Cited by 417Protein Degradation and InhibitorsGenomics and Chromatin DynamicsCardiac Fibrosis and Remodeling

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BET Bromodomains Mediate Transcriptional Pause Release in Heart Failure

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Anand, Priti, Brown, Jonathan D., Lin, Charles Y., Qi, Jun, Zhang, Rongli, Artero, Pedro Calderon, Alaiti, M. Amer, Bullard, Jace, Alazem, Kareem, Margulies, Kenneth B., Cappola, Thomas P., Lemieux, Madeleine, Plutzky, Jorge, Bradner, James E., Haldar, Saptarsi M.·2013·Cell

DOI 10.1016/j.cell.2013.07.013PMC PMC4090947

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Abstract

Heart failure (HF) is driven by the interplay between regulatory transcription factors and dynamic alterations in chromatin structure. Pathologic gene transactivation in HF is associated with recruitment of histone acetyl-transferases and local chromatin hyperacetylation. We therefore assessed the role of acetyl-lysine reader proteins, or bromodomains, in HF. Using a chemical genetic approach, we establish a central role for BET family bromodomain proteins in gene control during HF pathogenesis. BET inhibition potently suppresses cardiomyocyte hypertrophy in vitro and pathologic cardiac remodeling in vivo. Integrative transcriptional and epigenomic analyses reveal that BET proteins function mechanistically as pause-release factors critical to expression of genes that are central to HF pathogenesis and relevant to the pathobiology of failing human hearts. This study implicates epigenetic readers as essential effectors of transcriptional pause release during HF pathogenesis and identifies BET coactivator proteins as therapeutic targets in the heart.

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1 retracted

RETRACTED: Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy.
Rockman, H. A., Ross, R. S., Harris, A. N., Knowlton, K. U., Steinhelper, M. E., Field, L. J., Ross, J., & Chien, K. R. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.18.8277 · Cited by 807 · cited 1×
“model of cardiac pressure overload, which provides focal hemodynamic stress to the heart and recapitulates several cardinal aspects of pathologic hypertrophy and HF in humans (Rockman et al., 1991).”
Retracted
Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · cited 1×
“Using gene set enrichment analysis (GSEA) (Subramanian et al., 2005), we compared our set of TAC-induc-”
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849
Model-based Analysis of ChIP-Seq (MACS)
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“The pathologic nature of this process has been validated in large epidemiologic studies, which demonstrate that the presence of chronic cardiac hypertrophy is a robust predictor of subsequent HF and death (Hill and Olson, 2008; Levy et al., 1990).”
Selective inhibition of BET bromodomains
Filippakopoulos, P., Qi, J., Picaud, S., Shen, Y., Smith, W. B., Fedorov, O., Morse, E. M., Keates, T., Hickman, T. T., Felletar, I., et al. (2010) · Nature · doi:10.1038/nature09504 · Cited by 4,262 · cited 4×
“We and others have utilized this chemical genetic tool to probe BET function in a number of developmental and disease contexts, such as cancer (Delmore et al., 2011; Filippakopoulos et al., 2010), HIV infection (Banerjee et al.”
InfluentialSelf-citation
Selective Inhibition of Tumor Oncogenes by Disruption of Super-Enhancers
Lovén, J., Hoke, H. A., Lin, C. Y., Lau, A., Orlando, D. A., Vakoc, C. R., Bradner, J. E., Lee, T. I., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.03.036 · Cited by 2,961 · cited 3×
“Furthermore, the very recent discovery of asymmetrically loaded BRD4 on a critical subset of state-specific enhancers termed superenhancers (Lovén et al., 2013) raises the possibility that such superenhancers might also be active in the stressed myocardium and contribute to BET target specificity.”
Self-citation
BET Bromodomain Inhibition as a Therapeutic Strategy to Target c-Myc
Delmore, J. E., Issa, G. C., Lemieux, M. E., Rahl, P. B., Shi, J., Jacobs, H. M., Kastritis, E., Gilpatrick, T., Paranal, R. M., Qi, J., et al. (2011) · Cell · doi:10.1016/j.cell.2011.08.017 · Cited by 2,888 · cited 4×
“Prior studies from our laboratory and others have implicated BET bromodomains in neoplastic MYC transcription in hematopoietic tumors (Delmore et al., 2011; Zuber et al., 2011).”
InfluentialSelf-citation
Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals
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“Specifically, we studied the Broad Institute Molecular Signatures Database C3 motif gene sets (Xie et al., 2005), as well as three functional, in vivo signatures of CMspecific transcriptional effectors: Calcineurin-NFAT (Bousette et al.”
RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia
Zuber, J., Shi, J., Wang, E., Rappaport, A. R., Herrmann, H., Sison, E. A., Magoon, D., Qi, J., Blatt, K., Wunderlich, M., et al. (2011) · Nature · doi:10.1038/nature10334 · Cited by 1,870 · cited 2×
“Prior studies from our laboratory and others have implicated BET bromodomains in neoplastic MYC transcription in hematopoietic tumors (Delmore et al., 2011; Zuber et al., 2011).”
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“On a molecular level, it has been well established that many cardiac pathologies result from dynamic changes in gene expression and, conversely, that modulating key epigenetic factors (e.g., BRG1 13 , BET 14 , HDACs 15 ) have the capacity to prevent or abrogate injury or pathological remodeling.”

