The Evolutionary Landscape of Localized Prostate Cancers Drives Clinical Aggression

被引:170
作者
Espiritu, Shadrielle Melijah G. [1 ]
Liu, Lydia Y. [1 ]
Rubanova, Yulia [2 ,3 ]
Bhandari, Vinayak [1 ,4 ]
Holgersen, Erle M. [1 ]
Szyca, Lesia M. [1 ]
Fox, Natalie S. [1 ,4 ]
Chua, Melvin L. K. [5 ]
Yamaguchi, Takafumi N. [1 ]
Heisler, Lawrence E. [1 ]
Livingstone, Julie [1 ]
Wintersinger, Jeff [2 ,3 ]
Yousif, Fouad [1 ]
Lalonde, Emilie [1 ,4 ]
Rouette, Alexandre [1 ]
Salcedo, Adriana [1 ,4 ]
Houlahan, Kathleen E. [1 ,4 ]
Li, Constance H. [1 ,4 ]
Huang, Vincent [1 ]
Fraser, Michael [1 ,5 ]
Van der Kwast, Theodorus [6 ]
Morris, Quaid D. [2 ,3 ,5 ,8 ,9 ]
Bristow, Robert G. [4 ,5 ]
Boutros, Paul C. [1 ,4 ,7 ]
机构
[1] Ontario Inst Canc Res, Informat & Biocomp Program, Toronto, ON M5G 1L7, Canada
[2] Univ Toronto, Dept Comp Sci, Toronto, ON M5S 3G4, Canada
[3] Donnelly Ctr Cellular & Biomol Res, Toronto, ON M5S 3E1, Canada
[4] Univ Toronto, Dept Med Biophys, Toronto, ON M5G 1L7, Canada
[5] Univ Hlth Network, Princess Margaret Canc Ctr, Toronto, ON M5G 2M9, Canada
[6] Toronto Gen Hosp, Univ Hlth Network, Dept Pathol & Lab Med, Toronto, ON M5S 1A1, Canada
[7] Univ Toronto, Dept Pharmacol & Toxicol, Toronto, ON M5S 1A8, Canada
[8] Univ Toronto, Dept Mol Genet, Toronto, ON M5S 1A8, Canada
[9] Vector Inst Artificial Intelligence, Toronto, ON M5G 1M1, Canada
基金
加拿大自然科学与工程研究理事会; 加拿大健康研究院;
关键词
SEQUENCING DATA; INTRATUMOR HETEROGENEITY; TUMORS; MUTATIONS; TRACKING; HISTORY;
D O I
10.1016/j.cell.2018.03.029
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
The majority of newly diagnosed prostate cancers are slow growing, with a long natural life history. Yet a subset can metastasize with lethal consequences. We reconstructed the phylogenies of 293 localized prostate tumors linked to clinical outcome data. Multiple subclones were detected in 59% of patients, and specific subclonal architectures associate with adverse clinicopathological features. Early tumor development is characterized by point mutations and deletions followed by later subclonal amplifications and changes in trinucleotide mutational signatures. Specific genes are selectively mutated prior to or following subclonal diversification, including MTOR, NKX3-1, and RB1. Patients with low-risk monoclonal tumors rarely relapse after primary therapy (7%), while those with high-risk polyclonal tumors frequently do (61%). The presence of multiple subclones in an index biopsy may be necessary, but not sufficient, for relapse of localized prostate cancer, suggesting that evolution-aware biomarkers should be studied in prospective studies of low-risk tumors suitable for active surveillance.
引用
收藏
页码:1003 / +
页数:26
相关论文
共 52 条
[1]   The Molecular Taxonomy of Primary Prostate Cancer [J].
