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Title: The topography of mutational processes in breast cancer genomes

Abstract

Somatic mutations in human cancers show unevenness in genomic distribution that correlate with aspects of genome structure and function. These mutations are, however, generated by multiple mutational processes operating through the cellular lineage between the fertilized egg and the cancer cell, each composed of specific DNA damage and repair components and leaving its own characteristic mutational signature on the genome. Using somatic mutation catalogues from 560 breast cancer whole-genome sequences, here we show that each of 12 base substitution, 2 insertion/deletion (indel) and 6 rearrangement mutational signatures present in breast tissue, exhibit distinct relationships with genomic features relating to transcription, DNA replication and chromatin organization. This signature-based approach permits visualization of the genomic distribution of mutational processes associated with APOBEC enzymes, mismatch repair deficiency and homologous recombinational repair deficiency, as well as mutational processes of unknown aetiology. Lastly, it highlights mechanistic insights including a putative replication-dependent mechanism of APOBEC-related mutagenesis.

Authors:
 [1];  [2];  [3];  [3];  [3];  [4];  [5];  [6];  [3];  [3];  [3];  [7];  [4];  [8];  [9];  [3]; ORCiD logo [10];  [11]; ORCiD logo [12];  [13] more »;  [14];  [6];  [15];  [5];  [16];  [17];  [7];  [18];  [19]; ORCiD logo [19];  [3];  [1];  [20] « less
+ Show Author Affiliations
  1. European Bioinformatics Institute, Cambridgeshire (United Kingdom)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Wellcome Trust Sanger Institute, Cambridge (United Kingdom)
  3. Wellcome Trust Sanger Institute, Cambridge (United Kingdom)
  4. Lund Univ., Lund (Sweden)
  5. Erasmus Univ. Medical Center, Rotterdam (The Netherlands)
  6. Radboud Univ., Nijmegen (The Netherlands)
  7. Hanyang Univ., Seoul (South Korea)
  8. Univ. Libre de Bruxelles, Brussels (Belgium)
  9. European Bioinformatics Institute, Cambridgeshire (United Kingdom); UT MD Anderson Cancer Center, Houston, TX (United States)
  10. Radboud Univ. Medical Center, Nijmegen (The Netherlands)
  11. Univ. of Antwerp, Antwerp (Belgium)
  12. Univ. of Queensland, Queensland (Australia); The Royal Brisbane and Women's Hospital, Queensland (Australia)
  13. Univ. of Iceland (Iceland)
  14. Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States); Univ. of Dundee, Dundee (United Kingdom)
  15. Academic Medical Center, Amsterdam (The Netherlands)
  16. Oslo Univ. Hospital, The Norwegian Radium Hospital, Oslo (Norway); Univ. of Oslo, Oslo (Norway)
  17. Brigham and Women's Hospital, Boston, MA (United States); Dana-Farber Cancer Institute, Boston, MA (United States)
  18. Centre Leon Berard, Lyon Cedex (France)
  19. MRC Lab. of Molecular Biology, Cambridge (United Kingdom)
  20. Wellcome Trust Sanger Institute, Cambridge (United Kingdom); Cambridge Univ. Hospitals NHS Foundation Trust, Cambridge (United Kingdom)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1256099
Report Number(s):
LA-UR-15-26421
Journal ID: ISSN 2041-1723
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biological Science

