Section: Mathematical & Computational Biology
Topic: Biophysics and computational biology, Genetics/Genomics, Health sciences

Cancer phylogenetic tree inference at scale from 1000s of single cell genomes

10.24072/pcjournal.292 - Peer Community Journal, Volume 3 (2023), article no. e63.

Get full text PDF Peer reviewed and recommended by PCI

A new generation of scalable single cell whole genome sequencing (scWGS) methods allows unprecedented high resolution measurement of the evolutionary dynamics of cancer cell populations. Phylogenetic reconstruction is central to identifying sub-populations and distinguishing the mutational processes that gave rise to them. Existing phylogenetic tree building models do not scale to the tens of thousands of high resolution genomes achievable with current scWGS methods. We constructed a phylogenetic model and associated Bayesian inference procedure, sitka, specifically for scWGS data. The method is based on a novel phylogenetic encoding of copy number (CN) data, the sitka transformation, that simplifies the site dependencies induced by rearrangements while still forming a sound foundation to phylogenetic inference. The sitka transformation allows us to design novel scalable Markov chain Monte Carlo (MCMC) algorithms. Moreover, we introduce a novel point mutation calling method that incorporates the CN data and the underlying phylogenetic tree to overcome the low per-cell coverage of scWGS. We demonstrate our method on three single cell datasets, including a novel PDX series, and analyse the topological properties of the inferred trees. Sitka is freely available at https://github.com/UBC-Stat-ML/sitkatree.git

Published online:
DOI: 10.24072/pcjournal.292
Type: Research article
Keywords: Phylogenetics, Cancer evolution, Bayesian statistics, MCMC, Copy number evolution, PDX, Triple negative breast cancer
Salehi, Sohrab 1; Dorri, Fatemeh 2; Chern, Kevin 3; Kabeer, Farhia 4; Rusk, Nicole 1; Funnell, Tyler 1; Williams, Marc J. 1; Lai, Daniel 4, 5; Andronescu, Mirela 4, 5; Campbell, Kieran R. 6, 7, 8; McPherson, Andrew 1; Aparicio, Samuel 4, 5; Roth, Andrew 2, 4, 5; Shah, Sohrab P. 1; Bouchard-Côté, Alexandre 3

1 Computational Oncology, Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, USA
2 Department of Computer Science, University of British Columbia, Canada
3 Department of Statistics, University of British Columbia, Canada
4 Department of Pathology and Laboratory Medicine, University of British Columbia, Canada
5 Department of Molecular Oncology, BC Cancer Research Centre, Canada
6 Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Canada
7 Department of Molecular Genetics, University of Toronto, Canada
8 Department of Statistical Sciences, University of Toronto, Canada
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
@article{10_24072_pcjournal_292,
     author = {Salehi, Sohrab and Dorri, Fatemeh and Chern, Kevin and Kabeer, Farhia and Rusk, Nicole and Funnell, Tyler and Williams, Marc J. and Lai, Daniel and Andronescu, Mirela and Campbell, Kieran R. and McPherson, Andrew and Aparicio, Samuel and Roth, Andrew and Shah, Sohrab P. and Bouchard-C\^ot\'e, Alexandre},
     title = {Cancer phylogenetic tree inference at scale from 1000s of single cell genomes},
     journal = {Peer Community Journal},
     eid = {e63},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.292},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.292/}
}
TY  - JOUR
AU  - Salehi, Sohrab
AU  - Dorri, Fatemeh
AU  - Chern, Kevin
AU  - Kabeer, Farhia
AU  - Rusk, Nicole
AU  - Funnell, Tyler
AU  - Williams, Marc J.
AU  - Lai, Daniel
AU  - Andronescu, Mirela
AU  - Campbell, Kieran R.
AU  - McPherson, Andrew
AU  - Aparicio, Samuel
AU  - Roth, Andrew
AU  - Shah, Sohrab P.
AU  - Bouchard-Côté, Alexandre
TI  - Cancer phylogenetic tree inference at scale from 1000s of single cell genomes
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.292/
DO  - 10.24072/pcjournal.292
LA  - en
ID  - 10_24072_pcjournal_292
ER  - 
%0 Journal Article
%A Salehi, Sohrab
%A Dorri, Fatemeh
%A Chern, Kevin
%A Kabeer, Farhia
%A Rusk, Nicole
%A Funnell, Tyler
%A Williams, Marc J.
%A Lai, Daniel
%A Andronescu, Mirela
%A Campbell, Kieran R.
%A McPherson, Andrew
%A Aparicio, Samuel
%A Roth, Andrew
%A Shah, Sohrab P.
%A Bouchard-Côté, Alexandre
%T Cancer phylogenetic tree inference at scale from 1000s of single cell genomes
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.292/
%R 10.24072/pcjournal.292
%G en
%F 10_24072_pcjournal_292
Salehi, Sohrab; Dorri, Fatemeh; Chern, Kevin; Kabeer, Farhia; Rusk, Nicole; Funnell, Tyler; Williams, Marc J.; Lai, Daniel; Andronescu, Mirela; Campbell, Kieran R.; McPherson, Andrew; Aparicio, Samuel; Roth, Andrew; Shah, Sohrab P.; Bouchard-Côté, Alexandre. Cancer phylogenetic tree inference at scale from 1000s of single cell genomes. Peer Community Journal, Volume 3 (2023), article  no. e63. doi : 10.24072/pcjournal.292. https://peercommunityjournal.org/articles/10.24072/pcjournal.292/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.mcb.100112

