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1. Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells.

Author

Rosano, Dalia, Sofyali, Emre, Dhiman, Heena, Ghirardi, Chiara, Ivanoiu, Diana, Heide, Timon, Vingiani, Andrea, Bertolotti, Alessia, Pruneri, Giancarlo, Canale, Eleonora, Dewhurst, Hannah, Saha, Debjani, Barozzi, Iros, Li, Tong, Zemlyanskiy, Grigory, Phillips, Henry, James, Chela, Győrffy, Balázs, Lynn, Claire, Cresswell, George, Rehman, Farah, Noberini, Roberta, Bonaldi, Tiziana, Sottoriva, Andrea, Magnani, Luca, and Slaven, Neil

Subjects
Humans, Breast Neoplasms, Female, Epigenesis, Genetic, Neoplasm Recurrence, Local, Gene Expression Regulation, Neoplastic
Abstract

UNLABELLED: Patients with estrogen receptor-positive breast cancer receive adjuvant endocrine therapies (ET) that delay relapse by targeting clinically undetectable micrometastatic deposits. Yet, up to 50% of patients relapse even decades after surgery through unknown mechanisms likely involving dormancy. To investigate genetic and transcriptional changes underlying tumor awakening, we analyzed late relapse patients and longitudinally profiled a rare cohort treated with long-term neoadjuvant ETs until progression. Next, we developed an in vitro evolutionary study to record the adaptive strategies of individual lineages in unperturbed parallel experiments. Our data demonstrate that ETs induce nongenetic cell state transitions into dormancy in a stochastic subset of cells via epigenetic reprogramming. Single lineages with divergent phenotypes awaken unpredictably in the absence of recurrent genetic alterations. Targeting the dormant epigenome shows promising activity against adapting cancer cells. Overall, this study uncovers the contribution of epigenetic adaptation to the evolution of resistance to ETs. SIGNIFICANCE: This study advances the understanding of therapy-induced dormancy with potential clinical implications for breast cancer. Estrogen receptor-positive breast cancer cells adapt to endocrine treatment by entering a dormant state characterized by strong heterochromatinization with no recurrent genetic changes. Targeting the epigenetic rewiring impairs the adaptation of cancer cells to ETs. See related commentary by Llinas-Bertran et al., p. 704. This article is featured in Selected Articles from This Issue, p. 695.

Published
2024

2. The genomic landscape of 2,023 colorectal cancers

Author

Cornish, Alex J., Gruber, Andreas J., Kinnersley, Ben, Chubb, Daniel, Frangou, Anna, Caravagna, Giulio, Noyvert, Boris, Lakatos, Eszter, Wood, Henry M., Thorn, Steve, Culliford, Richard, Arnedo-Pac, Claudia, Househam, Jacob, Cross, William, Sud, Amit, Law, Philip, Leathlobhair, Maire Ni, Hawari, Aliah, Woolley, Connor, Sherwood, Kitty, Feeley, Nathalie, Gül, Güler, Fernandez-Tajes, Juan, Zapata, Luis, Alexandrov, Ludmil B., Murugaesu, Nirupa, Sosinsky, Alona, Mitchell, Jonathan, Lopez-Bigas, Nuria, Quirke, Philip, Church, David N., Tomlinson, Ian P. M., Sottoriva, Andrea, Graham, Trevor A., Wedge, David C., and Houlston, Richard S.

Published
2024
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3. Tumor evolution metrics predict recurrence beyond 10 years in locally advanced prostate cancer

Author

Fernandez-Mateos, Javier, Cresswell, George D., Trahearn, Nicholas, Webb, Katharine, Sakr, Chirine, Lampis, Andrea, Stuttle, Christine, Corbishley, Catherine M., Stavrinides, Vasilis, Zapata, Luis, Spiteri, Inmaculada, Heide, Timon, Gallagher, Lewis, James, Chela, Ramazzotti, Daniele, Gao, Annie, Kote-Jarai, Zsofia, Acar, Ahmet, Truelove, Lesley, Proszek, Paula, Murray, Julia, Reid, Alison, Wilkins, Anna, Hubank, Michael, Eeles, Ros, Dearnaley, David, and Sottoriva, Andrea

Published
2024
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4. Homopolymer switches mediate adaptive mutability in mismatch repair-deficient colorectal cancer

