Elite Suppressors Harbor Low Levels of Integrated HIV DNA and High Levels of 2-LTR Circular HIV DNA Compared to HIV+ Patients On and Off HAART

Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly active anti-retroviral therapy (HAART). Patients on HAART often achieve viral control to similar (undetectable) levels. Accurate and sensitive me...

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Published inPLoS pathogens Vol. 7; no. 2; p. e1001300
Main Authors Graf, Erin H., Mexas, Angela M., Yu, Jianqing J., Shaheen, Farida, Liszewski, Megan K., Di Mascio, Michele, Migueles, Stephen A., Connors, Mark, O'Doherty, Una
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2011
Public Library of Science (PLoS)
Subjects
Antiretroviral Therapy, Highly Active
CD4-Positive T-Lymphocytes - virology
Cohort Studies
Deoxyribonucleic acid
DNA
DNA, Circular - genetics
DNA, Viral - genetics
Drug therapy
Health aspects
Highly active antiretroviral therapy
HIV
HIV infection
HIV Infections - drug therapy
HIV Infections - virology
HIV Long Terminal Repeat - genetics
HIV patients
HIV-1 - genetics
Human immunodeficiency virus
Humans
Immune system
Immunology
Immunology/Immune Response
Immunology/Immunity to Infections
Methods
Patients
Physiological aspects
Viral Load
Virology
Virology/Host Antiviral Responses
Virology/Immunodeficiency Viruses
Virology/Mechanisms of Resistance and Susceptibility, including Host Genetics
Virology/Persistence and Latency
Virus Integration
United States
Online AccessGet full text

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Abstract Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly active anti-retroviral therapy (HAART). Patients on HAART often achieve viral control to similar (undetectable) levels. Accurate and sensitive methods to measure viral burden are needed to elucidate important differences between these two patient populations in order to better understand their mechanisms of control. Viral burden quantification in ES patients has been limited to measurements of total DNA in PBMC, and estimates of Infectious Units per Million cells (IUPM). There appears to be no significant difference in the level of total HIV DNA between cells from ES patients and patients on HAART. However, recovering infectious virus from ES patient samples is much more difficult, suggesting their reservoir size should be much smaller than that in patients on HAART. Here we find that there is a significant difference in the level of integrated HIV DNA in ES patients compared to patients on HAART, providing an explanation for the previous results. When comparing the level of total to integrated HIV DNA in these samples we find ES patients have large excesses of unintegrated HIV DNA. To determine the composition of unintegrated HIV DNA in these samples, we measured circular 2-LTR HIV DNA forms and found ES patients frequently have high levels of 2-LTR circles in PBMC. We further show that these high levels of 2-LTR circles are not the result of inefficient integration in ES cells, since HIV integrates with similar efficiency in ES and normal donor cells. Our findings suggest that measuring integration provides a better surrogate of viral burden than total HIV DNA in ES patients. Moreover, they add significantly to our understanding of the mechanisms that allow viral control and reservoir maintenance in this unique patient population.
AbstractList Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly active anti-retroviral therapy (HAART). Patients on HAART often achieve viral control to similar (undetectable) levels. Accurate and sensitive methods to measure viral burden are needed to elucidate important differences between these two patient populations in order to better understand their mechanisms of control. Viral burden quantification in ES patients has been limited to measurements of total DNA in PBMC, and estimates of Infectious Units per Million cells (IUPM). There appears to be no significant difference in the level of total HIV DNA between cells from ES patients and patients on HAART. However, recovering infectious virus from ES patient samples is much more difficult, suggesting their reservoir size should be much smaller than that in patients on HAART. Here we find that there is a significant difference in the level of integrated HIV DNA in ES patients compared to patients on HAART, providing an explanation for the previous results. When comparing the level of total to integrated HIV DNA in these samples we find ES patients have large excesses of unintegrated HIV DNA. To determine the composition of unintegrated HIV DNA in these samples, we measured circular 2-LTR HIV DNA forms and found ES patients frequently have high levels of 2-LTR circles in PBMC. We further show that these high levels of 2-LTR circles are not the result of inefficient integration in ES cells, since HIV integrates with similar efficiency in ES and normal donor cells. Our findings suggest that measuring integration provides a better surrogate of viral burden than total HIV DNA in ES patients. Moreover, they add significantly to our understanding of the mechanisms that allow viral control and reservoir maintenance in this unique patient population.
  Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly active anti-retroviral therapy (HAART). Patients on HAART often achieve viral control to similar (undetectable) levels. Accurate and sensitive methods to measure viral burden are needed to elucidate important differences between these two patient populations in order to better understand their mechanisms of control. Viral burden quantification in ES patients has been limited to measurements of total DNA in PBMC, and estimates of Infectious Units per Million cells (IUPM). There appears to be no significant difference in the level of total HIV DNA between cells from ES patients and patients on HAART. However, recovering infectious virus from ES patient samples is much more difficult, suggesting their reservoir size should be much smaller than that in patients on HAART. Here we find that there is a significant difference in the level of integrated HIV DNA in ES patients compared to patients on HAART, providing an explanation for the previous results. When comparing the level of total to integrated HIV DNA in these samples we find ES patients have large excesses of unintegrated HIV DNA. To determine the composition of unintegrated HIV DNA in these samples, we measured circular 2-LTR HIV DNA forms and found ES patients frequently have high levels of 2-LTR circles in PBMC. We further show that these high levels of 2-LTR circles are not the result of inefficient integration in ES cells, since HIV integrates with similar efficiency in ES and normal donor cells. Our findings suggest that measuring integration provides a better surrogate of viral burden than total HIV DNA in ES patients. Moreover, they add significantly to our understanding of the mechanisms that allow viral control and reservoir maintenance in this unique patient population.
Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly active anti-retroviral therapy (HAART). Patients on HAART often achieve viral control to similar (undetectable) levels. Accurate and sensitive methods to measure viral burden are needed to elucidate important differences between these two patient populations in order to better understand their mechanisms of control. Viral burden quantification in ES patients has been limited to measurements of total DNA in PBMC, and estimates of Infectious Units per Million cells (IUPM). There appears to be no significant difference in the level of total HIV DNA between cells from ES patients and patients on HAART. However, recovering infectious virus from ES patient samples is much more difficult, suggesting their reservoir size should be much smaller than that in patients on HAART. Here we find that there is a significant difference in the level of integrated HIV DNA in ES patients compared to patients on HAART, providing an explanation for the previous results. When comparing the level of total to integrated HIV DNA in these samples we find ES patients have large excesses of unintegrated HIV DNA. To determine the composition of unintegrated HIV DNA in these samples, we measured circular 2-LTR HIV DNA forms and found ES patients frequently have high levels of 2-LTR circles in PBMC. We further show that these high levels of 2-LTR circles are not the result of inefficient integration in ES cells, since HIV integrates with similar efficiency in ES and normal donor cells. Our findings suggest that measuring integration provides a better surrogate of viral burden than total HIV DNA in ES patients. Moreover, they add significantly to our understanding of the mechanisms that allow viral control and reservoir maintenance in this unique patient population. Although HIV infection usually results in a syndrome of immunodeficiency, there is a small group of people infected with the virus who naturally control the infection. These subjects (called elite suppressors) are capable of mounting a more effective immune response against the virus, which maintains virus levels below detectable limits without clearing the infection. When plasma virus levels are this low, however, it becomes difficult to determine how much virus is present, and whether there are changes in viral burden over time. Here we show that measuring the level of integrated HIV DNA in this patient population provides valuable information regarding the mechanisms involved in viral control. Specifically, we show that levels of integrated HIV DNA are much lower in elite suppressors compared to other patients on and off anti-retroviral drugs, consistent with having a smaller reservoir. We show that 2-LTR circles, comprised of DNA that is replication incompetent, are much more common in elite suppressors. Thus, we identified two important differences between elite suppressors and other HIV infected individuals. We further show that ES cells appear to be just as susceptible to HIV integration as those from uninfected donors, suggesting that the elevated 2-LTR circles are not the result of an inherent restriction to integration. We conclude that measuring integration of HIV DNA in patient samples may provide a surrogate measure of viral burden in these and other patients with HIV.
Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly active anti-retroviral therapy (HAART). Patients on HAART often achieve viral control to similar (undetectable) levels. Accurate and sensitive methods to measure viral burden are needed to elucidate important differences between these two patient populations in order to better understand their mechanisms of control. Viral burden quantification in ES patients has been limited to measurements of total DNA in PBMC, and estimates of Infectious Units per Million cells (IUPM). There appears to be no significant difference in the level of total HIV DNA between cells from ES patients and patients on HAART. However, recovering infectious virus from ES patient samples is much more difficult, suggesting their reservoir size should be much smaller than that in patients on HAART. Here we find that there is a significant difference in the level of integrated HIV DNA in ES patients compared to patients on HAART, providing an explanation for the previous results. When comparing the level of total to integrated HIV DNA in these samples we find ES patients have large excesses of unintegrated HIV DNA. To determine the composition of unintegrated HIV DNA in these samples, we measured circular 2-LTR HIV DNA forms and found ES patients frequently have high levels of 2-LTR circles in PBMC. We further show that these high levels of 2-LTR circles are not the result of inefficient integration in ES cells, since HIV integrates with similar efficiency in ES and normal donor cells. Our findings suggest that measuring integration provides a better surrogate of viral burden than total HIV DNA in ES patients. Moreover, they add significantly to our understanding of the mechanisms that allow viral control and reservoir maintenance in this unique patient population.Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly active anti-retroviral therapy (HAART). Patients on HAART often achieve viral control to similar (undetectable) levels. Accurate and sensitive methods to measure viral burden are needed to elucidate important differences between these two patient populations in order to better understand their mechanisms of control. Viral burden quantification in ES patients has been limited to measurements of total DNA in PBMC, and estimates of Infectious Units per Million cells (IUPM). There appears to be no significant difference in the level of total HIV DNA between cells from ES patients and patients on HAART. However, recovering infectious virus from ES patient samples is much more difficult, suggesting their reservoir size should be much smaller than that in patients on HAART. Here we find that there is a significant difference in the level of integrated HIV DNA in ES patients compared to patients on HAART, providing an explanation for the previous results. When comparing the level of total to integrated HIV DNA in these samples we find ES patients have large excesses of unintegrated HIV DNA. To determine the composition of unintegrated HIV DNA in these samples, we measured circular 2-LTR HIV DNA forms and found ES patients frequently have high levels of 2-LTR circles in PBMC. We further show that these high levels of 2-LTR circles are not the result of inefficient integration in ES cells, since HIV integrates with similar efficiency in ES and normal donor cells. Our findings suggest that measuring integration provides a better surrogate of viral burden than total HIV DNA in ES patients. Moreover, they add significantly to our understanding of the mechanisms that allow viral control and reservoir maintenance in this unique patient population.
Audience Academic
Author Shaheen, Farida
Migueles, Stephen A.
Yu, Jianqing J.
Connors, Mark
Graf, Erin H.
O'Doherty, Una
Mexas, Angela M.
Di Mascio, Michele
Liszewski, Megan K.
AuthorAffiliation 1 Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
Fred Hutchinson Cancer Research Center, United States of America
3 Biostatistics Research Branch and NIAID, National Institutes of Health, Bethesda, Maryland, United States of America
4 Laboratory of Immunoregulation, NIAID, National Institutes of Health, Bethesda, Maryland, United States of America
2 The Center for Aids Research, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
AuthorAffiliation_xml – name: 4 Laboratory of Immunoregulation, NIAID, National Institutes of Health, Bethesda, Maryland, United States of America
– name: 1 Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
– name: Fred Hutchinson Cancer Research Center, United States of America
– name: 2 The Center for Aids Research, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
– name: 3 Biostatistics Research Branch and NIAID, National Institutes of Health, Bethesda, Maryland, United States of America
Author_xml – sequence: 1
  givenname: Erin H.
  surname: Graf
  fullname: Graf, Erin H.
– sequence: 2
  givenname: Angela M.
  surname: Mexas
  fullname: Mexas, Angela M.
– sequence: 3
  givenname: Jianqing J.
  surname: Yu
  fullname: Yu, Jianqing J.