Citation Formats

Morganella, Sandro, Alexandrov, Ludmil B., Glodzik, Dominik, Zou, Xueqing, Davies, Helen, Staaf, Johan, Sieuwerts, Anieta M., Brinkman, Arie B., Martin, Sancha, Ramakrishna, Manasa, Butler, Adam, Kim, Hyung -Yong, Borg, Ake, Sotiriou, Christos, Futreal, P. Andrew, Campbell, Peter J., Span, Paul N., Van Laere, Steven, Lakhani, Sunil R., Eyfjord, Jorunn E., Thompson, Alastair M., Stunnenberg, Hendrik G., van de Vijver, Marc J., Martens, John W. M., Borresen-Dale, Anne -Lise, Richardson, Andrea L., Kong, Gu, Thomas, Gilles, Sale, Julian, Rada, Cristina, Stratton, Michael R., Birney, Ewan, and Nik-Zainal, Serena. The topography of mutational processes in breast cancer genomes. United States: N. p., 2016. Web. doi:10.1038/ncomms11383.
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Morganella, Sandro, Alexandrov, Ludmil B., Glodzik, Dominik, Zou, Xueqing, Davies, Helen, Staaf, Johan, Sieuwerts, Anieta M., Brinkman, Arie B., Martin, Sancha, Ramakrishna, Manasa, Butler, Adam, Kim, Hyung -Yong, Borg, Ake, Sotiriou, Christos, Futreal, P. Andrew, Campbell, Peter J., Span, Paul N., Van Laere, Steven, Lakhani, Sunil R., Eyfjord, Jorunn E., Thompson, Alastair M., Stunnenberg, Hendrik G., van de Vijver, Marc J., Martens, John W. M., Borresen-Dale, Anne -Lise, Richardson, Andrea L., Kong, Gu, Thomas, Gilles, Sale, Julian, Rada, Cristina, Stratton, Michael R., Birney, Ewan, & Nik-Zainal, Serena. The topography of mutational processes in breast cancer genomes. United States. https://doi.org/10.1038/ncomms11383
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Morganella, Sandro, Alexandrov, Ludmil B., Glodzik, Dominik, Zou, Xueqing, Davies, Helen, Staaf, Johan, Sieuwerts, Anieta M., Brinkman, Arie B., Martin, Sancha, Ramakrishna, Manasa, Butler, Adam, Kim, Hyung -Yong, Borg, Ake, Sotiriou, Christos, Futreal, P. Andrew, Campbell, Peter J., Span, Paul N., Van Laere, Steven, Lakhani, Sunil R., Eyfjord, Jorunn E., Thompson, Alastair M., Stunnenberg, Hendrik G., van de Vijver, Marc J., Martens, John W. M., Borresen-Dale, Anne -Lise, Richardson, Andrea L., Kong, Gu, Thomas, Gilles, Sale, Julian, Rada, Cristina, Stratton, Michael R., Birney, Ewan, and Nik-Zainal, Serena. Fri . "The topography of mutational processes in breast cancer genomes". United States. https://doi.org/10.1038/ncomms11383. https://www.osti.gov/servlets/purl/1256099.
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@article{osti_1256099,
title = {The topography of mutational processes in breast cancer genomes},
author = {Morganella, Sandro and Alexandrov, Ludmil B. and Glodzik, Dominik and Zou, Xueqing and Davies, Helen and Staaf, Johan and Sieuwerts, Anieta M. and Brinkman, Arie B. and Martin, Sancha and Ramakrishna, Manasa and Butler, Adam and Kim, Hyung -Yong and Borg, Ake and Sotiriou, Christos and Futreal, P. Andrew and Campbell, Peter J. and Span, Paul N. and Van Laere, Steven and Lakhani, Sunil R. and Eyfjord, Jorunn E. and Thompson, Alastair M. and Stunnenberg, Hendrik G. and van de Vijver, Marc J. and Martens, John W. M. and Borresen-Dale, Anne -Lise and Richardson, Andrea L. and Kong, Gu and Thomas, Gilles and Sale, Julian and Rada, Cristina and Stratton, Michael R. and Birney, Ewan and Nik-Zainal, Serena},
abstractNote = {Somatic mutations in human cancers show unevenness in genomic distribution that correlate with aspects of genome structure and function. These mutations are, however, generated by multiple mutational processes operating through the cellular lineage between the fertilized egg and the cancer cell, each composed of specific DNA damage and repair components and leaving its own characteristic mutational signature on the genome. Using somatic mutation catalogues from 560 breast cancer whole-genome sequences, here we show that each of 12 base substitution, 2 insertion/deletion (indel) and 6 rearrangement mutational signatures present in breast tissue, exhibit distinct relationships with genomic features relating to transcription, DNA replication and chromatin organization. This signature-based approach permits visualization of the genomic distribution of mutational processes associated with APOBEC enzymes, mismatch repair deficiency and homologous recombinational repair deficiency, as well as mutational processes of unknown aetiology. Lastly, it highlights mechanistic insights including a putative replication-dependent mechanism of APOBEC-related mutagenesis.},
doi = {10.1038/ncomms11383},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {Fri Jan 01 00:00:00 EST 2016},
month = {Fri Jan 01 00:00:00 EST 2016}
}
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https://doi.org/10.1038/ncomms11383
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journal, February 2015

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journal, December 2006

DNA replication timing and higher-order nuclear organization determine single-nucleotide substitution patterns in cancer genomes
journal, February 2013

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NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity
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  • Nature Communications, Vol. 4, Issue 1
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Human mutation rate associated with DNA replication timing
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journal, March 2008

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journal, December 2008

  • Hanawalt, Philip C.; Spivak, Graciela
  • Nature Reviews Molecular Cell Biology, Vol. 9, Issue 12
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Impact of chromatin structure on sequence variability in the human genome
journal, March 2011

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Molecular Combing of Single DNA Molecules on the 10 Megabase Scale
journal, January 2016