Author

Kayhanian, Hamzeh, Cross, William, van der Horst, Suzanne E. M., Barmpoutis, Panagiotis, Lakatos, Eszter, Caravagna, Giulio, Zapata, Luis, Van Hoeck, Arne, Middelkamp, Sjors, Litchfield, Kevin, Steele, Christopher, Waddingham, William, Patel, Dominic, Milite, Salvatore, Jin, Chen, Baker, Ann-Marie, Alexander, Daniel C., Khan, Khurum, Hochhauser, Daniel, Novelli, Marco, Werner, Benjamin, van Boxtel, Ruben, Hageman, Joris H., Buissant des Amorie, Julian R., Linares, Josep, Ligtenberg, Marjolijn J. L., Nagtegaal, Iris D., Laclé, Miangela M., Moons, Leon M. G., Brosens, Lodewijk A. A., Pillay, Nischalan, Sottoriva, Andrea, Graham, Trevor A., Rodriguez-Justo, Manuel, Shiu, Kai-Keen, Snippert, Hugo J. G., and Jansen, Marnix

Published
2024
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9. The co-evolution of the genome and epigenome in colorectal cancer

Author

Heide, Timon, Househam, Jacob, Cresswell, George D., Spiteri, Inmaculada, Lynn, Claire, Mossner, Maximilian, Kimberley, Chris, Fernandez-Mateos, Javier, Chen, Bingjie, Zapata, Luis, James, Chela, Barozzi, Iros, Chkhaidze, Ketevan, Nichol, Daniel, Gunasri, Vinaya, Berner, Alison, Schmidt, Melissa, Lakatos, Eszter, Baker, Ann-Marie, Costa, Helena, Mitchinson, Miriam, Piazza, Rocco, Jansen, Marnix, Caravagna, Giulio, Ramazzotti, Daniele, Shibata, Darryl, Bridgewater, John, Rodriguez-Justo, Manuel, Magnani, Luca, Graham, Trevor A., and Sottoriva, Andrea

Published
2022
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10. Phenotypic plasticity and genetic control in colorectal cancer evolution

Author

Househam, Jacob, Heide, Timon, Cresswell, George D., Spiteri, Inmaculada, Kimberley, Chris, Zapata, Luis, Lynn, Claire, James, Chela, Mossner, Maximilian, Fernandez-Mateos, Javier, Vinceti, Alessandro, Baker, Ann-Marie, Gabbutt, Calum, Berner, Alison, Schmidt, Melissa, Chen, Bingjie, Lakatos, Eszter, Gunasri, Vinaya, Nichol, Daniel, Costa, Helena, Mitchinson, Miriam, Ramazzotti, Daniele, Werner, Benjamin, Iorio, Francesco, Jansen, Marnix, Caravagna, Giulio, Barnes, Chris P., Shibata, Darryl, Bridgewater, John, Rodriguez-Justo, Manuel, Magnani, Luca, Sottoriva, Andrea, and Graham, Trevor A.

Published
2022
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12. Immunosuppressive niche engineering at the onset of human colorectal cancer

Author

Gatenbee, Chandler D., Baker, Ann-Marie, Schenck, Ryan O., Strobl, Maximilian, West, Jeffrey, Neves, Margarida P., Hasan, Sara Yakub, Lakatos, Eszter, Martinez, Pierre, Cross, William C. H., Jansen, Marnix, Rodriguez-Justo, Manuel, Whelan, Christopher J., Sottoriva, Andrea, Leedham, Simon, Robertson-Tessi, Mark, Graham, Trevor A., and Anderson, Alexander R. A.

Published
2022
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13. Supplementary Table 5 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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14. Supplementary Figure S12 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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15. Supplementary Table 3 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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16. Figure 1 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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17. Figure 5 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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18. Figure 6 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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19. Supplementary Table 8 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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20. Supplementary Table 2 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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21. Supplementary Table 7 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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22. Figure 4 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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23. Figure 3 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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24. Supplementary Table 6 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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25. Supplementary Table 4 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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26. Supplementary Table 1 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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27. Figure 2 from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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28. Data from Long-term Multimodal Recording Reveals Epigenetic Adaptation Routes in Dormant Breast Cancer Cells

Author

Rosano, Dalia, primary, Sofyali, Emre, primary, Dhiman, Heena, primary, Ghirardi, Chiara, primary, Ivanoiu, Diana, primary, Heide, Timon, primary, Vingiani, Andrea, primary, Bertolotti, Alessia, primary, Pruneri, Giancarlo, primary, Canale, Eleonora, primary, Dewhurst, Hannah F., primary, Saha, Debjani, primary, Slaven, Neil, primary, Barozzi, Iros, primary, Li, Tong, primary, Zemlyanskiy, Grigory, primary, Phillips, Henry, primary, James, Chela, primary, Győrffy, Balázs, primary, Lynn, Claire, primary, Cresswell, George D., primary, Rehman, Farah, primary, Noberini, Roberta, primary, Bonaldi, Tiziana, primary, Sottoriva, Andrea, primary, and Magnani, Luca, primary