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Abbosh, C.; Birkbak, N. J.; Wilson, G. A.; Jamal-Hanjani, M.; Constantin, T.; Salari, R.; Le Quesne, J.; Moore, D. A.; Veeriah, S.; Rosenthal, R.; Marafioti, T.; Kirkizlar, E.; Watkins, T. B. K.; McGranahan, N.; Ward, S.; Martinson, L.; Riley, J.; Fraioli, F.; Al Bakir, M.; Grönroos, E.; Zambrana, F.; Endozo, R.; Bi, W. L.; Fennessy, F. M.; Sponer, N.; Johnson, D.; Laycock, J.; Shafi, S.; Czyzewska-Khan, J.; Rowan, A.; Chambers, T.; Matthews, N.; Turajlic, S.; Hiley, C.; Lee, S. M.; Forster, M. D.; Ahmad, T.; Falzon, M.; Borg, E.; Lawrence, D.; Hayward, M.; Kolvekar, S.; Panagiotopoulos, N.; Janes, S. M.; Thakrar, R.; Ahmed, A.; Blackhall, F.; Summers, Y.; Hafez, D.; Naik, A.; Ganguly, A.; Kareht, S.; Shah, R.; Joseph, L.; Marie Quinn, A.; Crosbie, P. A.; Naidu, B.; Middleton, G.; Langman, G.; Trotter, S.; Nicolson, M.; Remmen, H.; Kerr, K.; Chetty, M.; Gomersall, L.; Fennell, D. A.; Nakas, A.; Rathinam, S.; Anand, G.; Khan, S.; Russell, P.; Ezhil, V.; Ismail, B.; Irvin-Sellers, M.; Prakash, V.; Lester, J. F.; Kornaszewska, M.; Attanoos, R.; Adams, H.; Davies, H.; Oukrif, D.; Akarca, A. U.; Hartley, J. A.; Lowe, H. L.; Lock, S.; Iles, N.; Bell, H.; Ngai, Y.; Elgar, G.; Szallasi, Z.; Schwarz, R. F.; Herrero, J.; Stewart, A.; Quezada, S. A.; Peggs, K. S.; Van Loo, P.; Dive, C.; Lin, C. J.; Rabinowitz, M.; Aerts, H. J. W. L.; Hackshaw, A.; Shaw, J. A.; Zimmermann, B. G.; Swanton, C. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution, Nature, Volume 545 (2017) no. 7655, pp. 446-451 | DOI

[2] Aldous, D. Probability Distributions on Cladograms, Random Discrete Structures, Springer New York, New York, NY, 1996, pp. 1-18 | DOI

[3] Baslan, T.; Kendall, J.; Rodgers, L.; Cox, H.; Riggs, M.; Stepansky, A.; Troge, J.; Ravi, K.; Esposito, D.; Lakshmi, B.; Wigler, M.; Navin, N.; Hicks, J. Genome-wide copy number analysis of single cells, Nature Protocols, Volume 7 (2012) no. 6, pp. 1024-1041 | DOI

[4] Blum, M. G. B.; François, O. Which Random Processes Describe the Tree of Life? A Large-Scale Study of Phylogenetic Tree Imbalance, Systematic Biology, Volume 55 (2006) no. 4, pp. 685-691 | DOI

