Functional Enhancers Shape Extrachromosomal Oncogene Amplifications

Non-coding regions amplified beyond oncogene borders have largely been ignored. Using a computational approach, we find signatures of significant co-amplification of non-coding DNA beyond the boundaries of amplified oncogenes across five cancer types. In glioblastoma, EGFR is preferentially co-ampli...

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Vydané v:	Cell Ročník 179; číslo 6; s. 1330
Hlavní autori:	Morton, Andrew R, Dogan-Artun, Nergiz, Faber, Zachary J, MacLeod, Graham, Bartels, Cynthia F, Piazza, Megan S, Allan, Kevin C, Mack, Stephen C, Wang, Xiuxing, Gimple, Ryan C, Wu, Qiulian, Rubin, Brian P, Shetty, Shashirekha, Angers, Stephane, Dirks, Peter B, Sallari, Richard C, Lupien, Mathieu, Rich, Jeremy N, Scacheri, Peter C
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States 27.11.2019
Predmet:	Acetylation Cell Line, Tumor Cell Survival - genetics Chromatin - metabolism Chromosomes, Human - genetics CRISPR-Cas Systems - genetics DNA, Neoplasm - genetics Enhancer Elements, Genetic ErbB Receptors - genetics ErbB Receptors - metabolism Gene Amplification Genes, Neoplasm Genetic Loci Glioblastoma - genetics Glioblastoma - pathology Histones - metabolism Humans Neuroglia - metabolism Oncogenes enhancer MYCN double minute glioblastoma epigenetic MYC oncogene amplification extrachromosomal DNA EGFR
ISSN:	1097-4172, 1097-4172
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Abstract	Non-coding regions amplified beyond oncogene borders have largely been ignored. Using a computational approach, we find signatures of significant co-amplification of non-coding DNA beyond the boundaries of amplified oncogenes across five cancer types. In glioblastoma, EGFR is preferentially co-amplified with its two endogenous enhancer elements active in the cell type of origin. These regulatory elements, their contacts, and their contribution to cell fitness are preserved on high-level circular extrachromosomal DNA amplifications. Interrogating the locus with a CRISPR interference screening approach reveals a diversity of additional elements that impact cell fitness. The pattern of fitness dependencies mirrors the rearrangement of regulatory elements and accompanying rewiring of the chromatin topology on the extrachromosomal amplicon. Our studies indicate that oncogene amplifications are shaped by regulatory dependencies in the non-coding genome.
AbstractList	Non-coding regions amplified beyond oncogene borders have largely been ignored. Using a computational approach, we find signatures of significant co-amplification of non-coding DNA beyond the boundaries of amplified oncogenes across five cancer types. In glioblastoma, EGFR is preferentially co-amplified with its two endogenous enhancer elements active in the cell type of origin. These regulatory elements, their contacts, and their contribution to cell fitness are preserved on high-level circular extrachromosomal DNA amplifications. Interrogating the locus with a CRISPR interference screening approach reveals a diversity of additional elements that impact cell fitness. The pattern of fitness dependencies mirrors the rearrangement of regulatory elements and accompanying rewiring of the chromatin topology on the extrachromosomal amplicon. Our studies indicate that oncogene amplifications are shaped by regulatory dependencies in the non-coding genome. Non-coding regions amplified beyond oncogene borders have largely been ignored. Using a computational approach, we find signatures of significant co-amplification of non-coding DNA beyond the boundaries of amplified oncogenes across five cancer types. In glioblastoma, EGFR is preferentially co-amplified with its two endogenous enhancer elements active in the cell type of origin. These regulatory elements, their contacts, and their contribution to cell fitness are preserved on high-level circular extrachromosomal DNA amplifications. Interrogating the locus with a CRISPR interference screening approach reveals a diversity of additional elements that impact cell fitness. The pattern of fitness dependencies mirrors the rearrangement of regulatory elements and accompanying rewiring of the chromatin topology on the extrachromosomal amplicon. Our studies indicate that oncogene amplifications are shaped by regulatory dependencies in the non-coding genome.Non-coding regions amplified beyond oncogene borders have largely been ignored. Using a computational approach, we find signatures of significant co-amplification of non-coding DNA beyond the boundaries of amplified oncogenes across five cancer types. In glioblastoma, EGFR is preferentially co-amplified with its two endogenous enhancer elements active in the cell type of origin. These regulatory elements, their contacts, and their contribution to cell fitness are preserved on high-level circular extrachromosomal DNA amplifications. Interrogating the locus with a CRISPR interference screening approach reveals a diversity of additional elements that impact cell fitness. The pattern of fitness dependencies mirrors the rearrangement of regulatory elements and accompanying rewiring of the chromatin topology on the extrachromosomal amplicon. Our studies indicate that oncogene amplifications are shaped by regulatory dependencies in the non-coding genome.
Author	Piazza, Megan S Morton, Andrew R Gimple, Ryan C Bartels, Cynthia F Allan, Kevin C Scacheri, Peter C Lupien, Mathieu Wu, Qiulian Sallari, Richard C Angers, Stephane Rich, Jeremy N Rubin, Brian P Shetty, Shashirekha MacLeod, Graham Faber, Zachary J Dirks, Peter B Wang, Xiuxing Dogan-Artun, Nergiz Mack, Stephen C
Author_xml	– sequence: 1 givenname: Andrew R surname: Morton fullname: Morton, Andrew R organization: Department of Genetics and Genome Sciences, Case Western Reserve University School of Medicine, Case Comprehensive Cancer Center, Cleveland, OH 44106, USA – sequence: 2 givenname: Nergiz surname: Dogan-Artun fullname: Dogan-Artun, Nergiz organization: Princess Margaret Cancer Centre, University Health Network, Toronto, ON M5G 1L7, Canada – sequence: 3 givenname: Zachary J surname: Faber fullname: Faber, Zachary J organization: Department of Genetics and Genome Sciences, Case Western Reserve University School of Medicine, Case Comprehensive Cancer Center, Cleveland, OH 44106, USA – sequence: 4 givenname: Graham surname: MacLeod fullname: MacLeod, Graham organization: Leslie Dan Faculty of Pharmacy, University of Toronto, Toronto, ON M5S 3M2, Canada – sequence: 5 givenname: Cynthia F surname: Bartels fullname: Bartels, Cynthia F organization: Department of Genetics and Genome Sciences, Case Western Reserve University School of Medicine, Case Comprehensive Cancer Center, Cleveland, OH 44106, USA – sequence: 6 givenname: Megan S surname: Piazza fullname: Piazza, Megan S organization: Center for Human Genetics Laboratory, University Hospitals, Cleveland, OH 44106, USA – sequence: 7 givenname: Kevin C surname: Allan fullname: Allan, Kevin C organization: Department of Genetics and Genome Sciences, Case Western Reserve University School of Medicine, Case Comprehensive Cancer Center, Cleveland, OH 44106, USA – sequence: 8 givenname: Stephen C surname: Mack fullname: Mack, Stephen C organization: Department of Pediatrics, Division of Hematology and Oncology, Baylor College of Medicine, Texas Children's Hospital, Houston, TX 77030, USA – sequence: 9 givenname: Xiuxing surname: Wang fullname: Wang, Xiuxing organization: Department of Medicine, Division of Regenerative Medicine, University of California, San Diego, La Jolla, CA 92037, USA – sequence: 10 givenname: Ryan C surname: Gimple fullname: Gimple, Ryan C organization: Department of Medicine, Division of Regenerative Medicine, University of California, San Diego, La Jolla, CA 92037, USA; Department of Pathology, Case Western Reserve University, Cleveland, OH 44120, USA – sequence: 11 givenname: Qiulian surname: Wu fullname: Wu, Qiulian organization: Department of Medicine, Division of Regenerative Medicine, University of California, San Diego, La Jolla, CA 92037, USA – sequence: 12 givenname: Brian P surname: Rubin fullname: Rubin, Brian P organization: Departments of Anatomic Pathology and Molecular Genetics, Cleveland Clinic, Lerner Research Institute and Taussig Cancer Center, Cleveland, OH 44195, USA – sequence: 13 givenname: Shashirekha surname: Shetty fullname: Shetty, Shashirekha organization: Center for Human Genetics Laboratory, University Hospitals, Cleveland, OH 44106, USA – sequence: 14 givenname: Stephane surname: Angers fullname: Angers, Stephane organization: Leslie Dan Faculty of Pharmacy, University of Toronto, Toronto, ON M5S 3M2, Canada; Department of Biochemistry, Faculty of Medicine, University of Toronto, Toronto, ON M5G 0A4, Canada – sequence: 15 givenname: Peter B surname: Dirks fullname: Dirks, Peter B organization: Developmental and Stem Cell Biology Program and Arthur and Sonia Labatt Brain Tumour Research Centre, The Hospital for Sick Children, Toronto, ON M5G 0A4, Canada; Ontario Institute for Cancer Research, Toronto, ON M5G 0A3, Canada – sequence: 16 givenname: Richard C surname: Sallari fullname: Sallari, Richard C organization: Axiotl Inc., Tucson, AZ 85701, USA – sequence: 17 givenname: Mathieu surname: Lupien fullname: Lupien, Mathieu organization: Princess Margaret Cancer Centre, University Health Network, Toronto, ON M5G 1L7, Canada; Ontario Institute for Cancer Research, Toronto, ON M5G 0A3, Canada; Department of Medical Biophysics, University of Toronto, Toronto, ON M5S 1A8, Canada – sequence: 18 givenname: Jeremy N surname: Rich fullname: Rich, Jeremy N email: drjeremyrich@gmail.com organization: Department of Medicine, Division of Regenerative Medicine, University of California, San Diego, La Jolla, CA 92037, USA; Department of Neurosciences, University of California, San Diego, School of Medicine, La Jolla, CA 92037, USA. Electronic address: drjeremyrich@gmail.com – sequence: 19 givenname: Peter C surname: Scacheri fullname: Scacheri, Peter C email: pxs183@case.edu organization: Department of Genetics and Genome Sciences, Case Western Reserve University School of Medicine, Case Comprehensive Cancer Center, Cleveland, OH 44106, USA. Electronic address: pxs183@case.edu
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Snippet	Non-coding regions amplified beyond oncogene borders have largely been ignored. Using a computational approach, we find signatures of significant...
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SubjectTerms	Acetylation Cell Line, Tumor Cell Survival - genetics Chromatin - metabolism Chromosomes, Human - genetics CRISPR-Cas Systems - genetics DNA, Neoplasm - genetics Enhancer Elements, Genetic ErbB Receptors - genetics ErbB Receptors - metabolism Gene Amplification Genes, Neoplasm Genetic Loci Glioblastoma - genetics Glioblastoma - pathology Histones - metabolism Humans Neuroglia - metabolism Oncogenes
Title	Functional Enhancers Shape Extrachromosomal Oncogene Amplifications
URI	https://www.ncbi.nlm.nih.gov/pubmed/31761532 https://www.proquest.com/docview/2317967293
Volume	179
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