1932

Abstract

During tumor evolution, cancer cells can acquire the ability to proliferate, invade neighboring tissues, evade the immune system, and spread systemically. Tracking this process remains challenging, as many key events occur stochastically and over long times, which could be addressed by studying the phylogenetic relationships among cancer cells. Several lineage tracing approaches have been developed and employed in many tumor models and contexts, providing critical insights into tumor evolution. Recent advances in single-cell lineage tracing have greatly expanded the resolution, scale, and readout of lineage tracing toolkits. In this review, we provide an overview of static lineage tracing methods, and then focus on evolving lineage tracing technologies that enable reconstruction of tumor phylogenies at unprecedented resolution. We also discuss in vivo applications of these technologies to profile subclonal dynamics, quantify tumor plasticity, and track metastasis. Finally, we highlight outstanding questions and emerging technologies for building comprehensive cancer evolution roadmaps.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cancerbio-061421-123301
2023-04-11
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/cancerbio/7/1/annurev-cancerbio-061421-123301.html?itemId=/content/journals/10.1146/annurev-cancerbio-061421-123301&mimeType=html&fmt=ahah

Literature Cited

  1. Abbosh C, Bikbak NJ, Wilson GA, Jamal-Hanjani M, Constantin T et al. 2017. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature 545:7655446–51
    [Google Scholar]
  2. Abyzov A, Vaccarino FM. 2020. Cell lineage tracing and cellular diversity in humans. Annu. Rev. Genom. Hum. Genet. 21:101–16
    [Google Scholar]
  3. Adamson B, Norman TM, Jost M, Cho MY, Nuñez JK et al. 2016. A multiplexed single-cell CRISPR screening platform enables systematic dissection of the unfolded protein response. Cell 167:71867–82.e21
    [Google Scholar]
  4. Al'Khafaji AM, Deatherage D, Brock A. 2018. Control of lineage-specific gene expression by functionalized gRNA barcodes. ACS Synthet. Biol. 7:102468–74
    [Google Scholar]
  5. Alemany A, Florescu M, Baron CS, Peterson-Maduro J, van Oudenaarden A. 2018. Whole-organism clone tracing using single-cell sequencing. Nature 556:7699108–12
    [Google Scholar]
  6. Amirouchene-Angelozzi N, Swanton C, Bardelli A. 2017. Tumor evolution as a therapeutic target. Cancer Discov. 7:8805–17
    [Google Scholar]
  7. Askary A, Sanchez-Guardado L, Linton JM, Chadly DM, Budde MW et al. 2020. In situ readout of DNA barcodes and single base edits facilitated by in vitro transcription. Nat. Biotechnol. 38:166–75
    [Google Scholar]
  8. Bailey C, Black JRM, Reading JL, Litchfield K, Turajlic S et al. 2021. Tracking cancer evolution through the disease course. Cancer Discov. 11:4916–32
    [Google Scholar]
  9. Bhang HC, Ruddy D, Radhakrishna VK, Caushi JX, Zhao R et al. 2015. Studying clonal dynamics in response to cancer therapy using high-complexity barcoding. Nat. Med. 21:5440–48
    [Google Scholar]
  10. Biddy BA, Kong W, Kamimoto K, Guo C, Waye SE et al. 2018. Single-cell mapping of lineage and identity in direct reprogramming. Nature 564:7735219–24
    [Google Scholar]
  11. Binnewies M, Robetts EW, Kersten K, Chan V, Fearon D et al. 2018. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat. Med. 24:5541–50
    [Google Scholar]
  12. Black JRM, McGranahan N. 2021. Genetic and non-genetic clonal diversity in cancer evolution. Nat. Rev. Cancer 21:6379–92
    [Google Scholar]
  13. Boumahdi S, de Sauvage FJ. 2020. The great escape: tumour cell plasticity in resistance to targeted therapy. Nat. Rev. Drug Discov. 19:139–56
