Transmission of Single HIV-1 Genomes and Dynamics of Early Immune Escape Revealed by Ultra-Deep Sequencing
We used ultra-deep sequencing to obtain tens of thousands of HIV-1 sequences from regions targeted by CD8+ T lymphocytes from longitudinal samples from three acutely infected subjects, and modeled viral evolution during the critical first weeks of infection. Previous studies suggested that a single...
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| Published in | PloS one Vol. 5; no. 8; p. e12303 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
20.08.2010
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0012303 |
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| Abstract | We used ultra-deep sequencing to obtain tens of thousands of HIV-1 sequences from regions targeted by CD8+ T lymphocytes from longitudinal samples from three acutely infected subjects, and modeled viral evolution during the critical first weeks of infection. Previous studies suggested that a single virus established productive infection, but these conclusions were tempered because of limited sampling; now, we have greatly increased our confidence in this observation through modeling the observed earliest sample diversity based on vastly more extensive sampling. Conventional sequencing of HIV-1 from acute/early infection has shown different patterns of escape at different epitopes; we investigated the earliest escapes in exquisite detail. Over 3-6 weeks, ultradeep sequencing revealed that the virus explored an extraordinary array of potential escape routes in the process of evading the earliest CD8 T-lymphocyte responses--using 454 sequencing, we identified over 50 variant forms of each targeted epitope during early immune escape, while only 2-7 variants were detected in the same samples via conventional sequencing. In contrast to the diversity seen within epitopes, non-epitope regions, including the Envelope V3 region, which was sequenced as a control in each subject, displayed very low levels of variation. In early infection, in the regions sequenced, the consensus forms did not have a fitness advantage large enough to trigger reversion to consensus amino acids in the absence of immune pressure. In one subject, a genetic bottleneck was observed, with extensive diversity at the second time point narrowing to two dominant escape forms by the third time point, all within two months of infection. Traces of immune escape were observed in the earliest samples, suggesting that immune pressure is present and effective earlier than previously reported; quantifying the loss rate of the founder virus suggests a direct role for CD8 T-lymphocyte responses in viral containment after peak viremia. Dramatic shifts in the frequencies of epitope variants during the first weeks of infection revealed a complex interplay between viral fitness and immune escape. |
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| AbstractList | We used ultra-deep sequencing to obtain tens of thousands of HIV-1 sequences from regions targeted by CD8+ T lymphocytes from longitudinal samples from three acutely infected subjects, and modeled viral evolution during the critical first weeks of infection. Previous studies suggested that a single virus established productive infection, but these conclusions were tempered because of limited sampling; now, we have greatly increased our confidence in this observation through modeling the observed earliest sample diversity based on vastly more extensive sampling. Conventional sequencing of HIV-1 from acute/early infection has shown different patterns of escape at different epitopes; we investigated the earliest escapes in exquisite detail. Over 3-6 weeks, ultradeep sequencing revealed that the virus explored an extraordinary array of potential escape routes in the process of evading the earliest CD8 T-lymphocyte responses--using 454 sequencing, we identified over 50 variant forms of each targeted epitope during early immune escape, while only 2-7 variants were detected in the same samples via conventional sequencing. In contrast to the diversity seen within epitopes, non-epitope regions, including the Envelope V3 region, which was sequenced as a control in each subject, displayed very low levels of variation. In early infection, in the regions sequenced, the consensus forms did not have a fitness advantage large enough to trigger reversion to consensus amino acids in the absence of immune pressure. In one subject, a genetic bottleneck was observed, with extensive diversity at the second time point narrowing to two dominant escape forms by the third time point, all within two months of infection. Traces of immune escape were observed in the earliest samples, suggesting that immune pressure is present and effective earlier than previously reported; quantifying the loss rate of the founder virus suggests a direct role for CD8 T-lymphocyte responses in viral containment after peak viremia. Dramatic shifts in the frequencies of epitope variants during the first weeks of infection revealed a complex interplay between viral fitness and immune escape. We used ultra-deep sequencing to obtain tens of thousands of HIV-1 sequences from regions targeted by CD8+ T lymphocytes from longitudinal samples from three acutely infected subjects, and modeled viral evolution during the critical first weeks of infection. Previous studies suggested that a single virus established productive infection, but