[5] Bortolussi, N.; Durand, E.; Blum, M.; François, O. apTreeshape: statistical analysis of phylogenetic tree shape, Bioinformatics, Volume 22 (2005) no. 3, pp. 363-364 | DOI

[6] Bouchard-Côté, A.; Chern, K.; Cubranic, D.; Hosseini, S.; Hume, J.; Lepur, M.; Ouyang, Z.; Sgarbi, G. Blang: Bayesian Declarative Modeling of General Data Structures and Inference via Algorithms Based on Distribution Continua, Journal of Statistical Software, Volume 103 (2022) no. 11 | DOI

[7] Robert, C. The Bayesian Choice, Springer Texts in Statistics, Springer New York, New York, NY, 2007 | DOI

[8] Campello, R. J. G. B.; Moulavi, D.; Sander, J. Density-Based Clustering Based on Hierarchical Density Estimates, Advances in Knowledge Discovery and Data Mining, Springer Berlin Heidelberg, Berlin, Heidelberg, 2013, pp. 160-172 | DOI

[9] Desper, R.; Gascuel, O. Fast and Accurate Phylogeny Reconstruction Algorithms Based on the Minimum-Evolution Principle, Journal of Computational Biology, Volume 9 (2002) no. 5, pp. 687-705 | DOI

[10] Eirew, P.; Steif, A.; Khattra, J.; Ha, G.; Yap, D.; Farahani, H.; Gelmon, K.; Chia, S.; Mar, C.; Wan, A.; Laks, E.; Biele, J.; Shumansky, K.; Rosner, J.; McPherson, A.; Nielsen, C.; Roth, A. J. L.; Lefebvre, C.; Bashashati, A.; de Souza, C.; Siu, C.; Aniba, R.; Brimhall, J.; Oloumi, A.; Osako, T.; Bruna, A.; Sandoval, J. L.; Algara, T.; Greenwood, W.; Leung, K.; Cheng, H.; Xue, H.; Wang, Y.; Lin, D.; Mungall, A. J.; Moore, R.; Zhao, Y.; Lorette, J.; Nguyen, L.; Huntsman, D.; Eaves, C. J.; Hansen, C.; Marra, M. A.; Caldas, C.; Shah, S. P.; Aparicio, S. Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution, Nature, Volume 518 (2014) no. 7539, pp. 422-426 | DOI

[11] Gao, R.; Davis, A.; McDonald, T. O.; Sei, E.; Shi, X.; Wang, Y.; Tsai, P.-C.; Casasent, A.; Waters, J.; Zhang, H.; Meric-Bernstam, F.; Michor, F.; Navin, N. E. Punctuated copy number evolution and clonal stasis in triple-negative breast cancer, Nature Genetics, Volume 48 (2016) no. 10, pp. 1119-1130 | DOI

[12] Gawad, C.; Koh, W.; Quake, S. R. Single-cell genome sequencing: current state of the science, Nature Reviews Genetics, Volume 17 (2016) no. 3, pp. 175-188 | DOI

[13] Geman, S.; Geman, D. Stochastic Relaxation, Gibbs Distributions, and the Bayesian Restoration of Images, IEEE Transactions on Pattern Analysis and Machine Intelligence, Volume PAMI-6 (1984) no. 6, pp. 721-741 | DOI

[14] Greenman, C. D.; Pleasance, E. D.; Newman, S.; Yang, F.; Fu, B.; Nik-Zainal, S.; Jones, D.; Lau, K. W.; Carter, N.; Edwards, P. A. W.; Futreal, P. A.; Stratton, M. R.; Campbell, P. J. Estimation of rearrangement phylogeny for cancer genomes, Genome Research, Volume 22 (2012) no. 2, pp. 346-361

[15] Greenman, C. D.; Pleasance, E. D.; Newman, S.; Yang, F.; Fu, B.; Nik-Zainal, S.; Jones, D.; Lau, K. W.; Carter, N.; Edwards, P. A.; Futreal, P. A.; Stratton, M. R.; Campbell, P. J. Estimation of rearrangement phylogeny for cancer genomes, Genome Research, Volume 22 (2011) no. 2, pp. 346-361 | DOI

[16] Guindon, S.; Gascuel, O. A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood, Systematic Biology, Volume 52 (2003) no. 5, pp. 696-704 | DOI