    [Google Scholar]
  14. Bowling S, Sritharan D, Osorio FG, Nguyen M, Cheung P, Rodriguez-Fraticelli A et al. 2020. An engineered CRISPR-Cas9 mouse line for simultaneous readout of lineage histories and gene expression profiles in single cells. Cell 181:61410–22.e27
    [Google Scholar]
  15. Cai H, Chew SK, Li C, Tsai MK, Andrejka L et al. 2021. A functional taxonomy of tumor suppression in oncogenic KRAS–driven lung cancer. Cancer Discov. 11:71754–73
    [Google Scholar]
  16. Camin JH, Sokal RR. 1965. A method for deducing branching sequences in phylogeny. Evol. Int. J. Org. Evol. 19:3311–26
    [Google Scholar]
  17. Caswell DR, Chuang C, Yang D, Chiou S, Cheemalavagu S et al. 2014. Obligate progression precedes lung adenocarcinoma dissemination. Cancer Discov. 4:7781–89
    [Google Scholar]
  18. Chaligne R, Gaiti F, Silverbush D, Schiffman JS, Weisman H et al. 2021. Epigenetic encoding, heritability and plasticity of glioma transcriptional cell states. Nat. Genet. 53:101469–79
    [Google Scholar]
  19. Chan MM, Smith ZD, Grosswendt S, Kretzmer H, Norman TM et al. 2019. Molecular recording of mammalian embryogenesis. Nature 570:775977–82
    [Google Scholar]
  20. Chang MT, Shanahan F, Nguyen TTT, Staben ST, Gazzard L et al. 2022. Identifying transcriptional programs underlying cancer drug response with TraCe-Seq. Nat. Biotechnol. 40:186–93
    [Google Scholar]
  21. Chen A, Liao S, Cheng M, Ma K, Wu L et al. 2022. Spatiotemporal transcriptomic atlas of mouse organogenesis using DNA nanoball-patterned arrays. Cell 185:101777–92.e21
    [Google Scholar]
  22. Chen J, Li Y, Yu T, McKay RM, Burns DK et al. 2012. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488:7412522–26
    [Google Scholar]
  23. Chen KH, Boettiger AN, Moffitt JR, Wang S, Zhuang X 2015. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348:6233aaa6090
    [Google Scholar]
  24. Chen W, Choi J, Nathans JF, Agarwal V, Martin B et al. 2021. Multiplex genomic recording of enhancer and signal transduction activity in mammalian cells. bioRxiv 2021.11.05.467434 https://doi.org/10.1101/2021.11.05.467434
    [Crossref]
  25. Chiou S, Winters IP, Wang J, Naranjo S, Dudgeon C et al. 2015. Pancreatic cancer modeling using retrograde viral vector delivery and in vivo CRISPR/Cas9-mediated somatic genome editing. Genes Dev. 29:141576–85
    [Google Scholar]
  26. Choi J, Chen W, Minkina A, Chardon FM, Suiter CC et al. 2022. A time-resolved, multi-symbol molecular recorder via sequential genome editing. Nature 608:792198–107
    [Google Scholar]
  27. Chow KK, Budde MW, Granados AA, Cabrera M, Yoon S et al. 2021. Imaging cell lineage with a synthetic digital recording system. Science 372:6538abb3099
    [Google Scholar]
  28. Chuang C, Greenside PG, Rodgers ZN, Brady JJ, Yang D et al. 2017. Molecular definition of a metastatic lung cancer state reveals a targetable CD109–Janus kinase–Stat axis. Nat. Med. 23:3291–300
    [Google Scholar]
  29. Cravens A, Jamil O, Kong D, Sockolosky JT, Smolke CD. 2021. Polymerase-guided base editing enables in vivo mutagenesis and rapid protein engineering. Nat. Commun. 12:1579
    [Google Scholar]
  30. Dixit A, Parnas O, Li B, Chen J, Fulco CP et al. 2016. Perturb-Seq: dissecting molecular circuits with scalable single-cell RNA profiling of pooled genetic screens. Cell 167:71853–66.e17
    [Google Scholar]
  31. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. 2012. Defining the mode of tumour growth by clonal analysis. Nature 488:7412527–30
    [Google Scholar]
  32. Emert BL, Cote CJ, Torre DA, Dardani IP, Jiang CL et al. 2021. Variability within rare cell states enables multiple paths toward drug resistance. Nat. Biotechnol. 39:7865–76