Abeshouse, Adam ;
Ahn, Jaeil ;
Akbani, Rehan ;
Ally, Adrian ;
Amin, Samirkumar ;
Andry, Christopher D. ;
Annala, Matti ;
Aprikian, Armen ;
Armenia, Joshua ;
Arora, Arshi ;
Auman, J. Todd ;
Balasundaram, Miruna ;
Balu, Saianand ;
Barbieri, Christopher E. ;
Bauer, Thomas ;
Benz, Christopher C. ;
Bergeron, Alain ;
Beroukhim, Rameen ;
Berrios, Mario ;
Bivol, Adrian ;
Bodenheimer, Tom ;
Boice, Lori ;
Bootwalla, Moiz S. ;
dos Reis, Rodolfo Borges ;
Boutros, Paul C. ;
Bowen, Jay ;
Bowlby, Reanne ;
Boyd, Jeffrey ;
Bradley, Robert K. ;
Breggia, Anne ;
Brimo, Fadi ;
Bristow, Christopher A. ;
Brooks, Denise ;
Broom, Bradley M. ;
Bryce, Alan H. ;
Bubley, Glenn ;
Burks, Eric ;
Butterfield, Yaron S. N. ;
Button, Michael ;
Canes, David ;
Carlotti, Carlos G. ;
Carlsen, Rebecca ;
Carmel, Michel ;
Carroll, Peter R. ;
Carter, Scott L. ;
Cartun, Richard ;
Carver, Brett S. ;
Chan, June M. ;
Chang, Matthew T. ;
Chen, Yu .
CELL, 2015, 163 (04) :1011-1025
[2]   Signatures of mutational processes in human cancer [J].
Alexandrov, Ludmil B. ;
Nik-Zainal, Serena ;
Wedge, David C. ;
Aparicio, Samuel A. J. R. ;
Behjati, Sam ;
Biankin, Andrew V. ;
Bignell, Graham R. ;
Bolli, Niccolo ;
Borg, Ake ;
Borresen-Dale, Anne-Lise ;
Boyault, Sandrine ;
Burkhardt, Birgit ;
Butler, Adam P. ;
Caldas, Carlos ;
Davies, Helen R. ;
Desmedt, Christine ;
Eils, Roland ;
Eyfjord, Jorunn Erla ;
Foekens, John A. ;
Greaves, Mel ;
Hosoda, Fumie ;
Hutter, Barbara ;
Ilicic, Tomislav ;
Imbeaud, Sandrine ;
Imielinsk, Marcin ;
Jaeger, Natalie ;
Jones, David T. W. ;
Jones, David ;
Knappskog, Stian ;
Kool, Marcel ;
Lakhani, Sunil R. ;
Lopez-Otin, Carlos ;
Martin, Sancha ;
Munshi, Nikhil C. ;
Nakamura, Hiromi ;
Northcott, Paul A. ;
Pajic, Marina ;
Papaemmanuil, Elli ;
Paradiso, Angelo ;
Pearson, John V. ;
Puente, Xose S. ;
Raine, Keiran ;
Ramakrishna, Manasa ;
Richardson, Andrea L. ;
Richter, Julia ;
Rosenstiel, Philip ;
Schlesner, Matthias ;
Schumacher, Ton N. ;
Span, Paul N. ;
Teague, Jon W. .
NATURE, 2013, 500 (7463) :415-+
[3]  
[Anonymous], 2004, MEASURING BIOL DIVER
[4]   Punctuated Evolution of Prostate Cancer Genomes [J].
Baca, Sylvan C. ;
Prandi, Davide ;
Lawrence, Michael S. ;
Mosquera, Juan Miguel ;
Romanel, Alessandro ;
Drier, Yotam ;
Park, Kyung ;
Kitabayashi, Naoki ;
MacDonald, Theresa Y. ;
Ghandi, Mahmoud ;
Van Allen, Eliezer ;
Kryukov, Gregory V. ;
Sboner, Andrea ;
Theurillat, Jean-Philippe ;
Soong, T. David ;
Nickerson, Elizabeth ;
Auclair, Daniel ;
Tewari, Ashutosh ;
Beltran, Himisha ;
Onofrio, Robert C. ;
Boysen, Gunther ;
Guiducci, Candace ;
Barbieri, Christopher E. ;
Cibulskis, Kristian ;
Sivachenko, Andrey ;
Carter, Scott L. ;
Saksena, Gordon ;
Voet, Douglas ;
Ramos, Alex H. ;
Winckler, Wendy ;
Cipicchio, Michelle ;
Ardlie, Kristin ;
Kantoff, Philip W. ;
Berger, Michael F. ;
Gabriel, Stacey B. ;
Golub, Todd R. ;
Meyerson, Matthew ;
Lander, Eric S. ;
Elemento, Olivier ;
Getz, Gad ;
Demichelis, Francesca ;
Rubin, Mark A. ;
Garraway, Levi A. .