[17] Househam, J.; Heide, T.; Cresswell, G. D.; Spiteri, I.; Kimberley, C.; Zapata, L.; Lynn, C.; James, C.; Mossner, M.; Fernandez-Mateos, J.; Vinceti, A.; Baker, A.-M.; Gabbutt, C.; Berner, A.; Schmidt, M.; Chen, B.; Lakatos, E.; Gunasri, V.; Nichol, D.; Costa, H.; Mitchinson, M.; Ramazzotti, D.; Werner, B.; Iorio, F.; Jansen, M.; Caravagna, G.; Barnes, C. P.; Shibata, D.; Bridgewater, J.; Rodriguez-Justo, M.; Magnani, L.; Sottoriva, A.; Graham, T. A. Phenotypic plasticity and genetic control in colorectal cancer evolution, Nature, Volume 611 (2022) no. 7937, pp. 744-753 | DOI

[18] Huelsenbeck, J. P.; Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees, Bioinformatics, Volume 17 (2001) no. 8, pp. 754-755 | DOI

[19] Jahn, K.; Kuipers, J.; Beerenwinkel, N. Tree inference for single-cell data, Genome Biology, Volume 17 (2016) no. 1 | DOI

[20] Kaufmann, T. L.; Petkovic, M.; Watkins, T. B. K.; Colliver, E. C.; Laskina, S.; Thapa, N.; Minussi, D. C.; Navin, N.; Swanton, C.; Van Loo, P.; Haase, K.; Tarabichi, M.; Schwarz, R. F. MEDICC2: whole-genome doubling aware copy-number phylogenies for cancer evolution, Genome Biology, Volume 23 (2022) no. 1 | DOI

[21] Kingman, J. The coalescent, Stochastic Processes and their Applications, Volume 13 (1982) no. 3, pp. 235-248 | DOI

[22] Kuhner, M.; Felsenstein, J. A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates., Molecular Biology and Evolution (1994) | DOI

[23] Laks, E.; McPherson, A.; Zahn, H.; Lai, D.; Steif, A.; Brimhall, J.; Biele, J.; Wang, B.; Masud, T.; Ting, J.; Grewal, D.; Nielsen, C.; Leung, S.; Bojilova, V.; Smith, M.; Golovko, O.; Poon, S.; Eirew, P.; Kabeer, F.; Ruiz de Algara, T.; Lee, S. R.; Taghiyar, M. J.; Huebner, C.; Ngo, J.; Chan, T.; Vatrt-Watts, S.; Walters, P.; Abrar, N.; Chan, S.; Wiens, M.; Martin, L.; Scott, R. W.; Underhill, T. M.; Chavez, E.; Steidl, C.; Da Costa, D.; Ma, Y.; Coope, R. J.; Corbett, R.; Pleasance, S.; Moore, R.; Mungall, A. J.; Mar, C.; Cafferty, F.; Gelmon, K.; Chia, S.; Marra, M. A.; Hansen, C.; Shah, S. P.; Aparicio, S.; Hannon, G. J.; Battistoni, G.; Bressan, D.; Cannell, I.; Casbolt, H.; Jauset, C.; Kovačević, T.; Mulvey, C.; Nugent, F.; Ribes, M. P.; Pearsall, I.; Qosaj, F.; Sawicka, K.; Wild, S.; Williams, E.; Aparicio, S.; Laks, E.; Li, Y.; O’Flanagan, C.; Smith, A.; Ruiz, T.; Balasubramanian, S.; Lee, M.; Bodenmiller, B.; Burger, M.; Kuett, L.; Tietscher, S.; Windager, J.; Boyden, E.; Alon, S.; Cui, Y.; Emenari, A.; Goodwin, D.; Karagiannis, E.; Sinha, A.; Wassie, A. T.; Caldas, C.; Bruna, A.; Callari, M.; Greenwood, W.; Lerda, G.; Lubling, Y.; Marti, A.; Rueda, O.; Shea, A.; Harris, O.; Becker, R.; Grimaldi, F.; Harris, S.; Vogl, S.; Joyce, J. A.; Hausser, J.; Watson, S.; Shah, S.; McPherson, A.; Vázquez-García, I.; Tavaré, S.; Dinh, K.; Fisher, E.; Kunes, R.; Walton, N. A.; Al Sa’d, M.; Chornay, N.; Dariush, A.; Solares, E. G.; Gonzalez-Fernandez, C.; Yoldas, A. K.; Millar, N.; Zhuang, X.; Fan, J.; Lee, H.; Duran, L. S.; Xia, C.; Zheng, P. Clonal Decomposition and DNA Replication States Defined by Scaled Single-Cell Genome Sequencing, Cell, Volume 179 (2019) no. 5 | DOI

