Super-enhancer acquisition drives oncogene expression in triple negative breast cancer
Triple Negative Breast Cancer (TNBC) is a heterogeneous disease lacking known molecular drivers and effective targeted therapies. Cytotoxic chemotherapy remains the mainstay of treatment for TNBCs, which have significantly poorer survival rates compared to other breast cancer subtypes. In addition t...
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| Published in | PloS one Vol. 15; no. 6; p. e0235343 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
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Public Library of Science
25.06.2020
Public Library of Science (PLoS) |
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| Abstract | Triple Negative Breast Cancer (TNBC) is a heterogeneous disease lacking known molecular drivers and effective targeted therapies. Cytotoxic chemotherapy remains the mainstay of treatment for TNBCs, which have significantly poorer survival rates compared to other breast cancer subtypes. In addition to changes within the coding genome, aberrant enhancer activity is a well-established contributor to tumorigenesis. Here we use H3K27Ac chromatin immunoprecipitation followed by sequencing (ChIP-Seq) to map the active cis-regulatory landscape in TNBC. We identify distinct disease subtypes associated with specific enhancer activity, and over 2,500 unique superenhancers acquired by tumor cells but absent from normal breast tissue. To identify potential actionable disease drivers, we probed the dependency on genes that associate with tumor-specific enhancers by CRISPR screening. In this way we identify a number of tumor-specific dependencies, including a previously uncharacterized dependency on the TGFβ pseudo-receptor BAMBI. |
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| AbstractList | Triple Negative Breast Cancer (TNBC) is a heterogeneous disease lacking known molecular drivers and effective targeted therapies. Cytotoxic chemotherapy remains the mainstay of treatment for TNBCs, which have significantly poorer survival rates compared to other breast cancer subtypes. In addition to changes within the coding genome, aberrant enhancer activity is a well-established contributor to tumorigenesis. Here we use H3K27Ac chromatin immunoprecipitation followed by sequencing (ChIP-Seq) to map the active cis-regulatory landscape in TNBC. We identify distinct disease subtypes associated with specific enhancer activity, and over 2,500 unique superenhancers acquired by tumor cells but absent from normal breast tissue. To identify potential actionable disease drivers, we probed the dependency on genes that associate with tumor-specific enhancers by CRISPR screening. In this way we identify a number of tumor-specific dependencies, including a previously uncharacterized dependency on the TGFβ pseudo-receptor BAMBI. Triple Negative Breast Cancer (TNBC) is a heterogeneous disease lacking known molecular drivers and effective targeted therapies. Cytotoxic chemotherapy remains the mainstay of treatment for TNBCs, which have significantly poorer survival rates compared to other breast cancer subtypes. In addition to changes within the coding genome, aberrant enhancer activity is a well-established contributor to tumorigenesis. Here we use H3K27Ac chromatin immunoprecipitation followed by sequencing (ChIP-Seq) to map the active cis-regulatory landscape in TNBC. We identify distinct disease subtypes associated with specific enhancer activity, and over 2,500 unique superenhancers acquired by tumor cells but absent from normal breast tissue. To identify potential actionable disease drivers, we probed the dependency on genes that associate with tumor-specific enhancers by CRISPR screening. In this way we identify a number of tumor-specific dependencies, including a previously uncharacterized dependency on the TGF[beta] pseudo-receptor BAMBI. |
| Audience | Academic |
| Author | Bainer, Russell Raisner, Ryan Benedetti, Kelli L Haverty, Peter M Gascoigne, Karen E |
| AuthorAffiliation | 2 Maze Therapeutics, South San Francisco, California, United States of America 3 Department of Bioinformatics, Genentech, Inc., South San Francisco, California, United States of America 1 Department of Discovery Oncology, Genentech, Inc., South San Francisco, California, United States of America 4 Department of Cell and Tissue Biology, University of California, San Francisco, California, United States of America Florida International University, UNITED STATES |