    [Google Scholar]
  33. Eng CL, Lawson M, Zhu Q, Dries R, Koulena N et al. 2019. Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+. Nature 568:7751235–39
    [Google Scholar]
  34. Eyler CE, Matsunaga H, Hovestadt V, Vantine SJ, van Galen P, Bernstein BE. 2020. Single-cell lineage analysis reveals genetic and epigenetic interplay in glioblastoma drug resistance. Genome Biol. 21:174
    [Google Scholar]
  35. Fang W, Bell C, Sapirstein A, Asami S, Leeper K et al. 2022. Quantitative fate mapping: reconstructing progenitor field dynamics via retrospective lineage barcoding. bioRxiv 10.1101/2022.02.13.480215. https://doi.org/10.1101/2022.02.13.480215
  36. Feldman D, Tsai F, Garrity AJ, O'Rourke R, Brenan L et al. 2020. CloneSifter: enrichment of rare clones from heterogeneous cell populations. BMC Biol. 18:177
    [Google Scholar]
  37. Feng J, DeWitt WS 3rd, McKenna A, Simon N, Willis AD, Matsen FA IV. 2021. Estimation of cell lineage trees by maximum-likelihood phylogenetics. Ann. Appl. Stat. 15:343–62
    [Google Scholar]
  38. Fennell KA, Vassiliadis D, Lam EYN, Martelotto LG, Balic JJ et al. 2022. Non-genetic determinants of malignant clonal fitness at single-cell resolution. Nature 601:7891125–31
    [Google Scholar]
  39. Flavahan WA, Gaskell E, Bernstein BE. 2017. Epigenetic plasticity and the hallmarks of cancer. Science 357:6348aal2380
    [Google Scholar]
  40. Foggetti G, Li C, Cai H, Hellyer JA, Lin W et al. 2021. Genetic determinants of EGFR-driven lung cancer growth and therapeutic response in vivo. Cancer Discov. 11:71736–53
    [Google Scholar]
  41. Forrow A, Schiebinger G. 2021. LineageOT is a unified framework for lineage tracing and trajectory inference. Nat. Commun. 12:4940
    [Google Scholar]
  42. Frieda KL, Linton JM, Hormoz S, Choi J, Chow KK et al. 2017. Synthetic recording and in situ readout of lineage information in single cells. Nature 541:7635107–11
    [Google Scholar]
  43. Gabbutt C, Schenck RO, Weisenberger DJ, Kimberley C, Berner A et al. 2022. Fluctuating methylation clocks for cell lineage tracing at high temporal resolution in human tissues. Nat. Biotechnol. 40:5720–30
    [Google Scholar]
  44. Ganesh K, Massagué J. 2021. Targeting metastatic cancer. Nat. Med. 27:134–44
    [Google Scholar]
  45. Gao R, Bai S, Henderson YC, Lin Y, Schalck A et al. 2021. Delineating copy number and clonal substructure in human tumors from single-cell transcriptomes. Nat. Biotechnol. 39:5599–608
    [Google Scholar]
  46. Garcia-Marques J, Epinosa-Medina I, Ku K, Yang C, Koyama M et al. 2020. A programmable sequence of reporters for lineage analysis. Nat. Neurosci. 23:121618–28
    [Google Scholar]
  47. Geisinger JM, Stearns T. 2020. CRISPR/Cas9 treatment causes extended TP53-dependent cell cycle arrest in human cells. Nucleic Acids Res. 48:169067–81
    [Google Scholar]
  48. Gerlinger M, McGranahan N, Dewhurst SM, Burrel RA, Tomlinson I, Swanton C. 2014. Cancer: evolution within a lifetime. Annu. Rev. Genet. 48:215–36
    [Google Scholar]
  49. Gerlinger M, Rowan AJ, Horswell S, Math M, Larkin J et al. 2012. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366:10883–92
    [Google Scholar]
  50. Gerrits A, Dykstra B, Kalmykowa OJ, Klauke K, Verovskaya E et al. 2010. Cellular barcoding tool for clonal analysis in the hematopoietic system. Blood 115:132610–18
    [Google Scholar]
  51. Gerstung M, Jolly C, Leshchiner I, Dentro SC, Gonzalez S et al. 2020. The evolutionary history of 2,658 cancers. Nature 578:7793122–28
    [Google Scholar]
  52. Gong W, Granados AA, Hu J, Jones MG, Raz O et al. 2021. Benchmarked approaches for reconstruction of in vitro cell lineages and in silico models of C. elegans and M. musculus developmental trees. Cell Syst. 12:8810–26.e4