CELL, 2013, 153 (03) :666-677
[5]   The genomic complexity of primary human prostate cancer [J].
Berger, Michael F. ;
Lawrence, Michael S. ;
Demichelis, Francesca ;
Drier, Yotam ;
Cibulskis, Kristian ;
Sivachenko, Andrey Y. ;
Sboner, Andrea ;
Esgueva, Raquel ;
Pflueger, Dorothee ;
Sougnez, Carrie ;
Onofrio, Robert ;
Carter, Scott L. ;
Park, Kyung ;
Habegger, Lukas ;
Ambrogio, Lauren ;
Fennell, Timothy ;
Parkin, Melissa ;
Saksena, Gordon ;
Voet, Douglas ;
Ramos, Alex H. ;
Pugh, Trevor J. ;
Wilkinson, Jane ;
Fisher, Sheila ;
Winckler, Wendy ;
Mahan, Scott ;
Ardlie, Kristin ;
Baldwin, Jennifer ;
Simons, Jonathan W. ;
Kitabayashi, Naoki ;
MacDonald, Theresa Y. ;
Kantoff, Philip W. ;
Chin, Lynda ;
Gabriel, Stacey B. ;
Gerstein, Mark B. ;
Golub, Todd R. ;
Meyerson, Matthew ;
Tewari, Ashutosh ;
Lander, Eric S. ;
Getz, Gad ;
Rubin, Mark A. ;
Garraway, Levi A. .
NATURE, 2011, 470 (7333) :214-220
[6]   Spatial genomic heterogeneity within localized, multifocal prostate cancer [J].
Boutros, Paul C. ;
Fraser, Michael ;
Harding, Nicholas J. ;
de Borja, Richard ;
Trudel, Dominique ;
Lalonde, Emilie ;
Meng, Alice ;
Hennings-Yeomans, Pablo H. ;
McPherson, Andrew ;
Sabelnykova, Veronica Y. ;
Zia, Amin ;
Fox, Natalie S. ;
Livingstone, Julie ;
Shiah, Yu-Jia ;
Wang, Jianxin ;
Beck, Timothy A. ;
Have, Cherry L. ;
Chong, Taryne ;
Sam, Michelle ;
Johns, Jeremy ;
Timms, Lee ;
Buchner, Nicholas ;
Wong, Ada ;
Watson, John D. ;
Simmons, Trent T. ;
P'ng, Christine ;
Zafarana, Gaetano ;
Nguyen, Francis ;
Luo, Xuemei ;
Chu, Kenneth C. ;
Prokopec, Stephenie D. ;
Sykes, Jenna ;
Dal Pra, Alan ;
Berlin, Alejandro ;
Brown, Andrew ;
Chan-Seng-Yue, Michelle A. ;
Yousif, Fouad ;
Denroche, Robert E. ;
Chong, Lauren C. ;
Chen, Gregory M. ;
Jung, Esther ;
Fung, Clement ;
Starmans, Maud H. W. ;
Chen, Hanbo ;
Govind, Shaylan K. ;
Hawley, James ;
D'Costa, Alister ;
Pintilie, Melania ;
Waggott, Daryl ;
Hach, Faraz .
NATURE GENETICS, 2015, 47 (07) :736-+
[7]   ContEst: estimating cross-contamination of human samples in next-generation sequencing data [J].
Cibulskis, Kristian ;
McKenna, Aaron ;
Fennell, Tim ;
Banks, Eric ;
DePristo, Mark ;
Getz, Gad .
