Cancer is an evolutionary process fueled by genetic or epigenetic alterations in the genome. Understanding the evolutionary dynamics that are operative at different stages of tumor progression might inform effective strategies in early detection, diagnosis, and treatment of cancer. However, our understanding on the dynamics of tumor evolution through time is very limited since it is usually impossible to sample patient tumors repeatedly. The recent advances in in vitro 3D organoid culture technologies have opened new avenues for the development of more realistic human cancer models that mimic many in vivo biological characteristics in human tumors. Here, we review recent progresses and challenges in cancer genomic evolution studies and advantages of using tumor organoids to study cancer evolution. We propose to establish an experimental evolution model based on continuous passages of patient-derived organoids and longitudinal sampling to study clonal dynamics and evolutionary patterns over time. Development and integration of population genetic theories and computational models into time-course genomic data in tumor organoids will help to pinpoint the key cellular mechanisms underlying cancer evolutionary dynamics, thus providing novel insights on therapeutic strategies for highly dynamic and heterogeneous tumors.
|
Alexandrov, L.B., Jones, P.H., Wedge, D.C., Sale, J.E., Campbell, P.J., Nik-Zainal, S., Stratton, M.R., 2015. Clock-like mutational processes in human somatic cells. Nat. Genet. 47, 1402-1407.
|
|
Armitage, P., Doll, R., 1954. The age distribution of cancer and a multi-stage theory of carcinogenesis. Br. J. Cancer 8, 1-12.
|
|
Baca, S.C., Prandi, D., Lawrence, M.S., Mosquera, J.M., Romanel, A., Drier, Y., Park, K., Kitabayashi, N., MacDonald, T.Y., Ghandi, M., et al., 2013. Punctuated evolution of prostate cancer genomes. Cell 153, 666-677.
|
|
Bakhoum, S.F., Landau, D.A., 2017. Cancer evolution:No room for negative selection. Cell 171, 987-989.
|
|
Barrick, J.E., Lenski, R.E., 2013. Genome dynamics during experimental evolution. Nat. Rev. Genet. 14, 827-839.
|
|
Ben-David, U., Beroukhim, R., Golub, T.R., 2019. Genomic evolution of cancer models:perils and opportunities. Nat. Rev. Cancer 19, 97-109.
|
|
Bhang, H.E., Ruddy, D.A., Krishnamurthy Radhakrishna, V., Caushi, J.X., Zhao, R., Hims, M.M., Singh, A.P., Kao, I., Rakiec, D., Shaw, P., et al., 2015. Studying clonal dynamics in response to cancer therapy using high-complexity barcoding. Nat. Med. 21, 440-448.
|
|
Bian, S., Hou, Y., Zhou, X., Li, X., Yong, J., Wang, Y., Wang, W., Yan, J., Hu, B., Guo, H., et al., 2018. Single-cell multiomics sequencing and analyses of human colorectal cancer. Science 362, 1060-1063.
|
|
Black, J.R.M., McGranahan, N., 2021. Genetic and non-genetic clonal diversity in cancer evolution. Nat. Rev. Cancer 21, 379-392.
|
|
Blount, Z.D., Borland, C.Z., Lenski, R.E., 2008. Historical contingency and the evolution of a key innovation in an experimental population of escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 105, 7899-7906.
|
|
Blount, Z.D., Lenski, R.E., Losos, J.B., 2018. Contingency and determinism in evolution:replaying life's tape. Science 362, eaam5979.
|
|
Bolhaqueiro, A.C.F., Ponsioen, B., Bakker, B., Klaasen, S.J., Kucukkose, E., van Jaarsveld, R.H., Vivie, J., Verlaan-Klink, I., Hami, N., Spierings, D.C.J., et al., 2019. Ongoing chromosomal instability and karyotype evolution in human colorectal cancer organoids. Nat. Genet. 51, 824-834.