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Interplay between mismatch repair and chromatin assembly
journal, January 2012

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Fission yeast switches mating type by a replication-recombination coupled process
journal, March 2000

Principles and Concepts of DNA Replication in Bacteria, Archaea, and Eukarya
journal, July 2013

  • O'Donnell, M.; Langston, L.; Stillman, B.
  • Cold Spring Harbor Perspectives in Biology, Vol. 5, Issue 7
  • DOI: 10.1101/cshperspect.a010108

RNase-sensitive DNA modification(s) initiates S. pombe mating-type switching
journal, April 2004

Heterogeneous polymerase fidelity and mismatch repair bias genome variation and composition
journal, September 2014

  • Lujan, Scott A.; Clausen, Anders R.; Clark, Alan B.
  • Genome Research, Vol. 24, Issue 11
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The spatial and temporal organization of origin firing during the S-phase of fission yeast
journal, February 2015

Making Sense of Eukaryotic DNA Replication Origins
journal, October 2001

Break-Induced Replication Repair of Damaged Forks Induces Genomic Duplications in Human Cells
journal, December 2013

  • Costantino, Lorenzo; Sotiriou, Sotirios K.; Rantala, Juha K.
  • Science, Vol. 343, Issue 6166
  • DOI: 10.1126/science.1243211

The AID/APOBEC family of nucleic acid mutators
journal, January 2008

Controls of Nucleosome Positioning in the Human Genome
journal, November 2012

Good Timing in the Cell Cycle for Precise DNA Repair by BRCA1
journal, June 2005

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    Intragenomic variability and extended sequence patterns in the mutational signature of ultraviolet light
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    Mutational signatures are jointly shaped by DNA damage and repair
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    Learning mutational signatures and their multidimensional genomic properties with TensorSignatures
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    APOBEC3A/B-induced mutagenesis is responsible for 20% of heritable mutations in the TpCpW context
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    Somatic evolution and global expansion of an ancient transmissible cancer lineage
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    APOBEC mutation drives early-onset squamous cell carcinomas in recessive dystrophic epidermolysis bullosa
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    Within-Host Variations of Human Papillomavirus Reveal APOBEC Signature Mutagenesis in the Viral Genome
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    Chromatin loop anchors are associated with genome instability in cancer and recombination hotspots in the germline
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    Recurrent mutations at estrogen receptor binding sites alter chromatin topology and distal gene expression in breast cancer
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    Repair of multiple simultaneous double-strand breaks causes bursts of genome-wide clustered hypermutation
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    The APOBEC3 genes and their role in cancer: insights from human papillomavirus
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    Perturbations in the Replication Program Contribute to Genomic Instability in Cancer
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    Chromatin Dynamics in Genome Stability: Roles in Suppressing Endogenous DNA Damage and Facilitating DNA Repair
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    Perturbation of base excision repair sensitizes breast cancer cells to APOBEC3 deaminase-mediated mutations
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    Error-prone bypass of DNA lesions during lagging-strand replication is a common source of germline and cancer mutations
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    APOBEC3A/B-induced mutagenesis is responsible for 20% of heritable mutations in the TpCpW context
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    Computational approaches for discovery of mutational signatures in cancer
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    Polyomavirus T-Antigen Induces APOBEC3B Expression using a LXCXE-Dependent and TP53-Independent Mechanism
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    Network-based approaches elucidate differences within APOBEC and clock-like signatures in breast cancer
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    Landscape of somatic mutations in 560 breast cancer whole-genome sequences.
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    • Nik-Zainal, Serena; Davies, Helen; Staaf, Johan
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    HRDetect is a predictor of BRCA1 and BRCA2 deficiency based on mutational signatures.
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    • Davies, Helen; Glodzik, Dominik; Morganella, Sandro
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    Intratumor heterogeneity defines treatment-resistant HER2+ breast tumors.
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    The repertoire of mutational signatures in human cancer
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    Hidden Markov Models Lead to Higher Resolution Maps of Mutation Signature Activity in Cancer
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    Computational approaches for discovery of mutational signatures in cancer.
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    Validating the concept of mutational signatures with isogenic cell models.
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    A somatic-mutational process recurrently duplicates germline susceptibility loci and tissue-specific super-enhancers in breast cancers
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    Mutational signatures are jointly shaped by DNA damage and repair.
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    Intratumor heterogeneity defines treatment-resistant HER2+ breast tumors
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    Multimodal Assessment of Estrogen Receptor mRNA Profiles to Quantify Estrogen Pathway Activity in Breast Tumors
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    The genomics of oxidative DNA damage, repair, and resulting mutagenesis
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    ESR1 mutations: Moving towards guiding treatment decision-making in metastatic breast cancer patients
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    A Sticky Multinomial Mixture Model of Strand-Coordinated Mutational Processes in Cancer
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    Replication stress response in cancer stem cells as a target for chemotherapy
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    The DNA cytosine deaminase APOBEC3H haplotype I likely contributes to breast and lung cancer mutagenesis
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    Mismatch repair prefers exons
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    • Massey, Dashiell J.; Koren, Amnon
    • Nature Genetics, Vol. 49, Issue 12
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    Nuclear topology modulates the mutational landscapes of cancer genomes
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    Author Correction: Characterization of Nigerian breast cancer reveals prevalent homologous recombination deficiency and aggressive molecular features
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    Replication timing and epigenome remodelling are associated with the nature of chromosomal rearrangements in cancer
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    Partially methylated domains are hypervariable in breast cancer and fuel widespread CpG island hypermethylation
    journal, April 2019

