A Subset of Latency-Reversing Agents Expose HIV-Infected Resting CD4+ T-Cells to Recognition by Cytotoxic T-Lymphocytes
Resting CD4+ T-cells harboring inducible HIV proviruses are a critical reservoir in antiretroviral therapy (ART)-treated subjects. These cells express little to no viral protein, and thus neither die by viral cytopathic effects, nor are efficiently cleared by immune effectors. Elimination of this re...
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| Published in | PLoS pathogens Vol. 12; no. 4; p. e1005545 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.04.2016
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7374 1553-7366 1553-7374 |
| DOI | 10.1371/journal.ppat.1005545 |
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| Abstract | Resting CD4+ T-cells harboring inducible HIV proviruses are a critical reservoir in antiretroviral therapy (ART)-treated subjects. These cells express little to no viral protein, and thus neither die by viral cytopathic effects, nor are efficiently cleared by immune effectors. Elimination of this reservoir is theoretically possible by combining latency-reversing agents (LRAs) with immune effectors, such as CD8+ T-cells. However, the relative efficacy of different LRAs in sensitizing latently-infected cells for recognition by HIV-specific CD8+ T-cells has not been determined. To address this, we developed an assay that utilizes HIV-specific CD8+ T-cell clones as biosensors for HIV antigen expression. By testing multiple CD8+ T-cell clones against a primary cell model of HIV latency, we identified several single agents that primed latently-infected cells for CD8+ T-cell recognition, including IL-2, IL-15, two IL-15 superagonists (IL-15SA and ALT-803), prostratin, and the TLR-2 ligand Pam3CSK4. In contrast, we did not observe CD8+ T-cell recognition of target cells following treatment with histone deacetylase inhibitors or with hexamethylene bisacetamide (HMBA). In further experiments we demonstrate that a clinically achievable concentration of the IL-15 superagonist 'ALT-803', an agent presently in clinical trials for solid and hematological tumors, primes the natural ex vivo reservoir for CD8+ T-cell recognition. Thus, our results establish a novel experimental approach for comparative evaluation of LRAs, and highlight ALT-803 as an LRA with the potential to synergize with CD8+ T-cells in HIV eradication strategies. |
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| AbstractList | Resting CD4+ T-cells harboring inducible HIV proviruses are a critical reservoir in antiretroviral therapy (ART)-treated subjects. These cells express little to no viral protein, and thus neither die by viral cytopathic effects, nor are efficiently cleared by immune effectors. Elimination of this reservoir is theoretically possible by combining latency-reversing agents (LRAs) with immune effectors, such as CD8+ T-cells. However, the relative efficacy of different LRAs in sensitizing latently-infected cells for recognition by HIV-specific CD8+ T-cells has not been determined. To address this, we developed an assay that utilizes HIV-specific CD8+ T-cell clones as biosensors for HIV antigen expression. By testing multiple CD8+ T-cell clones against a primary cell model of HIV latency, we identified several single agents that primed latently-infected cells for CD8+ T-cell recognition, including IL-2, IL-15, two IL-15 superagonists (IL-15SA and ALT-803), prostratin, and the TLR-2 ligand Pam3CSK4. In contrast, we did not observe CD8+ T-cell recognition of target cells following treatment with histone deacetylase inhibitors or with hexamethylene bisacetamide (HMBA). In further experiments we demonstrate that a clinically achievable concentration of the IL-15 superagonist 'ALT-803', an agent presently in clinical trials for solid and hematological tumors, primes the natural ex vivo reservoir for CD8+ T-cell recognition. Thus, our results establish a novel experimental approach for comparative evaluation of LRAs, and highlight ALT-803 as an LRA with the potential to synergize with CD8+ T-cells in HIV eradication strategies. Resting CD4+ T-cells harboring inducible HIV proviruses are a critical reservoir in