– sequence: 4
  givenname: Farida
  surname: Shaheen
  fullname: Shaheen, Farida
– sequence: 5
  givenname: Megan K.
  surname: Liszewski
  fullname: Liszewski, Megan K.
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  givenname: Michele
  surname: Di Mascio
  fullname: Di Mascio, Michele
– sequence: 7
  givenname: Stephen A.
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  fullname: Migueles, Stephen A.
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– sequence: 9
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/21383972$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2011 Public Library of Science
2011 Public Library of Science. 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: Citation: Graf EH, Mexas AM, Yu JJ, Shaheen F, Liszewski MK, et al. (2011) Elite Suppressors Harbor Low Levels of Integrated HIV DNA and High Levels of 2-LTR Circular HIV DNA Compared to HIV+ Patients On and Off HAART. PLoS Pathog 7(2): e1001300. doi:10.1371/journal.ppat.1001300
This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2011
2011 Public Library of Science. 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: Citation: Graf EH, Mexas AM, Yu JJ, Shaheen F, Liszewski MK, et al. (2011) Elite Suppressors Harbor Low Levels of Integrated HIV DNA and High Levels of 2-LTR Circular HIV DNA Compared to HIV+ Patients On and Off HAART. PLoS Pathog 7(2): e1001300. doi:10.1371/journal.ppat.1001300
Copyright_xml – notice: COPYRIGHT 2011 Public Library of Science
– notice: 2011 Public Library of Science. 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: Citation: Graf EH, Mexas AM, Yu JJ, Shaheen F, Liszewski MK, et al. (2011) Elite Suppressors Harbor Low Levels of Integrated HIV DNA and High Levels of 2-LTR Circular HIV DNA Compared to HIV+ Patients On and Off HAART. PLoS Pathog 7(2): e1001300. doi:10.1371/journal.ppat.1001300
– notice: This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2011
– notice: 2011 Public Library of Science. 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: Citation: Graf EH, Mexas AM, Yu JJ, Shaheen F, Liszewski MK, et al. (2011) Elite Suppressors Harbor Low Levels of Integrated HIV DNA and High Levels of 2-LTR Circular HIV DNA Compared to HIV+ Patients On and Off HAART. PLoS Pathog 7(2): e1001300. doi:10.1371/journal.ppat.1001300
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Conceived and designed the experiments: EHG AMM MKL UO. Performed the experiments: EHG AMM JJY. Analyzed the data: EHG AMM MDM SAM MC UO. Contributed reagents/materials/analysis tools: FS SAM MC UO. Wrote the paper: EHG AMM UO.
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Snippet Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly...
  Elite suppressors (ES) are a rare population of HIV-infected individuals that are capable of naturally controlling the infection without the use of highly...
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StartPage e1001300
SubjectTerms Antiretroviral Therapy, Highly Active
CD4-Positive T-Lymphocytes - virology
Cohort Studies
Deoxyribonucleic acid
DNA
DNA, Circular - genetics
DNA, Viral - genetics
Drug therapy
Health aspects
Highly active antiretroviral therapy
HIV
HIV infection
HIV Infections - drug therapy
HIV Infections - virology
HIV Long Terminal Repeat - genetics
HIV patients
HIV-1 - genetics
Human immunodeficiency virus
Humans
Immune system
Immunology
Immunology/Immune Response
Immunology/Immunity to Infections
Methods
Patients
Physiological aspects
Viral Load
Virology
Virology/Host Antiviral Responses
Virology/Immunodeficiency Viruses
Virology/Mechanisms of Resistance and Susceptibility, including Host Genetics
Virology/Persistence and Latency
Virus Integration
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Title Elite Suppressors Harbor Low Levels of Integrated HIV DNA and High Levels of 2-LTR Circular HIV DNA Compared to HIV+ Patients On and Off HAART
URI https://www.ncbi.nlm.nih.gov/pubmed/21383972
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https://pubmed.ncbi.nlm.nih.gov/PMC3044690
https://doaj.org/article/57cf1440b8ca40e1b555cb21e9c8c023
http://dx.doi.org/10.1371/journal.ppat.1001300
Volume 7
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