The Depsipeptide Romidepsin Reverses HIV-1 Latency In Vivo
Pharmacologically-induced activation of replication competent proviruses from latency in the presence of antiretroviral treatment (ART) has been proposed as a step towards curing HIV-1 infection. However, until now, approaches to reverse HIV-1 latency in humans have yielded mixed results. Here, we r...
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| Published in | PLoS pathogens Vol. 11; no. 9; p. e1005142 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.09.2015
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Pharmacologically-induced activation of replication competent proviruses from latency in the presence of antiretroviral treatment (ART) has been proposed as a step towards curing HIV-1 infection. However, until now, approaches to reverse HIV-1 latency in humans have yielded mixed results. Here, we report a proof-of-concept phase Ib/IIa trial where 6 aviremic HIV-1 infected adults received intravenous 5 mg/m2 romidepsin (Celgene) once weekly for 3 weeks while maintaining ART. Lymphocyte histone H3 acetylation, a cellular measure of the pharmacodynamic response to romidepsin, increased rapidly (maximum fold range: 3.7–7.7 relative to baseline) within the first hours following each romidepsin administration. Concurrently, HIV-1 transcription quantified as copies of cell-associated un-spliced HIV-1 RNA increased significantly from baseline during treatment (range of fold-increase: 2.4–5.0; p = 0.03). Plasma HIV-1 RNA increased from <20 copies/mL at baseline to readily quantifiable levels at multiple post-infusion time-points in 5 of 6 patients (range 46–103 copies/mL following the second infusion, p = 0.04). Importantly, romidepsin did not decrease the number of HIV-specific T cells or inhibit T cell cytokine production. Adverse events (all grade 1–2) were consistent with the known side effects of romidepsin. In conclusion, romidepsin safely induced HIV-1 transcription resulting in plasma HIV-1 RNA that was readily detected with standard commercial assays demonstrating that significant reversal of HIV-1 latency in vivo is possible without blunting T cell-mediated immune responses. These finding have major implications for future trials aiming to eradicate the HIV-1 reservoir.
clinicaltrials.gov NTC02092116. |
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| AbstractList | Pharmacologically-induced activation of replication competent proviruses from latency in the presence of antiretroviral treatment (ART) has been proposed as a step towards curing HIV-1 infection. However, until now, approaches to reverse HIV-1 latency in humans have yielded mixed results. Here, we report a proof-of-concept phase Ib/IIa trial where 6 aviremic HIV-1 infected adults received intravenous 5 mg/m
2
romidepsin (Celgene) once weekly for 3 weeks while maintaining ART. Lymphocyte histone H3 acetylation, a cellular measure of the pharmacodynamic response to romidepsin, increased rapidly (maximum fold range: 3.7–7.7 relative to baseline) within the first hours following each romidepsin administration. Concurrently, HIV-1 transcription quantified as copies of cell-associated un-spliced HIV-1 RNA increased significantly from baseline during treatment (range of fold-increase: 2.4–5.0; p = 0.03). Plasma HIV-1 RNA increased from <20 copies/mL at baseline to readily quantifiable levels at multiple post-infusion time-points in 5 of 6 patients (range 46–103 copies/mL following the second infusion, p = 0.04). Importantly, romidepsin did not decrease the number of HIV-specific T cells or inhibit T cell cytokine production. Adverse events (all grade 1–2) were consistent with the known side effects of romidepsin. In conclusion, romidepsin safely induced HIV-1 transcription resulting in plasma HIV-1 RNA that was readily detected with standard commercial assays demonstrating that significant reversal of HIV-1 latency
in vivo
is possible without blunting T cell-mediated immune responses. These finding have major implications for future trials aiming to eradicate the HIV-1 reservoir.