these conclusions were tempered because of limited sampling; now, we have greatly increased our confidence in this observation through modeling the observed earliest sample diversity based on vastly more extensive sampling. Conventional sequencing of HIV-1 from acute/early infection has shown different patterns of escape at different epitopes; we investigated the earliest escapes in exquisite detail. Over 3-6 weeks, ultradeep sequencing revealed that the virus explored an extraordinary array of potential escape routes in the process of evading the earliest CD8 T-lymphocyte responses--using 454 sequencing, we identified over 50 variant forms of each targeted epitope during early immune escape, while only 2-7 variants were detected in the same samples via conventional sequencing. In contrast to the diversity seen within epitopes, non-epitope regions, including the Envelope V3 region, which was sequenced as a control in each subject, displayed very low levels of variation. In early infection, in the regions sequenced, the consensus forms did not have a fitness advantage large enough to trigger reversion to consensus amino acids in the absence of immune pressure. In one subject, a genetic bottleneck was observed, with extensive diversity at the second time point narrowing to two dominant escape forms by the third time point, all within two months of infection. Traces of immune escape were observed in the earliest samples, suggesting that immune pressure is present and effective earlier than previously reported; quantifying the loss rate of the founder virus suggests a direct role for CD8 T-lymphocyte responses in viral containment after peak viremia. Dramatic shifts in the frequencies of epitope variants during the first weeks of infection revealed a complex interplay between viral fitness and immune escape.We used ultra-deep sequencing to obtain tens of thousands of HIV-1 sequences from regions targeted by CD8+ T lymphocytes from longitudinal samples from three acutely infected subjects, and modeled viral evolution during the critical first weeks of infection. Previous studies suggested that a single virus established productive infection, but these conclusions were tempered because of limited sampling; now, we have greatly increased our confidence in this observation through modeling the observed earliest sample diversity based on vastly more extensive sampling. Conventional sequencing of HIV-1 from acute/early infection has shown different patterns of escape at different epitopes; we investigated the earliest escapes in exquisite detail. Over 3-6 weeks, ultradeep sequencing revealed that the virus explored an extraordinary array of potential escape routes in the process of evading the earliest CD8 T-lymphocyte responses--using 454 sequencing, we identified over 50 variant forms of each targeted epitope during early immune escape, while only 2-7 variants were detected in the same samples via conventional sequencing. In contrast to the diversity seen within epitopes, non-epitope regions, including the Envelope V3 region, which was sequenced as a control in each subject, displayed very low levels of variation. In early infection, in the regions sequenced, the consensus forms did not have a fitness advantage large enough to trigger reversion to consensus amino acids in the absence of immune pressure. In one subject, a genetic bottleneck was observed, with extensive diversity at the second time point narrowing to two dominant escape forms by the third time point, all within two months of infection. Traces of immune escape were observed in the earliest samples, suggesting that immune pressure is present and effective earlier than previously reported; quantifying the loss rate of the founder virus suggests a direct role for CD8 T-lymphocyte responses in viral containment after peak viremia. Dramatic shifts in the frequencies of epitope variants during the first weeks of infection revealed a complex interplay between viral fitness and immune escape. |
| Audience | Academic |
| Author | Han, Cliff S. McMichael, Andrew J. Korber, Bette T. Giorgi, Elena E. Keele, Brandon F. Wang, Shuyi Green, Lance Hraber, Peter T. Hahn, Beatrice H. Ganusov, Vitaly V. Gleasner, Cheryl D. Borrow, Persephone Lo, Chien-Chi Fischer, Will Leitner, Thomas Perelson, Alan S. Nag, Ambarish Shaw, George M. Bhattacharya, Tanmoy Wallstrom, Timothy C. Haynes, Barton F. |
| AuthorAffiliation | 6 Weatherall Institute of Molecular Medicine, Oxford University, Oxford, United Kingdom University of California San Francisco, United States of America 3 Department of Mathematics and Statistics, University of Massachusetts, Amherst, Massachusetts, United States of America 5 Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, United States of America 8 The Jenner Institute, University of Oxford, Compton, United Kingdom 9 The Santa Fe Institute, Santa Fe, New Mexico, United States of America 1 Theoretical Biology, Los Alamos National Laboratory, Los Alamos, New Mexico, United States of America 2 Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America 7 Duke University Medical Center, Durham, North Carolina, United States of America 4 SAIC-Frederick, National Cancer Institute, Frederick, Maryland, United States of America |
