Whole Genome Deep Sequencing of HIV-1 Reveals the Impact of Early Minor Variants Upon Immune Recognition During Acute Infection
Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform...
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| Published in | PLoS pathogens Vol. 8; no. 3; p. e1002529 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.03.2012
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7374 1553-7366 1553-7374 |
| DOI | 10.1371/journal.ppat.1002529 |
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| Abstract | Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform that combines 454 pyrosequencing with novel assembly and variant detection algorithms. In one subject we combined these genetic data with detailed immunological analyses to comprehensively evaluate viral evolution and immune escape during the acute phase of HIV-1 infection. The majority of early, low frequency mutations represented viral adaptation to host CD8+ T cell responses, evidence of strong immune selection pressure occurring during the early decline from peak viremia. CD8+ T cell responses capable of recognizing these low frequency escape variants coincided with the selection and evolution of more effective secondary HLA-anchor escape mutations. Frequent, and in some cases rapid, reversion of transmitted mutations was also observed across the viral genome. When located within restricted CD8 epitopes these low frequency reverting mutations were sufficient to prime de novo responses to these epitopes, again illustrating the capacity of the immune response to recognize and respond to low frequency variants. More importantly, rapid viral escape from the most immunodominant CD8+ T cell responses coincided with plateauing of the initial viral load decline in this subject, suggestive of a potential link between maintenance of effective, dominant CD8 responses and the degree of early viremia reduction. We conclude that the early control of HIV-1 replication by immunodominant CD8+ T cell responses may be substantially influenced by rapid, low frequency viral adaptations not detected by conventional sequencing approaches, which warrants further investigation. These data support the critical need for vaccine-induced CD8+ T cell responses to target more highly constrained regions of the virus in order to ensure the maintenance of immunodominant CD8 responses and the sustained decline of early viremia. |
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| AbstractList | Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform that combines 454 pyrosequencing with novel assembly and variant detection algorithms. In one subject we combined these genetic data with detailed immunological analyses to comprehensively evaluate viral evolution and immune escape during the acute phase of HIV-1 infection. The majority of early, low frequency mutations represented viral adaptation to host CD8+ T cell responses, evidence of strong immune selection pressure occurring during the early decline from peak viremia. CD8+ T cell responses capable of recognizing these low frequency escape variants coincided with the selection and evolution of more effective secondary HLA-anchor escape mutations. Frequent, and in some cases rapid, reversion of transmitted mutations was also observed across the viral genome. When located within restricted CD8 epitopes these low frequency reverting mutations were sufficient to prime de novo responses to these epitopes, again illustrating the capacity of the immune response to recognize and respond to low frequency variants. More importantly, rapid viral escape from the most immunodominant CD8+ T cell responses coincided with plateauing of the initial viral load decline in this subject, suggestive of a potential link between maintenance of effective, dominant CD8 responses and the degree of early viremia reduction. We conclude that the early control of HIV-1 replication by immunodominant CD8+ T cell responses may be substantially influenced by rapid, low frequency viral adaptations not detected by conventional sequencing approaches, which warrants further investigation. These data support the critical need for vaccine-induced CD8+ T cell responses to target more highly constrained regions of the virus in order to ensure the maintenance of immunodominant CD8 responses and the sustained decline of early viremia. Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform that combines 454 pyrosequencing with novel assembly and variant detection algorithms. In one subject we combined these genetic data with detailed immunological analyses to comprehensively evaluate viral evolution and immune escape during the acute phase of HIV-1 infection. The majority of early, low frequency mutations represented viral adaptation to host CD8+ T cell responses, evidence of strong immune selection pressure occurring during the early decline from peak viremia. CD8+ T cell responses capable of recognizing these low frequency escape variants coincided with the selection and evolution of more effective secondary HLA-anchor escape mutations. Frequent, and in some cases rapid, reversion of transmitted mutations was also observed across the viral genome. When located within restricted CD8 epitopes these low frequency reverting mutations were sufficient to prime de novo responses to these epitopes, again illustrating the capacity of the immune response to recognize and respond to low frequency variants. More importantly, rapid viral escape from the most immunodominant CD8+ T cell responses coincided with plateauing of the initial viral load decline in this subject, suggestive of a potential link between maintenance of effective, dominant CD8 responses and the degree of early viremia reduction. We conclude that the early control of HIV-1 replication by immunodominant CD8+ T cell responses may be substantially influenced by rapid, low frequency viral adaptations not detected by conventional sequencing approaches, which warrants further investigation. These data support the critical need for vaccine-induced CD8+ T cell responses to target more highly constrained regions of the virus in order to ensure the maintenance of immunodominant CD8 responses and the sustained decline of early viremia. The ability of HIV-1 and other highly variable pathogens to rapidly mutate to escape vaccine-induced immune responses represents a major hurdle to the development of effective vaccines to these highly persistent pathogens. Application of next-generation or deep sequencing technologies to the study of host pathogens could significantly improve our understanding of the mechanisms by which these pathogens subvert host immunity, and aid in the development of novel vaccines and therapeutics. Here, we developed a 454 deep sequencing approach to enable the sensitive detection of low-frequency viral variants across the entire HIV-1 genome. When applied to the acute phase of HIV-1 infection we observed that the majority of early, low frequency mutations represented viral adaptations to host cellular immune responses, evidence of strong host immunity developing during the early decline of peak viral load. Rapid viral escape from the most dominant immune responses however correlated with loss of this initial viral control, suggestive of the importance of mounting immune responses against more conserved regions of the virus. These data provide a greater understanding of the early evolutionary events subverting the ability of host immune responses to control early HIV-1 replication, yielding important insight into the design of more effective vaccine strategies. Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform that combines 454 pyrosequencing with novel assembly and variant detection algorithms. In one subject we combined these genetic data with detailed immunological analyses to comprehensively evaluate viral evolution and immune escape during the acute phase of HIV-1 infection. The majority of early, low frequency mutations represented viral adaptation to host CD8+ T cell responses, evidence of strong immune selection pressure occurring during the early decline from peak viremia. CD8+ T cell responses capable of recognizing these low frequency escape variants coincided with the selection and evolution of more effective secondary HLA-anchor escape mutations. Frequent, and in some cases rapid, reversion of transmitted mutations was also observed across the viral genome. When located within restricted CD8 epitopes these low frequency reverting mutations were sufficient to prime de novo responses to these epitopes, again illustrating the capacity of the immune response to recognize and respond to low frequency variants. More importantly, rapid viral escape from the most immunodominant CD8+ T cell responses coincided with plateauing of the initial viral load decline in this subject, suggestive of a potential link between maintenance of effective, dominant CD8 responses and the degree of early viremia reduction. We conclude that the early control of HIV-1 replication by immunodominant CD8+ T cell responses may be substantially influenced by rapid, low frequency viral adaptations not detected by conventional sequencing approaches, which warrants further investigation. These data support the critical need for vaccine-induced CD8+ T cell responses to target more highly constrained regions of the virus in order to ensure the maintenance of immunodominant CD8 responses and the sustained decline of early viremia. Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform that combines 454 pyrosequencing with novel assembly and variant detection algorithms. In one subject we combined these genetic data with detailed immunological analyses to comprehensively evaluate viral evolution and immune escape during the acute phase of HIV-1 infection. The majority of early, low frequency mutations represented viral adaptation to host CD8+ T cell responses, evidence of strong immune selection pressure occurring during the early decline from peak viremia. CD8+ T cell responses capable of recognizing these low frequency escape variants coincided with the selection and evolution of more effective secondary HLA-anchor escape mutations. Frequent, and in some cases rapid, reversion of transmitted