Tracking the origins and drivers of subclonal metastatic expansion in prostate cancer

Hong, Matthew K. H.; Macintyre, Geoff; Wedge, David C.; Van Loo, Peter; Patel, Keval; Lunke, Sebastian; Alexandrov, Ludmil B.; Sloggett, Clare; Cmero, Marek; Marass, Francesco; Tsui, Dana; Mangiola, Stefano; Lonie, Andrew; Naeem, Haroon; Sapre, Nikhil; Phal, Pramit M.; Kurganovs, Natalie; Chin, Xiaowen; Kerger, Michael; Warren, Anne Y.; Neal, David; Gnanapragasam, Vincent; Rosenfeld, Nitzan; Pedersen, John S.; Ryan, Andrew; Haviv, Izhak; Costello, Anthony J.; Corcoran, Niall M.; Hovens, Christopher M.

doi:10.1038/ncomms7605

Title: Tracking the origins and drivers of subclonal metastatic expansion in prostate cancer

Journal Article · Wed Apr 01 00:00:00 EDT 2015 · Nature Communications

DOI:https://doi.org/10.1038/ncomms7605· OSTI ID:1236642

Hong, Matthew K. H. ^[1]; Macintyre, Geoff ^[2]; Wedge, David C. ^[3];

^[4]; Patel, Keval ^[5]; Lunke, Sebastian ^[6];

^[7]; Sloggett, Clare ^[6]; Cmero, Marek ^[8]; Marass, Francesco ^[9]; Tsui, Dana ^[9]; Mangiola, Stefano ^[6]; Lonie, Andrew ^[6]; Naeem, Haroon ^[6]; Sapre, Nikhil ^[1]; Phal, Pramit M. ^[10]; Kurganovs, Natalie ^[1]; Chin, Xiaowen ^[1];

^[1]; Warren, Anne Y. ^[11] more »

Royal Melbourne Hospital and Univ. of Melbourne, Victoria (Australia); Epworth Hospital, Victoria (Australia)
Univ. of Melbourne, Victoria (Australia); Univ. of Cambridge, Cambridge (United Kingdom)
Wellcome Trust Sanger Institute, Hinxton (United Kingdom)
Wellcome Trust Sanger Institute, Hinxton (United Kingdom); KU Leuven, Leuven (Belgium), Cancer Research UK London Research Institute, London (United Kingdom)
Univ. of Cambridge, Cambridge (United Kingdom); Cambridge Univ., Cambridge (United Kingdom)
Univ. of Melbourne, Victoria (Australia)
Wellcome Trust Sanger Institute, Hinxton (United Kingdom); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Royal Melbourne Hospital and Univ. of Melbourne, Victoria (Australia); Epworth Hospital, Victoria (Australia); Univ. of Melbourne, Victoria (Australia)
Univ. of Cambridge, Cambridge (United Kingdom)
Royal Melbourne Hospital, Victoria (Australia)
Univ. Cambridge Hospitals, Cambridge (United Kingdom)
Univ. of Cambridge, Cambridge (United Kingdom); Addenbrookes Hospital, Cambridge Univ., Hospitals NHS Foundation Trust, Cambridge (United Kingdom)
TissuPath Specialist Pathology, Victoria (Australia); Monash Univ. Faculty of Medicine, Victoria (Australia)
TissuPath Specialist Pathology, Victoria (Australia)
Bar-Ilan Univ. Medical School, Safad (Israel)

Tumour heterogeneity in primary prostate cancer is a well-established phenomenon. However, how the subclonal diversity of tumours changes during metastasis and progression to lethality is poorly understood. Here we reveal the precise direction of metastatic spread across four lethal prostate cancer patients using whole-genome and ultra-deep targeted sequencing of longitudinally collected primary and metastatic tumours. We find one case of metastatic spread to the surgical bed causing local recurrence, and another case of cross-metastatic site seeding combining with dynamic remoulding of subclonal mixtures in response to therapy. By ultra-deep sequencing end-stage blood, we detect both metastatic and primary tumour clones, even years after removal of the prostate. As a result, analysis of mutations associated with metastasis reveals an enrichment of TP53 mutations, and additional sequencing of metastases from 19 patients demonstrates that acquisition of TP53 mutations is linked with the expansion of subclones with metastatic potential which we can detect in the blood.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1236642

Report Number(s):: LA-UR-14-29031; ncomms7605

Journal Information:: Nature Communications, Vol. 6, Issue C; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 259 works

Citation information provided by
Web of Science

References (68)