    [Google Scholar]
  53. Gong W, Kim HJ, Garry DJ, Kwak I 2022. Single cell lineage reconstruction using distance-based algorithms and the R package, DCLEAR. BMC Bioinformat. 23:103
    [Google Scholar]
  54. Granja JM, Klemm S, McGinnis LM, Kathiria AS, Mezger A et al. 2019. Single-cell multiomic analysis identifies regulatory programs in mixed-phenotype acute leukemia. Nat. Biotechnol. 37:121458–65
    [Google Scholar]
  55. Greaves M, Maley CC. 2012. Clonal evolution in cancer. Nature 481:7381306–13
    [Google Scholar]
  56. Greenman C, Stephens P, Smith R, Dalgliesh GL, Hunter C et al. 2007. Patterns of somatic mutation in human cancer genomes. Nature 446:7132153–58
    [Google Scholar]
  57. Grüner BM, Schulze CJ, Yang D, Ogasawara D, Dix MM et al. 2016. An in vivo multiplexed small-molecule screening platform. Nat. Methods 13:10883–89
    [Google Scholar]
  58. Gutierrez C, Al'Khafaji AM, Brenner E, Johson KE, Gohil SH et al. 2021. Multifunctional barcoding with ClonMapper enables high-resolution study of clonal dynamics during tumor evolution and treatment. Nat. Cancer 2:7758–72
    [Google Scholar]
  59. Gutierrez C, Vilas CK, Wu CJ, Al'Khafaji AM 2022. Functionalized lineage tracing can enable the development of homogenization-based therapeutic strategies in cancer. Front. Immunol. 13:859032
    [Google Scholar]
  60. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:5646–74
    [Google Scholar]
  61. Hata AN, Niederst MJ, Archibald HL, Gomez-Caraballo M, Siddiqui FM et al. 2016. Tumor cells can follow distinct evolutionary paths to become resistant to epidermal growth factor receptor inhibition. Nat. Med. 22:3262–69
    [Google Scholar]
  62. He L, Li Y, Li Y, Pu W, Huang X et al. 2017. Enhancing the precision of genetic lineage tracing using dual recombinases. Nat. Med. 23:121488–98
    [Google Scholar]
  63. He Z, Maynard A, Jain A, Gerber T, Petri R et al. 2022. Lineage recording in human cerebral organoids. Nat. Methods 19:90–99
    [Google Scholar]
  64. Hirrlinger J, Scheller A, Hirrlinger PG, Kellert B, Tang W et al. 2009. Split-Cre complementation indicates coincident activity of different genes in vivo. PLOS ONE 4:e4286
    [Google Scholar]
  65. Hu Z, Li Z, Zhicheng M, Curtis C. 2020. Multi-cancer analysis of clonality and the timing of systemic spread in paired primary tumors and metastases. Nat. Genet. 52:7701–8
    [Google Scholar]
  66. Hussmann JA, Ling J, Ravisankar P, Yan J, Cirincione A et al. 2021. Mapping the genetic landscape of DNA double-strand break repair. Cell 184:225653–69.e25
    [Google Scholar]
  67. Hwang B, Lee W, Lee W, Yum S, Jeon Y et al. 2019. Lineage tracing using a Cas9-deaminase barcoding system targeting endogenous L1 elements. Nat. Commun. 10:1234
    [Google Scholar]
  68. Ihry RJ, Worringer KA, Salick MR, Frias E, Ho D et al. 2018. p53 inhibits CRISPR–Cas9 engineering in human pluripotent stem cells. Nat. Med. 24:7939–46
    [Google Scholar]
  69. Jamal-Hanjani M, Quezada SA, Larkin J, Swanton C. 2015. Translational implications of tumor heterogeneity. Clin. Cancer Res. 21:61258–66
    [Google Scholar]
  70. Jin X, Demere Z, Nair K, Ali A, Ferraro G et al. 2020. A metastasis map of human cancer cell lines. Nature 588:7837331–36
    [Google Scholar]
  71. Jones MG, Khodaverdian A, Quinn JJ, Chan MM, Hussman JA et al. 2020. Inference of single-cell phylogenies from lineage tracing data using Cassiopeia. Genome Biol. 21:92
    [Google Scholar]
  72. Jones MG, Rosen Y, Yosef N. 2022. Interactive, integrated analysis of single-cell transcriptomic and phylogenetic data with PhyloVision. Cell Rep. Methods 2:4100200