mutations was also observed across the viral genome. When located within restricted CD8 epitopes these low frequency reverting mutations were sufficient to prime de novo responses to these epitopes, again illustrating the capacity of the immune response to recognize and respond to low frequency variants. More importantly, rapid viral escape from the most immunodominant CD8+ T cell responses coincided with plateauing of the initial viral load decline in this subject, suggestive of a potential link between maintenance of effective, dominant CD8 responses and the degree of early viremia reduction. We conclude that the early control of HIV-1 replication by immunodominant CD8+ T cell responses may be substantially influenced by rapid, low frequency viral adaptations not detected by conventional sequencing approaches, which warrants further investigation. These data support the critical need for vaccine-induced CD8+ T cell responses to target more highly constrained regions of the virus in order to ensure the maintenance of immunodominant CD8 responses and the sustained decline of early viremia.Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform that combines 454 pyrosequencing with novel assembly and variant detection algorithms. In one subject we combined these genetic data with detailed immunological analyses to comprehensively evaluate viral evolution and immune escape during the acute phase of HIV-1 infection. The majority of early, low frequency mutations represented viral adaptation to host CD8+ T cell responses, evidence of strong immune selection pressure occurring during the early decline from peak viremia. CD8+ T cell responses capable of recognizing these low frequency escape variants coincided with the selection and evolution of more effective secondary HLA-anchor escape mutations. Frequent, and in some cases rapid, reversion of transmitted mutations was also observed across the viral genome. When located within restricted CD8 epitopes these low frequency reverting mutations were sufficient to prime de novo responses to these epitopes, again illustrating the capacity of the immune response to recognize and respond to low frequency variants. More importantly, rapid viral escape from the most immunodominant CD8+ T cell responses coincided with plateauing of the initial viral load decline in this subject, suggestive of a potential link between maintenance of effective, dominant CD8 responses and the degree of early viremia reduction. We conclude that the early control of HIV-1 replication by immunodominant CD8+ T cell responses may be substantially influenced by rapid, low frequency viral adaptations not detected by conventional sequencing approaches, which warrants further investigation. These data support the critical need for vaccine-induced CD8+ T cell responses to target more highly constrained regions of the virus in order to ensure the maintenance of immunodominant CD8 responses and the sustained decline of early viremia. Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to sensitively characterize rapidly evolving viral quasispecies. Here, we report on a high-throughput whole HIV-1 genome deep sequencing platform that combines 454 pyrosequencing with novel assembly and variant detection algorithms. In one subject we combined these genetic data with detailed immunological analyses to comprehensively evaluate viral evolution and immune escape during the acute phase of HIV-1 infection. The majority of early, low frequency mutations represented viral adaptation to host CD8+ T cell responses, evidence of strong immune selection pressure occurring during the early decline from peak viremia. CD8+ T cell responses capable of recognizing these low frequency escape variants coincided with the selection and evolution of more effective secondary HLA-anchor escape mutations. Frequent, and in some cases rapid, reversion of transmitted mutations was also observed across the viral genome. When located within restricted CD8 epitopes these low frequency reverting mutations were sufficient to prime de novo responses to these epitopes, again illustrating the capacity of the immune response to recognize and respond to low frequency variants. More importantly, rapid viral escape from the most immunodominant CD8+ T cell responses coincided with plateauing of the initial viral load decline in this subject, suggestive of a potential link between maintenance of effective, dominant CD8 responses and the degree of early viremia reduction. We conclude that the early control of HIV-1 replication by immunodominant CD8+ T cell responses may be substantially influenced by rapid, low frequency viral adaptations not detected by conventional sequencing approaches, which warrants further investigation. These data support the critical need for vaccine-induced CD8+ T cell responses to target more highly constrained regions of the virus in order to ensure the maintenance of immunodominant CD8 responses and the sustained decline of early viremia. The ability of HIV-1 and other highly variable pathogens to rapidly mutate to escape vaccine-induced immune responses represents a major hurdle