The genomic complexity of primary human prostate cancer Berger, Michael F.; Lawrence, Michael S.; Demichelis, Francesca Nature, Vol. 470, Issue 7333 https://doi.org/10.1038/nature09744	journal	February 2011
Integrative Genomic Profiling of Human Prostate Cancer Taylor, Barry S.; Schultz, Nikolaus; Hieronymus, Haley Cancer Cell, Vol. 18, Issue 1 https://doi.org/10.1016/j.ccr.2010.05.026	journal	July 2010
Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer Barbieri, Christopher E.; Baca, Sylvan C.; Lawrence, Michael S. Nature Genetics, Vol. 44, Issue 6 https://doi.org/10.1038/ng.2279	journal	May 2012
Integrative Genomic Analyses Reveal an Androgen-Driven Somatic Alteration Landscape in Early-Onset Prostate Cancer Weischenfeldt, Joachim; Simon, Ronald; Feuerbach, Lars Cancer Cell, Vol. 23, Issue 2 https://doi.org/10.1016/j.ccr.2013.01.002	journal	February 2013
Exome sequencing identifies a spectrum of mutation frequencies in advanced and lethal prostate cancers Kumar, A.; White, T. A.; MacKenzie, A. P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 41 https://doi.org/10.1073/pnas.1108745108	journal	September 2011
The mutational landscape of lethal castration-resistant prostate cancer Grasso, Catherine S.; Wu, Yi-Mi; Robinson, Dan R. Nature, Vol. 487, Issue 7406 https://doi.org/10.1038/nature11125	journal	May 2012
Punctuated Evolution of Prostate Cancer Genomes Baca, Sylvan C.; Prandi, Davide; Lawrence, Michael S. Cell, Vol. 153, Issue 3 https://doi.org/10.1016/j.cell.2013.03.021	journal	April 2013
Distant metastasis occurs late during the genetic evolution of pancreatic cancer Yachida, Shinichi; Jones, Siân; Bozic, Ivana Nature, Vol. 467, Issue 7319 https://doi.org/10.1038/nature09515	journal	October 2010
The patterns and dynamics of genomic instability in metastatic pancreatic cancer Campbell, Peter J.; Yachida, Shinichi; Mudie, Laura J. Nature, Vol. 467, Issue 7319 https://doi.org/10.1038/nature09460	journal	October 2010
Spatial and temporal diversity in genomic instability processes defines lung cancer evolution de Bruin, E. C.; McGranahan, N.; Mitter, R. Science, Vol. 346, Issue 6206 https://doi.org/10.1126/science.1253462	journal	October 2014
Intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing Zhang, J.; Fujimoto, J.; Zhang, J. Science, Vol. 346, Issue 6206 https://doi.org/10.1126/science.1256930	journal	October 2014
The Life History of 21 Breast Cancers Nik-Zainal, Serena; Van Loo, Peter; Wedge, David C. Cell, Vol. 149, Issue 5 https://doi.org/10.1016/j.cell.2012.04.023	journal	May 2012
Prognostic impact of positive surgical margins in surgically treated prostate cancer: Multi-institutional assessment of 5831 patients Karakiewicz, Pierre I.; Eastham, James A.; Graefen, Markus Urology, Vol. 66, Issue 6 https://doi.org/10.1016/j.urology.2005.06.108	journal	December 2005
The Syk tyrosine kinase: A new negative regulator in tumor growth and progression Coopman, Peter J.; Mueller, Susette C. Cancer Letters, Vol. 241, Issue 2 https://doi.org/10.1016/j.canlet.2005.11.004	journal	September 2006
Research on the reactivation of Syk expression caused by the inhibition of DNA promoter methylation in the lung cancer Dong, S.; Ma, L.; Xu, N. Neoplasma, Vol. 58, Issue 1 https://doi.org/10.4149/neo_2011_01_89	journal	January 2011
Spleen tyrosine kinase as a novel candidate tumor suppressor gene for human oral squamous cell carcinoma Ogane, Satoru; Onda, Takeshi; Takano, Nobuo International Journal of Cancer, Vol. 124, Issue 11 https://doi.org/10.1002/ijc.24237	journal	December 2008
Recurrent PTPRB and PLCG1 mutations in angiosarcoma Behjati, Sam; Tarpey, Patrick S.; Sheldon, Helen Nature Genetics, Vol. 46, Issue 4 https://doi.org/10.1038/ng.2921	journal	March 2014
Mutational signatures: the patterns of somatic mutations hidden in cancer genomes Alexandrov, Ludmil B.; Stratton, Michael R. Current Opinion in Genetics & Development, Vol. 24 https://doi.org/10.1016/j.gde.2013.11.014	journal	February 2014
Signatures of mutational processes in human cancer Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C. Nature, Vol. 500, Issue 7463 https://doi.org/10.1038/nature12477	journal	August 2013
Mutational Processes Molding the Genomes of 21 Breast Cancers Nik-Zainal, Serena; Alexandrov, Ludmil B.; Wedge, David C. Cell, Vol. 149, Issue 5 https://doi.org/10.1016/j.cell.2012.04.024	journal	May 2012
Chromothripsis and beyond: rapid genome evolution from complex chromosomal rearrangements Zhang, C. -Z.; Leibowitz, M. L.; Pellman, D. Genes & Development, Vol. 27, Issue 23 https://doi.org/10.1101/gad.229559.113	journal	December 2013
Chromoplexy: A New Category of Complex Rearrangements in the Cancer Genome Shen, Michael M. Cancer Cell, Vol. 23, Issue 5 https://doi.org/10.1016/j.ccr.2013.04.025	journal	May 2013