Published
2024
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29. Classifying the evolutionary and ecological features of neoplasms

Author

Maley, Carlo C, Aktipis, Athena, Graham, Trevor A, Sottoriva, Andrea, Boddy, Amy M, Janiszewska, Michalina, Silva, Ariosto S, Gerlinger, Marco, Yuan, Yinyin, Pienta, Kenneth J, Anderson, Karen S, Gatenby, Robert, Swanton, Charles, Posada, David, Wu, Chung-I, Schiffman, Joshua D, Hwang, E Shelley, Polyak, Kornelia, Anderson, Alexander RA, Brown, Joel S, Greaves, Mel, and Shibata, Darryl

Subjects
Biomedical and Clinical Sciences, Health Sciences, Cancer, Antigens, Neoplasm, Biological Evolution, Ecological and Environmental Phenomena, Gene Expression, Genetic Variation, Humans, Microbiota, Neoplasms, Phenotype, Reactive Oxygen Species, Time Factors, Tumor Hypoxia, Tumor Microenvironment, Medical and Health Sciences, Oncology & Carcinogenesis, Biomedical and clinical sciences, Health sciences
Abstract

Neoplasms change over time through a process of cell-level evolution, driven by genetic and epigenetic alterations. However, the ecology of the microenvironment of a neoplastic cell determines which changes provide adaptive benefits. There is widespread recognition of the importance of these evolutionary and ecological processes in cancer, but to date, no system has been proposed for drawing clinically relevant distinctions between how different tumours are evolving. On the basis of a consensus conference of experts in the fields of cancer evolution and cancer ecology, we propose a framework for classifying tumours that is based on four relevant components. These are the diversity of neoplastic cells (intratumoural heterogeneity) and changes over time in that diversity, which make up an evolutionary index (Evo-index), as well as the hazards to neoplastic cell survival and the resources available to neoplastic cells, which make up an ecological index (Eco-index). We review evidence demonstrating the importance of each of these factors and describe multiple methods that can be used to measure them. Development of this classification system holds promise for enabling clinicians to personalize optimal interventions based on the evolvability of the patient's tumour. The Evo- and Eco-indices provide a common lexicon for communicating about how neoplasms change in response to interventions, with potential implications for clinical trials, personalized medicine and basic cancer research.

Published
2017

30. Reconstructing single-cell karyotype alterations in colorectal cancer identifies punctuated and gradual diversification patterns

Author

Bollen, Yannik, Stelloo, Ellen, van Leenen, Petra, van den Bos, Myrna, Ponsioen, Bas, Lu, Bingxin, van Roosmalen, Markus J., Bolhaqueiro, Ana C. F., Kimberley, Christopher, Mossner, Maximilian, Cross, William C. H., Besselink, Nicolle J. M., van der Roest, Bastiaan, Boymans, Sander, Oost, Koen C., de Vries, Sippe G., Rehmann, Holger, Cuppen, Edwin, Lens, Susanne M. A., Kops, Geert J. P. L., Kloosterman, Wigard P., Terstappen, Leon W. M. M., Barnes, Chris P., Sottoriva, Andrea, Graham, Trevor A., and Snippert, Hugo J. G.

Published
2021
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31. Tumor evolution metrics predict recurrence beyond 10 years in locally advanced prostate cancer

