Comparative Analysis of Measures of Viral Reservoirs in HIV-1 Eradication Studies

HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory CD4(+) T cells carrying latent but replication-competent viral genomes. Because strategies targeti...

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Published in	PLoS pathogens Vol. 9; no. 2; p. e1003174
Main Authors	Eriksson, Susanne, Graf, Erin H., Dahl, Viktor, Strain, Matthew C., Yukl, Steven A., Lysenko, Elena S., Bosch, Ronald J., Lai, Jun, Chioma, Stanley, Emad, Fatemeh, Abdel-Mohsen, Mohamed, Hoh, Rebecca, Hecht, Frederick, Hunt, Peter, Somsouk, Ma, Wong, Joseph, Johnston, Rowena, Siliciano, Robert F., Richman, Douglas D., O'Doherty, Una, Palmer, Sarah, Deeks, Steven G., Siliciano, Janet D.
Format	Journal Article
Language	English
Published	United States Public Library of Science 01.02.2013 Public Library of Science (PLoS)
Subjects	Acquired immune deficiency syndrome Adult Aged AIDS Antiretroviral agents Antiretroviral Therapy, Highly Active CD4-Positive T-Lymphocytes - drug effects Clinical trials Deoxyribonucleic acid Disease Reservoirs - virology DNA DNA, Viral - analysis DNA, Viral - drug effects DNA, Viral - genetics Drug therapy Experiments Female Genomes Grants Health aspects HIV HIV - genetics HIV - growth & development HIV - isolation & purification HIV Infections - drug therapy HIV Infections - genetics HIV Infections - virology HIV patients Human immunodeficiency virus Humans Infections Leukocytes, Mononuclear - drug effects Leukocytes, Mononuclear - virology Longitudinal Studies Lymphocytes Male Medicine Middle Aged Normal distribution Physiological aspects Plasma Polymerase Chain Reaction Proviruses - genetics Proviruses - growth & development Proviruses - isolation & purification RNA, Viral - analysis RNA, Viral - drug effects RNA, Viral - genetics Statistical methods T cells Viral Load - drug effects Virulence (Microbiology) Virus Integration - drug effects United States
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Abstract	HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory CD4(+) T cells carrying latent but replication-competent viral genomes. Because strategies targeting this latent reservoir are now being tested in clinical trials, well-validated high-throughput assays that quantify this reservoir are urgently needed. Here we compare eleven different approaches for quantitating persistent HIV-1 in 30 patients on HAART, using the original viral outgrowth assay for resting CD4(+) T cells carrying inducible, replication-competent viral genomes as a standard for comparison. PCR-based assays for cells containing HIV-1 DNA gave infected cell frequencies at least 2 logs higher than the viral outgrowth assay, even in subjects who started HAART during acute/early infection. This difference may reflect defective viral genomes. The ratio of infected cell frequencies determined by viral outgrowth and PCR-based assays varied dramatically between patients. Although strong correlations with the viral outgrowth assay could not be formally excluded for most assays, correlations achieved statistical significance only for integrated HIV-1 DNA in peripheral blood mononuclear cells and HIV-1 RNA/DNA ratio in rectal CD4(+) T cells. Residual viremia was below the limit of detection in many subjects and did not correlate with the viral outgrowth assays. The dramatic differences in infected cell frequencies and the lack of a precise correlation between culture and PCR-based assays raise the possibility that the successful clearance of latently infected cells may be masked by a larger and variable pool of cells with defective proviruses. These defective proviruses are detected by PCR but may not be affected by reactivation strategies and may not require eradication to accomplish an effective cure. A molecular understanding of the discrepancy between infected cell frequencies measured by viral outgrowth versus PCR assays is an urgent priority in HIV-1 cure research.