antiretroviral therapy (ART)-treated subjects. These cells express little to no viral protein, and thus neither die by viral cytopathic effects, nor are efficiently cleared by immune effectors. Elimination of this reservoir is theoretically possible by combining latency-reversing agents (LRAs) with immune effectors, such as CD8+ T-cells. However, the relative efficacy of different LRAs in sensitizing latently-infected cells for recognition by HIV-specific CD8+ T-cells has not been determined. To address this, we developed an assay that utilizes HIV-specific CD8+ T-cell clones as biosensors for HIV antigen expression. By testing multiple CD8+ T-cell clones against a primary cell model of HIV latency, we identified several single agents that primed latently-infected cells for CD8+ T-cell recognition, including IL-2, IL-15, two IL-15 superagonists (IL-15SA and ALT-803), prostratin, and the TLR-2 ligand Pam3CSK4. In contrast, we did not observe CD8+ T-cell recognition of target cells following treatment with histone deacetylase inhibitors or with hexamethylene bisacetamide (HMBA). In further experiments we demonstrate that a clinically achievable concentration of the IL-15 superagonist ‘ALT-803’, an agent presently in clinical trials for solid and hematological tumors, primes the natural ex vivo reservoir for CD8+ T-cell recognition. Thus, our results establish a novel experimental approach for comparative evaluation of LRAs, and highlight ALT-803 as an LRA with the potential to synergize with CD8+ T-cells in HIV eradication strategies. Although modern therapies have greatly improved the lives of HIV-positive people with access to care, a cure remains elusive. This leaves these individuals burdened by a lifelong commitment to medication, and fails to fully restore health. Curing infection would likely require therapies that combine the ability to force the virus out the ‘latent state’ in which it hides, with immune responses able to kill unmasked infected cells, the so called “shock and kill” strategy. A critical aspect of this strategy is identifying drugs that are effective at shocking virus out of latency, known as latency reversing agents. In this study, we took the novel approach of using CD8+ T-cells, immune cells responsible for killing infected cells, as biosensors able to detect the unmasking of latently-infected cells. Using this method, we screened a panel of potential latency reversing agents. We found that while a subset of these agents exposed infected cells to the immune system, others did not. Our results establish a new method for screening potential latency reversing agents, and support the prioritization of the agents that were shown to be effective for combination with CD8+ T-cells in shock and kill strategies aimed at curing HIV infection. Resting CD4+ T-cells harboring inducible HIV proviruses are a critical reservoir in antiretroviral therapy (ART)-treated subjects. These cells express little to no viral protein, and thus neither die by viral cytopathic effects, nor are efficiently cleared by immune effectors. Elimination of this reservoir is theoretically possible by combining latency-reversing agents (LRAs) with immune effectors, such as CD8+ T-cells. However, the relative efficacy of different LRAs in sensitizing latently-infected cells for recognition by HIV-specific CD8+ T-cells has not been determined. To address this, we developed an assay that utilizes HIV-specific CD8+ T-cell clones as biosensors for HIV antigen expression. By testing multiple CD8+ T-cell clones against a primary cell model of HIV latency, we identified several single agents that primed latently-infected cells for CD8+ T-cell recognition, including IL-2, IL-15, two IL-15 superagonists (IL-15SA and ALT-803), prostratin, and the TLR-2 ligand Pam3CSK4. In contrast, we did not observe CD8+ T-cell recognition of target cells following treatment with histone deacetylase inhibitors or with hexamethylene bisacetamide (HMBA). In further experiments we demonstrate that a clinically achievable concentration of the IL-15 superagonist 'ALT-803', an agent presently in clinical trials for solid and hematological tumors, primes the natural ex vivo reservoir for CD8+ T-cell recognition. Thus, our results establish a novel experimental approach for comparative evaluation of LRAs, and highlight ALT-803 as an LRA with the potential to synergize with CD8+ T-cells in HIV eradication strategies. |
