Cistrome Partitioning Reveals Convergence of Somatic Mutations and Risk Variants on Master Transcription Regulators in Primary Prostate Tumors

Cancer Cell - Tập 36 - Trang 674-689.e6 - 2019
Parisa Mazrooei1,2, Ken J. Kron1, Yanyun Zhu3, Stanley Zhou1,2, Giacomo Grillo1, Tahmid Mehdi1, Musaddeque Ahmed1, Tesa M. Severson3, Paul Guilhamon1, Nicholas Sinnott Armstrong4, Vincent Huang5, Takafumi N. Yamaguchi5, Michael Fraser1,5, Theodorus van der Kwast6, Paul C. Boutros2,5,7, Housheng Hansen He1,2, Andries M. Bergman3, Robert G. Bristow8, Wilbert Zwart3,9, Mathieu Lupien1,2,5
1Princess Margaret Cancer Centre, University Health Network, Toronto, ON, M5G 1L7, Canada
2Department of Medical Biophysics, University of Toronto, Toronto, ON M5G 1L7, Canada
3Division of Oncogenomics, Oncode Institute, The Netherlands Cancer Institute, Amsterdam, The Netherlands
4Department of Genetics, Stanford University, Stanford, CA 94305, USA
5Ontario Institute for Cancer Research, Toronto, ON M5G 0A3, Canada
6Department of Pathology and Laboratory Medicine, Toronto General Hospital, University Health Network, Toronto, ON M5G 2C4, Canada
7Department of Pharmacology and Toxicology, University of Toronto, Toronto, ON M5S 1A8, Canada
8CRUK Manchester Institute and Manchester Cancer Research Centre, University of Manchester, Manchester M20 4GJ, UK
9Laboratory of Chemical Biology and Institute for Complex Molecular Systems, Department of Biomedical Engineering, Eindhoven University of Technology, PO Box 513, 5600 MB Eindhoven, The Netherlands

Tài liệu tham khảo

Adamo, 2016, The oncogene ERG: a key factor in prostate cancer, Oncogene, 35, 403, 10.1038/onc.2015.109 Ahmadiyeh, 2010, 8q24 prostate, breast, and colon cancer risk loci show tissue-specific long-range interaction with MYC, Proc. Natl. Acad. Sci. U S A, 107, 9742, 10.1073/pnas.0910668107 Ahmed, 2017, Variant Set Enrichment: an R package to identify disease-associated functional genomic regions, BioData Min, 10, 9, 10.1186/s13040-017-0129-5 Al Olama, 2009, Multiple loci on 8q24 associated with prostate cancer susceptibility, Nat. Genet., 41, 1058, 10.1038/ng.452 Amundadottir, 2006, A common variant associated with prostate cancer in European and African populations, Nat. Genet., 38, 652, 10.1038/ng1808 Baca, 2013, Punctuated evolution of prostate cancer genomes, Cell, 153, 666, 10.1016/j.cell.2013.03.021 Bailey, 2015, ZNF143 provides sequence specificity to secure chromatin interactions at gene promoters, Nat. Commun., 2, 6186, 10.1038/ncomms7186 Bailey, 2016, Noncoding somatic and inherited single-nucleotide variants converge to promote ESR1 expression in breast cancer, Nat. Genet., 48, 1260, 10.1038/ng.3650 Barbieri, 2012, Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer, Nat. Genet., 44, 685, 10.1038/ng.2279 Brechka, 2017, HOXB13 mutations and binding partners in prostate development and cancer: function, clinical significance, and future directions, Genes Dis., 4, 75, 10.1016/j.gendis.2017.01.003 Cairns, 1997, Frequent inactivation of PTEN/MMAC1 in primary prostate cancer, Cancer Res., 57, 4997 Cancer Genome Atlas Research Network, 2015, The molecular taxonomy of primary prostate cancer, Cell, 163, 1011, 10.1016/j.cell.2015.10.025 Chen, 2015, Systematic enrichment analysis of potentially functional regions for 103 prostate cancer risk-associated loci, Prostate, 75, 1264, 10.1002/pros.23008 Chen, 