Author

Fernandez-Mateos, J, Cresswell, G, Trahearn, N, Webb, K, Sakr, C, Lampis, A, Stuttle, C, Corbishley, C, Stavrinides, V, Zapata, L, Spiteri, I, Heide, T, Gallagher, L, James, C, Ramazzotti, D, Gao, A, Kote-Jarai, Z, Acar, A, Truelove, L, Proszek, P, Murray, J, Reid, A, Wilkins, A, Hubank, M, Eeles, R, Dearnaley, D, Sottoriva, A, Fernandez-Mateos, Javier, Cresswell, George D., Trahearn, Nicholas, Webb, Katharine, Sakr, Chirine, Lampis, Andrea, Stuttle, Christine, Corbishley, Catherine M., Stavrinides, Vasilis, Zapata, Luis, Spiteri, Inmaculada, Heide, Timon, Gallagher, Lewis, James, Chela, Ramazzotti, Daniele, Gao, Annie, Kote-Jarai, Zsofia, Acar, Ahmet, Truelove, Lesley, Proszek, Paula, Murray, Julia, Reid, Alison, Wilkins, Anna, Hubank, Michael, Eeles, Ros, Dearnaley, David, Sottoriva, Andrea, Fernandez-Mateos, J, Cresswell, G, Trahearn, N, Webb, K, Sakr, C, Lampis, A, Stuttle, C, Corbishley, C, Stavrinides, V, Zapata, L, Spiteri, I, Heide, T, Gallagher, L, James, C, Ramazzotti, D, Gao, A, Kote-Jarai, Z, Acar, A, Truelove, L, Proszek, P, Murray, J, Reid, A, Wilkins, A, Hubank, M, Eeles, R, Dearnaley, D, Sottoriva, A, Fernandez-Mateos, Javier, Cresswell, George D., Trahearn, Nicholas, Webb, Katharine, Sakr, Chirine, Lampis, Andrea, Stuttle, Christine, Corbishley, Catherine M., Stavrinides, Vasilis, Zapata, Luis, Spiteri, Inmaculada, Heide, Timon, Gallagher, Lewis, James, Chela, Ramazzotti, Daniele, Gao, Annie, Kote-Jarai, Zsofia, Acar, Ahmet, Truelove, Lesley, Proszek, Paula, Murray, Julia, Reid, Alison, Wilkins, Anna, Hubank, Michael, Eeles, Ros, Dearnaley, David, and Sottoriva, Andrea

Abstract

Cancer evolution lays the groundwork for predictive oncology. Testing evolutionary metrics requires quantitative measurements in controlled clinical trials. We mapped genomic intratumor heterogeneity in locally advanced prostate cancer using 642 samples from 114 individuals enrolled in clinical trials with a 12-year median follow-up. We concomitantly assessed morphological heterogeneity using deep learning in 1,923 histological sections from 250 individuals. Genetic and morphological (Gleason) diversity were independent predictors of recurrence (hazard ratio (HR) = 3.12 and 95% confidence interval (95% CI) = 1.34-7.3; HR = 2.24 and 95% CI = 1.28-3.92). Combined, they identified a group with half the median time to recurrence. Spatial segregation of clones was also an independent marker of recurrence (HR = 2.3 and 95% CI = 1.11-4.8). We identified copy number changes associated with Gleason grade and found that chromosome 6p loss correlated with reduced immune infiltration. Matched profiling of relapse, decades after diagnosis, confirmed that genomic instability is a driving force in prostate cancer progression. This study shows that combining genomics with artificial intelligence-aided histopathology leads to the identification of clinical biomarkers of evolution.

Published
2024

32. Homopolymer switches mediate adaptive mutability in mismatch repair-deficient colorectal cancer

Author

CMM Groep Snippert, CMM Groep Cuppen, Cancer, Pathologie Pathologen staf, MS MDL 1, Kayhanian, Hamzeh, Cross, William, van der Horst, Suzanne E M, Barmpoutis, Panagiotis, Lakatos, Eszter, Caravagna, Giulio, Zapata, Luis, Van Hoeck, Arne, Middelkamp, Sjors, Litchfield, Kevin, Steele, Christopher, Waddingham, William, Patel, Dominic, Milite, Salvatore, Jin, Chen, Baker, Ann-Marie, Alexander, Daniel C, Khan, Khurum, Hochhauser, Daniel, Novelli, Marco, Werner, Benjamin, van Boxtel, Ruben, Hageman, Joris H, Buissant des Amorie, Julian R, Linares, Josep, Ligtenberg, Marjolijn J L, Nagtegaal, Iris D, Laclé, Miangela M, Moons, Leon M G, Brosens, Lodewijk A A, Pillay, Nischalan, Sottoriva, Andrea, Graham, Trevor A, Rodriguez-Justo, Manuel, Shiu, Kai-Keen, Snippert, Hugo J G, Jansen, Marnix, CMM Groep Snippert, CMM Groep Cuppen, Cancer, Pathologie Pathologen staf, MS MDL 1, Kayhanian, Hamzeh, Cross, William, van der Horst, Suzanne E M, Barmpoutis, Panagiotis, Lakatos, Eszter, Caravagna, Giulio, Zapata, Luis, Van Hoeck, Arne, Middelkamp, Sjors, Litchfield, Kevin, Steele, Christopher, Waddingham, William, Patel, Dominic, Milite, Salvatore, Jin, Chen, Baker, Ann-Marie, Alexander, Daniel C, Khan, Khurum, Hochhauser, Daniel, Novelli, Marco, Werner, Benjamin, van Boxtel, Ruben, Hageman, Joris H, Buissant des Amorie, Julian R, Linares, Josep, Ligtenberg, Marjolijn J L, Nagtegaal, Iris D, Laclé, Miangela M, Moons, Leon M G, Brosens, Lodewijk A A, Pillay, Nischalan, Sottoriva, Andrea, Graham, Trevor A, Rodriguez-Justo, Manuel, Shiu, Kai-Keen, Snippert, Hugo J G, and Jansen, Marnix

