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The SMARCA2/4 ATPase Domain Surpasses the Bromodomain as a Drug Target in SWI/SNF-Mutant Cancers: Insights from cDNA Rescue and PFI-3 Inhibitor Studies
Open accessPublished version of a preprint
Abstract
The SWI/SNF multisubunit complex modulates chromatin structure through the activity of two mutually exclusive catalytic subunits, SMARCA2 and SMARCA4, which both contain a bromodomain and an ATPase domain. Using RNAi, cancer-specific vulnerabilities have been identified in SWI/SNF-mutant tumors, including SMARCA4-deficient lung cancer; however, the contribution of conserved, druggable protein domains to this anticancer phenotype is unknown. Here, we functionally deconstruct the SMARCA2/4 paralog dependence of cancer cells using bioinformatics, genetic, and pharmacologic tools. We evaluate a selective SMARCA2/4 bromodomain inhibitor (PFI-3) and characterize its activity in chromatin-binding and cell-functional assays focusing on cells with altered SWI/SNF complex (e.g., lung, synovial sarcoma, leukemia, and rhabdoid tumors). We demonstrate that PFI-3 is a potent, cell-permeable probe capable of displacing ectopically expressed, GFP-tagged SMARCA2-bromodomain from chromatin, yet contrary to target knockdown, the inhibitor fails to display an antiproliferative phenotype. Mechanistically, the lack of pharmacologic efficacy is reconciled by the failure of bromodomain inhibition to displace endogenous, full-length SMARCA2 from chromatin as determined by in situ cell extraction, chromatin immunoprecipitation, and target gene expression studies. Furthermore, using inducible RNAi and cDNA complementation (bromodomain- and ATPase-dead constructs), we unequivocally identify the ATPase domain, and not the bromodomain of SMARCA2, as the relevant therapeutic target with the catalytic activity suppressing defined transcriptional programs. Taken together, our complementary genetic and pharmacologic studies exemplify a general strategy for multidomain protein drug-target validation and in case of SMARCA2/4 highlight the potential for drugging the more challenging helicase/ATPase domain to deliver on the promise of synthetic-lethality therapy. Cancer Res; 75(18); 3865–78. ©2015 AACR.
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“In all cases, the targeted proteins also harbored multiple other functional domains and are often participating in intricate protein–protein interactions that appeared to be bromodomain independent.”
From Advancing Targeted Protein Degradation via Multiomics Profiling and Artificial Intelligence (2023) · cites this paper as [21]
In the citing paper
“While these efforts culminated in potent, specific, and well-characterized ligands for the individual bromodomains, ensuing functional analyses revealed that they are largely lacking cellular efficacy.21”
From Advancing Targeted Protein Degradation via Multiomics Profiling and Artificial Intelligence (2023) · cites this paper as [21]
In the citing paper
“However, such inhibitors have failed to inhibit tumor cell growth [48] because the ATPase domain but not the bromodomain is essential for tumor cell growth [169].”
From Proteolysis targeting chimeras (PROTACs) are emerging therapeutics for hematologic malignancies (2020) · cites this paper as [169]
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Metadata
- Authors
- Vangamudi, B., Paul, T. A., Shah, P. K., Kost-Alimova, M., Nottebaum, L., Shi, X., Zhan, Y., Leo, E., Mahadeshwar, H. S., Protopopov, A., Futreal, A., Tieu, T. N., Peoples, M., Heffernan, T. P., Marszalek, J. R., Toniatti, C., Petrocchi, A., Verhelle, D., Owen, D. R., Draetta, G., Jones, P., Palmer, W. S., Sharma, S., & Andersen, J. N.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- Pfizer (United States) (US)
- 1Institute for Applied Cancer Science, The University of Texas MD Anderson Cancer Center, Houston, Texas.
- 3Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, Texas.
- Corresponding author
- Sharma, Shikhar
- Andersen, Jannik N.
- ORCID
- Venue
- Cancer Research
- Published
- 2015-09-14
- Volume
- 75
- Issue
- 18
- Pages
- 3865-3878
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- PMC
- PMC4755107
- OpenAlex
- W2137511124
- Cited by
- 281
- References
- 50
- Citations by year
- 2026: 22 · 2025: 31 · 2024: 28 · 2023: 36 · 2022: 22 · 2021: 24 · 2020: 25 · 2019: 19 · 2018: 20 · 2017: 26 · 2016: 22 · 2015: 6
- FWCI
- 11.30
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- American Association for Cancer Research
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- National Cancer Institute (P30CA016672)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- 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
- Keywords
- SMARCA2, SMARCA4, SWI/SNF complex, ATPase domain, bromodomain, bromodomain inhibitors, drug target validation, synthetic lethality, chromatin binding, cDNA rescue, rhabdoid tumor, synovial sarcoma, leukemia, transcriptional programs, chromatin immunoprecipitation
- MeSH terms
- Binding, Competitive, Catalysis, Chromatin, Chromosomal Proteins, Non-Histone, DNA Helicases, Genetic Complementation Test, Humans, Lung Neoplasms, Neoplasm Proteins, Neoplasms, Nuclear Proteins, Pyridines, Sarcoma, Synovial, Transcription Factors, Protein Structure, Tertiary, DNA, Complementary, Rhabdoid Tumor, RNA Interference, RNA, Small Interfering, Chromatin Assembly and Disassembly, Cell Line, Tumor, Microarray Analysis, Azabicyclo Compounds, Gene Knockout Techniques, Molecular Targeted Therapy
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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