Spatial genomic heterogeneity within localized, multifocal prostate cancer

Nature Genetics

Volumn 47, Issue 7, 2015, Pages 736-745

  Boutros, Paul C ^a,b,c   Fraser, Michael ^d   Harding, Nicholas J ^a   De Borja, Richard ^a   Trudel, Dominique ^e   Lalonde, Emilie ^a,b   Meng, Alice ^c   Hennings Yeomans, Pablo H ^a   McPherson, Andrew ^f   Sabelnykova, Veronica Y ^a   Zia, Amin ^a   Fox, Natalie S ^a,b   Livingstone, Julie ^a   Shiah, Yu Jia ^a   Wang, Jianxin ^a   Beck, Timothy A ^a   Have, Cherry L ^e   Chong, Taryne ^a   Sam, Michelle ^a   Johns, Jeremy ^a   Timms, Lee ^a   Buchner, Nicholas ^a   Wong, Ada ^a   Watson, John D ^a   Simmons, Trent T ^a   P'ng, Christine ^a   Zafarana, Gaetano ^d   Nguyen, Francis ^a   Luo, Xuemei ^a   Chu, Kenneth C ^a   Prokopec, Stephenie D ^a   Sykes, Jenna ^d   Pra, Alan Dal ^b   Berlin, Alejandro ^b   Brown, Andrew ^a   Chan Seng Yue, Michelle A ^a   Yousif, Fouad ^a   Denroche, Robert E ^a   Chong, Lauren C ^a   Chen, Gregory M ^a   Jung, Esther ^a   Fung, Clement ^a   Starmans, Maud H W ^a   Chen, Hanbo ^a   Govind, Shaylan K ^a   Hawley, James ^a   D'Costa, Alister ^a   Pintilie, Melania ^d   Waggott, Daryl ^a   Hach, Faraz ^f   Lambin, Philippe ^g   Muthuswamy, Lakshmi B ^a   Cooper, Colin ^h,i,j   Eeles, Rosalind ^h,k   Neal, David ^l,m   Tetu, Bernard ⁿ   Sahinalp, Cenk ^f   Stein, Lincoln D ^a   Fleshner, Neil ^d   Shah, Sohrab P ^o,p   Collins, Colin C ^o,q   Hudson, Thomas J ^a   McPherson, John D ^a   Van Der Kwast, Theodorus ^e   Bristow, Robert G ^b,d   more..

^a ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d PRINCESS MARGARET HOSPITAL   (Canada)

^e TORONTO GENERAL HOSPITAL   (Canada)

^f SIMON FRASER UNIVERSITY   (Canada)

^g MAASTRICHT UNIVERSITY   (Netherlands)

^h INSTITUTE OF CANCER RESEARCH   (United Kingdom)

ⁱ UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^j UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^k INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^l CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^m UNIVERSITY OF CAMBRIDGE   (United Kingdom)

ⁿ UNIVERSITÉ LAVAL   (Canada)

^o UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^p BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^q VANCOUVER PROSTATE CENTRE   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD147 ANTIGEN; FIBROBLAST GROWTH FACTOR 1; MESSENGER RNA; MYC PROTEIN; MYCL1 PROTEIN, HUMAN;

ARTICLE; CANCER PROGNOSIS; CHROMOSOME 8P; CHROMOSOME 8Q; COPY NUMBER VARIATION; CYSTECTOMY; DNA DAMAGE; GENETIC HETEROGENEITY; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; GENOMICS; GLEASON SCORE; HUMAN; MULTIPLE CANCER; NEUROBLASTOMA; NONHUMAN; ONCOGENE; ONCOGENE MYC; PRIORITY JOURNAL; PROSTATE CANCER; SINGLE NUCLEOTIDE POLYMORPHISM; CANCER GRADING; GENETIC ASSOCIATION; GENETICS; HUMAN GENOME; MALE; MIDDLE AGED; PATHOLOGY; POINT MUTATION; PROSTATE TUMOR; TUMOR CELL LINE;

CELL LINE, TUMOR; DNA COPY NUMBER VARIATIONS; GENETIC ASSOCIATION STUDIES; GENETIC HETEROGENEITY; GENOME, HUMAN; HUMANS; MALE; MIDDLE AGED; NEOPLASM GRADING; POINT MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC;

EID: 84933277410     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3315     Document Type: Article

References (65)