Published
2024

33. Heterogeneity and evolution of DNA mutation rates in microsatellite stable colorectal cancer

Author

Grassi, Elena, primary, Vurchio, Valentina, additional, Cresswell, George David, additional, Catalano, Irene, additional, Lupo, Barbara, additional, Sassi, Francesco, additional, Galimi, Francesco, additional, Borgato, Sofia, additional, Ferri, Martina, additional, Viviani, Marco, additional, Pompei, Simone, additional, Urgese, Gianvito, additional, Chen, Bingjie, additional, Zanella, Eugenia Rosalinda, additional, Cottino, Francesca, additional, Bardelli, Alberto, additional, Cosentino Lagormarsino, Marco, additional, Sottoriva, Andrea, additional, Trusolino, Livio, additional, and Bertotti, Andrea, additional

Published
2024
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34. Epigenome and early selection determine the tumour-immune evolutionary trajectory of colorectal cancer

Author

Lakatos, Eszter, primary, Gunasri, Vinaya, additional, Zapata, Luis, additional, Househam, Jacob, additional, Heide, Timon, additional, Trahearn, Nicholas, additional, Swinyard, Ottilie, additional, Cisneros, Luis, additional, Lynn, Claire, additional, Mossner, Maximilian, additional, Kimberley, Chris, additional, Spiteri, Inmaculada, additional, Cresswell, George D., additional, Llibre-Palomar, Gerard, additional, Mitchison, Miriam, additional, Maley, Carlo C., additional, Jansen, Marnix, additional, Rodriguez-Justo, Manuel, additional, Bridgewater, John, additional, Baker, Ann-Marie, additional, Sottoriva, Andrea, additional, and Graham, Trevor A., additional

Published
2024
Full Text
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35. Evolutionary dynamics of neoantigens in growing tumors

Author

Lakatos, Eszter, Williams, Marc J., Schenck, Ryan O., Cross, William C. H., Househam, Jacob, Zapata, Luis, Werner, Benjamin, Gatenbee, Chandler, Robertson-Tessi, Mark, Barnes, Chris P., Anderson, Alexander R. A., Sottoriva, Andrea, and Graham, Trevor A.

Published
2020
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38. Cancer Evolution: A Multifaceted Affair

Author

Ciriello, Giovanni, primary, Magnani, Luca, additional, Aitken, Sarah J., additional, Akkari, Leila, additional, Behjati, Sam, additional, Hanahan, Douglas, additional, Landau, Dan A., additional, Lopez-Bigas, Nuria, additional, Lupiáñez, Darío G., additional, Marine, Jean-Christophe, additional, Martin-Villalba, Ana, additional, Natoli, Gioacchino, additional, Obenauf, Anna C., additional, Oricchio, Elisa, additional, Scaffidi, Paola, additional, Sottoriva, Andrea, additional, Swarbrick, Alexander, additional, Tonon, Giovanni, additional, Vanharanta, Sakari, additional, and Zuber, Johannes, additional

Published
2023
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41. Patient-derived organoids model treatment response of metastatic gastrointestinal cancers

Author

Vlachogiannis, Georgios, Hedayat, Somaieh, Vatsiou, Alexandra, Jamin, Yann, Fernández-Mateos, Javier, Khan, Khurum, Lampis, Andrea, Eason, Katherine, Huntingford, Ian, Burke, Rosemary, Rata, Mihaela, Koh, Dow-Mu, Tunariu, Nina, Collins, David, Hulkki-Wilson, Sanna, Ragulan, Chanthirika, Spiteri, Inmaculada, Moorcraft, Sing Yu, Chau, Ian, Rao, Sheela, Watkins, David, Fotiadis, Nicos, Bali, Maria, Darvish-Damavandi, Mahnaz, Lote, Hazel, Eltahir, Zakaria, Smyth, Elizabeth C., Begum, Ruwaida, Clarke, Paul A., Hahne, Jens C., Dowsett, Mitchell, de Bono, Johann, Workman, Paul, Sadanandam, Anguraj, Fassan, Matteo, Sansom, Owen J., Eccles, Suzanne, Starling, Naureen, Braconi, Chiara, Sottoriva, Andrea, Robinson, Simon P., Cunningham, David, and Valeri, Nicola

Published
2018

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