[24] Lambert, A. Phylogenetic reconstruction from copy number aberration in large scale, low-depth genome-wide single-cell data, Peer Community in Mathematical and Computational Biology, 2023 | DOI

[25] Leung, M. L.; Davis, A.; Gao, R.; Casasent, A.; Wang, Y.; Sei, E.; Vilar, E.; Maru, D.; Kopetz, S.; Navin, N. E. Single-cell DNA sequencing reveals a late-dissemination model in metastatic colorectal cancer, Genome Research, Volume 27 (2017) no. 8, pp. 1287-1299 | DOI

[26] Coronado, T. M.; Mir, A.; Rosselló, F.; Rotger, L. On Sackin’s original proposal: the variance of the leaves’ depths as a phylogenetic balance index, BMC Bioinformatics, Volume 21 (2020) no. 1 | DOI

[27] Ma, J.; Ratan, A.; Raney, B. J.; Suh, B. B.; Miller, W.; Haussler, D. The infinite sites model of genome evolution, Proceedings of the National Academy of Sciences, Volume 105 (2008) no. 38, pp. 14254-14261 | DOI

[28] Malikic, S.; Jahn, K.; Kuipers, J.; Sahinalp, S. C.; Beerenwinkel, N. Integrative inference of subclonal tumour evolution from single-cell and bulk sequencing data, Nature Communications, Volume 10 (2019) no. 1 | DOI

[29] Mallory, X. F.; Edrisi, M.; Navin, N.; Nakhleh, L. Methods for copy number aberration detection from single-cell DNA-sequencing data, Genome Biology, Volume 21 (2020) no. 1 | DOI

[30] McPherson, A. Clonal decomposition and DNA replication states defined by scaled single cell genome sequencing (Version v2) [Data set]., Zenodo, 2019 | DOI

[31] Miller, C. A.; White, B. S.; Dees, N. D.; Griffith, M.; Welch, J. S.; Griffith, O. L.; Vij, R.; Tomasson, M. H.; Graubert, T. A.; Walter, M. J.; Ellis, M. J.; Schierding, W.; DiPersio, J. F.; Ley, T. J.; Mardis, E. R.; Wilson, R. K.; Ding, L. SciClone: Inferring Clonal Architecture and Tracking the Spatial and Temporal Patterns of Tumor Evolution, PLoS Computational Biology, Volume 10 (2014) no. 8 | DOI

[32] Mishra, S.; Whetstine, J. R. Different Facets of Copy Number Changes: Permanent, Transient, and Adaptive, Molecular and Cellular Biology, Volume 36 (2016) no. 7, pp. 1050-1063 | DOI

[33] Neal, R. M. Slice sampling, The Annals of Statistics, Volume 31 (2003) no. 3 | DOI

[34] Neher, R. A.; Hallatschek, O. Genealogies of rapidly adapting populations, Proceedings of the National Academy of Sciences, Volume 110 (2012) no. 2, pp. 437-442 | DOI

[35] Paradis, E. Analysis of Phylogenetics and Evolution with R, Springer New York, New York, NY, 2012 | DOI

[36] Pellegrino, M.; Sciambi, A.; Treusch, S.; Durruthy-Durruthy, R.; Gokhale, K.; Jacob, J.; Chen, T. X.; Geis, J. A.; Oldham, W.; Matthews, J.; Kantarjian, H.; Futreal, P. A.; Patel, K.; Jones, K. W.; Takahashi, K.; Eastburn, D. J. High-throughput single-cell DNA sequencing of acute myeloid leukemia tumors with droplet microfluidics, Genome Research, Volume 28 (2018) no. 9, pp. 1345-1352 | DOI

[37] Quinn, J. J.; Jones, M. G.; Okimoto, R. A.; Nanjo, S.; Chan, M. M.; Yosef, N.; Bivona, T. G.; Weissman, J. S. Single-cell lineages reveal the rates, routes, and drivers of metastasis in cancer xenografts, Science, Volume 371 (2021) no. 6532 | DOI

[38] Robinson, D.; Foulds, L. Comparison of phylogenetic trees, Mathematical Biosciences, Volume 53 (1981) no. 1-2, pp. 131-147 | DOI

