Genomic and Molecular Landscape of DNA Damage Repair Deficiency across The Cancer Genome Atlas

Authors

Theo A. Knijnenburg, Institute for Systems Biology
Linghua Wang, University of Texas MD Anderson Cancer Center
Michael T. Zimmermann, Medical College of Wisconsin
Nyasha Chambwe, Institute for Systems Biology
Galen F. Gao, Massachusetts Institute of Technology
Andrew D. Cherniack, Massachusetts Institute of Technology
Huihui Fan, Van Andel Research Institute
Hui Shen, Van Andel Research Institute
Gregory P. Way, University of Pennsylvania Perelman School of Medicine
Casey S. Greene, University of Pennsylvania Perelman School of Medicine
Yuexin Liu, University of Texas MD Anderson Cancer Center
Rehan Akbani, University of Texas MD Anderson Cancer Center
Bin Feng, TESARO, Inc.
Lawrence A. Donehower, Baylor College of Medicine
Chase Miller, Baylor College of Medicine
Yang Shen, Texas A&M University
Mostafa Karimi, Texas A&M University
Haoran Chen, Texas A&M University
Pora Kim, University of Texas Health Science Center at Houston
Peilin Jia, University of Texas Health Science Center at Houston
Eve Shinbrot, Baylor College of Medicine
Shaojun Zhang, University of Texas MD Anderson Cancer Center
Jianfang Liu, Chan Soon-Shiong Institute of Molecular Medicine at Windber
Hai Hu, Chan Soon-Shiong Institute of Molecular Medicine at Windber
Matthew H. Bailey, Washington University in St. Louis
Christina Yau, University of California, San Francisco
Denise Wolf, University of California, San Francisco
Zhongming Zhao, University of Texas Health Science Center at Houston
John N. Weinstein, University of Texas MD Anderson Cancer Center
Lei Li, University of Texas MD Anderson Cancer Center
Li Ding, Washington University in St. Louis
Gordon B. Mills, University of Texas MD Anderson Cancer Center
Peter W. Laird, Van Andel Research Institute

Document Type

Journal Article

Publication Date

4-3-2018

Journal

Cell Reports

Volume

23

Issue

1

DOI

10.1016/j.celrep.2018.03.076

Keywords

DNA damage footprints; DNA damage repair; epigenetic silencing; integrative statistical analysis; mutational signatures; protein structure analysis; somatic copy-number alterations; somatic mutations; The Cancer Genome Atlas PanCanAtlas project

Abstract

© 2018 The Author(s) DNA damage repair (DDR) pathways modulate cancer risk, progression, and therapeutic response. We systematically analyzed somatic alterations to provide a comprehensive view of DDR deficiency across 33 cancer types. Mutations with accompanying loss of heterozygosity were observed in over 1/3 of DDR genes, including TP53 and BRCA1/2. Other prevalent alterations included epigenetic silencing of the direct repair genes EXO5, MGMT, and ALKBH3 in ∼20% of samples. Homologous recombination deficiency (HRD) was present at varying frequency in many cancer types, most notably ovarian cancer. However, in contrast to ovarian cancer, HRD was associated with worse outcomes in several other cancers. Protein structure-based analyses allowed us to predict functional consequences of rare, recurrent DDR mutations. A new machine-learning-based classifier developed from gene expression data allowed us to identify alterations that phenocopy deleterious TP53 mutations. These frequent DDR gene alterations in many human cancers have functional consequences that may determine cancer progression and guide therapy. Knijnenburg et al. present The Cancer Genome Atlas (TCGA) Pan-Cancer analysis of DNA damage repair (DDR) deficiency in cancer. They use integrative genomic and molecular analyses to identify frequent DDR alterations across 33 cancer types, correlate gene- and pathway-level alterations with genome-wide measures of genome instability and impaired function, and demonstrate the prognostic utility of DDR deficiency scores.

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