AbstractList	HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory CD4 + T cells carrying latent but replication-competent viral genomes. Because strategies targeting this latent reservoir are now being tested in clinical trials, well-validated high-throughput assays that quantify this reservoir are urgently needed. Here we compare eleven different approaches for quantitating persistent HIV-1 in 30 patients on HAART, using the original viral outgrowth assay for resting CD4 + T cells carrying inducible, replication-competent viral genomes as a standard for comparison. PCR-based assays for cells containing HIV-1 DNA gave infected cell frequencies at least 2 logs higher than the viral outgrowth assay, even in subjects who started HAART during acute/early infection. This difference may reflect defective viral genomes. The ratio of infected cell frequencies determined by viral outgrowth and PCR-based assays varied dramatically between patients. Although strong correlations with the viral outgrowth assay could not be formally excluded for most assays, correlations achieved statistical significance only for integrated HIV-1 DNA in peripheral blood mononuclear cells and HIV-1 RNA/DNA ratio in rectal CD4 + T cells. Residual viremia was below the limit of detection in many subjects and did not correlate with the viral outgrowth assays. The dramatic differences in infected cell frequencies and the lack of a precise correlation between culture and PCR-based assays raise the possibility that the successful clearance of latently infected cells may be masked by a larger and variable pool of cells with defective proviruses. These defective proviruses are detected by PCR but may not be affected by reactivation strategies and may not require eradication to accomplish an effective cure. A molecular understanding of the discrepancy between infected cell frequencies measured by viral outgrowth versus PCR assays is an urgent priority in HIV-1 cure research. Efforts to cure HIV-1 infection have focused on a small pool of CD4 + T cells that carry viral genetic information in a latent form. These cells persist even in patients on optimal antiretroviral therapy. Novel therapeutic strategies targeting latently infected cells are being developed, and therefore practical assays for measuring latently infected cells are urgently needed. These cells were discovered using a virus culture assay in which the cells are induced to release virus particles that are then expanded in culture. This assay is difficult, time-consuming, and expensive. Here we evaluate alternative approaches for measuring persistent HIV-1, all of which rely on the detection of viral genetic information using the polymerase chain reaction (PCR). None of the PCR-based assays correlated precisely with the virus culture assay. The fundamental problem is that infected cell frequencies determined by PCR are at least 2 logs higher than frequencies determined by the culture assay. Much of this difference may be due to cells carrying defective forms of the virus. These cells may not be eliminated by strategies designed to target latently infected cells. In this situation, successful clearance of latently infected cells might be masked by a large unchanging pool of cells carrying defective HIV-1. HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory CD4(+) T cells carrying latent but replication-competent viral genomes. Because strategies targeting this latent reservoir are now being tested in clinical trials, well-validated high-throughput assays that quantify this reservoir are urgently needed. Here we compare eleven different approaches for quantitating persistent HIV-1 in 30 patients on HAART, using the original viral outgrowth assay for resting CD4(+) T cells carrying inducible, replication-competent viral genomes as a standard for comparison. PCR-based assays for cells containing HIV-1 DNA gave infected cell frequencies at least 2 logs higher than the viral outgrowth assay, even in subjects who started HAART during acute/early infection. This difference may reflect defective viral genomes. The ratio of infected cell frequencies determined by viral outgrowth and PCR-based assays varied dramatically between patients. Although strong correlations with the viral outgrowth assay could not be formally excluded for most assays, correlations achieved statistical significance only for integrated HIV-1 DNA in peripheral blood mononuclear cells and HIV-1 RNA/DNA ratio in rectal CD4(+) T cells. Residual viremia was below the limit of detection in many subjects and did not correlate with the viral outgrowth assays. The dramatic differences in infected cell frequencies and the lack of a precise correlation between culture and PCR-based assays raise the possibility that the successful clearance of latently infected cells may be masked by a larger and variable pool of cells with defective proviruses. These defective proviruses are detected by PCR but may not be affected by reactivation strategies and may not require eradication to accomplish an effective cure. A molecular understanding of the discrepancy between infected cell frequencies measured by viral outgrowth versus PCR assays is an urgent priority in HIV-1 cure research. HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory CD4(+) T cells carrying latent but replication-competent viral genomes. Because strategies targeting this latent reservoir are now being tested in clinical trials, well-validated high-throughput assays that quantify this reservoir are urgently needed. Here we compare eleven different approaches for quantitating persistent HIV-1 in 30 patients on HAART, using the original viral outgrowth assay for resting CD4(+) T cells carrying inducible, replication-competent viral genomes as a standard for comparison. PCR-based assays for cells containing HIV-1 DNA gave infected cell frequencies at least 2 logs higher than the viral outgrowth assay, even in subjects who started HAART during acute/early infection. This difference may reflect defective viral genomes. The ratio of infected cell frequencies determined by viral outgrowth and PCR-based assays varied dramatically between patients. Although strong correlations with the viral outgrowth assay could not be formally excluded for most assays, correlations achieved statistical significance only for integrated HIV-1 DNA in peripheral blood mononuclear cells and HIV-1 RNA/DNA ratio in rectal CD4(+) T cells. Residual viremia was below the limit of detection in many subjects and did not correlate with the viral outgrowth