[39] Ross, E. M.; Markowetz, F. OncoNEM: inferring tumor evolution from single-cell sequencing data, Genome Biology, Volume 17 (2016) no. 1 | DOI

[40] Sainudiin, R.; Véber, A. A Beta-splitting model for evolutionary trees, Royal Society Open Science, Volume 3 (2016) no. 5 | DOI

[41] Saitou, N.; Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees., Molecular Biology and Evolution, Volume 4 (1987), pp. 406-425 | DOI

[42] Salehi, S. UBC-Stat-ML/sitka_data: Sitka data publication (Dataset), Zenodo, 2023 | DOI

[43] Salehi, S.; Dorri, F.; Chern, K. B.-C. A. (. UBC-Stat-ML/sitkatree: Sitka publication (Code), Zenodo, 2023 | DOI

[44] Salehi, S.; Kabeer, F.; Ceglia, N.; Andronescu, M.; Williams, M. J.; Campbell, K. R.; Masud, T.; Wang, B.; Biele, J.; Brimhall, J.; Gee, D.; Lee, H.; Ting, J.; Zhang, A. W.; Tran, H.; O’Flanagan, C.; Dorri, F.; Rusk, N.; de Algara, T. R.; Lee, S. R.; Cheng, B. Y. C.; Eirew, P.; Kono, T.; Pham, J.; Grewal, D.; Lai, D.; Moore, R.; Mungall, A. J.; Marra, M. A.; Hannon, G. J.; Battistoni, G.; Bressan, D.; Cannell, I. G.; Casbolt, H.; Fatemi, A.; Jauset, C.; Kovačević, T.; Mulvey, C. M.; Nugent, F.; Ribes, M. P.; Pearsall, I.; Qosaj, F.; Sawicka, K.; Wild, S. A.; Williams, E.; Laks, E.; Li, Y.; O’Flanagan, C. H.; Smith, A.; Ruiz, T.; Lai, D.; Roth, A.; Balasubramanian, S.; Lee, M.; Bodenmiller, B.; Burger, M.; Kuett, L.; Tietscher, S.; Windhager, J.; Boyden, E. S.; Alon, S.; Cui, Y.; Emenari, A.; Goodwin, D.; Karagiannis, E. D.; Sinha, A.; Wassie, A. T.; Caldas, C.; Bruna, A.; Callari, M.; Greenwood, W.; Lerda, G.; Eyal-Lubling, Y.; Rueda, O. M.; Shea, A.; Harris, O.; Becker, R.; Grimaldi, F.; Harris, S.; Vogl, S. L.; Weselak, J.; Joyce, J. A.; Watson, S. S.; Vázquez-Garćıa, I.; Tavaré, S.; Dinh, K. N.; Fisher, E.; Kunes, R.; Walton, N. A.; Sa’d, M. A.; Chornay, N.; Dariush, A.; González-Solares, E. A.; González-Fernández, C.; Yoldas, A. K.; Millar, N.; Whitmarsh, T.; Zhuang, X.; Fan, J.; Lee, H.; Sepúlveda, L. A.; Xia, C.; Zheng, P.; McPherson, A.; Bouchard-Côté, A.; Aparicio, S.; Shah, S. P. Clonal fitness inferred from time-series modelling of single-cell cancer genomes, Nature, Volume 595 (2021) no. 7868, pp. 585-590 | DOI

[45] Satas, G.; Zaccaria, S.; Mon, G.; Raphael, B. J. SCARLET: Single-Cell Tumor Phylogeny Inference with Copy-Number Constrained Mutation Losses, Cell Systems, Volume 10 (2020) no. 4 | DOI

[46] Schliep, K. P. phangorn: phylogenetic analysis in R, Bioinformatics, Volume 27 (2010) no. 4, pp. 592-593 | DOI

[47] Schwartz, R.; Schäffer, A. A. The evolution of tumour phylogenetics: principles and practice, Nature Reviews Genetics, Volume 18 (2017) no. 4, pp. 213-229 | DOI

[48] Singer, J.; Kuipers, J.; Jahn, K.; Beerenwinkel, N. SCIΦ: Single-cell mutation identification via phylogenetic inference | DOI

[49] Sokal, R. R. A statistical method for evaluating systematic relationships., Univ. Kansas, Sci. Bull., Volume 38 (1958), pp. 1409-1438

[50] Som, A. ML or NJ-MCL? A comparison between two robust phylogenetic methods, Computational Biology and Chemistry, Volume 33 (2009) no. 5, pp. 373-378 | DOI