    [Google Scholar]
  73. Jones S, Chen W, Parmigiani G, Diehl F, Beerenwinkel N et al. 2008. Comparative lesion sequencing provides insights into tumor evolution. PNAS 105:114283–88
    [Google Scholar]
  74. Kalhor R, Mali P, Church GM. 2017. Rapidly evolving homing CRISPR barcodes. Nat. Methods 14:2195–200
    [Google Scholar]
  75. Kim C, Gao R, Sei E, Brandt R, Hartman J et al. 2018. Chemoresistance evolution in triple-negative breast cancer delineated by single-cell sequencing. Cell 173:4879–93.e13
    [Google Scholar]
  76. Kretzschmar K, Watt FM. 2012. Lineage TRACING. Cell 148:1–233–45
    [Google Scholar]
  77. LaFave LM, Kartha VK, Ma S, Meli K, Del Priore I et al. 2020. Epigenomic state transitions characterize tumor progression in mouse lung adenocarcinoma. Cancer Cell 38:2212–28.e13
    [Google Scholar]
  78. Lamprecht S, Schmidt EM, Blaj C, Hermeking H, Jung A et al. 2017. Multicolor lineage tracing reveals clonal architecture and dynamics in colon cancer. Nat. Commun. 8:1406
    [Google Scholar]
  79. Le Magnen C, Shen MM, Abate-Shen C. 2018. Lineage plasticity in cancer progression and treatment. Annu. Rev. Cancer Biol. 2:271–89
    [Google Scholar]
  80. Li C, Lin W, Rizvi H, Cai H, McFarland CD et al. 2021. Quantitative in vivo analyses reveal a complex pharmacogenomic landscape in lung adenocarcinoma. Cancer Res. 81:174570–80
    [Google Scholar]
  81. Li Y, Lv Z, Zhang S, Wang Z, He L et al. 2020. Genetic fate mapping of transient cell fate reveals N-cadherin activity and function in tumor metastasis. Dev. Cell 54:5593–607.e5
    [Google Scholar]
  82. Lin D, Li X, Park P, Tang B, Shen H et al. 2021. Time-tagged ticker tapes for intracellular recordings. bioRxiv 10.1101/2021.10.13.463862. https://doi.org/10.1101/2021.10.13.463862
  83. Liu K, Deng S, Ye C, Yao Z, Wang J et al. 2021. Mapping single-cell-resolution cell phylogeny reveals cell population dynamics during organ development. Nat. Methods 18:121506–14
    [Google Scholar]
  84. Liu K, Jin H, Zhou B 2020. Genetic lineage tracing with multiple DNA recombinases: a user's guide for conducting more precise cell fate mapping studies. J. Biol. Chem. 295:196413–24
    [Google Scholar]
  85. Liu Q, Liu K, Cui G, Huang X, Yao S et al. 2019. Lung regeneration by multipotent stem cells residing at the bronchioalveolar-duct junction. Nat. Genet. 51:4728–38
    [Google Scholar]
  86. Livet J, Weissman TA, Kang H, Draft RW, Lu J et al. 2007. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450:716656–62
    [Google Scholar]
  87. Loveless TB, Carlson CK, Hu VJ, Helmy CAD, Liang G et al. 2021a. Molecular recording of sequential cellular events into DNA. bioRxiv 10.1101/2021.11.05.467507. https://doi.org/10.1101/2021.11.05.467507
  88. Loveless TB, Grotts JH, Schecter MW, Forouzmand E, Carlson CK et al. 2021b. Lineage tracing and analog recording in mammalian cells by single-site DNA writing. Nat. Chem. Biol. 17:6739–47
    [Google Scholar]
  89. Ludwig LS, Lareau CA, Ulirsch JC, Christian E, Muus C et al. 2019. Lineage tracing in humans enabled by mitochondrial mutations and single-cell genomics. Cell 176:61325–39.e22
    [Google Scholar]
  90. Lüönd F, Sugiyama N, Bill R, Bornes L, Hager C et al. 2021. Distinct contributions of partial and full EMT to breast cancer malignancy. Dev. Cell 56:233203–21.e11
    [Google Scholar]
  91. Maddipati R, Stranger BZ. 2015. Pancreatic cancer metastases harbor evidence of polyclonality. Cancer Discov. 5:101086–97
    [Google Scholar]
  92. Marjanovic ND, Hofree M, Chan JE, Canner D, Wu K et al. 2020. Emergence of a high-plasticity cell state during lung cancer evolution. Cancer Cell 38:2229–46.e13