|
|
Brastianos, P.K., Carter, S.L., Santagata, S., Cahill, D.P., Taylor-Weiner, A., Jones, R.T., Van Allen, E.M., Lawrence, M.S., Horowitz, P.M., Cibulskis, K., et al., 2015. Genomic characterization of brain metastases reveals branched evolution and potential therapeutic targets. Cancer Discov. 5, 1164-1177.
|
|
Broutier, L., Mastrogiovanni, G., Verstegen, M.M., Francies, H.E., Gavarro, L.M., Bradshaw, C.R., Allen, G.E., Arnes-Benito, R., Sidorova, O., Gaspersz, M.P., et al., 2017. Human primary liver cancer-derived organoid cultures for disease modeling and drug screening. Nat. Med. 23, 1424-1435.
|
|
Buenrostro, J.D., Wu, B., Litzenburger, U.M., Ruff, D., Gonzales, M.L., Snyder, M.P., Chang, H.Y., Greenleaf, W.J., 2015. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523, 486-490.
|
|
Campbell, P.J., Yachida, S., Mudie, L.J., Stephens, P.J., Pleasance, E.D., Stebbings, L.A., Morsberger, L.A., Latimer, C., McLaren, S., Lin, M.L., et al., 2010. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467, 1109-1113.
|
|
Chen, X.X., Zhong, Q., Liu, Y., Yan, S.M., Chen, Z.H., Jin, S.Z., Xia, T.L., Li, R.Y., Zhou, A.J., Su, Z., et al., 2017. Genomic comparison of esophageal squamous cell carcinoma and its precursor lesions by multi-region whole-exome sequencing. Nat. Commun. 8, 524.
|
|
Clevers, H., Tuveson, D.A., 2019. Organoid models for cancer research. Annu. Rev. Cancer Biol. 3, 223-234.
|
|
Cross, W., Kovac, M., Mustonen, V., Temko, D., Davis, H., Baker, A.M., Biswas, S., Arnold, R., Chegwidden, L., Gatenbee, C., et al., 2018. The evolutionary landscape of colorectal tumorigenesis. Nat. Ecol. Evol. 2, 1661-1672.
|
|
Curtius, K., Wright, N.A., Graham, T.A., 2017. Evolution of premalignant disease. Cold Spring Harb Perspect. Med. 7, a026542.
|
|
Davis, A., Gao, R., Navin, N., 2017. Tumor evolution:linear, branching, neutral or punctuated? Biochim. Biophys. Acta Rev. Cancer 1867, 151-161.
|
|
Della Chiara, G., Gervasoni, F., Fakiola, M., Godano, C., D'Oria, C., Azzolin, L., Bonnal, R.J.P., Moreni, G., Drufuca, L., Rossetti, G., et al., 2021. Epigenomic landscape of human colorectal cancer unveils an aberrant core of pan-cancer enhancers orchestrated by YAP/TA. Nat. Commun. 12, 2340.
|
|
Devarasetty, M., Forsythe, S.D., Shelkey, E., Soker, S., 2020. In vitro modeling of the tumor microenvironment in tumor organoids. Tissue Eng. Regen. Med. 17, 759-771.
|
|
Diaz Jr., L.A., Williams, R.T., Wu, J., Kinde, I., Hecht, J.R., Berlin, J., Allen, B., Bozic, I., Reiter, J.G., Nowak, M.A., et al., 2012. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486, 537-540.
|
|
Ding, L., Ley, T.J., Larson, D.E., Miller, C.A., Koboldt, D.C., Welch, J.S., Ritchey, J.K., Young, M.A., Lamprecht, T., McLellan, M.D., et al., 2012. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 481, 506-510.
|
|
Doglioni, G., Parik, S., Fendt, S.M., 2019. Interactions in the (pre)metastatic niche support metastasis formation. Front. Oncol. 9, 219.