[51] Staab, P. R.; Metzler, D. Coala: an R framework for coalescent simulation, Bioinformatics, Volume 32 (2016) no. 12, pp. 1903-1904 | DOI

[52] Teh, Y.; et al. Dirichlet Process, Encyclopedia of Machine Learning, Springer US, Boston, MA, 2011, pp. 280-287 | DOI

[53] Wang, F.; Wang, Q.; Mohanty, V.; Liang, S.; Dou, J.; Han, J.; Minussi, D. C.; Gao, R.; Ding, L.; Navin, N.; Chen, K. MEDALT: single-cell copy number lineage tracing enabling gene discovery, Genome Biology, Volume 22 (2021) no. 1 | DOI

[54] Wang, Y.; Waters, J.; Leung, M. L.; Unruh, A.; Roh, W.; Shi, X.; Chen, K.; Scheet, P.; Vattathil, S.; Liang, H.; Multani, A.; Zhang, H.; Zhao, R.; Michor, F.; Meric-Bernstam, F.; Navin, N. E. Clonal evolution in breast cancer revealed by single nucleus genome sequencing, Nature, Volume 512 (2014) no. 7513, pp. 155-160 | DOI

[55] Williams, T.; Moret, B. An investigation of phylogenetic likelihood methods, Third IEEE Symposium on Bioinformatics and Bioengineering, 2003. Proceedings. (2003), pp. 79-86 | DOI

[56] Wilson, D. Generating Random Spanning Trees More Quickly Than the Cover Time, In: Proceedings of the Twenty-eighth Annual ACM Symposium on Theory of Computing. STOC ’96. New York, NY, USA, 1996, pp. 296-303 | DOI

[57] Xu, X.; Hou, Y.; Yin, X.; Bao, L.; Tang, A.; Song, L.; Li, F.; Tsang, S.; Wu, K.; Wu, H.; He, W.; Zeng, L.; Xing, M.; Wu, R.; Jiang, H.; Liu, X.; Cao, D.; Guo, G.; Hu, X.; Gui, Y.; Li, Z.; Xie, W.; Sun, X.; Shi, M.; Cai, Z.; Wang, B.; Zhong, M.; Li, J.; Lu, Z.; Gu, N.; Zhang, X.; Goodman, L.; Bolund, L.; Wang, J.; Yang, H.; Kristiansen, K.; Dean, M.; Li, Y.; Wang, J. Single-Cell Exome Sequencing Reveals Single-Nucleotide Mutation Characteristics of a Kidney Tumor, Cell, Volume 148 (2012) no. 5, pp. 886-895 | DOI

[58] Yi, K.; Ju, Y. S. Patterns and mechanisms of structural variations in human cancer, Experimental & Molecular Medicine, Volume 50 (2018) no. 8, pp. 1-11 | DOI

[59] Youden, W. J. Index for rating diagnostic tests, Cancer, Volume 3 (1950) no. 1, pp. 32-35 | DOI

[60] Yu, C.; Yu, J.; Yao, X.; Wu, W. K.; Lu, Y.; Tang, S.; Li, X.; Bao, L.; Li, X.; Hou, Y.; Wu, R.; Jian, M.; Chen, R.; Zhang, F.; Xu, L.; Fan, F.; He, J.; Liang, Q.; Wang, H.; Hu, X.; He, M.; Zhang, X.; Zheng, H.; Li, Q.; Wu, H.; Chen, Y.; Yang, X.; Zhu, S.; Xu, X.; Yang, H.; Wang, J.; Zhang, X.; Sung, J. J.; Li, Y.; Wang, J. Discovery of biclonal origin and a novel oncogene SLC12A5 in colon cancer by single-cell sequencing, Cell Research, Volume 24 (2014) no. 6, pp. 701-712 | DOI

[61] Zafar, H.; Tzen, A.; Navin, N.; Chen, K.; Nakhleh, L. SiFit: inferring tumor trees from single-cell sequencing data under finite-sites models, Genome Biology, Volume 18 (2017) no. 1 | DOI

[62] Zahn, H.; Steif, A.; Laks, E.; Eirew, P.; VanInsberghe, M.; Shah, S. P.; Aparicio, S.; Hansen, C. L. Scalable whole-genome single-cell library preparation without preamplification, Nature Methods, Volume 14 (2017) no. 2, pp. 167-173 | DOI

Cited by Sources: