Curtius, K., Wright, N. A. & Graham, T. A. Evolution of premalignant disease. Cold Spring Harb. Perspect. Med. 7, a026542 (2017).
Rane, J. K., Frankell, A. M., Weeden, C. E. & Swanton, C. Clonal evolution in healthy and premalignant tissues: implications for early cancer interception strategies. Cancer Prev. Res. 16, 369â378 (2023).
Zhang, S. et al. Tumor initiation and early tumorigenesis: molecular mechanisms and interventional targets. Signal Transduct. Target. Ther. 9, 149 (2024).
Liu, K. et al. Mapping single-cell-resolution cell phylogeny reveals cell population dynamics during organ development. Nat. Methods 18, 1506â1514 (2021).
Curtius, K., Wright, N. A. & Graham, T. A. An evolutionary perspective on field cancerization. Nat. Rev. Cancer 18, 19â32 (2018).
Dekker, E., Tanis, P. J., Vleugels, J. L. A., Kasi, P. M. & Wallace, M. B. Colorectal cancer. Lancet 394, 1467â1480 (2019).
Fearon, E. R. & Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell 61, 759â767 (1990).
Gerstung, M. et al. The evolutionary history of 2,658 cancers. Nature 578, 122â128 (2020).
Parsons, B. L. Multiclonal tumor origin: evidence and implications. Mutat. Res. Rev. Mutat. Res. 777, 1â18 (2018).
Chen, B. et al. Very large hidden genetic diversity in one single tumor: evidence for tumors-in-tumor. Natl Sci. Rev. 9, nwac250 (2022).
McKenna, A. et al. Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science 353, aaf7907 (2016).
Chan, M. M. et al. Molecular recording of mammalian embryogenesis. Nature 570, 77â82 (2019).
Wagner, D. E. & Klein, A. M. Lineage tracing meets single-cell omics: opportunities and challenges. Nat. Rev. Genet. 21, 410â427 (2020).
Yang, D. et al. Lineage tracing reveals the phylodynamics, plasticity, and paths of tumor evolution. Cell 185, 1905â1923 e1925 (2022).
Wirtz, S. et al. Chemically induced mouse models of acute and chronic intestinal inflammation. Nat. Protoc. 12, 1295â1309 (2017).
Pan, Q. et al. Genomic variants in mouse model induced by azoxymethane and dextran sodium sulfate improperly mimic human colorectal cancer. Sci Rep. 7, 25 (2017).
Roerink, S. F. et al. Intra-tumour diversification in colorectal cancer at the single-cell level. Nature 556, 457â462 (2018).
Leystra, A. A. et al. Multi-ancestral origin of intestinal tumors: Impact on growth, progression, and drug efficacy. Cancer Rep. 5, e1459 (2022).
Novelli, M. R. et al. Polyclonal origin of colonic adenomas in an XO/XY patient with FAP. Science 272, 1187â1190 (1996).
Merritt, A. J., Gould, K. A. & Dove, W. F. Polyclonal structure of intestinal adenomas in ApcMin/+ mice with concomitant loss of Apc+ from all tumor lineages. Proc. Natl Acad. Sci. USA 94, 13927â13931 (1997).
Halberg, R. B. & Dove, W. F. Polyclonal tumors in the mammalian intestine: are interactions among multiple initiated clones necessary for tumor initiation, growth, and progression? Cell Cycle 6, 44â51 (2007).
Deng, S., Gong, H., Zhang, D., Zhang, M. & He, X. A statistical method for quantifying progenitor cells reveals incipient cell fate commitments. Nat. Methods 21, 597â608 (2024).
Olafsson, S. et al. Somatic evolution in non-neoplastic IBD-affected colon. Cell 182, 672â684.e611 (2020).
Martincorena, I. et al. Universal patterns of selection in cancer and somatic tissues. Cell 171, 1029â1041.e1021 (2017).
Hu, Z. et al. Quantitative evidence for early metastatic seeding in colorectal cancer. Nat. Genet. 51, 1113â1122 (2019).