Authors: Anand, P., Brown, J. D., Lin, C. Y., Qi, J., Zhang, R., Artero, P. C., Alaiti, M. A., Bullard, J., Alazem, K., Margulies, K. B., Cappola, T. P., Lemieux, M., Plutzky, J., Bradner, J. E., & Haldar, S. M.
Affiliations: University Hospitals of Cleveland (US)
Brigham and Women's Hospital (US)
Dana-Farber Cancer Institute (US)
University of Pennsylvania (US)
Harvard University (US)
Corresponding author: Bradner, James E.
Haldar, Saptarsi M.
ORCID: Brown, Jonathan D.
Lin, Charles Y.
Qi, Jun
Zhang, Rongli
Alaiti, M. Amer
Alazem, Kareem
Margulies, Kenneth B.
Cappola, Thomas P.
Lemieux, Madeleine
Plutzky, Jorge
Bradner, James E.
Haldar, Saptarsi M.
Venue: Cell
Publisher: Elsevier BV
Published: 2013-08
Volume: 154
Issue: 3
Pages: 569-582
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2013.07.013
PMC: PMC4090947
OpenAlex: W2154924534
Cited by: 406
References: 63
Citations by year: 2026: 21 · 2025: 26 · 2024: 18 · 2023: 25 · 2022: 25 · 2021: 36 · 2020: 49 · 2019: 33 · 2018: 28 · 2017: 29 · 2016: 36 · 2015: 42 · 2014: 30 · 2013: 6
FWCI: 17.01
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 365 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Wellcome Trust
National Heart, Lung, and Blood Institute (T32HL105338, K08HL105678, K08HL086614, R01HL105993, P01HL048743)
National Cancer Institute (K08CA128972)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK093821)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Degradation and Inhibitors
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
Keywords: heart failure, BET proteins, chromatin acetylation, histone acetyltransferase, cardiac remodeling, cardiomyocyte hypertrophy, epigenetic reader protein, BET inhibition, gene expression regulation, chemical genetics
MeSH terms: Animals, Chromatin, Disease Models, Animal, Heart, Cardiomegaly, Heart Failure, Humans, Mice, Inbred C57BL, Transcription Factors, Transcription, Genetic, Protein Structure, Tertiary, Myocytes, Cardiac, Epigenesis, Genetic, Mice, Rats, Transcriptome

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BET Bromodomains Mediate Transcriptional Pause Release in Heart Failure

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