One proposed way of curing HIV is to activate virus transcription and kill latently infected cells while the presence of antiretroviral therapy prevents spreading the infection. Induction of global T cell activation by mitogenic or other potent activators effectively reverses HIV-1 from latency
ex vivo
, but such compounds are generally too toxic for clinical use. Therefore, investigating the capacity of small molecule latency reversing agents to induce production of virus without causing global T cell activation has been a top research priority for scientists in recent years. In the present clinical trial, we demonstrate that significant viral reactivation can be safely induced using the depsipeptide romidepsin (HDAC inhibitor) in long-term suppressed HIV-1 individuals on antiretroviral therapy. Following each romidepsin infusion, we observed clear increases in lymphocyte H3 acetylation, HIV-1 transcription, and plasma HIV-1 RNA. Importantly, this reversal of HIV-1 latency could be measured using standard clinical assays for detection of plasma HIV-1 RNA. Furthermore, romidepsin did not alter the proportion of HIV-specific T cells or inhibit T cell cytokine production which is critically important for future trials combining HDAC inhibitors with interventions (e.g. therapeutic HIV-1 vaccination) designed to enhance killing of latently infected cells. Pharmacologically-induced activation of replication competent proviruses from latency in the presence of antiretroviral treatment (ART) has been proposed as a step towards curing HIV-1 infection. However, until now, approaches to reverse HIV-1 latency in humans have yielded mixed results. Here, we report a proof-of-concept phase Ib/IIa trial where 6 aviremic HIV-1 infected adults received intravenous 5 mg/m2 romidepsin (Celgene) once weekly for 3 weeks while maintaining ART. Lymphocyte histone H3 acetylation, a cellular measure of the pharmacodynamic response to romidepsin, increased rapidly (maximum fold range: 3.7-7.7 relative to baseline) within the first hours following each romidepsin administration. Concurrently, HIV-1 transcription quantified as copies of cell-associated un-spliced HIV-1 RNA increased significantly from baseline during treatment (range of fold-increase: 2.4-5.0; p = 0.03). Plasma HIV-1 RNA increased from <20 copies/mL at baseline to readily quantifiable levels at multiple post-infusion time-points in 5 of 6 patients (range 46-103 copies/mL following the second infusion, p = 0.04). Importantly, romidepsin did not decrease the number of HIV-specific T cells or inhibit T cell cytokine production. Adverse events (all grade 1-2) were consistent with the known side effects of romidepsin. In conclusion, romidepsin safely induced HIV-1 transcription resulting in plasma HIV-1 RNA that was readily detected with standard commercial assays demonstrating that significant reversal of HIV-1 latency in vivo is possible without blunting T cell-mediated immune responses. These finding have major implications for future trials aiming to eradicate the HIV-1 reservoir. Trial Registration clinicaltrials.gov NTC02092116 UNLABELLEDPharmacologically-induced activation of replication competent proviruses from latency in the presence of antiretroviral treatment (ART) has been proposed as a step towards curing HIV-1 infection. However, until now, approaches to reverse HIV-1 latency in humans have yielded mixed results. Here, we report a proof-of-concept phase Ib/IIa trial where 6 aviremic HIV-1 infected adults received intravenous 5 mg/m2 romidepsin (Celgene) once weekly for 3 weeks while maintaining ART. Lymphocyte histone H3 acetylation, a cellular measure of the pharmacodynamic response to romidepsin, increased rapidly (maximum fold range: 3.7–7.7 relative to baseline) within the first hours following each romidepsin administration. Concurrently, HIV-1 transcription quantified as copies of cell-associated un-spliced HIV-1 RNA increased significantly from baseline during treatment (range of fold-increase: 2.4–5.0; p = 0.03). Plasma HIV-1 RNA increased from <20 copies/mL at baseline to readily quantifiable levels at multiple post-infusion time-points in 5 of 6 patients (range 46–103 copies/mL following the second infusion, p = 0.04). Importantly, romidepsin did not decrease the number of HIV-specific T cells or inhibit T cell cytokine production. Adverse events (all grade 1–2) were consistent with the known side effects of romidepsin. In conclusion, romidepsin safely induced HIV-1 transcription resulting in plasma HIV-1 RNA that was readily detected with standard commercial assays demonstrating that significant reversal of HIV-1 latency in vivo is possible without blunting T cell-mediated immune responses. These finding have major implications