| AuthorAffiliation_xml | – name: 1 Department of Discovery Oncology, Genentech, Inc., South San Francisco, California, United States of America – name: 2 Maze Therapeutics, South San Francisco, California, United States of America – name: 3 Department of Bioinformatics, Genentech, Inc., South San Francisco, California, United States of America – name: Florida International University, UNITED STATES – name: 4 Department of Cell and Tissue Biology, University of California, San Francisco, California, United States of America |
| Author_xml | – sequence: 1 givenname: Ryan surname: Raisner fullname: Raisner, Ryan organization: Department of Discovery Oncology, Genentech, Inc., South San Francisco, California, United States of America – sequence: 2 givenname: Russell orcidid: 0000-0002-0830-7029 surname: Bainer fullname: Bainer, Russell organization: Maze Therapeutics, South San Francisco, California, United States of America – sequence: 3 givenname: Peter M surname: Haverty fullname: Haverty, Peter M organization: Department of Bioinformatics, Genentech, Inc., South San Francisco, California, United States of America – sequence: 4 givenname: Kelli L orcidid: 0000-0001-6330-2602 surname: Benedetti fullname: Benedetti, Kelli L organization: Department of Cell and Tissue Biology, University of California, San Francisco, California, United States of America – sequence: 5 givenname: Karen E orcidid: 0000-0002-9407-2982 surname: Gascoigne fullname: Gascoigne, Karen E organization: Department of Discovery Oncology, Genentech, Inc., South San Francisco, California, United States of America |
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| CitedBy_id | crossref_primary_10_1038_s41467_021_22445_0 crossref_primary_10_1093_nargab_lqac006 crossref_primary_10_1038_s41698_024_00529_6 crossref_primary_10_1016_j_heliyon_2024_e27727 crossref_primary_10_3390_cancers14184353 crossref_primary_10_1038_s41419_021_04060_5 crossref_primary_10_1101_gr_276313_121 crossref_primary_10_3390_cancers13143606 crossref_primary_10_1136_jitc_2023_007870 crossref_primary_10_3390_ijms231911680 crossref_primary_10_1016_j_csbj_2022_05_045 crossref_primary_10_1038_s41467_024_50071_z crossref_primary_10_1016_j_mtbio_2022_100450 crossref_primary_10_1186_s13058_021_01479_8 crossref_primary_10_3390_ijms25063103 crossref_primary_10_1016_j_celrep_2023_113564 crossref_primary_10_1186_s13059_022_02627_9 crossref_primary_10_1007_s13577_024_01091_w |
| Cites_doi | 10.1158/2159-8290.CD-17-0399 10.1093/bioinformatics/btq033 10.1016/j.cell.2013.09.053 10.1172/JCI45014 10.1016/j.cell.2013.03.035 10.1101/gr.226019.117 10.1073/pnas.1016071107 10.1016/j.cell.2013.03.036 10.1038/ncomms14400 10.1038/nature17987 10.1038/46794 10.1126/science.aav1898 10.1016/j.ccr.2013.11.003 |
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| Copyright | COPYRIGHT 2020 Public Library of Science 2020 Raisner et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2020 Raisner et al 2020 Raisner et al |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: I have read the journal's policy and the authors of this manuscript have the following competing interests: Ryan Raisner, Peter M Haverty, & Karen E Gascoigne are employees of Genentech and shareholders of Roche. This does not alter our adherence to PLOS ONE policies on sharing data and materials. |
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| SubjectTerms | Analysis Biology and Life Sciences Breast cancer Cell Line, Tumor Chemotherapy Chromatin Chromatin Immunoprecipitation CRISPR Cytotoxicity Dependence Development and progression Diagnosis Engineering and Technology Enhancer Elements, Genetic - genetics Enhancers Female Gene Editing Gene expression Gene Expression Regulation, Neoplastic Genetic aspects Genomes Histones - chemistry Histones - genetics Histones - metabolism Humans Immunoprecipitation Medicine and Health Sciences Membrane Proteins - genetics Membrane Proteins - metabolism Oncogenes Oncogenes - genetics RNA, Guide, CRISPR-Cas Systems - metabolism Survival Triple Negative Breast Neoplasms - genetics Triple Negative Breast Neoplasms - pathology Tumor cells Tumorigenesis Tumors |
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| Title | Super-enhancer acquisition drives oncogene expression in triple negative breast cancer |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/32584896 https://www.proquest.com/docview/2417365784/abstract/ https://search.proquest.com/docview/2418120711 https://pubmed.ncbi.nlm.nih.gov/PMC7316302 https://doaj.org/article/2eb954b511d14a9e8b98f36265b05fcc http://dx.doi.org/10.1371/journal.pone.0235343 |
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