to the development of effective vaccines to these highly persistent pathogens. Application of next-generation or deep sequencing technologies to the study of host pathogens could significantly improve our understanding of the mechanisms by which these pathogens subvert host immunity, and aid in the development of novel vaccines and therapeutics. Here, we developed a 454 deep sequencing approach to enable the sensitive detection of low-frequency viral variants across the entire HIV-1 genome. When applied to the acute phase of HIV-1 infection we observed that the majority of early, low frequency mutations represented viral adaptations to host cellular immune responses, evidence of strong host immunity developing during the early decline of peak viral load. Rapid viral escape from the most dominant immune responses however correlated with loss of this initial viral control, suggestive of the importance of mounting immune responses against more conserved regions of the virus. These data provide a greater understanding of the early evolutionary events subverting the ability of host immune responses to control early HIV-1 replication, yielding important insight into the design of more effective vaccine strategies. |
| Audience | Academic |
| Author | Zeng, Qiandong Ryan, Elizabeth M. Tully, Damien Zody, Michael C. Mayer, Ken H. Axten, Karen L. Shea, Terrance P. Tinsley, Jake P. Gladden, Adrianne D. Rychert, Jenna Henn, Matthew R. Dudek, Tim Brander, Christian Levin, Joshua Z. Birren, Bruce W. Walker, Bruce D. Battis, Laura Brumme, Chanson J. Streeck, Hendrik Boutwell, Christian L. Rosenberg, Eric Allen, Todd M. Pereyra, Florencia Erlich, Rachel L. Gnerre, Sante Wang, Yaoyu Günthard, Huldrych F. Berlin, Aaron M. Young, Sarah K. Hess, Christoph Zedlack, Carmen Gujja, Sharvari Brumme, Zabrina L. Gasser, Olivier Bloom, Allyson K. Lennon, Niall J. Bazner, Suzane Green, Lisa M. Macalalad, Alexander R. Malboeuf, Christine M. Charlebois, Patrick Berical, Andrew Casali, Monica Kemper, Michael Power, Karen A. Jessen, Heiko Altfeld, Marcus Newman, Ruchi |
| AuthorAffiliation | 1 Broad Institute of MIT and Harvard, Cambridge, Massachusetts, United States of America 8 Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, United States of America 9 The Fenway Institute, Fenway Health, Boston, Massachusetts, United States of America 2 Ragon Institute of MGH, MIT and Harvard, Boston, Massachusetts, United States of America 10 Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America 6 Irsicaixa AIDS Research Institute-HIVACAT, Hospital University Germans Trias I Pujol, Badalona, Spain 7 Division of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Switzerland 4 Immunobiology Lab, Department of Biomedicine, University Hospital Basel, Basel, Switzerland 3 HIV Clinic Praxis. Jessen, Berlin, Germany 5 Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain Nationwide Children's Hospital, United States of America |
| AuthorAffiliation_xml | – name: 4 Immunobiology Lab, Department of Biomedicine, University Hospital Basel, Basel, Switzerland – name: 7 Division of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Switzerland – name: 2 Ragon Institute of MGH, MIT and Harvard, Boston, Massachusetts, United States of America – name: 5 Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain – name: 9 The Fenway Institute, Fenway Health, Boston, Massachusetts, United States of America – name: 10 Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America – name: 6 Irsicaixa AIDS Research Institute-HIVACAT, Hospital University Germans Trias I Pujol, Badalona, Spain – name: 1 Broad Institute of MIT and Harvard, Cambridge, Massachusetts, United States of America – name: Nationwide Children's Hospital, United States of America – name: 3 HIV Clinic Praxis. Jessen, Berlin, Germany – name: 8 Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, United States of America |
| Author_xml | – sequence: 1 givenname: Matthew R. surname: Henn fullname: Henn, Matthew R. – sequence: 2 givenname: Christian L. surname: Boutwell fullname: Boutwell, Christian L. – sequence: 3 givenname: Patrick surname: Charlebois fullname: Charlebois, Patrick – sequence: 4 givenname: Niall J. surname: Lennon fullname: Lennon, Niall J. – sequence: 5 givenname: Karen A. surname: Power fullname: Power, Karen A. – sequence: 6 givenname: Alexander R. surname: Macalalad fullname: Macalalad, Alexander R. – sequence: 7 givenname: Aaron M. surname: Berlin fullname: Berlin, Aaron M. – sequence: 8 givenname: Christine M. surname: Malboeuf fullname: Malboeuf, Christine M. – sequence: 9 givenname: Elizabeth M. surname: Ryan fullname: Ryan, Elizabeth M. – sequence: 10 givenname: Sante surname: Gnerre fullname: Gnerre, Sante – sequence: 11 givenname: Michael C. surname: Zody fullname: Zody, Michael C. – sequence: 12 givenname: Rachel L. surname: Erlich fullname: Erlich, Rachel L. – sequence: 13 givenname: Lisa M. surname: Green fullname: Green, Lisa M. – sequence: 14 givenname: Andrew surname: Berical fullname: Berical, Andrew – sequence: 15 givenname: Yaoyu surname: Wang fullname: Wang, Yaoyu – sequence: 16 givenname: Monica surname: Casali fullname: Casali, Monica – sequence: 17 givenname: Hendrik surname: Streeck fullname: Streeck, Hendrik – sequence: 18 givenname: Allyson K. surname: Bloom fullname: Bloom, Allyson K. – sequence: 19 givenname: Tim surname: Dudek fullname: Dudek, Tim – sequence: 20 givenname: Damien surname: Tully fullname: Tully, Damien – sequence: 21 givenname: Ruchi surname: Newman fullname: Newman, Ruchi – sequence: 22 givenname: Karen L. surname: Axten fullname: Axten, Karen L. – sequence: 23 givenname: Adrianne D. surname: Gladden fullname: Gladden, Adrianne D. – sequence: 24 givenname: Laura surname: Battis fullname: Battis, Laura – sequence: 25 givenname: Michael surname: Kemper fullname: Kemper, Michael – sequence: 26 givenname: Qiandong surname: Zeng fullname: Zeng, Qiandong – sequence: 27 givenname: Terrance P. surname: Shea fullname: Shea, Terrance P. – sequence: 28 givenname: Sharvari surname: Gujja fullname: Gujja, Sharvari – sequence: 29 givenname: Carmen surname: Zedlack fullname: Zedlack, Carmen – sequence: 30 givenname: Olivier surname: Gasser fullname: Gasser, Olivier – sequence: 31 givenname: Christian surname: Brander fullname: Brander, Christian – sequence: 32 givenname: Christoph surname: Hess fullname: Hess, Christoph – sequence: 33 givenname: Huldrych F. surname: Günthard fullname: Günthard, Huldrych F. – sequence: 34 givenname: Zabrina L. surname: Brumme fullname: Brumme, Zabrina L. – sequence: 35 givenname: Chanson J. surname: Brumme fullname: Brumme, Chanson J. – sequence: 36 givenname: Suzane surname: Bazner fullname: Bazner, Suzane – sequence: 37 givenname: Jenna surname: Rychert fullname: Rychert, Jenna – sequence: 38 givenname: Jake P. surname: Tinsley fullname: Tinsley, Jake P. – sequence: 39 givenname: Ken H. surname: Mayer fullname: Mayer, Ken H. – sequence: 40 givenname: Eric surname: Rosenberg fullname: Rosenberg, Eric – sequence: 41 givenname: Florencia surname: Pereyra fullname: Pereyra, Florencia – sequence: 42 givenname: Joshua Z. surname: Levin fullname: Levin, Joshua Z. – sequence: 43 givenname: Sarah K. surname: Young fullname: Young, Sarah K. – sequence: 44 givenname: Heiko surname: Jessen fullname: Jessen, Heiko – sequence: 45 givenname: Marcus surname: Altfeld fullname: Altfeld, Marcus – sequence: 46 givenname: Bruce W. surname: Birren fullname: Birren, Bruce W. – sequence: 47 givenname: Bruce D. surname: Walker fullname: Walker, Bruce D. – sequence: 48 givenname: Todd M. surname: Allen fullname: Allen, Todd M. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22412369$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2012 Public Library of Science 2012 Henn et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Henn MR, Boutwell CL, Charlebois P, Lennon NJ, Power KA, et al. (2012) Whole Genome Deep Sequencing of HIV-1 Reveals the Impact of Early Minor Variants Upon Immune Recognition During Acute Infection. PLoS Pathog 8(3): e1002529. doi:10.1371/journal.ppat.1002529 Henn et al. 2012 |
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| Keywords | HIV Infections HIV-1 Genome, Viral Genome-Wide Association Study Oligonucleotide Array Sequence Analysis Humans CD8-Positive T-Lymphocytes Genetic Variation Genomic Structural Variation Immune Evasion Sequence Analysis, RNA RNA, Viral Viral Vaccines |
| Language | English |
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| Snippet | Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to... Deep sequencing technologies have the potential to transform the study of highly variable viral pathogens by providing a rapid and cost-effective approach to... |
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| SubjectTerms | Adaptations Algorithms Biology CD8 antigen CD8-Positive T-Lymphocytes - immunology Data processing DNA sequencing Epitopes Evolution Genetic aspects Genetic Variation Genome, Viral - genetics Genome-Wide Association Study Genomes Genomic Structural Variation Genomics Health aspects Histocompatibility antigen HLA HIV (Viruses) HIV Infections - immunology HIV Infections - prevention & control HIV Infections - virology HIV-1 - genetics HIV-1 - immunology HIV-1 - pathogenicity Human immunodeficiency virus 1 Humans Immune Evasion - genetics Immune Evasion - immunology Immune response Immune system Immunity Immunology Infection Infections Lymphocytes T Medicine Mutation Nucleotide sequencing Oligonucleotide Array Sequence Analysis Pathogens Physiological aspects Replication Reversion RNA, Viral - analysis Sequence Analysis, RNA Vaccines Viral genetics Viral Vaccines - immunology Viremia |
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| Title | Whole Genome Deep Sequencing of HIV-1 Reveals the Impact of Early Minor Variants Upon Immune Recognition During Acute Infection |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/22412369 https://www.proquest.com/docview/1289082096 https://www.proquest.com/docview/1017965462 https://www.proquest.com/docview/927990241 https://pubmed.ncbi.nlm.nih.gov/PMC3297584 https://doaj.org/article/7846f6a69b894bfaae962b545cdfe22c http://dx.doi.org/10.1371/journal.ppat.1002529 |
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