2019, Widespread and functional RNA circularization in localized prostate cancer, Cell, 176, 831, 10.1016/j.cell.2019.01.025 Chung, 2011, Association of a novel long non-coding RNA in 8q24 with prostate cancer susceptibility, Cancer Sci., 102, 245, 10.1111/j.1349-7006.2010.01737.x Copeland, 2018, The androgen receptor malignancy shift in prostate cancer, Prostate, 78, 521, 10.1002/pros.23497 Cowper-Sal-lari, 2012, Breast cancer risk-associated SNPs modulate the affinity of chromatin for FOXA1 and alter gene expression, Nat. Genet., 44, 1191, 10.1038/ng.2416 Culig, 2014, Androgen receptor signaling in prostate cancer, Cancer Metastasis Rev., 33, 413, 10.1007/s10555-013-9474-0 Dubois-Chevalier, 2018, Organizing combinatorial transcription factor recruitment at cis-regulatory modules, Transcription, 9, 233, 10.1080/21541264.2017.1394424 Dubois-Chevalier, 2017, The logic of transcriptional regulator recruitment architecture at cis-regulatory modules controlling liver functions, Genome Res., 27, 985, 10.1101/gr.217075.116 Economides, 2003, Hoxb13 is required for normal differentiation and secretory function of the ventral prostate, Development, 130, 2061, 10.1242/dev.00432 2011, A user’s guide to the encyclopedia of DNA elements (ENCODE), PLoS Biol., 9, e1001046, 10.1371/journal.pbio.1001046 Ernst, 2011, Mapping and analysis of chromatin state dynamics in nine human cell types, Nature, 473, 43, 10.1038/nature09906 Espiritu, 2018, The evolutionary landscape of localized prostate cancers drives clinical aggression, Cell, 173, 1003, 10.1016/j.cell.2018.03.029 Francis, 2018, SOX9 is a driver of aggressive prostate cancer by promoting invasion, cell fate and cytoskeleton alterations and epithelial to mesenchymal transition, Oncotarget, 9, 7604, 10.18632/oncotarget.24123 Fraser, 2017, Genomic hallmarks of localized, non-indolent prostate cancer, Nature, 541, 359, 10.1038/nature20788 Friedman, 2006, The Foxa family of transcription factors in development and metabolism, Cell. Mol. Life Sci., 63, 2317, 10.1007/s00018-006-6095-6 Gelfman, 2017, Annotating pathogenic non-coding variants in genic regions, Nat. Commun., 8, 236, 10.1038/s41467-017-00141-2 Georgakopoulos-Soares, 2017, MPRAnator: a web-based tool for the design of massively parallel reporter assay experiments, Bioinformatics, 33, 137, 10.1093/bioinformatics/btw584 Gerhardt, 2012, FOXA1 promotes tumor progression in prostate cancer and represents a novel hallmark of castration-resistant prostate cancer, Am. J. Pathol., 180, 848, 10.1016/j.ajpath.2011.10.021 Ghoussaini, 2014, Evidence that breast cancer risk at the 2q35 locus is mediated through IGFBP5 regulation, Nat. Commun., 4, 4999, 10.1038/ncomms5999 Gudmundsson, 2007, Genome-wide association study identifies a second prostate cancer susceptibility variant at 8q24, Nat. Genet., 39, 631, 10.1038/ng1999 Guo, 2016, Modulation of long noncoding RNAs by risk SNPs underlying genetic predispositions to prostate cancer, Nat. Genet., 48, 1142, 10.1038/ng.3637 Hawksworth, 2010, Overexpression of C-MYC oncogene in prostate cancer predicts biochemical recurrence, Prostate Cancer Prostatic Dis., 13, 311, 10.1038/pcan.2010.31 He, 2010, Nucleosome dynamics define transcriptional enhancers, Nat. Genet., 42, 343, 10.1038/ng.545 Heinlein, 2004, Androgen receptor in prostate cancer, Endocr. Rev., 25, 276, 10.1210/er.2002-0032 Heintzman, 