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    journal, July 2019

    • Koedoot, Esmee; Fokkelman, Michiel; Rogkoti, Vasiliki-Maria
    • Nature Communications, Vol. 10, Issue 1
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    The Rad51 paralogs facilitate a novel DNA strand specific damage tolerance pathway
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    5-Fluorouracil treatment induces characteristic T>G mutations in human cancer
    journal, October 2019

    • Christensen, Sharon; Van der Roest, Bastiaan; Besselink, Nicolle
    • Nature Communications, Vol. 10, Issue 1
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    Breast cancers are rare diseases—and must be treated as such
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    The repertoire of mutational signatures in human cancer
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    Error-prone bypass of DNA lesions during lagging-strand replication is a common source of germline and cancer mutations
    journal, December 2018

    • Seplyarskiy, Vladimir B.; Akkuratov, Evgeny E.; Akkuratova, Natalia
    • Nature Genetics, Vol. 51, Issue 1
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    The genomic landscape of metastatic breast cancer highlights changes in mutation and signature frequencies
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    The evolution of hematopoietic cells under cancer therapy
    journal, October 2020

    Uncovering the signaling landscape controlling breast cancer cell migration identifies splicing factor PRPF4B as a metastasis driver
    journal, December 2018

    • Fokkelman, Michiel; Koedoot, Esmee; Rogkoti, Vasiliki-Maria
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    Intragenomic variability and extended sequence patterns in the mutational signature of ultraviolet light
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    • Lindberg, Markus; Boström, Martin; Elliott, Kerryn
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    Detection and genomic characterization of a mammary-like adenocarcinoma
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    • Grewal, Jasleen K.; Eirew, Peter; Jones, Martin
    • Molecular Case Studies, Vol. 3, Issue 6
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    DNA Repair Footprint Uncovers Contribution of DNA Repair Mechanism to Mutational Signatures
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    Reactivation of dormant anti-tumor immunity – a clinical perspective of therapeutic immune checkpoint modulation
    journal, January 2017

    • Greil, Richard; Hutterer, Evelyn; Hartmann, Tanja Nicole
    • Cell Communication and Signaling, Vol. 15, Issue 1
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    Mutational signature distribution varies with DNA replication timing and strand asymmetry
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    Recurrent mutations at estrogen receptor binding sites alter chromatin topology and distal gene expression in breast cancer
    journal, November 2018

    Hidden Markov models lead to higher resolution maps of mutation signature activity in cancer
    journal, July 2019

    APOBEC3A is a prominent cytidine deaminase in breast cancer
    journal, December 2019

    Progressive APOBEC3B mRNA expression in distant breast cancer metastases
    journal, January 2017

    Validating the concept of mutational signatures with isogenic cell models.
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    • Zou, Xueqing; Owusu, Michel; Harris, Rebecca
    • Apollo - University of Cambridge Repository
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    From genome integrity to cancer.
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    DNA Repair Pathway Alterations in Bladder Cancer
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    Risks at the DNA Replication Fork: Effects upon Carcinogenesis and Tumor Heterogeneity
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    Perturbations in the Replication Program Contribute to Genomic Instability in Cancer
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    • Blumenfeld, Britny; Ben-Zimra, Micha; Simon, Itamar
    • International Journal of Molecular Sciences, Vol. 18, Issue 6
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    Chromatin Dynamics in Genome Stability: Roles in Suppressing Endogenous DNA Damage and Facilitating DNA Repair
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    • Nair, Nidhi; Shoaib, Muhammad; Sørensen, Claus Storgaard
    • International Journal of Molecular Sciences, Vol. 18, Issue 7
    • DOI: 10.3390/ijms18071486
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