|
|
Drost, J., van Jaarsveld, R.H., Ponsioen, B., Zimberlin, C., van Boxtel, R., Buijs, A., Sachs, N., Overmeer, R.M., Offerhaus, G.J., Begthel, H., et al., 2015. Sequential cancer mutations in cultured human intestinal stem cells. Nature 521, 43-47.
|
|
Fearon, E.R., Vogelstein, B., 1990. A genetic model for colorectal tumorigenesis. Cell 61, 759-767.
|
|
Flavahan, W.A., Gaskell, E., Bernstein, B.E., 2017. Epigenetic plasticity and the hallmarks of cancer. Science 357, eaal2380.
|
|
Forment, J.V., Kaidi, A., Jackson, S.P., 2012. Chromothripsis and cancer:causes and consequences of chromosome shattering. Nat. Rev. Cancer 12, 663-670.
|
|
Fujii, M., Shimokawa, M., Date, S., Takano, A., Matano, M., Nanki, K., Ohta, Y., Toshimitsu, K., Nakazato, Y., Kawasaki, K., et al., 2016. A colorectal tumor organoid library demonstrates progressive loss of niche factor requirements during tumorigenesis. Cell Stem Cell 18, 827-838.
|
|
Gao, R., Davis, A., McDonald, T.O., Sei, E., Shi, X., Wang, Y., Tsai, P.C., Casasent, A., Waters, J., Zhang, H., et al., 2016. Punctuated copy number evolution and clonal stasis in triple-negative breast cancer. Nat. Genet. 48, 1119-1130.
|
|
Gerlinger, M., Horswell, S., Larkin, J., Rowan, A.J., Salm, M.P., Varela, I., Fisher, R., McGranahan, N., Matthews, N., Santos, C.R., et al., 2014. Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing. Nat. Genet. 46, 225-233.
|
|
Gerlinger, M., Rowan, A.J., Horswell, S., Math, M., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., et al., 2012. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892.
|
|
Gerrish, P.J., Lenski, R.E., 1998. The fate of competing beneficial mutations in an asexual population. Genetica 102-103, 127-144.
|
|
Good, B.H., McDonald, M.J., Barrick, J.E., Lenski, R.E., Desai, M.M., 2017. The dynamics of molecular evolution over 60,000 generations. Nature 551, 45-50.
|
|
Gould, S.J., 2002. The structure of evolutionary theory. Belknap Press, Cambridge, Massachusetts and London.
|
|
Greaves, M., 2015. Evolutionary determinants of cancer. Cancer Discov. 5, 806-820.
|
|
Greaves, M., Maley, C.C., 2012. Clonal evolution in cancer. Nature 481, 306-313.
|
|
Hartl, D.L., Clark, A.G., 2007. Principles of Population Genetics. Sinauer Associates, Inc., Sunderland, Massachusetts.
|
|
Hill, W.G., Robertson, A., 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8, 269-294.
|
|
Hope, E.A., Amorosi, C.J., Miller, A.W., Dang, K., Heil, C.S., Dunham, M.J., 2017. Experimental evolution reveals favored adaptive routes to cell aggregation in yeast. Genetics 206, 1153-1167.
|
|
Hu, Z., Ding, J., Ma, Z., Sun, R., Seoane, J.A., Scott Shaffer, J., Suarez, C.J., Berghoff, A.S., Cremolini, C., Falcone, A., et al., 2019. Quantitative evidence for early metastatic seeding in colorectal cancer. Nat. Genet. 51, 1113-1122.
|
|
Hu, Z., Li, Z., Ma, Z., Curtis, C., 2020. Multi-cancer analysis of clonality and the timing of systemic spread in paired primary tumors and metastases. Nat. Genet. 52, 701-708.
|
|
Hu, Z., Sun, R., Curtis, C., 2017. A population genetics perspective on the determinants of intra-tumor heterogeneity. Biochim. Biophys. Acta. Rev. Cancer 1867, 109-126.
