Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversal

The latent HIV reservoir is a major barrier to HIV cure. Combining latency reversal agents (LRAs) with differing mechanisms of action such as AZD5582, a non-canonical NF-kB activator, and I-BET151, a bromodomain inhibitor is appealing toward inducing HIV-1 reactivation. However, even this LRA combin...

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Main Authors: Carley N Gray, Manickam Ashokkumar, Derek H Janssens, Jennifer L Kirchherr, Brigitte Allard, Emily Hsieh, Terry L Hafer, Nancie M Archin, Edward P Browne, Michael Emerman
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-04-01
Series:eLife
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Online Access:https://elifesciences.org/articles/103064
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author Carley N Gray
Manickam Ashokkumar
Derek H Janssens
Jennifer L Kirchherr
Brigitte Allard
Emily Hsieh
Terry L Hafer
Nancie M Archin
Edward P Browne
Michael Emerman
author_facet Carley N Gray
Manickam Ashokkumar
Derek H Janssens
Jennifer L Kirchherr
Brigitte Allard
Emily Hsieh
Terry L Hafer
Nancie M Archin
Edward P Browne
Michael Emerman
author_sort Carley N Gray
collection DOAJ
description The latent HIV reservoir is a major barrier to HIV cure. Combining latency reversal agents (LRAs) with differing mechanisms of action such as AZD5582, a non-canonical NF-kB activator, and I-BET151, a bromodomain inhibitor is appealing toward inducing HIV-1 reactivation. However, even this LRA combination needs improvement as it is inefficient at activating proviruses in cells of people living with HIV (PLWH). We performed a CRISPR screen in conjunction with AZD5582 & I-BET151 and identified a member of the Integrator complex as a target to improve this LRA combination, specifically Integrator complex subunit 12 (INTS12). Integrator functions as a genome-wide attenuator of transcription that acts on elongation through its RNA cleavage and phosphatase modules. Knockout of INTS12 improved latency reactivation at the transcriptional level and is more specific to the HIV-1 provirus than AZD5582 & I-BET151 treatment alone. We found that INTS12 is present on chromatin at the promoter of HIV and therefore its effect on HIV may be direct. Additionally, we observed more RNAPII in the gene body of HIV only with the combination of INTS12 knockout with AZD5582 & I-BET151, indicating that INTS12 induces a transcriptional elongation block to viral reactivation. Moreover, knockout of INTS12 increased HIV-1 reactivation in CD4 T cells from virally suppressed PLWH ex vivo, and we detected viral RNA in the supernatant from CD4 T cells of all three virally suppressed PLWH tested upon INTS12 knockout, suggesting that INTS12 prevents full-length HIV RNA production in primary T cells. Finally, we found that INTS12 more generally limits the efficacy of a variety of LRAs with different mechanisms of action.
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spelling doaj-art-1c7e365caabc458b9385585f60d8526e2025-08-20T02:16:49ZengeLife Sciences Publications LtdeLife2050-084X2025-04-011310.7554/eLife.103064Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversalCarley N Gray0https://orcid.org/0009-0008-5173-2769Manickam Ashokkumar1Derek H Janssens2https://orcid.org/0000-0003-1079-9525Jennifer L Kirchherr3https://orcid.org/0000-0003-3559-7356Brigitte Allard4Emily Hsieh5Terry L Hafer6Nancie M Archin7Edward P Browne8https://orcid.org/0000-0001-9070-7015Michael Emerman9https://orcid.org/0000-0002-4181-6335Department of Microbiology, University of Washington, Seattle, United StatesDivision of Infectious Diseases, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, United States; UNC HIV Cure Center, University of North Carolina at Chapel Hill, Chapel Hill, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, United StatesUNC HIV Cure Center, University of North Carolina at Chapel Hill, Chapel Hill, United StatesUNC HIV Cure Center, University of North Carolina at Chapel Hill, Chapel Hill, United StatesMolecular and Cellular Biology Graduate Program, University of Washington, Seattle, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, United States; Division of Human Biology, Fred Hutchinson Cancer Center, Seattle, United StatesDivision of Infectious Diseases, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, United States; UNC HIV Cure Center, University of North Carolina at Chapel Hill, Chapel Hill, United StatesDivision of Infectious Diseases, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, United States; UNC HIV Cure Center, University of North Carolina at Chapel Hill, Chapel Hill, United States; Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, United States; Division of Human Biology, Fred Hutchinson Cancer Center, Seattle, United StatesThe latent HIV reservoir is a major barrier to HIV cure. Combining latency reversal agents (LRAs) with differing mechanisms of action such as AZD5582, a non-canonical NF-kB activator, and I-BET151, a bromodomain inhibitor is appealing toward inducing HIV-1 reactivation. However, even this LRA combination needs improvement as it is inefficient at activating proviruses in cells of people living with HIV (PLWH). We performed a CRISPR screen in conjunction with AZD5582 & I-BET151 and identified a member of the Integrator complex as a target to improve this LRA combination, specifically Integrator complex subunit 12 (INTS12). Integrator functions as a genome-wide attenuator of transcription that acts on elongation through its RNA cleavage and phosphatase modules. Knockout of INTS12 improved latency reactivation at the transcriptional level and is more specific to the HIV-1 provirus than AZD5582 & I-BET151 treatment alone. We found that INTS12 is present on chromatin at the promoter of HIV and therefore its effect on HIV may be direct. Additionally, we observed more RNAPII in the gene body of HIV only with the combination of INTS12 knockout with AZD5582 & I-BET151, indicating that INTS12 induces a transcriptional elongation block to viral reactivation. Moreover, knockout of INTS12 increased HIV-1 reactivation in CD4 T cells from virally suppressed PLWH ex vivo, and we detected viral RNA in the supernatant from CD4 T cells of all three virally suppressed PLWH tested upon INTS12 knockout, suggesting that INTS12 prevents full-length HIV RNA production in primary T cells. Finally, we found that INTS12 more generally limits the efficacy of a variety of LRAs with different mechanisms of action.https://elifesciences.org/articles/103064HIVlatencyIntegratorIntegrator complexINTS12transcription elongation
spellingShingle Carley N Gray
Manickam Ashokkumar
Derek H Janssens
Jennifer L Kirchherr
Brigitte Allard
Emily Hsieh
Terry L Hafer
Nancie M Archin
Edward P Browne
Michael Emerman
Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversal
eLife
HIV
latency
Integrator
Integrator complex
INTS12
transcription elongation
title Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversal
title_full Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversal
title_fullStr Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversal
title_full_unstemmed Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversal
title_short Integrator complex subunit 12 knockout overcomes a transcriptional block to HIV latency reversal
title_sort integrator complex subunit 12 knockout overcomes a transcriptional block to hiv latency reversal
topic HIV
latency
Integrator
Integrator complex
INTS12
transcription elongation
url https://elifesciences.org/articles/103064
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