    [Google Scholar]
  93. Marusyk A, Polyak K. 2010. Tumor heterogeneity: causes and consequences. Biochim. Biophys. Acta Rev. Cancer 1805:105–17
    [Google Scholar]
  94. McGranahan N, Swanton C. 2017. Clonal heterogeneity and tumor evolution: past, present, and the future. Cell 168:4613–28
    [Google Scholar]
  95. McKenna A, Findlay GM, Gagnon JA, Horwitz MS, Schier AF, Shendure J. 2016. Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science 353:6298aaf7907
    [Google Scholar]
  96. McKenna A, Gangon JA. 2019. Recording development with single cell dynamic lineage tracing. Development 146:12dev169730
    [Google Scholar]
  97. Merino D, Weber TS, Serrano A, Vaillant F, Liu K et al. 2019. Barcoding reveals complex clonal behavior in patient-derived xenografts of metastatic triple negative breast cancer. Nat. Commun. 10:766
    [Google Scholar]
  98. Michlits G, Hubmann M, Wu S, Vainorius G, Boudusan E et al. 2017. CRISPR-UMI: single-cell lineage tracing of pooled CRISPR–Cas9 screens. Nat. Methods 14:121191–97
    [Google Scholar]
  99. Minussi DC, Nicholson MD, Ye H, Davis A, Wang K et al. 2021. Breast tumours maintain a reservoir of subclonal diversity during expansion. Nature 592:7853302–8
    [Google Scholar]
  100. Moffitt JR, Hao J, Wang G, Chen KH, Babcok HP, Zhuang X. 2016. High-throughput single-cell gene-expression profiling with multiplexed error-robust fluorescence in situ hybridization. PNAS 113:3911046–51
    [Google Scholar]
  101. Nagy A. 2000. Cre recombinase: the universal reagent for genome tailoring. Genesis 26:299–109
    [Google Scholar]
  102. Navin N, Kendall J, Troge J, Andrews P, Rodgers L et al. 2011. Tumour evolution inferred by single-cell sequencing. Nature 472:734190–94
    [Google Scholar]
  103. Navin NE, Hicks J. 2010. Tracing the tumor lineage. Mol. Oncol. 4:3267–83
    [Google Scholar]
  104. Neftel C, Laffy J, Filbin MG, Hara T, Shore ME et al. 2019. An integrative model of cellular states, plasticity, and genetics for glioblastoma. Cell 178:4835–49.e21
    [Google Scholar]
  105. Nguyen LV, Pellacani D, Lefort S, Kannan N, Osako T et al. 2015. Barcoding reveals complex clonal dynamics of de novo transformed human mammary cells. Nature 528:7581267–71
    [Google Scholar]
  106. Nowell PC. 1976. The clonal evolution of tumor cell populations. Science 194:426023–28
    [Google Scholar]
  107. Ogbeide S, Giannese F, Mincarelli L, Macaulay IC. 2022. Into the multiverse: advances in single-cell multiomic profiling. Trends Genet. 38:8831–43
    [Google Scholar]
  108. Oren Y, Tsabar M, Cuoco MS, Amir-Zilberstein L, Cabanos HF et al. 2021. Cycling cancer persister cells arise from lineages with distinct programs. Nature 596:7873576–82
    [Google Scholar]
  109. Ouardini K, Lopez R, Jones MG, Prillo S, Zhang R et al. 2021. Reconstructing unobserved cellular states from paired single-cell lineage tracing and transcriptomics data. bioRxiv 10.1101/2021.05.28.446021. https://doi.org/10.1101/2021.05.28.446021
  110. Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM et al. 2014. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344:61901396–401
    [Google Scholar]
  111. Pei W, Feyerabend TB, Rössler J, Wang X, Postrach D et al. 2017. Polylox barcoding reveals haematopoietic stem cell fates realized in vivo. Nature 548:7668456–60
    [Google Scholar]
  112. Penter L, Gohil SH, Lareau C, Ludwig LS, Parry EM et al. 2021a. Longitudinal single-cell dynamics of chromatin accessibility and mitochondrial mutations in chronic lymphocytic leukemia mirror disease history. Cancer Discov. 11:123048–63
    [Google Scholar]
  113. Penter L, Gohil SH, Wu CJ. 2021b. Natural barcodes for longitudinal single cell tracking of leukemic and immune cell dynamics. Front. Immunol. 12:788891