Germline and somatic polymerase ϵ and δ mutations define a new class of hypermutated colorectal and endometrial cancers: DNA polymerase mutations in colorectal and endometrial cancers Briggs, Sarah; Tomlinson, Ian The Journal of Pathology, Vol. 230, Issue 2 https://doi.org/10.1002/path.4185	journal	May 2013
Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas Palles, Claire; Cazier, Jean-Baptiste; Howarth, Kimberley M. Nature Genetics, Vol. 45, Issue 2 https://doi.org/10.1038/ng.2503	journal	December 2012
Complex MSH2 and MSH6 mutations in hypermutated microsatellite unstable advanced prostate cancer Pritchard, Colin C.; Morrissey, Colm; Kumar, Akash Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5988	journal	September 2014
Noninvasive Identification and Monitoring of Cancer Mutations by Targeted Deep Sequencing of Plasma DNA Forshew, T.; Murtaza, M.; Parkinson, C. Science Translational Medicine, Vol. 4, Issue 136 https://doi.org/10.1126/scitranslmed.3003726	journal	May 2012
Tumor clone dynamics in lethal prostate cancer Carreira, S.; Romanel, A.; Goodall, J. Science Translational Medicine, Vol. 6, Issue 254 https://doi.org/10.1126/scitranslmed.3009448	journal	September 2014
Gain of Function of a p53 Hot Spot Mutation in a Mouse Model of Li-Fraumeni Syndrome Lang, Gene A.; Iwakuma, Tomoo; Suh, Young-Ah Cell, Vol. 119, Issue 6 https://doi.org/10.1016/j.cell.2004.11.006	journal	December 2004
Mutant p53 Gain of Function in Two Mouse Models of Li-Fraumeni Syndrome Olive, Kenneth P.; Tuveson, David A.; Ruhe, Zachary C. Cell, Vol. 119, Issue 6 https://doi.org/10.1016/j.cell.2004.11.004	journal	December 2004
P53 expression in breast cancer Cattoretti, Giorgio; Rilke, Franco; Andreola, Salvatore International Journal of Cancer, Vol. 41, Issue 2 https://doi.org/10.1002/ijc.2910410204	journal	February 1988
TP53 Mutations in Human Cancer: Database Reassessment and Prospects for the Next Decade Leroy, Bernard; Anderson, Martha; Soussi, Thierry Human Mutation, Vol. 35, Issue 6 https://doi.org/10.1002/humu.22552	journal	May 2014
The prostate cancer genome: Perspectives and potential Barbieri, Christopher E.; Tomlins, Scott A. Urologic Oncology: Seminars and Original Investigations, Vol. 32, Issue 1 https://doi.org/10.1016/j.urolonc.2013.08.025	journal	January 2014
The Mutational Landscape of Prostate Cancer Barbieri, Christopher E.; Bangma, Chris H.; Bjartell, Anders European Urology, Vol. 64, Issue 4 https://doi.org/10.1016/j.eururo.2013.05.029	journal	October 2013
Genomic Profiling Defines Subtypes of Prostate Cancer with the Potential for Therapeutic Stratification Schoenborn, J. R.; Nelson, P.; Fang, M. Clinical Cancer Research, Vol. 19, Issue 15 https://doi.org/10.1158/1078-0432.CCR-12-3606	journal	May 2013
The complexity of prostate cancer: genomic alterations and heterogeneity Boyd, Lara K.; Mao, Xueying; Lu, Yong-Jie Nature Reviews Urology, Vol. 9, Issue 11 https://doi.org/10.1038/nrurol.2012.185	journal	November 2012
PTEN losses exhibit heterogeneity in multifocal prostatic adenocarcinoma and are associated with higher Gleason grade Yoshimoto, Maisa; Ding, Keyue; Sweet, Joan M. Modern Pathology, Vol. 26, Issue 3 https://doi.org/10.1038/modpathol.2012.162	journal	September 2012
Regional biases in mutation screening due to intratumoural heterogeneity of prostate cancer: Genetic intratumoural heterogeneity in unifocal prostate cancer Kim, Tae-Min; Jung, Seung-Hyun; Baek, In-Pyo The Journal of Pathology, Vol. 233, Issue 4 https://doi.org/10.1002/path.4380	journal	July 2014
Percutaneous image-guided biopsy of prostate cancer metastases yields samples suitable for genomics and personalised oncology Hong, Matthew K. H.; Sapre, Nikhil; Phal, Pramit M. Clinical & Experimental Metastasis, Vol. 31, Issue 2 https://doi.org/10.1007/s10585-013-9617-2	journal	October 2013
SomaticSniper: identification of somatic point mutations in whole genome sequencing data Larson, David E.; Harris, Christopher C.; Chen, Ken Bioinformatics, Vol. 28, Issue 3 https://doi.org/10.1093/bioinformatics/btr665	journal	December 2011
Human Genome Sequencing Using Unchained Base Reads on Self-Assembling DNA Nanoarrays Drmanac, R.; Sparks, A. B.; Callow, M. J. Science, Vol. 327, Issue 5961 https://doi.org/10.1126/science.1181498	journal	November 2009
Socrates: identification of genomic rearrangements in tumour genomes by re-aligning soft clipped reads Schröder, Jan; Hsu, Arthur; Boyle, Samantha E. Bioinformatics, Vol. 30, Issue 8 https://doi.org/10.1093/bioinformatics/btt767	journal	January 2014
Allele-specific copy number analysis of tumors Van Loo, P.; Nordgard, S. H.; Lingjaerde, O. C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 39 https://doi.org/10.1073/pnas.1009843107	journal	September 2010