|
|
Huang, S., 2021. Reconciling non-genetic plasticity with somatic evolution in cancer. Trends Cancer 7, 309-322.
|
|
Jimenez-Sanchez, A., Memon, D., Pourpe, S., Veeraraghavan, H., Li, Y., Vargas, H.A., Gill, M.B., Park, K.J., Zivanovic, O., Konner, J., et al., 2017. Heterogeneous tumor-immune microenvironments among differentially growing metastases in an ovarian cancer patient. Cell 170, 927-938. e920.
|
|
Johnson, B.E., Mazor, T., Hong, C., Barnes, M., Aihara, K., McLean, C.Y., Fouse, S.D., Yamamoto, S., Ueda, H., Tatsuno, K., et al., 2014. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 343, 189-193.
|
|
Knudson Jr., A.G., 1971. Mutation and cancer:statistical study of retinoblastoma. Proc. Natl. Acad. Sci. U. S. A. 68, 820-823.
|
|
Kram, K.E., Geiger, C., Ismail, W.M., Lee, H., Tang, H., Foster, P.L., Finkel, S.E., 2017. Adaptation of Escherichia coli to long-term serial passage in complex medium:evidence of parallel evolution. mSystems 2, e00192-16.
|
|
Krieger, T.G., LeBlanc-Soto, S., Jabs, J., Ten, F.W., Ishaque, N., Jechow, K., Giri, A., Eils, R., Strobel, O., Conrad, C., 2020. Single-cell analysis of patient-derived PDAC organoids reveals cell state heterogeneity and a conserved developmental hierarchy. bioRxiv. https://doi.org/10.1101/2020.08.23.263160.
|
|
Lakatos, E., Williams, M.J., Schenck, R.O., Cross, W.C.H., Househam, J., Zapata, L., Werner, B., Gatenbee, C., Robertson-Tessi, M., Barnes, C.P., et al., 2020. Evolutionary dynamics of neoantigens in growing tumors. Nat. Genet. 52, 1057-1066.
|
|
Lamprecht, S., Schmidt, E.M., Blaj, C., Hermeking, H., Jung, A., Kirchner, T., Horst, D., 2017. Multicolor lineage tracing reveals clonal architecture and dynamics in colon cancer. Nat. Commun. 8, 1406.
|
|
Lancaster, M.A., Knoblich, J.A., 2014. Organogenesis in a dish:modeling development and disease using organoid technologies. Science 345, 1247125.
|
|
Li, L., Knutsdottir, H., Hui, K., Weiss, M.J., He, J., Philosophe, B., Cameron, A.M., Wolfgang, C.L., Pawlik, T.M., Ghiaur, G., et al., 2019. Human primary liver cancer organoids reveal intratumor and interpatient drug response heterogeneity. JCI Insight 4, e121490.
|
|
Lee, S.H., Hu, W., Matulay, J.T., Silva, M.V., Owczarek, T.B., Kim, K., Chua, C.W., Barlow, L.J., Kandoth, C., Williams, A.B., et al., 2018. Tumor evolution and drug response in patient-derived organoid models of bladder cancer. Cell 173, 515-528. e517.
|
|
Li, X., Francies, H.E., Secrier, M., Perner, J., Miremadi, A., Galeano-Dalmau, N., Barendt, W.J., Letchford, L., Leyden, G.M., Goffin, E.K., et al., 2018. Organoid cultures recapitulate esophageal adenocarcinoma heterogeneity providing a model for clonality studies and precision therapeutics. Nat. Commun. 9, 2983.
|
|
Ling, S., Hu, Z., Yang, Z., Yang, F., Li, Y., Lin, P., Chen, K., Dong, L., Cao, L., Tao, Y., et al., 2015. Extremely high genetic diversity in a single tumor points to prevalence of non-darwinian cell evolution. Proc. Natl. Acad. Sci. U. S. A. 112, E6496-E6505.