for future trials aiming to eradicate the HIV-1 reservoir.TRIAL REGISTRATIONclinicaltrials.gov NTC02092116. Pharmacologically-induced activation of replication competent proviruses from latency in the presence of antiretroviral treatment (ART) has been proposed as a step towards curing HIV-1 infection. However, until now, approaches to reverse HIV-1 latency in humans have yielded mixed results. Here, we report a proof-of-concept phase Ib/IIa trial where 6 aviremic HIV-1 infected adults received intravenous 5 mg/m2 romidepsin (Celgene) once weekly for 3 weeks while maintaining ART. Lymphocyte histone H3 acetylation, a cellular measure of the pharmacodynamic response to romidepsin, increased rapidly (maximum fold range: 3.7–7.7 relative to baseline) within the first hours following each romidepsin administration. Concurrently, HIV-1 transcription quantified as copies of cell-associated un-spliced HIV-1 RNA increased significantly from baseline during treatment (range of fold-increase: 2.4–5.0; p = 0.03). Plasma HIV-1 RNA increased from <20 copies/mL at baseline to readily quantifiable levels at multiple post-infusion time-points in 5 of 6 patients (range 46–103 copies/mL following the second infusion, p = 0.04). Importantly, romidepsin did not decrease the number of HIV-specific T cells or inhibit T cell cytokine production. Adverse events (all grade 1–2) were consistent with the known side effects of romidepsin. In conclusion, romidepsin safely induced HIV-1 transcription resulting in plasma HIV-1 RNA that was readily detected with standard commercial assays demonstrating that significant reversal of HIV-1 latency in vivo is possible without blunting T cell-mediated immune responses. These finding have major implications for future trials aiming to eradicate the HIV-1 reservoir. clinicaltrials.gov NTC02092116. |
| Author | Søgaard, Ole S Fromentin, Remi Graversen, Mette E Denton, Paul W Nissen, Sara K Brinkmann, Christel R Kjaer, Anne Sofie Chomont, Nicolas Sommerfelt, Maja Hey-Cunningham, William J Krogsgaard, Kim Schleimann, Mariane H Pantaleo, Giuseppe Olesen, Rikke Rasmussen, Thomas A Østergaard, Lars Tolstrup, Martin Koelsch, Kersten K Leth, Steffen |
| AuthorAffiliation | 7 Centre de Recherche du CHUM, Montreal, Quebec, Canada John Hopkins University, UNITED STATES 2 Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark 5 Division of Immunology and Allergy, Lausanne University Hospital, Lausanne, Switzerland 1 Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark 4 Kirby Institute, University of New South Wales Medicine, University of New South Wales Australia, Sydney, Australia 8 Department of Microbiology, Infectiology, and Immunology, Université de Montréal, Faculty of Medicine, Montreal, Quebec, Canada 6 Bionor Pharma ASA, Oslo, Norway 3 Aarhus Institute for Advanced Studies, Aarhus University, Denmark |
| AuthorAffiliation_xml | – name: 4 Kirby Institute, University of New South Wales Medicine, University of New South Wales Australia, Sydney, Australia – name: 6 Bionor Pharma ASA, Oslo, Norway – name: 1 Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark – name: 7 Centre de Recherche du CHUM, Montreal, Quebec, Canada – name: 5 Division of Immunology and Allergy, Lausanne University Hospital, Lausanne, Switzerland – name: 3 Aarhus Institute for Advanced Studies, Aarhus University, Denmark – name: 2 Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark – name: John Hopkins University, UNITED STATES – name: 8 Department of Microbiology, Infectiology, and Immunology, Université de Montréal, Faculty of Medicine, Montreal, Quebec, Canada |
| Author_xml | – sequence: 1 givenname: Ole S surname: Søgaard fullname: Søgaard, Ole S organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark – sequence: 2 givenname: Mette E surname: Graversen fullname: Graversen, Mette E organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark; Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark – sequence: 3 givenname: Steffen surname: Leth fullname: Leth, Steffen organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark; Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark – sequence: 4 givenname: Rikke surname: Olesen fullname: Olesen, Rikke organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark – sequence: 5 givenname: Christel R surname: Brinkmann fullname: Brinkmann, Christel R organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark – sequence: 6 givenname: Sara K surname: Nissen fullname: Nissen, Sara K organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark – sequence: 7 givenname: Anne Sofie surname: Kjaer fullname: Kjaer, Anne Sofie organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark; Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark – sequence: 8 givenname: Mariane H surname: Schleimann fullname: Schleimann, Mariane H organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark; Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark – sequence: 9 givenname: Paul W surname: Denton fullname: Denton, Paul W organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark; Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark; Aarhus Institute for Advanced Studies, Aarhus University, Denmark – sequence: 10 givenname: William J surname: Hey-Cunningham fullname: Hey-Cunningham, William J organization: Kirby Institute, University of New South Wales Medicine, University of New South Wales Australia, Sydney, Australia – sequence: 11 givenname: Kersten K surname: Koelsch fullname: Koelsch, Kersten K organization: Kirby Institute, University of New South Wales Medicine, University of New South Wales Australia, Sydney, Australia – sequence: 12 givenname: Giuseppe surname: Pantaleo fullname: Pantaleo, Giuseppe organization: Division of Immunology and Allergy, Lausanne University Hospital, Lausanne, Switzerland – sequence: 13 givenname: Kim surname: Krogsgaard fullname: Krogsgaard, Kim organization: Bionor Pharma ASA, Oslo, Norway – sequence: 14 givenname: Maja surname: Sommerfelt fullname: Sommerfelt, Maja organization: Bionor Pharma ASA, Oslo, Norway – sequence: 15 givenname: Remi surname: Fromentin fullname: Fromentin, Remi organization: Centre de Recherche du CHUM, Montreal, Quebec, Canada – sequence: 16 givenname: Nicolas surname: Chomont fullname: Chomont, Nicolas organization: Centre de Recherche du CHUM, Montreal, Quebec, Canada; Department of Microbiology, Infectiology, and Immunology, Université de Montréal, Faculty of Medicine, Montreal, Quebec, Canada – sequence: 17 givenname: Thomas A surname: Rasmussen fullname: Rasmussen, Thomas A organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark – sequence: 18 givenname: Lars surname: Østergaard fullname: Østergaard, Lars organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark; Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark – sequence: 19 givenname: Martin surname: Tolstrup fullname: Tolstrup, Martin organization: Department of Infectious Diseases, Aarhus University Hospital, Aarhus, Denmark; Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26379282$$D View this record in MEDLINE/PubMed |
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| Copyright | 2015 Søgaard et al 2015 Søgaard et al 2015 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: . PLoS Pathog 11(9): e1005142. doi:10.1371/journal.ppat.1005142 |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 Conceived and designed the experiments: OSS TAR LØ MT SL. Performed the experiments: OSS SL MEG CRB RO ASK MHS PWD SKN WJHC KKK GP MS KK RF NC TAR MT. Analyzed the data: OSS SL CRB RO ASK MHS PWD SKN WJHC KKK GP RF NC TAR MT. Contributed reagents/materials/analysis tools: CRB RO ASK MHS PWD SKN WJHC KKK GP MS KK RF NC. Wrote the paper: OSS TAR LØ MT RO PWD. I have read the journal's policy and the authors of this manuscript have the following competing interests: MS is an employee of Bionor Pharma ASA and has shares in the company. KK is a consultant to Bionor Pharma ASA. The other authors declare no competing interests. This does not alter our adherence to all PLOS policies on sharing data and materials. |
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| SubjectTerms | Acetylation - drug effects Acquired immune deficiency syndrome Adult AIDS AIDS Vaccines - adverse effects AIDS Vaccines - therapeutic use Anti-HIV Agents - administration & dosage Anti-HIV Agents - adverse effects Anti-HIV Agents - therapeutic use Antiretroviral Therapy, Highly Active - adverse effects Biomarkers - blood Biomarkers - metabolism Cohort Studies Curing Cytokines Depsipeptides - administration & dosage Depsipeptides - adverse effects Depsipeptides - therapeutic use Drug Interactions Drug therapy Female Follow-Up Studies Histones - blood Histones - metabolism HIV HIV Infections - drug therapy HIV Infections - immunology HIV Infections - metabolism HIV Infections - virology HIV-1 - drug effects HIV-1 - immunology HIV-1 - isolation & purification HIV-1 - physiology Human immunodeficiency virus Humans Infections Infusions, Intravenous Lymphocytes Lymphocytes - drug effects Lymphocytes - immunology Lymphocytes - metabolism Male Middle Aged Plasma Protein Processing, Post-Translational - drug effects RNA, Viral - blood RNA, Viral - metabolism Studies Viral Load - drug effects Virus Activation - drug effects Virus Latency - drug effects |
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| Title | The Depsipeptide Romidepsin Reverses HIV-1 Latency In Vivo |
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