CP: Cancer; CRISPR screen; breast cancer; histone demethylase; mitochondrial signaling; Transcription Factors; DNA-Binding Proteins; KDM5A protein, human; ZBTB7A protein, human; Retinoblastoma-Binding Protein 2; Histones; NF-kappa B; Humans; Female; Cell Line, Tumor; Gene Regulatory Networks; Retinoblastoma-Binding Protein 2/metabolism; Retinoblastoma-Binding Protein 2/genetics; Histones/metabolism; Promoter Regions, Genetic/genetics; NF-kappa B/metabolism; Animals; Breast Neoplasms/genetics; Breast Neoplasms/pathology; Breast Neoplasms/metabolism; Transcription Factors/metabolism; Transcription Factors/genetics; DNA-Binding Proteins/metabolism; DNA-Binding Proteins/genetics; Gene Expression Regulation, Neoplastic; Breast Neoplasms; Promoter Regions, Genetic; Biochemistry, Genetics and Molecular Biology (all)
Abstract :
[en] We previously described that the KDM5B histone H3 lysine 4 demethylase is an oncogene in estrogen-receptor-positive breast cancer. Here, we report that KDM5A is amplified and overexpressed in basal breast tumors, and KDM5 inhibition (KDM5i) suppresses the growth of KDM5-amplified breast cancer cell lines. Using CRISPR knockout screens in a basal breast cancer cell line with or without KDM5i, we found that deletion of the ZBTB7A transcription factor and core SAGA complex sensitizes cells to KDM5i, whereas deletion of RHO-GTPases leads to resistance. Chromatin immunoprecipitation sequencing (ChIP-seq) and RNA sequencing (RNA-seq) revealed co-localization of ZBTB7A and KDM5A/B at promoters with high histone H3K4me3 and dependence of KDM5A chromatin binding on ZBTB7A. ZBTB7A knockout altered the transcriptional response to KDM5i at NF-κB targets and mitochondrion-related pathways. High expression of ZBTB7A in triple-negative breast cancer is significantly associated with poor response to neoadjuvant chemotherapy. Our work furthers the understanding of KDM5-mediated gene regulation and identifies mediators of sensitivity to KDM5i.
Disciplines :
Oncology
Author, co-author :
DiCiaccio, Benedetto; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA
Seehawer, Marco; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA
Li, Zheqi; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA
Patmanidis, Andriana; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA
Bui, Triet; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA
Foidart, Pierre ; Université de Liège - ULiège > Département des sciences cliniques ; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA
Nishida, Jun; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA
D'Santos, Clive S; Cambridge Research Institute, University of Cambridge, Cambridge, UK
Papachristou, Evangelia K; Cambridge Research Institute, University of Cambridge, Cambridge, UK
Papanastasiou, Malvina; The Eli and Edythe L. Broad Institute, Cambridge, MA 02142, USA
Reiter, Andrew H; The Eli and Edythe L. Broad Institute, Cambridge, MA 02142, USA
Qiu, Xintao; Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, MA 02215, USA
Li, Rong; Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, MA 02215, USA
Jiang, Yijia; Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, MA 02215, USA
Huang, Xiao-Yun; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA
Simeonov, Anton; National Center for Advancing Translational Sciences, National Institutes of Health, Bethesda, MD 20892, USA
Kales, Stephen C; National Center for Advancing Translational Sciences, National Institutes of Health, Bethesda, MD 20892, USA
Rai, Ganesha; National Center for Advancing Translational Sciences, National Institutes of Health, Bethesda, MD 20892, USA
Lal-Nag, Madhu; National Center for Advancing Translational Sciences, National Institutes of Health, Bethesda, MD 20892, USA
Jadhav, Ajit; National Center for Advancing Translational Sciences, National Institutes of Health, Bethesda, MD 20892, USA
Brown, Myles; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA
Carroll, Jason S; Cambridge Research Institute, University of Cambridge, Cambridge, UK
Long, Henry W; Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, MA 02215, USA
Polyak, Kornelia ; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA, Department of Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA, Department of Medicine, Harvard Medical School, Boston, MA 02115, USA, The Eli and Edythe L. Broad Institute, Cambridge, MA 02142, USA, Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Boston, MA 02215, USA, The Ludwig Center at Harvard, Boston, MA 02115, USA. Electronic address: kornelia_polyak@dfci.harvard.edu
NCI - National Cancer Institute NCATS - National Center for Advancing Translational Sciences NIH - National Institutes of Health
Funding text :
We thank members of our laboratories for their critical reading of the manuscript and useful discussions. We thank the Dana-Farber Cancer Institute Molecular Biology Core Facility for their outstanding sequencing service. This research was supported by National Cancer Institute R35 CA197623 (K.P.) and P01 CA250959 (K.P., H.W.L., and M.B.), by the Ludwig Center at Harvard (K.P.), and in part by the Intramural Research Program of the National Center for Advancing Translational Sciences (NCATS), National Institutes of Health (A.S., S.C.K., G.R., M.L.-N., and A.J). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.We thank members of our laboratories for their critical reading of the manuscript and useful discussions. We thank the Dana-Farber Cancer Institute Molecular Biology Core Facility for their outstanding sequencing service. This research was supported by National Cancer Institute R35 CA197623 (K.P.) and P01 CA250959 (K.P., H.W.L., and M.B.), by the Ludwig Center at Harvard (K.P.), and in part by the Intramural Research Program of the National Center for Advancing Translational Sciences ( NCATS ), National Institutes of Health (A.S., S.C.K., G.R., M.L.-N., D.J.M., and A.J). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health .
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