    [Google Scholar]
  114. Perli SD, Cui CH, Lu TK. 2016. Continuous genetic recording with self-targeting CRISPR-Cas in human cells. Science 353:6304aag0511
    [Google Scholar]
  115. Pierce SE, Granja JM, Greenleaf WJ. 2021. High-throughput single-cell chromatin accessibility CRISPR screens enable unbiased identification of regulatory networks in cancer. Nat. Commun. 12:2969
    [Google Scholar]
  116. Powles T, Assaf ZJ, Davarpanah N, Bancheraeu R, Szabados B et al. 2021. ctDNA guiding adjuvant immunotherapy in urothelial carcinoma. Nature 595:432–37
    [Google Scholar]
  117. Quinn JJ, Jones MG, Okomito RA, Najo S, Chan MM et al. 2021. Single-cell lineages reveal the rates, routes, and drivers of metastasis in cancer xenografts. Science 371:6532abc1944
    [Google Scholar]
  118. Quintanal-Villalonga A, Chan JM, Yu HA, Pe'er D, Sawyers CL et al. 2020. Lineage plasticity in cancer: a shared pathway of therapeutic resistance. Nat. Rev. Clin. Oncol. 17:6360–71
    [Google Scholar]
  119. Raj B, Wagner DE, McKenna A, Pandey S, Klein A et al. 2018. Simultaneous single-cell profiling of lineages and cell types in the vertebrate brain. Nat. Biotechnol. 36:5442–50
    [Google Scholar]
  120. Reeves MQ, 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. 20:6699–709
    [Google Scholar]
  121. Rios AC, Capaldo BD, Vaillant F, Pal B, van Ineveld R et al. 2019. Intraclonal plasticity in mammary tumors revealed through large-scale single-cell resolution 3D imaging. Cancer Cell 35:6953
    [Google Scholar]
  122. Rogers ZN, McFarland CD, Winters IP, Naranjo S, Chuang C et al. 2017. A quantitative and multiplexed approach to uncover the fitness landscape of tumor suppression in vivo. Nat. Methods 14:7737–42
    [Google Scholar]
  123. Roh V, Abramowski P, Hiou-Feige A, Cornils K, Rivals J et al. 2018. Cellular barcoding identifies clonal substitution as a hallmark of local recurrence in a surgical model of head and neck squamous cell carcinoma. Cell Rep. 25:82208–22.e7
    [Google Scholar]
  124. Rovira-Clavé X, Drainas AP, Jiang S, Bai Y, Baron M et al. 2021. Spatial epitope barcoding reveals subclonal tumor patch behaviors. bioRxiv 10.1101/2021.06.29.449991. https://doi.org/10.1101/2021.06.29.449991
  125. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:4406–25
    [Google Scholar]
  126. Salehi S, Kabeer F, Ceglia N, Andronesu M, Williams M et al. 2021. Clonal fitness inferred from time-series modelling of single-cell cancer genomes. Nature 595:7868585–90
    [Google Scholar]
  127. Salvador-Martínez I, Grillo M, Averof M, Telford MJ. 2019. Is it possible to reconstruct an accurate cell lineage using CRISPR recorders?. eLife 8:e40292
    [Google Scholar]
  128. Salvador-Martínez I, Grillo M, Averof M, Telford MJ. 2021. CeLaVi: an interactive cell lineage visualization tool. Nucleic Acids Res. 49:W1W80–85
    [Google Scholar]
  129. Schepers AG, Snipper HJ, Stange DE, van den Born M, van Es JH et al. 2012. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337:6095730–35
    [Google Scholar]
  130. Schepers K, Swart E, van Heijst JWJ, Gerlach C, Castrucci M et al. 2008. Dissecting T cell lineage relationships by cellular barcoding. J. Exp. Med. 205:102309–18
    [Google Scholar]
  131. Schmidt F, Cherepkova MY, Platt RJ. 2018. Transcriptional recording by CRISPR spacer acquisition from RNA. Nature 562:7727380–85
    [Google Scholar]
  132. Schmierer B, Botla SK, Zhang J, Turnen M, Kivioja T, Taipale J. 2017. CRISPR/Cas9 screening using unique molecular identifiers. Mol. Syst. Biol. 13:10945
    [Google Scholar]