assays. The dramatic differences in infected cell frequencies and the lack of a precise correlation between culture and PCR-based assays raise the possibility that the successful clearance of latently infected cells may be masked by a larger and variable pool of cells with defective proviruses. These defective proviruses are detected by PCR but may not be affected by reactivation strategies and may not require eradication to accomplish an effective cure. A molecular understanding of the discrepancy between infected cell frequencies measured by viral outgrowth versus PCR assays is an urgent priority in HIV-1 cure research.HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory CD4(+) T cells carrying latent but replication-competent viral genomes. Because strategies targeting this latent reservoir are now being tested in clinical trials, well-validated high-throughput assays that quantify this reservoir are urgently needed. Here we compare eleven different approaches for quantitating persistent HIV-1 in 30 patients on HAART, using the original viral outgrowth assay for resting CD4(+) T cells carrying inducible, replication-competent viral genomes as a standard for comparison. PCR-based assays for cells containing HIV-1 DNA gave infected cell frequencies at least 2 logs higher than the viral outgrowth assay, even in subjects who started HAART during acute/early infection. This difference may reflect defective viral genomes. The ratio of infected cell frequencies determined by viral outgrowth and PCR-based assays varied dramatically between patients. Although strong correlations with the viral outgrowth assay could not be formally excluded for most assays, correlations achieved statistical significance only for integrated HIV-1 DNA in peripheral blood mononuclear cells and HIV-1 RNA/DNA ratio in rectal CD4(+) T cells. Residual viremia was below the limit of detection in many subjects and did not correlate with the viral outgrowth assays. The dramatic differences in infected cell frequencies and the lack of a precise correlation between culture and PCR-based assays raise the possibility that the successful clearance of latently infected cells may be masked by a larger and variable pool of cells with defective proviruses. These defective proviruses are detected by PCR but may not be affected by reactivation strategies and may not require eradication to accomplish an effective cure. A molecular understanding of the discrepancy between infected cell frequencies measured by viral outgrowth versus PCR assays is an urgent priority in HIV-1 cure research. HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory [CD4.sup.+] T cells carrying latent but replication-competent viral genomes. Because strategies targeting this latent reservoir are now being tested in clinical trials, well-validated high-throughput assays that quantify this reservoir are urgently needed. Here we compare eleven different approaches for quantitating persistent HIV-1 in 30 patients on HAART, using the original viral outgrowth assay for resting [CD4.sup.+] T cells carrying inducible, replication-competent viral genomes as a standard for comparison. PCR-based assays for cells containing HIV-1 DNA gave infected cell frequencies at least 2 logs higher than the viral outgrowth assay, even in subjects who started HAART during acute/early infection. This difference may reflect defective viral genomes. The ratio of infected cell frequencies determined by viral outgrowth and PCR-based assays varied dramatically between patients. Although strong correlations with the viral outgrowth assay could not be formally excluded for most assays, correlations achieved statistical significance only for integrated HIV-1 DNA in peripheral blood mononuclear cells and HIV-1 RNA/DNA ratio in rectal [CD4.sup.+] T cells. Residual viremia was below the limit of detection in many subjects and did not correlate with the viral outgrowth assays. The dramatic differences in infected cell frequencies and the lack of a precise correlation between culture and PCR- based assays raise the possibility that the successful clearance of latently infected cells may be masked by a larger and variable pool of cells with defective proviruses. These defective proviruses are detected by PCR but may not be affected by reactivation strategies and may not require eradication to accomplish an effective cure. A molecular understanding of the discrepancy between infected cell frequencies measured by viral outgrowth versus PCR assays is an urgent priority in HIV-1 cure research. HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small, difficult-to-quantify pool of resting memory CD4+ T cells carrying latent but replication-competent viral genomes. Because strategies targeting this latent reservoir are now being tested in clinical trials, well-validated high-throughput assays that quantify this reservoir are urgently needed. Here we compare eleven different approaches for quantitating persistent HIV-1 in 30 patients on HAART, using the original viral outgrowth assay for resting CD4+ T cells carrying inducible, replication-competent viral genomes as a standard for comparison. PCR-based assays for cells containing HIV-1 DNA gave infected cell frequencies at least 2 logs higher than the viral outgrowth assay, even in subjects who started HAART during acute/early infection. This difference may reflect defective viral genomes. The ratio of infected cell frequencies determined by viral outgrowth and PCR-based assays varied dramatically between patients. Although strong correlations with the viral outgrowth assay could not be formally excluded for most assays, correlations achieved statistical significance only for integrated HIV-1 DNA in peripheral blood mononuclear cells and HIV-1 RNA/DNA ratio in rectal CD4+ T cells. Residual viremia was below the limit of detection in many subjects and did not correlate with the viral outgrowth assays. The dramatic differences in infected cell frequencies and the lack of a precise correlation between culture and PCR-based assays raise the possibility that the successful clearance of latently infected cells may be masked by a larger and variable pool of cells with defective proviruses. These defective proviruses are detected by PCR but may not be affected by reactivation strategies and may not require eradication to accomplish an effective cure. A molecular understanding of the discrepancy between infected cell frequencies measured by viral outgrowth versus PCR assays is an urgent priority in HIV-1 cure research.