1. Mohler, J. et al. NCCN clinical practice guidelines in oncology: prostate cancer. J. Natl. Compr. Canc. Netw. 8, 162-200 (2010).
2. D'Amico, A.V. et al. Cancer-specific mortality after surgery or radiation for patients with clinically localized prostate cancer managed during the prostate-specific antigen era. J. Clin. Oncol. 21, 2163-2172 (2003).
3. Buyyounouski, M.K., Pickles, T., Kestin, L.L., Allison, R. & Williams, S.G. Validating the interval to biochemical failure for the identification of potentially lethal prostate cancer. J. Clin. Oncol. 30, 1857-1863 (2012).
4. Villers, A., McNeal, J.E., Freiha, F.S. & Stamey, T.A. Multiple cancers in the prostate. Morphologic features of clinically recognized versus incidental tumors. Cancer 70, 2313-2318 (1992).
5. Nichol, A.M., Warde, P. & Bristow, R.G. Optimal treatment of intermediate-risk prostate carcinoma with radiotherapy: clinical and translational issues. Cancer 104, 891-905 (2005).
6. Taylor, B.S. et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 18, 11-22 (2010).
7. Lapointe, J. et al. Genomic profiling reveals alternative genetic pathways of prostate tumorigenesis. Cancer Res. 67, 8504-8510 (2007).
8. Paris, P.L. et al. Whole genome scanning identifies genotypes associated with recurrence and metastasis in prostate tumors. Hum. Mol. Genet. 13, 1303-1313 (2004).
9. Penney, K.L. et al. MRNA expression signature of Gleason grade predicts lethal prostate cancer. J. Clin. Oncol. 29, 2391-2396 (2011).
10. Lalonde, E. et al. Tumour genomic and microenvironmental heterogeneity for integrated prediction of 5-year biochemical recurrence of prostate cancer: A retrospective cohort study. Lancet Oncol. 15, 1521-1532 (2014).
11. Olmos, D. et al. Prognostic value of blood mRNA expression signatures in castration-resistant prostate cancer: A prospective, two-stage study. Lancet Oncol. 13, 1114-1124 (2012).
12. Cortese, R. et al. Epigenetic markers of prostate cancer in plasma circulating DNA. Hum. Mol. Genet. 21, 3619-3631 (2012).
13. Ruijter, E.T., van de Kaa, C.A., Schalken, J.A., Debruyne, F.M. & Ruiter, D.J. Histological grade heterogeneity in multifocal prostate cancer. Biological and clinical implications. J. Pathol. 180, 295-299 (1996).
14. Lindberg, J. et al. Exome sequencing of prostate cancer supports the hypothesis of independent tumour origins. Eur. Urol. 63, 347-353 (2013).
15. Grasso, C.S. et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 487, 239-243 (2012).
16. Barbieri, C.E. et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat. Genet. 44, 685-689 (2012).
17. Ren, S. et al. RNA-seq analysis of prostate cancer in the Chinese population identifies recurrent gene fusions, cancer-associated long noncoding RNAs and aberrant alternative splicings. Cell Res. 22, 806-821 (2012).
18. Prensner, J.R. et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat. Biotechnol. 29, 742-749 (2011).
19. Kumar, A. et al. Exome sequencing identifies a spectrum of mutation frequencies in advanced and lethal prostate cancers. Proc. Natl. Acad. Sci. USA 108, 17087-17092 (2011).
20. Weischenfeldt, J. et al. Integrative genomic analyses reveal an androgen-driven somatic alteration landscape in early-onset prostate cancer. Cancer Cell 23, 159-170 (2013).
21. Baca, S.C. et al. Punctuated evolution of prostate cancer genomes. Cell 153, 666-677 (2013).
22. Zhou, Z. et al. Synergy of p53 and Rb deficiency in a conditional mouse model for metastatic prostate cancer. Cancer Res. 66, 7889-7898 (2006).
23. Edwards, J., Krishna, N.S., Witton, C.J. & Bartlett, J.M. Gene amplifications associated with the development of hormone-resistant prostate cancer. Clin. Cancer Res. 9, 5271-5281 (2003).
24. Pugh, T.J. et al. The genetic landscape of high-risk neuroblastoma. Nat. Genet. 45, 279-284 (2013).
25. Rushlow, D.E. et al. Characterisation of retinoblastomas without RB1 mutations: genomic, gene expression, and clinical studies. Lancet Oncol. 14, 327-334 (2013).
26. Penn, L.J., Brooks, M.W., Laufer, E.M. & Land, H. Negative autoregulation of c-Myc transcription. EMBO J. 9, 1113-1121 (1990).
27. Gerlinger, M. et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892 (2012).
28. Bashashati, A. et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J. Pathol. 231, 21-34 (2013).
29. Song, S. et al. qpure: A tool to estimate tumor cellularity from genome-wide single-nucleotide polymorphism profiles. PLoS ONE 7, e45835 (2012).
30. Beroukhim, R. et al. The landscape of somatic copy-number alteration across human cancers. Nature 463, 899-905 (2010).
31. Berger, M.F. et al. The genomic complexity of primary human prostate cancer. Nature 470, 214-220 (2011).
32. Lindberg, J. et al. The mitochondrial and autosomal mutation landscapes of prostate cancer. Eur. Urol. 63, 702-708 (2013).
33. Samuels, Y. et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 304, 554 (2004).
34. Janku, F. et al. PIK3CA mutation H1047R is associated with response to PI3K/AKT/mTOR signaling pathway inhibitors in early-phase clinical trials. Cancer Res. 73, 276-284 (2013).
35. Sangai, T. et al. Biomarkers of response to Akt inhibitor MK-2206 in breast cancer. Clin. Cancer Res. 18, 5816-5828 (2012).
36. Djulbegovic, M. et al. Screening for prostate cancer: systematic review and meta-analysis of randomised controlled trials. BMJ 341, c4543 (2010).
37. Zafarana, G. et al. Copy number alterations of c-MYC and PTEN are prognostic factors for relapse after prostate cancer radiotherapy. Cancer 118, 4053-4062 (2012).
38. Locke, J.A. et al. NKX3.1 haploinsufficiency is prognostic for prostate cancer relapse following surgery or image-guided radiotherapy. Clin. Cancer Res. 18, 308-316 (2012).
39. Locke, J.A. et al. Allelic loss of the loci containing the androgen synthesis gene, StAR, is prognostic for relapse in intermediate-risk prostate cancer. Prostate 72, 1295-1305 (2012).
40. Cooper, C.S. et al. Analysis of the genetic phylogeny of multifocal prostate cancer identifies multiple independent clonal expansions in neoplastic and morphologically normal prostate tissue. Nat. Genet. 47, 367-372 (2015).
41. Ishkanian, A.S. et al. High-resolution array CGH identifies novel regions of genomic alteration in intermediate-risk prostate cancer. Prostate 69, 1091-1100 (2009).
42. Harrow, J. et al. GENCODE: The reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760-1774 (2012).
43. Mermel, C.H. et al. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol. 12, R41 (2011).
44. Dai, M. et al. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175 (2005).
45. Gentleman, R.C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
46. Irizarry, R.A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003).
47. Smyth, G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004).
48. Fisher, S. et al. A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biol. 12, R1 (2011).
49. O'Connor, B.D., Merriman, B. & Nelson, S.F. SeqWare Query Engine: storing and searching sequence data in the cloud. BMC Bioinformatics 11 (suppl. 12), S2 (2010).
50. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
51. McKenna, A. et al. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
52. DePristo, M.A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
53. NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 41, D8-D20 (2013).
54. Li, H. Tabix: fast retrieval of sequence features from generic TAB-delimited files. Bioinformatics 27, 718-719 (2011).
55. Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).
56. Ouedraogo, M. et al. The duplicated genes database: identification and functional annotation of co-localised duplicated genes across genomes. PLoS ONE 7, e50653 (2012).
57. Gerstein, M.B. et al. Architecture of the human regulatory network derived from ENCODE data. Nature 489, 91-100 (2012).
58. Fuentes Fajardo, K.V. et al. Detecting false-positive signals in exome sequencing. Hum. Mutat. 33, 609-613 (2012).
59. Forbes, S.A. et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 39, D945-D950 (2011).
60. McPherson, A. et al. nFuse: discovery of complex genomic rearrangements in cancer using high-throughput sequencing. Genome Res. 22, 2250-2261 (2012).
61. Wang, J. et al. CREST maps somatic structural variation in cancer genomes with base-pair resolution. Nat. Methods 8, 652-654 (2011).
62. Quinlan, A.R. & Hall, I.M. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
63. Ewing, B., Hillier, L., Wendl, M.C. & Green, P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8, 175-185 (1998).
64. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595 (2010).
65. Chen, H. & Boutros, P.C. VennDiagram: A package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 12, 35 (2011).