Potten, C. S. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos. Trans. R. Soc. B 353, 821â830 (1998).
van der Flier, L. G. & Clevers, H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol. 71, 241â260 (2009).
Hu, Z., Li, Z., Ma, Z. & Curtis, C. Multi-cancer analysis of clonality and the timing of systemic spread in paired primary tumors and metastases. Nat. Genet. 52, 701â708 (2020).
Huang, K. K. et al. Spatiotemporal genomic profiling of intestinal metaplasia reveals clonal dynamics of gastric cancer progression. Cancer Cell 41, 2019â2037.e8 (2023).
Gay, D. M. et al. Loss of BCL9/9l suppresses Wnt driven tumourigenesis in models that recapitulate human cancer. Nat. Commun. 10, 723 (2019).
Lee-Six, H. et al. The landscape of somatic mutation in normal colorectal epithelial cells. Nature 574, 532â537 (2019).
Heide, T. et al. The co-evolution of the genome and epigenome in colorectal cancer. Nature 611, 733â743 (2022).
Vega, P. N. et al. Cancer-associated fibroblasts and squamous epithelial cells constitute a unique microenvironment in a mouse model of inflammation-induced colon cancer. Front. Oncol. 12, 878920 (2022).
Ma, R. Y., Black, A. & Qian, B. Z. Macrophage diversity in cancer revisited in the era of single-cell omics. Trends Immunol. 43, 546â563 (2022).
Katzenelenbogen, Y. et al. Coupled scRNA-seq and intracellular protein activity reveal an immunosuppressive role of TREM2 in cancer. Cell 182, 872â885.e819 (2020).
Jin, S. et al. Inference and analysis of cellâcell communication using CellChat. Nat. Commun. 12, 1088 (2021).
Teller, I. C. & Beaulieu, J. F. Interactions between laminin and epithelial cells in intestinal health and disease. Expert Rev. Mol. Med. https://doi.org/10.1017/S1462399401003623 (2001).
Thliveris, A. T. et al. Polyclonality of familial murine adenomas: analyses of mouse chimeras with low tumor multiplicity suggest short-range interactions. Proc. Natl Acad. Sci. USA 102, 6960â6965 (2005).
Tabassum, D. P. & Polyak, K. Tumorigenesis: it takes a village. Nat. Rev. Cancer 15, 473â483 (2015).
Lee, N. D., Kaveh, K. & Bozic, I. Clonal interactions in cancer: Integrating quantitative models with experimental and clinical data. Semin. Cancer Biol. 92, 61â73 (2023).
Reeves, M. Q., Kandyba, E., Harris, S., Del Rosario, R. & Balmain, A. Multicolour lineage tracing reveals clonal dynamics of squamous carcinoma evolution from initiation to metastasis. Nat. Cell Biol. 20, 699â709 (2018).
Johnson, K. E. et al. Cancer cell population growth kinetics at low densities deviate from the exponential growth model and suggest an Allee effect. PLoS Biol. 17, e3000399 (2019).
Martinez, P. et al. Dynamic clonal equilibrium and predetermined cancer risk in Barrettâs oesophagus. Nat. Commun. 7, 12158 (2016).
Zhang, D., Zhang, A., He, X. & Deng, S. Variation in cancer risk between organs can not be explained by the degree of somatic clonal expansion. Adv. Biotechnol. 2, 18 (2024).
Li, H. New strategies to improve minimap2 alignment accuracy. Bioinformatics 37, 4572â4574 (2021).
Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460â2461 (2010).
Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530â1534 (2020).
Gschwantler, M. et al. High-grade dysplasia and invasive carcinoma in colorectal adenomas: a multivariate analysis of the impact of adenoma and patient characteristics. Eur. J. Gastroenterol. Hepatol. 14, 183â188 (2002).
Sawhney, M. S., Dickstein, J., LeClair, J., Lembo, C. & Yee, E. Adenomas with high-grade dysplasia and early adenocarcinoma are more likely to be sessile in the proximal colon. Colorectal Dis. 17, 682â688 (2015).