2007, Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome, Nat. Genet., 39, 311, 10.1038/ng1966 Heintzman, 2009, Histone modifications at human enhancers reflect global cell-type-specific gene expression, Nature, 459, 108, 10.1038/nature07829 Heinz, 2010, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities, Mol. Cell, 38, 576, 10.1016/j.molcel.2010.05.004 Horn, 2013, TERT promoter mutations in familial and sporadic melanoma, Science, 339, 959, 10.1126/science.1230062 Hu, 2017, Dynamic maps of UV damage formation and repair for the human genome, Proc. Natl. Acad. Sci. U S A, 114, 6758, 10.1073/pnas.1706522114 Huang, 2013, Highly recurrent TERT promoter mutations in human melanoma, Science, 339, 957, 10.1126/science.1229259 Huang, 2014, A prostate cancer susceptibility allele at 6q22 increases RFX6 expression by modulating HOXB13 chromatin binding, Nat. Genet., 46, 126, 10.1038/ng.2862 Jenkins, 1997, Detection of c-myc oncogene amplification and chromosomal anomalies in metastatic prostatic carcinoma by fluorescence in situ hybridization, Cancer Res., 57, 524 Jozwik, 2012, Pioneer factors in hormone-dependent cancers, Nat. Rev. Cancer, 12, 381, 10.1038/nrc3263 Katainen, 2015, CTCF/cohesin-binding sites are frequently mutated in cancer, Nat. Genet., 47, 818, 10.1038/ng.3335 Kiemeney, 2008, Sequence variant on 8q24 confers susceptibility to urinary bladder cancer, Nat. Genet., 40, 1307, 10.1038/ng.229 Killela, 2013, TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal, Proc. Natl. Acad. Sci. U S A, 110, 6021, 10.1073/pnas.1303607110 Kim, 2016, Chromatin structure–based prediction of recurrent noncoding mutations in cancer, Nat. Genet., 48, 1321, 10.1038/ng.3682 Kim, 2014, HOXB13 downregulates intracellular zinc and increases NF-κB signaling to promote prostate cancer metastasis, Oncogene, 33, 4558, 10.1038/onc.2013.404 Koivisto, 1997, Androgen receptor gene amplification: a possible molecular mechanism for androgen deprivation therapy failure in prostate cancer, Cancer Res., 57, 314 Korhonen, 2009, MOODS: fast search for position weight matrix matches in DNA sequences, Bioinformatics, 25, 3181, 10.1093/bioinformatics/btp554 Kron, 2014, Enhancer alterations in cancer: a source for a cell identity crisis, Genome Med., 6, 77, 10.1186/s13073-014-0077-3 Kron, 2017, TMPRSS2-ERG fusion co-opts master transcription factors and activates NOTCH signaling in primary prostate cancer, Nat. Genet., 49, 1336, 10.1038/ng.3930 Li, 2004, Genotyping with TaqMAMA, Genomics, 83, 311, 10.1016/j.ygeno.2003.08.005 Lin, 2016, Active medulloblastoma enhancers reveal subgroup-specific cellular origins, Nature, 530, 57, 10.1038/nature16546 Liu, 2006, Contrasting effects of phosphatidylinositol- and phosphatidylcholine-specific phospholipase C on apoptosis in cultured endothelial cells, Endothelium, 13, 205, 10.1080/10623320600760423 Lupien, 2009, Cistromics of hormone-dependent cancer, Endocr. Relat. Cancer, 16, 381, 10.1677/ERC-09-0038 Lupien, 2008, FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription, Cell, 132, 958, 10.1016/j.cell.2008.01.018 Lupien, 2010, Growth factor stimulation induces a distinct ER(alpha) cistrome underlying breast cancer endocrine resistance, Genes Dev., 24, 2219, 10.1101/gad.1944810 Ma, 2016, SOX9 drives WNT pathway activation in prostate cancer, J. Clin. Invest., 126, 1745, 10.1172/JCI78815 Mack, 2018, Therapeutic targeting of ependymoma as