|
|
Lopez, S., Lim, E.L., Horswell, S., Haase, K., Huebner, A., Dietzen, M., Mourikis, T.P., Watkins, T.B.K., Rowan, A., Dewhurst, S.M., et al., 2020. Interplay between whole-genome doubling and the accumulation of deleterious alterations in cancer evolution. Nat. Genet. 52, 283-293.
|
|
Maddison, W.P., Knowles, L.L., 2006. Inferring phylogeny despite incomplete lineage sorting. Syst. Biol. 55, 21-30.
|
|
Martens, E.A., Kostadinov, R., Maley, C.C., Hallatschek, O., 2011. Spatial structure increases the waiting time for cancer. New J. Phys. 13, 115014.
|
|
Martincorena, I., Raine, K.M., Gerstung, M., Dawson, K.J., Haase, K., Van Loo, P., Davies, H., Stratton, M.R., Campbell, P.J., 2017. Universal patterns of selection in cancer and somatic tissues. Cell 171, 1029-1041. e1021.
|
|
McFarland, C.D., Mirny, L.A., Korolev, K.S., 2014. Tug-of-war between driver and passenger mutations in cancer and other adaptive processes. Proc. Natl. Acad. Sci. U. S. A. 111, 15138-15143.
|
|
McFarland, C.D., Yaglom, J.A., Wojtkowiak, J.W., Scott, J.G., Morse, D.L., Sherman, M.Y., Mirny, L.A., 2017. The damaging effect of passenger mutations on cancer progression. Cancer Res. 77, 4763-4772.
|
|
McGranahan, N., Swanton, C., 2017. Clonal heterogeneity and tumor evolution:past, present, and the future. Cell 168, 613-628.
|
|
McKenna, A., Findlay, G.M., Gagnon, J.A., Horwitz, M.S., Schier, A.F., Shendure, J., 2016. Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science 353, aaf7907.
|
|
Neal, J.T., Li, X., Zhu, J., Giangarra, V., Grzeskowiak, C.L., Ju, J., Liu, I.H., Chiou, S.H., Salahudeen, A.A., Smith, A.R., et al., 2018. Organoid modeling of the tumor immune microenvironment. Cell 175, 1972-1988. e1916.
|
|
Nik-Zainal, S., Alexandrov, L.B., Wedge, D.C., Van Loo, P., Greenman, C.D., Raine, K., Jones, D., Hinton, J., Marshall, J., Stebbings, L.A., et al., 2012.
|
|
Mutational processes molding the genomes of 21 breast cancers. Cell 149, 979-993.
|
|
Noble, R., Burri, D., Kather, J.N., Beerenwinkel, N., 2019. Spatial structure governs the mode of tumour evolution. bioRxiv. https://doi.org/10.1101/586735.
|
|
Nordling, C.O., 1953. A new theory on cancer-inducing mechanism. Br. J. Cancer 7, 68-72.
|
|
Nowell, P.C., 1976. The clonal evolution of tumor cell populations. Science 194, 23-28.
|
|
O'Rourke, K.P., Loizou, E., Livshits, G., Schatoff, E.M., Baslan, T., Manchado, E., Simon, J., Romesser, P.B., Leach, B., Han, T., et al., 2017. Transplantation of engineered organoids enables rapid generation of metastatic mouse models of colorectal cancer. Nat. Biotechnol. 35, 577-582.
|
|
Quinn, J.J., Jones, M.G., Okimoto, R.A., Nanjo, S., Chan, M.M., Yosef, N., Bivona, T.G., Weissman, J.S., 2021. Single-cell lineages reveal the rates, routes, and drivers of metastasis in cancer xenografts. Science 371, eabc1944.
|
|
Reeves, M.Q., Kandyba, E., Harris, S., Del Rosario, R., Balmain, A., 2018. Multicolour lineage tracing reveals clonal dynamics of squamous carcinoma evolution from initiation to metastasis. Nat. Cell Biol. 20, 699-709.