Gibson, J. A. & Odze, R. D. Pathology of premalignant colorectal neoplasia. Dig. Endosc. 28, 312â323 (2016).
Kuo, E., Wang, K. & Liu, X. A focused review on advances in risk stratification of malignant polyps. Gastroenterology Res. 13, 163â183 (2020).
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884âi890 (2018).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754â1760 (2009).
McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297â1303 (2010).
DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491â498 (2011).
Van der Auwera, G. A. et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinformatics 43, 11 10 11â11 10 33 (2013).
Benjamin, D. et al. Calling somatic SNVs and indels with Mutect2. Preprint at bioRxiv https://doi.org/10.1101/861054v1 (2019).
Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).
Ha, G. et al. TITAN: inference of copy number architectures in clonal cell populations from tumor whole-genome sequence data. Genome Res. 24, 1881â1893 (2014).
Tarabichi, M. et al. A practical guide to cancer subclonal reconstruction from DNA sequencing. Nat. Methods 18, 144â155 (2021).
Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24â26 (2011).
Lange, S. et al. Analysis pipelines for cancer genome sequencing in mice. Nat. Protoc. 15, 266â315 (2020).
Ellis, P. et al. Reliable detection of somatic mutations in solid tissues by laser-capture microdissection and low-input DNA sequencing. Nat. Protoc. 16, 841â871 (2021).
Kim, S. et al. Strelka2: fast and accurate calling of germline and somatic variants. Nat. Methods 15, 591â594 (2018).
Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406â425 (1987).
Cock, P. J. et al. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25, 1422â1423 (2009).
Favero, F. et al. Sequenza: allele-specific copy number and mutation profiles from tumor sequencing data. Ann. Oncol. 26, 64â70 (2015).
Lips, E. H. et al. Genomic analysis defines clonal relationships of ductal carcinoma in situ and recurrent invasive breast cancer. Nat. Genet. 54, 850â860 (2022).
Li, J. et al. Genomic and transcriptomic profiling of carcinogenesis in patients with familial adenomatous polyposis. Gut 69, 1283â1293 (2020).
Bailey, M. H. et al. Comprehensive characterization of cancer driver genes and mutations. Cell 173, 371â385.e318 (2018).
Martin, F. J. et al. Ensembl 2023. Nucleic Acids Res. 51, D933âD941 (2023).
Hao, Y. et al. Dictionary learning for integrative, multimodal and scalable single-cell analysis. Nat. Biotechnol. 42, 293â304 (2024).
McGinnis, C. S., Murrow, L. M. & Gartner, Z. J. DoubletFinder: doublet detection in single-cell RNA sequencing data using artificial nearest neighbors. Cell Syst. 8, 329â337 e324 (2019).
Hafemeister, C. & Satija, R. Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. Genome Biol. 20, 296 (2019).
Choudhary, S. & Satija, R. Comparison and evaluation of statistical error models for scRNA-seq. Genome Biol. 23, 27 (2022).
Korsunsky, I. et al. Fast, sensitive and accurate integration of single-cell data with Harmony. Nat. Methods 16, 1289â1296 (2019).
Wu, T. et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation 2, 100141 (2021).
Hanzelmann, S., Castelo, R. & Guinney, J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics 14, 7 (2013).
Dann, E., Henderson, N. C., Teichmann, S. A., Morgan, M. D. & Marioni, J. C. Differential abundance testing on single-cell data using k-nearest neighbor graphs. Nat. Biotechnol. 40, 245â253 (2022).
Browaeys, R. et al. MultiNicheNet: a flexible framework for differential cell-cell communication analysis from multi-sample multi-condition single-cell transcriptomics data. Preprint at bioRxiv https://doi.org/10.1101/2023.06.13.544751v1 (2023).
Lu. Z. et al. Systematic lineage tracing unveils polyclonal origin and evolution in colorectal precancer. Zenodo https://doi.org/10.5281/zenodo.11647317 (2024).