A Flexible and Accurate Genotype Imputation Method for the Next Generation of Genome-Wide Association Studies Howie, Bryan N.; Donnelly, Peter; Marchini, Jonathan PLoS Genetics, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pgen.1000529	journal	June 2009
The 1000 Genomes Project: data management and community access Clarke, Laura; Zheng-Bradley, Xiangqun; Smith, Richard Nature Methods, Vol. 9, Issue 5 https://doi.org/10.1038/nmeth.1974	journal	April 2012
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics Lohse, M.; Bolger, A. M.; Nagel, A. Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks540	journal	June 2012
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Genome Biology, Vol. 14, Issue 4 https://doi.org/10.1186/gb-2013-14-4-r36	journal	January 2013
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
Deciphering Signatures of Mutational Processes Operative in Human Cancer Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C. Cell Reports, Vol. 3, Issue 1 https://doi.org/10.1016/j.celrep.2012.12.008	journal	January 2013
Heterogeneity of genomic evolution and mutational profiles in multiple myeloma Bolli, Niccolo; Avet-Loiseau, Hervé; Wedge, David C. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms3997	journal	January 2014
A census of human cancer genes Futreal, P. Andrew; Coin, Lachlan; Marshall, Mhairi Nature Reviews Cancer, Vol. 4, Issue 3 https://doi.org/10.1038/nrc1299	journal	March 2004
Comprehensive identification of mutational cancer driver genes across 12 tumor types Tamborero, David; Gonzalez-Perez, Abel; Perez-Llamas, Christian Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02650	journal	October 2013
ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data Wang, K.; Li, M.; Hakonarson, H. Nucleic Acids Research, Vol. 38, Issue 16 https://doi.org/10.1093/nar/gkq603	journal	July 2010
SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation Zoch, Ansgar; Auchynnikava, Tania; Berrens, Rebecca V. Nature, Vol. 584, Issue 7822 https://doi.org/10.1038/s41586-020-2557-5	journal	July 2020
Database resources of the National Center for Biotechnology Information Wheeler, D. L. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj158	journal	January 2006
Impact of concurrency on the performance of a whole exome sequencing pipeline Dall’Olio, Daniele; Curti, Nico; Fonzi, Eugenio BMC Bioinformatics, Vol. 22, Issue 1 https://doi.org/10.1186/s12859-020-03780-3	journal	February 2021
Allele-specific copy number analysis of tumors B., Naume,; W., Sun,; C., Lingjaerde, O. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/2zsb-7679	text	January 2010
Heterogeneity of genomic evolution and mutational profiles in multiple myeloma. Bolli, Niccolo; Avet-Loiseau, Hervé; Wedge, David C. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.33452	text	January 2014
The life history of 21 breast cancers. Nik-Zainal, Serena; Van Loo, Peter; Wedge, David C. Elsevier BV https://doi.org/10.17863/cam.56803	journalarticle	January 2012
Deciphering signatures of mutational processes operative in human cancer. Alexandrov, Ludmil B.; Nik-Zainal Abidin, Serena; Wedge, David C. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.60112	text	January 2013
The Life History of 21 Breast Cancers Nik-Zainal, Serena; Van Loo, Peter; Wedge, David C. Cell, Vol. 162, Issue 4 https://doi.org/10.1016/j.cell.2015.07.039	journal	August 2015
Database resources of the National Center for Biotechnology Information Sayers, Eric W.; Beck, Jeffrey; Bolton, Evan E. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa892	journal	October 2020
Signatures of mutational processes in human cancer. Alexandrov, Ludmil B.; Nik-Zainal Abidin, Serena; Wedge, David C. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.31889	text	January 2013
Database resources of the National Center for Biotechnology Information Wheeler, D. L.; Barrett, T.; Benson, D. A. Nucleic Acids Research, Vol. 36, Issue Database https://doi.org/10.1093/nar/gkm1000	journal	December 2007
Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer Barbieri, Christopher E.; Al, Et Nature Publishing Group https://doi.org/10.5167/uzh-62954	text	January 2012
Database resources of the National Center for Biotechnology Information Sayers, Eric W.; Agarwala, Richa; Bolton, Evan E. Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1069	journal	November 2018
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Springer Nature https://doi.org/10.13016/7jyb-2sdy	text	January 2013
Prostate Cancer Genomics: Progress and Promise Varambally, Sooryanarayana European Urology, Vol. 64, Issue 4 https://doi.org/10.1016/j.eururo.2013.06.006	journal	October 2013

Cited By (71)

Discordant and heterogeneous clinically relevant genomic alterations in circulating tumor cells vs plasma DNA from men with metastatic castration resistant prostate cancer Gupta, Santosh; Hovelson, Daniel H.; Kemeny, Gabor Genes, Chromosomes and Cancer, Vol. 59, Issue 4 https://doi.org/10.1002/gcc.22824	journal	November 2019
Transcriptional profiling of breast cancer‐associated lymphatic vessels reveals VCAM‐1 as regulator of lymphatic invasion and permeability Dieterich, Lothar C.; Kapaklikaya, Kübra; Cetintas, Timur International Journal of Cancer, Vol. 145, Issue 10 https://doi.org/10.1002/ijc.32594	journal	February 2019
Tumor cell heterogeneity and resistance; report from the 2018 Coffey‐Holden Prostate Cancer Academy Meeting Miyahira, Andrea K.; Den, Robert B.; Carlo, Maria I. The Prostate, Vol. 79, Issue 3 https://doi.org/10.1002/pros.23729	journal	October 2018
A qualitative transcriptional signature for predicting the biochemical recurrence risk of prostate cancer patients after radical prostatectomy Li, Xiang; Huang, Haiyan; Zhang, Jiahui The Prostate, Vol. 80, Issue 5 https://doi.org/10.1002/pros.23952	journal	January 2020
Clinical implications of intratumor heterogeneity: challenges and opportunities Ramón y. Cajal, Santiago; Sesé, Marta; Capdevila, Claudia Journal of Molecular Medicine, Vol. 98, Issue 2 https://doi.org/10.1007/s00109-020-01874-2	journal	January 2020
Reconsidering the role of pelvic lymph node dissection with radical prostatectomy for prostate cancer in an era of improving radiological staging techniques Yaxley, J. W.; Dagher, J.; Delahunt, B. World Journal of Urology, Vol. 36, Issue 1 https://doi.org/10.1007/s00345-017-2119-0	journal	November 2017
Discovery and validation of a serum microRNA signature to characterize oligo- and polymetastatic prostate cancer: not ready for prime time Dhondt, Bert; De Bleser, Elise; Claeys, Tom World Journal of Urology, Vol. 37, Issue 12 https://doi.org/10.1007/s00345-018-2609-8	journal	December 2018
Detection of Circulating Tumor DNA with a Single-Molecule Sequencing Analysis Validated for Targeted and Immunotherapy Selection Atkins, Alexander; Gupta, Pratyush; Zhang, Bing Melody Molecular Diagnosis & Therapy, Vol. 23, Issue 4 https://doi.org/10.1007/s40291-019-00406-0	journal	June 2019
Human cancer-associated fibroblasts enhance glutathione levels and antagonize drug-induced prostate cancer cell death Cheteh, Emarndeena H.; Augsten, Martin; Rundqvist, Helene Cell Death & Disease, Vol. 8, Issue 6 https://doi.org/10.1038/cddis.2017.225	journal	June 2017
The Genomics of Prostate Cancer: emerging understanding with technologic advances Rubin, Mark A.; Demichelis, Francesca Modern Pathology, Vol. 31, Issue S1 https://doi.org/10.1038/modpathol.2017.166	journal	January 2018
The complex seeds of metastasis Shen, Michael M. Nature, Vol. 520, Issue 7547 https://doi.org/10.1038/nature14377	journal	April 2015
Whole-genome plasma sequencing reveals focal amplifications as a driving force in metastatic prostate cancer Ulz, Peter; Belic, Jelena; Graf, Ricarda Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12008	journal	June 2016
Phylogenetic analysis of metastatic progression in breast cancer using somatic mutations and copy number aberrations Brown, David; Smeets, Dominiek; Székely, Borbála Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14944	journal	April 2017
Limited heterogeneity of known driver gene mutations among the metastases of individual patients with pancreatic cancer Makohon-Moore, Alvin P.; Zhang, Ming; Reiter, Johannes G. Nature Genetics, Vol. 49, Issue 3 https://doi.org/10.1038/ng.3764	journal	January 2017
Positively selected enhancer elements endow osteosarcoma cells with metastatic competence Morrow, James J.; Bayles, Ian; Funnell, Alister P. W. Nature Medicine, Vol. 24, Issue 2 https://doi.org/10.1038/nm.4475	journal	January 2018
Targeting metastasis Steeg, Patricia S. Nature Reviews Cancer, Vol. 16, Issue 4 https://doi.org/10.1038/nrc.2016.25	journal	March 2016
Bone metastasis: the importance of the neighbourhood Croucher, Peter I.; McDonald, Michelle M.; Martin, T. John Nature Reviews Cancer, Vol. 16, Issue 6 https://doi.org/10.1038/nrc.2016.44	journal	May 2016
Genetic insights into the morass of metastatic heterogeneity Hunter, Kent W.; Amin, Ruhul; Deasy, Sarah Nature Reviews Cancer, Vol. 18, Issue 4 https://doi.org/10.1038/nrc.2017.126	journal	February 2018
Translational and clinical implications of the genetic landscape of prostate cancer Spratt, Daniel E.; Zumsteg, Zachary S.; Feng, Felix Y. Nature Reviews Clinical Oncology, Vol. 13, Issue 10 https://doi.org/10.1038/nrclinonc.2016.76	journal	June 2016
Tumour heterogeneity and resistance to cancer therapies Dagogo-Jack, Ibiayi; Shaw, Alice T. Nature Reviews Clinical Oncology, Vol. 15, Issue 2 https://doi.org/10.1038/nrclinonc.2017.166	journal	November 2017
The evolution of tumour phylogenetics: principles and practice Schwartz, Russell; Schäffer, Alejandro A. Nature Reviews Genetics, Vol. 18, Issue 4 https://doi.org/10.1038/nrg.2016.170	journal	February 2017
Androgen deprivation leads to increased carbohydrate metabolism and hexokinase 2-mediated survival in Pten/Tp53-deficient prostate cancer Martin, P. L.; Yin, J-J; Seng, V. Oncogene, Vol. 36, Issue 4 https://doi.org/10.1038/onc.2016.223	journal	July 2016
The effects of mutational processes and selection on driver mutations across cancer types Temko, Daniel; Tomlinson, Ian P. M.; Severini, Simone Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04208-6	journal	May 2018
Spatial maps of prostate cancer transcriptomes reveal an unexplored landscape of heterogeneity Berglund, Emelie; Maaskola, Jonas; Schultz, Niklas Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04724-5	journal	June 2018
Translational models of prostate cancer bone metastasis Berish, Richard B.; Ali, Aymon N.; Telmer, Patrick G. Nature Reviews Urology, Vol. 15, Issue 7 https://doi.org/10.1038/s41585-018-0020-2	journal	May 2018
Mutations in BRCA2 and taxane resistance in prostate cancer Nientiedt, Cathleen; Heller, Martina; Endris, Volker Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-04897-x	journal	July 2017
Association Of Plasma And Urinary Mutant DNA With Clinical Outcomes In Muscle Invasive Bladder Cancer Patel, K. M.; van der Vos, K. E.; Smith, C. G. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-05623-3	journal	July 2017
Genomic Analyses of Breast Cancer Progression Reveal Distinct Routes of Metastasis Emergence Krøigård, Anne Bruun; Larsen, Martin Jakob; Brasch-Andersen, Charlotte Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43813	journal	March 2017
Loss of p53 function at late stages of tumorigenesis confers ARF-dependent vulnerability to p53 reactivation therapy Klimovich, Boris; Mutlu, Samet; Schneikert, Jean Proceedings of the National Academy of Sciences, Vol. 116, Issue 44 https://doi.org/10.1073/pnas.1910255116	journal	October 2019
Understanding mutagenesis through delineation of mutational signatures in human cancer Petljak, Mia; Alexandrov, Ludmil B. Carcinogenesis, Vol. 37, Issue 6 https://doi.org/10.1093/carcin/bgw055	journal	May 2016
Concordance of Circulating Tumor DNA and Matched Metastatic Tissue Biopsy in Prostate Cancer Wyatt, Alexander W.; Annala, Matti; Aggarwal, Rahul JNCI: Journal of the National Cancer Institute, Vol. 109, Issue 12 https://doi.org/10.1093/jnci/djx118	journal	June 2017
Radiation resistant cancer cells enhance the survival and resistance of sensitive cells in prostate spheroids Kannan, Pavitra; Paczkowski, Marcin; Miar, Ana BioRxiv https://doi.org/10.1101/564724	posted_content	March 2019
Prostate Stem Cells and Cancer Stem Cells Li, Jia J.; Shen, Michael M. Cold Spring Harbor Perspectives in Medicine, Vol. 9, Issue 6 https://doi.org/10.1101/cshperspect.a030395	journal	October 2018
Genetics and biology of prostate cancer Wang, Guocan; Zhao, Di; Spring, Denise J. Genes & Development, Vol. 32, Issue 17-18 https://doi.org/10.1101/gad.315739.118	journal	September 2018
Late biochemical recurrence after radical prostatectomy is associated with a slower rate of progression Chow, Ken; Herrera, Pia; Stuchbery, Ryan BJU International, Vol. 123, Issue 6 https://doi.org/10.1111/bju.14556	journal	October 2018
Metastasis as an evolutionary process Turajlic, S.; Swanton, C. Science, Vol. 352, Issue 6282 https://doi.org/10.1126/science.aaf2784	journal	April 2016
Minimal functional driver gene heterogeneity among untreated metastases Reiter, Johannes G.; Makohon-Moore, Alvin P.; Gerold, Jeffrey M. Science, Vol. 361, Issue 6406 https://doi.org/10.1126/science.aat7171	journal	September 2018
Circulating tumour cells from patients with colorectal cancer have cancer stem cell hallmarks in ex vivo culture Grillet, Fanny; Bayet, Elsa; Villeronce, Olivia Gut, Vol. 66, Issue 10 https://doi.org/10.1136/gutjnl-2016-311447	journal	July 2016
Frequent clonal relations between metastases and non-index prostate cancer lesions Kneppers, Jeroen; Krijgsman, Oscar; Melis, Monique JCI Insight, Vol. 4, Issue 2 https://doi.org/10.1172/jci.insight.124756	journal	January 2019
Vimentin and Ki67 expression in circulating tumour cells derived from castrate-resistant prostate cancer Lindsay, C. R.; Le Moulec, S.; Billiot, F. BMC Cancer, Vol. 16, Issue 1 https://doi.org/10.1186/s12885-016-2192-6	journal	February 2016
Insulin-like growth factor 1 receptor affects the survival of primary prostate cancer patients depending on TMPRSS2-ERG status Mancarella, Caterina; Casanova-Salas, Irene; Calatrava, Ana BMC Cancer, Vol. 17, Issue 1 https://doi.org/10.1186/s12885-017-3356-8	journal	May 2017
p53 mutant-type in human prostate cancer cells determines the sensitivity to phenethyl isothiocyanate induced growth inhibition Aggarwal, Monika; Saxena, Rahul; Asif, Nasir Journal of Experimental & Clinical Cancer Research, Vol. 38, Issue 1 https://doi.org/10.1186/s13046-019-1267-z	journal	July 2019
Timing somatic events in the evolution of cancer Jolly, Clemency; Van Loo, Peter Genome Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s13059-018-1476-3	journal	July 2018
The Subclonal Architecture of Metastatic Breast Cancer: Results from a Prospective Community-Based Rapid Autopsy Program “CASCADE” Savas, Peter; Teo, Zhi Ling; Lefevre, Christophe PLOS Medicine, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pmed.1002204	journal	December 2016
Stem cells in genetically-engineered mouse models of prostate cancer Shibata, Maho; Shen, Michael M. Endocrine-Related Cancer, Vol. 22, Issue 6 https://doi.org/10.1530/erc-15-0367	journal	September 2015
Clonal origin and spread of metastatic prostate cancer Van Etten, Jamie L.; Dehm, Scott M. Endocrine-Related Cancer, Vol. 23, Issue 4 https://doi.org/10.1530/erc-16-0049	journal	April 2016
Precision Oncology: The Promise of Big Data and the Legacy of Small Data Capobianco, Enrico Frontiers in ICT, Vol. 4 https://doi.org/10.3389/fict.2017.00022	journal	August 2017
Sleeping Beauty Mouse Models of Cancer: Microenvironmental Influences on Cancer Genetics Guimaraes-Young, Amy; Feddersen, Charlotte R.; Dupuy, Adam J. Frontiers in Oncology, Vol. 9 https://doi.org/10.3389/fonc.2019.00611	journal	July 2019
Tumour Heterogeneity: The Key Advantages of Single-Cell Analysis Tellez-Gabriel, Marta; Ory, Benjamin; Lamoureux, Francois International Journal of Molecular Sciences, Vol. 17, Issue 12 https://doi.org/10.3390/ijms17122142	journal	December 2016
Cellular and Molecular Mechanisms Underlying Prostate Cancer Development: Therapeutic Implications Testa, Ugo; Castelli, Germana; Pelosi, Elvira Medicines, Vol. 6, Issue 3 https://doi.org/10.3390/medicines6030082	journal	July 2019
A comprehensive analysis of coregulator recruitment, androgen receptor function and gene expression in prostate cancer Liu, Song; Kumari, Sangeeta; Hu, Qiang eLife, Vol. 6 https://doi.org/10.7554/elife.28482	journal	August 2017
Developments in oligometastatic hormone-sensitive prostate cancer Chow, Ken; McCoy, Patrick; Stuchbery, Ryan World Journal of Urology, Vol. 37, Issue 12 https://doi.org/10.1007/s00345-018-2542-x	journal	October 2018
Unexpected contribution of lymphatic vessels to promotion of distant metastatic tumor spread Ma, Qiaoli; Dieterich, Lothar C.; Ikenberg, Kristian ETH Zurich https://doi.org/10.3929/ethz-b-000284331	text	January 2018
Transcriptional profiling of breast cancer-associated lymphatic vessels reveals VCAM-1 as regulator of lymphatic invasion and permeability Dieterich, Lothar C.; Kapaklikaya, Kübra; Cetintas, Timur Wiley-Blackwell Publishing, Inc. https://doi.org/10.5167/uzh-178866	text	January 2019
Clinical implications of intratumor heterogeneity: challenges and opportunities Cajal, Santiago Ramón Y.; Sesé, Marta; Capdevila, Claudia figshare https://doi.org/10.6084/m9.figshare.11702424	text	January 2020
The Genomics of Prostate Cancer: emerging understanding with technologic advances. Rubin, Mark Andrew; Demichelis, Francesca Nature Publishing Group https://doi.org/10.7892/boris.110878	text	January 2018
Association Of Plasma And Urinary Mutant DNA With Clinical Outcomes In Muscle Invasive Bladder Cancer Patel, Km; Van Der Vos, Ke; Smith, Christopher Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.12822	text	January 2017
Unexpected contribution of lymphatic vessels to promotion of distant metastatic tumor spread Ma, Qiaoli; Dieterich, Lothar C.; Ikenberg, Kristian American Association for the Advancement of Science https://doi.org/10.5167/uzh-153234	text	January 2018
The effects of mutational processes and selection on driver mutations across cancer types Temko, Daniel; Tomlinson, Ian P. M.; Severini, Simone bioRxiv https://doi.org/10.1101/149096	posted_content	June 2017
Unexpected contribution of lymphatic vessels to promotion of distant metastatic tumor spread Ma, Qiaoli; Dieterich, Lothar C.; Ikenberg, Kristian Science Advances, Vol. 4, Issue 8 https://doi.org/10.1126/sciadv.aat4758	journal	August 2018
Transcriptional profiling of breast cancer-associated lymphatic vessels reveals VCAM-1 as regulator of lymphatic invasion and permeability. Dieterich, Lothar C.; Kapaklikaya, Kübra; Cetintas, Timur Wiley-Blackwell https://doi.org/10.7892/boris.134687	text	January 2019
Clinical implications of intratumor heterogeneity: challenges and opportunities Cajal, Santiago Ramón Y.; Sesé, Marta; Capdevila, Claudia figshare https://doi.org/10.6084/m9.figshare.11702424.v1	text	January 2020
Oligometastatic prostate cancer: Reality or figment of imagination? Foster, Corey C.; Weichselbaum, Ralph R.; Pitroda, Sean P. Cancer, Vol. 125, Issue 3 https://doi.org/10.1002/cncr.31860	journal	December 2018
Corrigendum to “Integration of Copy Number and Transcriptomics Provides Risk Stratification in Prostate Cancer: A Discovery and Validation Cohort Study” [EBioMedicine 2 (9) (2015) 1133–1144] Ross-Adams, H.; Lamb, A. D.; Dunning, M. J. EBioMedicine, Vol. 17 https://doi.org/10.1016/j.ebiom.2017.03.010	journal	March 2017
Comparing nodal versus bony metastatic spread using tumour phylogenies Mangiola, Stefano; Hong, Matthew K. H.; Cmero, Marek Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33918	journal	September 2016
The role of chemotherapy and new targeted agents in the management of primary prostate cancer Kumar, Sanjeev Srinivas; Pacey, Simon Journal of Clinical Urology, Vol. 9, Issue 2_suppl https://doi.org/10.1177/2051415816685211	journal	December 2016
Characterizing the heterogeneity of tumor tissues from spatially resolved molecular measures Graf, John F.; Zavodszky, Maria I. PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0188878	journal	November 2017
Molecular determinants of prostate cancer metastasis Rycaj, Kiera; Tang, Dean G. Oncotarget, Vol. 8, Issue 50 https://doi.org/10.18632/oncotarget.21085	journal	September 2017
Oligometastatic Prostate Cancer: Molecular Imaging and Clinical Management Implications in the Era of Precision Oncology Jadvar, Hossein Journal of Nuclear Medicine, Vol. 59, Issue 9 https://doi.org/10.2967/jnumed.118.213470	journal	July 2018
Phylogenetic Tree Inference: A Top-Down Approach to Track Tumor Evolution Wu, Pin; Hou, Linjun; Zhang, Yingdong Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.01371	journal	February 2020
Correction: A comprehensive analysis of coregulator recruitment, androgen receptor function and gene expression in prostate cancer Liu, Song; Kumari, Sangeeta; Hu, Qiang eLife, Vol. 6 https://doi.org/10.7554/elife.33738	journal	November 2017

Similar Records

BRCA1 loss pre-existing in small subpopulations of prostate cancer is associated with advanced disease and metastatic spread to lymph nodes and peripheral blood

Technical Report · Fri Mar 19 00:00:00 EDT 2010 · OSTI ID:1236642

Bednarz, Natalia; Eltze, Elke; Semjonow, Axel; +9 more

Subclonal diversification of primary breast cancer revealed by multiregion sequencing

Journal Article · Mon Jun 22 00:00:00 EDT 2015 · Nature Medicine · OSTI ID:1236642

Yates, Lucy R.; Gerstung, Moritz; Knappskog, Stian; +35 more

Predictors of Metastatic Disease After Prostate Brachytherapy

Journal Article · Fri Jun 01 00:00:00 EDT 2012 · International Journal of Radiation Oncology, Biology and Physics · OSTI ID:1236642

Forsythe, Kevin; Burri, Ryan; Stone, Nelson

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
biological sciences
cancer
genetics

Title: Tracking the origins and drivers of subclonal metastatic expansion in prostate cancer

Citation Formats

References (68)

Cited By (71)

Similar Records

Related Subjects