BIOINFORMATICS, 2011, 27 (18) :2601-2602
[8]   Analysis of the genetic phylogeny of multifocal prostate cancer identifies multiple independent clonal expansions in neoplastic and morphologically normal prostate tissue [J].
Cooper, Colin S. ;
Eeles, Rosalind ;
Wedge, David C. ;
Van Loo, Peter ;
Gundem, Gunes ;
Alexandrov, Ludmil B. ;
Kremeyer, Barbara ;
Butler, Adam ;
Lynch, Andrew G. ;
Camacho, Niedzica ;
Massie, Charlie E. ;
Kay, Jonathan ;
Luxton, Hayley J. ;
Edwards, Sandra ;
Kote-Jarai, Zsofia ;
Dennis, Nening ;
Merson, Sue ;
Leongamornlert, Daniel ;
Zamora, Jorge ;
Corbishley, Cathy ;
Thomas, Sarah ;
Nik-Zainal, Serena ;
O'Meara, Sarah ;
Matthews, Lucy ;
Clark, Jeremy ;
Hurst, Rachel ;
Mithen, Richard ;
Bristow, Robert G. ;
Boutros, Paul C. ;
Fraser, Michael ;
Cooke, Susanna ;
Raine, Keiran ;
Jones, David ;
Menzies, Andrew ;
Stebbings, Lucy ;
Hinton, Jon ;
Teague, Jon ;
McLaren, Stuart ;
Mudie, Laura ;
Hardy, Claire ;
Anderson, Elizabeth ;
Joseph, Olivia ;
Goody, Victoria ;
Robinson, Ben ;
Maddison, Mark ;
Gamble, Stephen ;
Greenman, Christopher ;
Berney, Dan ;
Hazell, Steven ;
Livni, Naomi .
NATURE GENETICS, 2015, 47 (04) :367-U118
[9]   Prognostic value of an RNA expression signature derived from cell cycle proliferation genes in patients with prostate cancer: a retrospective study [J].
Cuzick, Jack ;
Swanson, Gregory P. ;
Fisher, Gabrielle ;
Brothman, Arthur R. ;
Berney, Daniel M. ;
Reid, Julia E. ;
Mesher, David ;
Speights, V. O. ;
Stankiewicz, Elzbieta ;
Foster, Christopher S. ;
Moller, Henrik ;
Scardino, Peter ;
Warren, Jorja D. ;
Park, Jimmy ;
Younus, Adib ;
Flake, Dart D., II ;
Wagner, Susanne ;
Gutin, Alexander ;
Lanchbury, Jerry S. ;
Stone, Steven .
LANCET ONCOLOGY, 2011, 12 (03) :245-255
[10]   Spatial and temporal diversity in genomic instability processes defines lung cancer evolution [J].
de Bruin, Elza C. ;
McGranahan, Nicholas ;
Mitter, Richard ;
Salm, Max ;
Wedge, David C. ;
Yates, Lucy ;
Jamal-Hanjani, Mariam ;
Shafi, Seema ;
Murugaesu, Nirupa ;
Rowan, Andrew J. ;
Groenroos, Eva ;
Muhammad, Madiha A. ;
Horswell, Stuart ;
Gerlinger, Marco ;
Varela, Ignacio ;
Jones, David ;
Marshall, John ;
Voet, Thierry ;
Van Loo, Peter ;
Rassl, Doris M. ;
Rintoul, Robert C. ;
Janes, Sam M. ;
Lee, Siow-Ming ;
Forster, Martin ;
Ahmad, Tanya ;
Lawrence, David ;
Falzon, Mary ;
Capitanio, Arrigo ;
Harkins, Timothy T. ;
Lee, Clarence C. ;
Tom, Warren ;
Teefe, Enock ;
Chen, Shann-Ching ;
Begum, Sharmin ;
Rabinowitz, Adam ;
Phillimore, Benjamin ;
Spencer-Dene, Bradley ;
Stamp, Gordon ;
Szallasi, Zoltan ;
Matthews, Nik ;
Stewart, Aengus ;
Campbell, Peter ;
Swanton, Charles .
SCIENCE, 2014, 346 (6206) :251-256