|
|
Roe, J.S., Hwang, C.I., Somerville, T.D.D., Milazzo, J.P., Lee, E.J., Da Silva, B., Maiorino, L., Tiriac, H., Young, C.M., Miyabayashi, K., et al., 2017. Enhancer reprogramming promotes pancreatic cancer metastasis. Cell 170, 875-888. e820.
|
|
Roerink, S.F., Sasaki, N., Lee-Six, H., Young, M.D., Alexandrov, L.B., Behjati, S., Mitchell, T.J., Grossmann, S., Lightfoot, H., Egan, D.A., et al., 2018. Intra-tumour diversification in colorectal cancer at the single-cell level. Nature 556, 457-462.
|
|
Schumacher, D., Andrieux, G., Boehnke, K., Keil, M., Silvestri, A., Silvestrov, M., Keilholz, U., Haybaeck, J., Erdmann, G., Sachse, C., et al., 2019. Heterogeneous pathway activation and drug response modelled in colorectal-tumor-derived 3D cultures. PLoS Genet. 15, e1008076.
|
|
Shi, H., Hugo, W., Kong, X., Hong, A., Koya, R.C., Moriceau, G., Chodon, T., Guo, R., Johnson, D.B., Dahlman, K.B., et al., 2014. Acquired resistance and clonal evolution in melanoma during braf inhibitor therapy. Cancer Discov 4, 80-93.
|
|
Sottoriva, A., Kang, H., Ma, Z., Graham, T.A., Salomon, M.P., Zhao, J., Marjoram, P., Siegmund, K., Press, M.F., Shibata, D., et al., 2015. A big bang model of human colorectal tumor growth. Nat. Genet. 47, 209-216.
|
|
Stephens, P.J., Greenman, C.D., Fu, B., Yang, F., Bignell, G.R., Mudie, L.J., Pleasance, E.D., Lau, K.W., Beare, D., Stebbings, L.A., et al., 2011. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144, 27-40.
|
|
Sun, R., Hu, Z., Sottoriva, A., Graham, T.A., Harpak, A., Ma, Z., Fischer, J.M., Shibata, D., Curtis, C., 2017. Between-region genetic divergence reflects the mode and tempo of tumor evolution. Nat. Genet. 49, 1015-1024.
|
|
Swanton, C., 2020. Take lessons from cancer evolution to the clinic. Nature 581, 382-383.
|
|
Tabernero, J., Lenz, H.J., Siena, S., Sobrero, A., Falcone, A., Ychou, M., Humblet, Y., Bouche, O., Mineur, L., Barone, C., et al., 2015. Analysis of circulating DNA and protein biomarkers to predict the clinical activity of regorafenib and assess prognosis in patients with metastatic colorectal cancer:a retrospective, exploratory analysis of the correct trial. Lancet Oncol. 16, 937-948.
|
|
Tao, Y., Kang, B., Petkovich, D.A., Bhandari, Y.R., In, J., Stein-O'Brien, G., Kong, X., Xie, W., Zachos, N., Maegawa, S., et al., 2019. Aging-like spontaneous epigenetic silencing facilitates wnt activation, stemness, and brafv600e-induced tumorigenesis. Cancer Cell 35, 315-328. e316.
|
|
Tirosh, I., Izar, B., Prakadan, S.M., Wadsworth 2nd, M.H., Treacy, D., Trombetta, J.J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al., 2016. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-Seq. Science 352, 189-196.
|
|
Vasudevan, A., Schukken, K.M., Sausville, E.L., Girish, V., Adebambo, O.A., Sheltzer, J.M., 2021. Aneuploidy as a promoter and suppressor of malignant growth. Nat. Rev. Cancer 21, 89-103.