informed by oncogenic enhancer profiling, Nature, 553, 101, 10.1038/nature25169 McFarland, 2018, Improved estimation of cancer dependencies from large-scale RNAi screens using model-based normalization and data integration, Nat. Commun., 9, 4610, 10.1038/s41467-018-06916-5 Melnikov, 2012, Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay, Nat. Biotechnol., 30, 271, 10.1038/nbt.2137 Melnikov, 2014, Massively parallel reporter assays in cultured mammalian cells, J. Vis. Exp., 90, e51719 Melton, 2015, Recurrent somatic mutations in regulatory regions of human cancer genomes, Nat. Genet., 47, 710, 10.1038/ng.3332 Mularoni, 2016, OncodriveFML: a general framework to identify coding and non-coding regions with cancer driver mutations, Genome Biol., 17, 128, 10.1186/s13059-016-0994-0 Nakagawa, 2013, Prostate cancer genomics by high-throughput technologies: genome-wide association study and sequencing analysis, Endocr. Relat. Cancer, 20, R171, 10.1530/ERC-13-0113 Nault, 2013, High frequency of telomerase reverse-transcriptase promoter somatic mutations in hepatocellular carcinoma and preneoplastic lesions, Nat. Commun., 4, 2218, 10.1038/ncomms3218 Northcott, 2014, Enhancer hijacking activates GFI1 family oncogenes in medulloblastoma, Nature, 511, 428, 10.1038/nature13379 Pasqualucci, 2003, Mutations of the BCL6 proto-oncogene disrupt its negative autoregulation in diffuse large B-cell lymphoma, Blood, 101, 2914, 10.1182/blood-2002-11-3387 Pfeifer, 1992, Binding of transcription factors creates hot spots for UV photoproducts in vivo, Mol. Cell. Biol., 12, 1798, 10.1128/MCB.12.4.1798 Polak, 2015, Cell-of-origin chromatin organization shapes the mutational landscape of cancer, Nature, 518, 360, 10.1038/nature14221 Pomerantz, 2015, The androgen receptor cistrome is extensively reprogrammed in human prostate tumorigenesis, Nat. Genet., 47, 1346, 10.1038/ng.3419 Poulos, 2016, Functional mutations form at CTCF-cohesin binding sites in melanoma due to uneven nucleotide excision repair across the motif, Cell Rep., 17, 2865, 10.1016/j.celrep.2016.11.055 Prensner, 2011, Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression, Nat. Biotechnol., 29, 742, 10.1038/nbt.1914 Quinlan, 2010, BEDTools: a flexible suite of utilities for comparing genomic features, Bioinformatics, 26, 841, 10.1093/bioinformatics/btq033 Robinson, 2015, Integrative clinical genomics of advanced prostate cancer, Cell, 161, 1215, 10.1016/j.cell.2015.05.001 Robinson, 2014, Elevated levels of FOXA1 facilitate androgen receptor chromatin binding resulting in a CRPC-like phenotype, Oncogene, 33, 5666, 10.1038/onc.2013.508 Sabarinathan, 2016, Nucleotide excision repair is impaired by binding of transcription factors to DNA, Nature, 532, 264, 10.1038/nature17661 Sallari, 2017, Convergence of dispersed regulatory mutations predicts driver genes in prostate cancer, BioRxiv Schones, 2008, Dynamic regulation of nucleosome positioning in the human genome, Cell, 132, 887, 10.1016/j.cell.2008.02.022 Schumacher, 2018, Association analyses of more than 140,000 men identify 63 new prostate cancer susceptibility loci, Nat. Genet., 50, 928, 10.1038/s41588-018-0142-8 Severson, 2018, Characterizing steroid hormone receptor chromatin binding landscapes in male and female breast cancer, Nat. Commun., 9, 482, 10.1038/s41467-018-02856-2 Shin, 2009, CEAS: cis-regulatory element annotation system, Bioinformatics, 