapy appears to restrict resting CD4+ cell HIV-1 infection without accelerating the decay of latent infection
journal, May 2012

  • Archin, N. M.; Vaidya, N. K.; Kuruc, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 24
  • DOI: 10.1073/pnas.1120248109

Recent Origin of Human Immunodeficiency Virus Type 1 Variants in Resting CD4 + T Lymphocytes in Untreated and Suboptimally Treated Subjects
journal, December 2001

  • Karlsson, Annika C.; Lindkvist, Annica; Lindbäck, Stefan
  • The Journal of Infectious Diseases, Vol. 184, Issue 11
  • DOI: 10.1086/324405

Forward Mutation Rate of Human Immunodeficiency Virus Type 1 in a T Lymphoid Cell Line*
journal, March 1996

New insights into the evolutionary rate of HIV-1 at the within-host and epidemiological levels
journal, May 2012

  • Lythgoe, Katrina A.; Fraser, Christophe
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1741
  • DOI: 10.1098/rspb.2012.0595

Recombination increases human immunodeficiency virus fitness, but not necessarily diversity
journal, June 2008

HIV Latency
journal, September 2011

Quantitative Image Analysis of HIV-1 Infection in Lymphoid Tissue
journal, November 1996

Within-host and between-host evolutionary rates across the HIV-1 genome
journal, May 2013

Reduced evolutionary rates in HIV-1 reveal extensive latency periods among replicating lineages
journal, October 2014

Viral and Latent Reservoir Persistence in HIV-1–Infected Patients on Therapy
journal, January 2006

Treatment-Mediated Alterations in HIV Fitness Preserve CD4+ T Cell Counts but Have Minimal Effects on Viral Load
journal, November 2010

Stochastic Theory of Early Viral Infection: Continuous versus Burst Production of Virions
journal, February 2011

Stochastic Simulations Suggest that HIV-1 Survives Close to Its Error Threshold
journal, September 2012

The Genealogical Population Dynamics of HIV-1 in a Large Transmission Chain: Bridging within and among Host Evolutionary Rates
journal, April 2014

Transmission of Single and Multiple Viral Variants in Primary HIV-1 Subtype C Infection
journal, February 2011

Impact of Multi-Targeted Antiretroviral Treatment on Gut T Cell Depletion and HIV Reservoir Seeding during Acute HIV Infection
journal, March 2012

Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape
journal, May 2012

Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection
text, January 2008

  • F., Salazar-Gonzalez, Jesus; P., Busch, Michael; S., Perelson, Alan
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/f6s9-vz03

Predicting the outcomes of treatment to eradicate the latent reservoir for HIV-1
text, January 2014

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