|
|
Voronina, N., Wong, J.K.L., Hubschmann, D., Hlevnjak, M., Uhrig, S., Heilig, C.E., Horak, P., Kreutzfeldt, S., Mock, A., Stenzinger, A., et al., 2020. The landscape of chromothripsis across adult cancer types. Nat. Commun. 11, 2320.
|
|
Wagner, D.E., Klein, A.M., 2020. Lineage tracing meets single-cell omics:opportunities and challenges. Nat. Rev. Genet. 21, 410-427.
|
|
Wang, J., Cazzato, E., Ladewig, E., Frattini, V., Rosenbloom, D.I., Zairis, S., Abate, F., Liu, Z., Elliott, O., Shin, Y.J., et al., 2016. Clonal evolution of glioblastoma under therapy. Nat. Genet. 48, 768-776.
|
|
Wang, Y., Waters, J., Leung, M.L., Unruh, A., Roh, W., Shi, X., Chen, K., Scheet, P., Vattathil, S., Liang, H., et al., 2014. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 512, 155-160.
|
|
Watkins, T.B.K., Lim, E.L., Petkovic, M., Elizalde, S., Birkbak, N.J., Wilson, G.A., Moore, D.A., Gronroos, E., Rowan, A., Dewhurst, S.M., et al., 2020. Pervasive chromosomal instability and karyotype order in tumour evolution. Nature 587, 126-132.
|
|
Werner, B., Case, J., Williams, M.J., Chkhaidze, K., Temko, D., Fernandez-Mateos, J., Cresswell, G.D., Nichol, D., Cross, W., Spiteri, I., et al., 2020. Measuring single cell divisions in human tissues from multi-region sequencing data. Nat. Commun. 11, 1035.
|
|
Wichman, H.A., Badgett, M.R., Scott, L.A., Boulianne, C.M., Bull, J.J., 1999. Different trajectories of parallel evolution during viral adaptation. Science 285, 422-424.
|
|
Williams, M.J., Werner, B., Barnes, C.P., Graham, T.A., Sottoriva, A., 2016. Identification of neutral tumor evolution across cancer types. Nat. Genet. 48, 238-244.
|
|
Wu, C.I., Wang, H.Y., Ling, S., Lu, X., 2016. The ecology and evolution of cancer:the ultra-microevolutionary process. Annu. Rev. Genet. 50, 347-369.
|
|
Yates, L.R., Gerstung, M., Knappskog, S., Desmedt, C., Gundem, G., Van Loo, P., Aas, T., Alexandrov, L.B., Larsimont, D., Davies, H., et al., 2015. Subclonal diversification of primary breast cancer revealed by multiregion sequencing. Nat. Med. 21, 751-759.
|
|
Yates, L.R., Knappskog, S., Wedge, D., Farmery, J.H.R., Gonzalez, S., Martincorena, I., Alexandrov, L.B., Van Loo, P., Haugland, H.K., Lilleng, P.K., et al., 2017. Genomic evolution of breast cancer metastasis and relapse. Cancer Cell 32, 169-184. e167.
|
|
Zhai, W., Lim, T.K., Zhang, T., Phang, S.T., Tiang, Z., Guan, P., Ng, M.H., Lim, J.Q., Yao, F., Li, Z., et al., 2017. The spatial organization of intra-tumour heterogeneity and evolutionary trajectories of metastases in hepatocellular carcinoma. Nat. Commun. 8, 4565.
|
|
Zhang, J., Fujimoto, J., Zhang, J., Wedge, D.C., Song, X., Zhang, J., Seth, S., Chow, C.W., Cao, Y., Gumbs, C., et al., 2014. Intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing. Science 346, 256-259.
|
|
Zhao, Z., Goldin, L., Liu, S., Wu, L., Zhou, W., Lou, H., Yu, Q., Tsang, S.X., Jiang, M., Li, F., et al., 2016. Evolution of multiple cell clones over a 29-year period of a CLL patient. Nat. Commun. 7, 13765.
|
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