Audience	Academic
Author	Siliciano, Janet D. Yukl, Steven A. Johnston, Rowena Emad, Fatemeh Lai, Jun Deeks, Steven G. Graf, Erin H. Wong, Joseph Bosch, Ronald J. Lysenko, Elena S. Abdel-Mohsen, Mohamed Palmer, Sarah Strain, Matthew C. Somsouk, Ma Siliciano, Robert F. Hunt, Peter Dahl, Viktor Chioma, Stanley Richman, Douglas D. O'Doherty, Una Eriksson, Susanne Hoh, Rebecca Hecht, Frederick
AuthorAffiliation	7 Department of Medicine Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America 9 Howard Hughes Medical Institute, Baltimore, Maryland, United States of America 5 Department of Medicine, University of California, San Francisco, San Francisco, California, United States of America 3 University of California San Diego, La Jolla, California and Veterans Affairs San Diego Healthcare System, San Diego, California, United States of America 4 San Francisco VA Medical Center, San Francisco, California, United States of America National Institutes of Health, National Institute of Allergy and Infectious Diseases, United States of America 1 Department of Diagnostics and Vaccinology, Swedish Institute for Communicable Diseases and Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Solna, Sweden 8 amfAR, The Foundation for AIDS Research, New York, New York, United States of America 6 Department of Biostatistics, Harvard School of Public Health, Bos
AuthorAffiliation_xml	– name: 8 amfAR, The Foundation for AIDS Research, New York, New York, United States of America – name: 2 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America – name: 5 Department of Medicine, University of California, San Francisco, San Francisco, California, United States of America – name: 4 San Francisco VA Medical Center, San Francisco, California, United States of America – name: 9 Howard Hughes Medical Institute, Baltimore, Maryland, United States of America – name: National Institutes of Health, National Institute of Allergy and Infectious Diseases, United States of America – name: 1 Department of Diagnostics and Vaccinology, Swedish Institute for Communicable Diseases and Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Solna, Sweden – name: 3 University of California San Diego, La Jolla, California and Veterans Affairs San Diego Healthcare System, San Diego, California, United States of America – name: 6 Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, United States of America – name: 7 Department of Medicine Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/23459007$$D View this record in MEDLINE/PubMed http://kipublications.ki.se/Default.aspx?queryparsed=id:126344962$$DView record from Swedish Publication Index
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ContentType	Journal Article
Copyright	COPYRIGHT 2013 Public Library of Science 2013 Eriksson 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: Eriksson S, Graf EH, Dahl V, Strain MC, Yukl SA, et al. (2013) Comparative Analysis of Measures of Viral Reservoirs in HIV-1 Eradication Studies. PLoS Pathog 9(2): e1003174. doi:10.1371/journal.ppat.1003174 2013 Eriksson et al 2013 Eriksson et al
Copyright_xml	– notice: COPYRIGHT 2013 Public Library of Science – notice: 2013 Eriksson 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: Eriksson S, Graf EH, Dahl V, Strain MC, Yukl SA, et al. (2013) Comparative Analysis of Measures of Viral Reservoirs in HIV-1 Eradication Studies. PLoS Pathog 9(2): e1003174. doi:10.1371/journal.ppat.1003174 – notice: 2013 Eriksson et al 2013 Eriksson et al
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Article-2 ObjectType-Feature-1 content type line 23 Conceived and designed the experiments: RJ JDS SGD. Performed the experiments: SE EHG VD MCS SAY ESL JL SC FE MAM MS. Analyzed the data: MS SAY RJB JW RFS DDR UOD SP SGD JDS. Contributed reagents/materials/analysis tools: RH FH PH SGD. Wrote the paper: RFS JDS. The authors have declared that no competing interests exist.
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Snippet	HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small,... HIV-1 reservoirs preclude virus eradication in patients receiving highly active antiretroviral therapy (HAART). The best characterized reservoir is a small,...
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SubjectTerms	Acquired immune deficiency syndrome Adult Aged AIDS Antiretroviral agents Antiretroviral Therapy, Highly Active CD4-Positive T-Lymphocytes - drug effects Clinical trials Deoxyribonucleic acid Disease Reservoirs - virology DNA DNA, Viral - analysis DNA, Viral - drug effects DNA, Viral - genetics Drug therapy Experiments Female Genomes Grants Health aspects HIV HIV - genetics HIV - growth & development HIV - isolation & purification HIV Infections - drug therapy HIV Infections - genetics HIV Infections - virology HIV patients Human immunodeficiency virus Humans Infections Leukocytes, Mononuclear - drug effects Leukocytes, Mononuclear - virology Longitudinal Studies Lymphocytes Male Medicine Middle Aged Normal distribution Physiological aspects Plasma Polymerase Chain Reaction Proviruses - genetics Proviruses - growth & development Proviruses - isolation & purification RNA, Viral - analysis RNA, Viral - drug effects RNA, Viral - genetics Statistical methods T cells Viral Load - drug effects Virulence (Microbiology) Virus Integration - drug effects
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Title	Comparative Analysis of Measures of Viral Reservoirs in HIV-1 Eradication Studies
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