| Author | O’Connor, Rachel Kovacs, Colin Rimpel, Katherine Tsai, Angela Geleziunas, Romas Irvine, Darrell J. Walker, Bruce D. Mueller, Stefanie Whitney, James B. Murry, Jeffrey P. Jeng, Emily K. Trocha, Alicja Thomas, Allison S. Buzon, Maria J. Lichterfeld, Mathias Jones, R. Brad Karel, Dan Benko, Erika Yu, Helen Huang, Szu-Han Ostrowski, Mario A. Irrinki, Alivelu Karandish, Sara Lim, So-Yon Sloan, Derek D. Wong, Hing C. |
| AuthorAffiliation | 5 Altor BioScience Corporation, Miramar, Florida, United States of America 6 Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, United States of America 8 Department of Medicine, University of Toronto, Toronto, Ontario, Canada 7 The Maple Leaf Medical Clinic, Toronto, Ontario, Canada 3 Department of Microbiology Immunology and Tropical Medicine, The George Washington University, Washington, D.C., United States of America 9 Li Ka Shing Medical Institute, St. Michael’s Hospital, Toronto, Ontario, Canad 10 Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America University of Wisconsin, UNITED STATES 11 Department of Biological Engineering, MIT, Cambridge, Massachusetts, United States of America 4 Gilead Sciences, Foster City, California, United States of America 1 The Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology, and Harvard University, Cambridge, Massachu |
| AuthorAffiliation_xml | – name: 1 The Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology, and Harvard University, Cambridge, Massachusetts, United States of America – name: 7 The Maple Leaf Medical Clinic, Toronto, Ontario, Canada – name: 4 Gilead Sciences, Foster City, California, United States of America – name: 3 Department of Microbiology Immunology and Tropical Medicine, The George Washington University, Washington, D.C., United States of America – name: 10 Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America – name: 6 Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, United States of America – name: 2 Koch Institute for Integrative Cancer Research, MIT, Cambridge, Massachusetts, United States of America – name: 5 Altor BioScience Corporation, Miramar, Florida, United States of America – name: 11 Department of Biological Engineering, MIT, Cambridge, Massachusetts, United States of America – name: University of Wisconsin, UNITED STATES – name: 8 Department of Medicine, University of Toronto, Toronto, Ontario, Canada – name: 9 Li Ka Shing Medical Institute, St. Michael’s Hospital, Toronto, Ontario, Canad |
| Author_xml | – sequence: 1 givenname: R. Brad surname: Jones fullname: Jones, R. Brad – sequence: 2 givenname: Stefanie surname: Mueller fullname: Mueller, Stefanie – sequence: 3 givenname: Rachel surname: O’Connor fullname: O’Connor, Rachel – sequence: 4 givenname: Katherine surname: Rimpel fullname: Rimpel, Katherine – sequence: 5 givenname: Derek D. surname: Sloan fullname: Sloan, Derek D. – sequence: 6 givenname: Dan surname: Karel fullname: Karel, Dan – sequence: 7 givenname: Hing C. surname: Wong fullname: Wong, Hing C. – sequence: 8 givenname: Emily K. surname: Jeng fullname: Jeng, Emily K. – sequence: 9 givenname: Allison S. surname: Thomas fullname: Thomas, Allison S. – sequence: 10 givenname: James B. surname: Whitney fullname: Whitney, James B. – sequence: 11 givenname: So-Yon surname: Lim fullname: Lim, So-Yon – sequence: 12 givenname: Colin surname: Kovacs fullname: Kovacs, Colin – sequence: 13 givenname: Erika surname: Benko fullname: Benko, Erika – sequence: 14 givenname: Sara surname: Karandish fullname: Karandish, Sara – sequence: 15 givenname: Szu-Han surname: Huang fullname: Huang, Szu-Han – sequence: 16 givenname: Maria J. surname: Buzon fullname: Buzon, Maria J. – sequence: 17 givenname: Mathias surname: Lichterfeld fullname: Lichterfeld, Mathias – sequence: 18 givenname: Alivelu surname: Irrinki fullname: Irrinki, Alivelu – sequence: 19 givenname: Jeffrey P. surname: Murry fullname: Murry, Jeffrey P. – sequence: 20 givenname: Angela surname: Tsai fullname: Tsai, Angela – sequence: 21 givenname: Helen surname: Yu fullname: Yu, Helen – sequence: 22 givenname: Romas surname: Geleziunas fullname: Geleziunas, Romas – sequence: 23 givenname: Alicja surname: Trocha fullname: Trocha, Alicja – sequence: 24 givenname: Mario A. surname: Ostrowski fullname: Ostrowski, Mario A. – sequence: 25 givenname: Darrell J. surname: Irvine fullname: Irvine, Darrell J. – sequence: 26 givenname: Bruce D. surname: Walker fullname: Walker, Bruce D. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27082643$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2016 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: T-Cells to Recognition by Cytotoxic T-Lymphocytes. PLoS Pathog 12(4): e1005545. doi:10.1371/journal.ppat.1005545 2016 Jones et al 2016 Jones et al 2016 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: T-Cells to Recognition by Cytotoxic T-Lymphocytes. PLoS Pathog 12(4): e1005545. doi:10.1371/journal.ppat.1005545 |
| Copyright_xml | – notice: 2016 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: T-Cells to Recognition by Cytotoxic T-Lymphocytes. PLoS Pathog 12(4): e1005545. doi:10.1371/journal.ppat.1005545 – notice: 2016 Jones et al 2016 Jones et al – notice: 2016 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: T-Cells to Recognition by Cytotoxic T-Lymphocytes. PLoS Pathog 12(4): e1005545. doi:10.1371/journal.ppat.1005545 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 DJI and BDW are co-senior authors. Conceived and designed the experiments: RBJ SM RO KR AST DK MJB DDS AI JPM ATs HY MAO DJI BDW ML RG. Performed the experiments: RBJ SM RO KR AST DK MJB DDS AI JPM ATs ATr HY SL SHH JBW SK. Analyzed the data: RBJ SM RO KR AST DK MJB DDS AI JPM ATs HY SHH JBW SL RG. Contributed reagents/materials/analysis tools: HCW EKJ EB CK. Wrote the paper: RBJ. Supervised the project: BDW DJI MAO ML RG. I have read the journal's policy and the authors of the manuscript have the following competing interests: DDS, AI, ATs, JPM, and HY are employed by, and own stock and/or stock options in Gilead Sciences, Inc. This does not alter our adherence to all PLoS Pathogens policies on sharing data and materials. HCW and EKJ are employees and stockholders of Altor BioScience Corporation. This does not alter our adherence to all PLOS Pathogens policies on sharing data and materials. The authors declare that they have no other competing financial interests. |
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| Snippet | Resting CD4+ T-cells harboring inducible HIV proviruses are a critical reservoir in antiretroviral therapy (ART)-treated subjects. These cells express little... Resting CD4+ T-cells harboring inducible HIV proviruses are a critical reservoir in antiretroviral therapy (ART)-treated subjects. These cells express little... |
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| SubjectTerms | Acquired immune deficiency syndrome AIDS Antigens Antiretroviral agents Antiviral Agents - pharmacology Biology and Life Sciences Biosensors CD4-Positive T-Lymphocytes - virology Cloning Cytotoxicity Deoxyribonucleic acid DNA Enzyme-Linked Immunosorbent Assay Enzyme-Linked Immunospot Assay Enzymes Experiments Flow Cytometry HIV HIV Infections - immunology Human immunodeficiency virus Humans Infections Information sharing Lentivirus Lymphocytes Medicine and Health Sciences Pathogens Polymerase Chain Reaction Proteins - pharmacology Research and Analysis Methods Software Studies T-Lymphocytes, Cytotoxic - immunology Virus Activation - drug effects Virus Latency - drug effects |
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| Title | A Subset of Latency-Reversing Agents Expose HIV-Infected Resting CD4+ T-Cells to Recognition by Cytotoxic T-Lymphocytes |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/27082643 https://www.proquest.com/docview/1789548532 https://www.proquest.com/docview/1782216032 https://www.proquest.com/docview/1802201001 https://pubmed.ncbi.nlm.nih.gov/PMC4833318 https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1005545&type=printable https://doaj.org/article/8d9eef0385234f16ae9fba721f3491fb http://dx.doi.org/10.1371/journal.ppat.1005545 |
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