25, 2605, 10.1093/bioinformatics/btp479 Stelloo, 2018, Endogenous androgen receptor proteomic profiling reveals genomic subcomplex involved in prostate tumorigenesis, Oncogene, 37, 313, 10.1038/onc.2017.330 Taplin, 1995, Mutation of the androgen-receptor gene in metastatic androgen-independent prostate cancer, N. Engl. J. Med., 332, 1393, 10.1056/NEJM199505253322101 Thomsen, 2010, SOX9 elevation in the prostate promotes proliferation and cooperates with PTEN loss to drive tumor formation, Cancer Res., 70, 979, 10.1158/0008-5472.CAN-09-2370 Tomlins, 2005, Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer, Science, 310, 644, 10.1126/science.1117679 Tomlinson, 2007, A genome-wide association scan of tag SNPs identifies a susceptibility variant for colorectal cancer at 8q24.21, Nat. Genet., 39, 984, 10.1038/ng2085 Ulirsch, 2016, Systematic functional dissection of common genetic variation affecting red blood cell traits, Cell, 165, 1530, 10.1016/j.cell.2016.04.048 Umer, 2016, A significant regulatory mutation burden at a high-affinity position of the CTCF motif in gastrointestinal cancers, Hum. Mutat., 37, 904, 10.1002/humu.23014 Valouev, 2011, Determinants of nucleosome organization in primary human cells, Nature, 474, 516, 10.1038/nature10002 Vinagre, 2013, Frequency of TERT promoter mutations in human cancers, Nat. Commun., 4, 2185, 10.1038/ncomms3185 Wang, 2007, SOX9 is expressed in normal prostate basal cells and regulates androgen receptor expression in prostate cancer cells, Cancer Res., 67, 528, 10.1158/0008-5472.CAN-06-1672 Wang, 2008, SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion, Cancer Res., 68, 1625, 10.1158/0008-5472.CAN-07-5915 Ward, 2012, HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants, Nucleic Acids Res., 40, D930, 10.1093/nar/gkr917 Wasserman, 2010, An 8q24 gene desert variant associated with prostate cancer risk confers differential in vivo activity to a MYC enhancer, Genome Res., 20, 1191, 10.1101/gr.105361.110 Weinhold, 2014, Genome-wide analysis of noncoding regulatory mutations in cancer, Nat. Genet., 46, 1160, 10.1038/ng.3101 Weirauch, 2014, Determination and inference of eukaryotic transcription factor sequence specificity, Cell, 158, 1431, 10.1016/j.cell.2014.08.009 Xu, 2017, Long non-coding RNA PCAT-1 contributes to tumorigenesis by regulating FSCN1 via miR-145-5p in prostate cancer, Biomed. Pharmacother., 95, 1112, 10.1016/j.biopha.2017.09.019 Zabalza, 2015, HOXB13 overexpression is an independent predictor of early PSA recurrence in prostate cancer treated by radical prostatectomy, Oncotarget, 6, 12822, 10.18632/oncotarget.3431 Zhang, 2018, A global transcriptional network connecting noncoding mutations to changes in tumor gene expression, Nat. Genet., 50, 613, 10.1038/s41588-018-0091-2 Zhang, 2012, Integrative functional genomics identifies an enhancer looping to the SOX9 gene disrupted by the 17q24.3 prostate cancer risk locus, Genome Res., 22, 1437, 10.1101/gr.135665.111 Zhang, 2014, Laying a solid foundation for Manhattan – “setting the functional basis for the post-GWAS era, Trends Genet., 30, 140, 10.1016/j.tig.2014.02.006 Zhang, 2008, Model-based analysis of ChIP-seq (MACS), Genome Biol., 9, R137, 10.1186/gb-2008-9-9-r137 Zhou, 2016, Emergence of the noncoding cancer genome: a target of genetic and epigenetic alterations, Cancer Discov., 6, 1215, 10.1158/2159-8290.CD-16-0745