| AuthorAffiliation_xml | – name: 7 Duke University Medical Center, Durham, North Carolina, United States of America – name: 8 The Jenner Institute, University of Oxford, Compton, United Kingdom – name: 9 The Santa Fe Institute, Santa Fe, New Mexico, United States of America – name: University of California San Francisco, United States of America – name: 6 Weatherall Institute of Molecular Medicine, Oxford University, Oxford, United Kingdom – name: 2 Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America – name: 1 Theoretical Biology, Los Alamos National Laboratory, Los Alamos, New Mexico, United States of America – name: 5 Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, United States of America – name: 3 Department of Mathematics and Statistics, University of Massachusetts, Amherst, Massachusetts, United States of America – name: 4 SAIC-Frederick, National Cancer Institute, Frederick, Maryland, United States of America |
| Author_xml | – sequence: 1 givenname: Will surname: Fischer fullname: Fischer, Will – sequence: 2 givenname: Vitaly V. surname: Ganusov fullname: Ganusov, Vitaly V. – sequence: 3 givenname: Elena E. surname: Giorgi fullname: Giorgi, Elena E. – sequence: 4 givenname: Peter T. surname: Hraber fullname: Hraber, Peter T. – sequence: 5 givenname: Brandon F. surname: Keele fullname: Keele, Brandon F. – sequence: 6 givenname: Thomas surname: Leitner fullname: Leitner, Thomas – sequence: 7 givenname: Cliff S. surname: Han fullname: Han, Cliff S. – sequence: 8 givenname: Cheryl D. surname: Gleasner fullname: Gleasner, Cheryl D. – sequence: 9 givenname: Lance surname: Green fullname: Green, Lance – sequence: 10 givenname: Chien-Chi surname: Lo fullname: Lo, Chien-Chi – sequence: 11 givenname: Ambarish surname: Nag fullname: Nag, Ambarish – sequence: 12 givenname: Timothy C. surname: Wallstrom fullname: Wallstrom, Timothy C. – sequence: 13 givenname: Shuyi surname: Wang fullname: Wang, Shuyi – sequence: 14 givenname: Andrew J. surname: McMichael fullname: McMichael, Andrew J. – sequence: 15 givenname: Barton F. surname: Haynes fullname: Haynes, Barton F. – sequence: 16 givenname: Beatrice H. surname: Hahn fullname: Hahn, Beatrice H. – sequence: 17 givenname: Alan S. surname: Perelson fullname: Perelson, Alan S. – sequence: 18 givenname: Persephone surname: Borrow fullname: Borrow, Persephone – sequence: 19 givenname: George M. surname: Shaw fullname: Shaw, George M. – sequence: 20 givenname: Tanmoy surname: Bhattacharya fullname: Bhattacharya, Tanmoy – sequence: 21 givenname: Bette T. surname: Korber fullname: Korber, Bette T. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20808830$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1627420$$D View this record in Osti.gov |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2010 Public Library of Science 2010 Fischer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Fischer et al. 2010 |
| Copyright_xml | – notice: COPYRIGHT 2010 Public Library of Science – notice: 2010 Fischer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: Fischer et al. 2010 |
| CorporateAuthor | Los Alamos National Laboratory (LANL), Los Alamos, NM (United States) |
| CorporateAuthor_xml | – name: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States) |
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| DOI | 10.1371/journal.pone.0012303 |
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| Snippet | We used ultra-deep sequencing to obtain tens of thousands of HIV-1 sequences from regions targeted by CD8+ T lymphocytes from longitudinal samples from three... |
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| SubjectTerms | Amino acids Analysis Antigenic determinants BASIC BIOLOGICAL SCIENCES Biology CD8 antigen Computational Biology/Comparative Sequence Analysis Computational Biology/Evolutionary Modeling Computational Biology/Macromolecular Sequence Analysis Consensus Sequence Containment Disease transmission Epitopes Epitopes - genetics Epitopes - immunology Evolution Evolution, Molecular Evolutionary Biology/Microbial Evolution and Genomics Fitness Gene sequencing Genome, Viral - genetics Genomes Genomics Health aspects HIV HIV Infections - immunology HIV-1 - genetics HIV-1 - immunology HIV-1 - physiology Human immunodeficiency virus Human immunodeficiency virus 1 Humans Immune evasion Immune Evasion - genetics immune response Immunology/Immune Response Immunology/Immunity to Infections Infection Infections Lymphocytes Lymphocytes T Medical research Medicine microbial mutation Mutation natural selection phylogenetic analysis Phylogenetics polymerase chain reaction Pressure Public Health and Epidemiology/Infectious Diseases Reproductive fitness Reversion Sampling Selection, Genetic Sequence Analysis, DNA T cells Time Factors viral load viral replication Viremia Virology/Host Antiviral Responses Virology/Immune Evasion Virology/Immunodeficiency Viruses Virology/Vaccines Virology/Virus Evolution and Symbiosis Virus diseases Viruses |
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| Title | Transmission of Single HIV-1 Genomes and Dynamics of Early Immune Escape Revealed by Ultra-Deep Sequencing |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/20808830 https://www.proquest.com/docview/1318934910 https://www.proquest.com/docview/754001338 https://www.proquest.com/docview/762279293 https://www.osti.gov/servlets/purl/1627420 https://pubmed.ncbi.nlm.nih.gov/PMC2924888 https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0012303&type=printable https://doaj.org/article/afa37f91dc9343a28a83f2d70db231e1 http://dx.doi.org/10.1371/journal.pone.0012303 |
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