  133. Shah SP, Morin RD, Khattra J, Prentice L, Puge T et al. 2009. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461:7265809–13
    [Google Scholar]
  134. Shipman SL, Nivala J, Macklis JD, Church GM. 2016. Molecular recordings by directed CRISPR spacer acquisition. Science 353:6298aaf1175
    [Google Scholar]
  135. Simeonov KP, Byrns CN, Clark ML, Norgard RJ, Martin B et al. 2021. Single-cell lineage tracing of metastatic cancer reveals selection of hybrid EMT states. Cancer Cell 39:81150–62.e9
    [Google Scholar]
  136. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M et al. 2010. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143:1134–44
    [Google Scholar]
  137. Sottoriva A, Kang H, Ma Z, Graham T, Salomon MP et al. 2015. A big bang model of human colorectal tumor growth. Nat. Genet. 47:3209–16
    [Google Scholar]
  138. Spanjaard B, Hu B, Mitic N, Olivares-Chauvet P, Janjuha S et al. 2018. Simultaneous lineage tracing and cell-type identification using CRISPR–Cas9-induced genetic scars. Nat. Biotechnol. 36:5469–73
    [Google Scholar]
  139. Ståhl PL, Salmén F, Vickovic S, Lundmark A, Navaro JF et al. 2016. Visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 353:629478–82
    [Google Scholar]
  140. Stickels RR, Murray E, Kuman P, Li J, Marshall JL et al. 2021. Highly sensitive spatial transcriptomics at near-cellular resolution with Slide-seqV2. Nat. Biotechnol. 39:3313–19
    [Google Scholar]
  141. Tanay A, Regev A. 2017. Scaling single-cell genomics from phenomenology to mechanism. Nature 541:7637331–38
    [Google Scholar]
  142. Tang W, Liu DR. 2018. Rewritable multi-event analog recording in bacterial and mammalian cells. Science 360:63856385
    [Google Scholar]
  143. Tao L, Raz O, Marx Z, Ghosh MS, Huber S, Greindl-Junghans J et al. 2021. Retrospective cell lineage reconstruction in humans by using short tandem repeats. Cell Rep. Methods 1:3100054
    [Google Scholar]
  144. Tarabichi M, Salcedo A, Deshwar AG, Leathlobhair M, Wintersinger J et al. 2021. A practical guide to cancer subclonal reconstruction from DNA sequencing. Nat. Methods 18:2144–55
    [Google Scholar]
  145. Torborg SR, Li Z, Chan JE, Tammela T. 2022. Cellular and molecular mechanisms of plasticity in cancer. Trends Cancer Res. 8:9735–46
    [Google Scholar]
  146. Tulpule A, Bivona TG. 2020. Acquired resistance in lung cancer. Annu. Rev. Cancer Biol. 4:279–97
    [Google Scholar]
  147. Turajlic S, Sottoriva A, Graham T, Swanton C. 2019. Resolving genetic heterogeneity in cancer. Nat. Rev. Genet. 20:7404–16
    [Google Scholar]
  148. Turajlic S, Xu H, Litchfield K, Rowan A, Chambers T et al. 2018. Tracking cancer evolution reveals constrained routes to metastases: TRACERx renal. Cell 173:3581–94.e12
    [Google Scholar]
  149. Umkehrer C, Holstein F, Formenti L, Jude J, Froussious K et al. 2021. Isolating live cell clones from barcoded populations using CRISPRa-inducible reporters. Nat. Biotechnol. 39:2174–78
    [Google Scholar]
  150. VanHorn S, Morris SA. 2021. Next-generation lineage tracing and fate mapping to interrogate development. Dev. Cell 56:7–21
    [Google Scholar]
  151. Vendramin R, Litchfield K, Swanton C. 2021. Cancer evolution: Darwin and beyond. EMBO J. 40:18e108389
    [Google Scholar]
  152. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Dias LA, Kinzler KW. 2013. Cancer genome landscapes. Science 339:61271546–58
    [Google Scholar]
  153. Wagner DE, Klein AM. 2020. Lineage tracing meets single-cell omics: opportunities and challenges. Nat. Rev. Genet. 21:410–27
    [Google Scholar]
  154. Wagner DE, Weinreb C, Collins ZM, Briggs JA, Megason SG, Klein AM. 2018. Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo. Science 360:6392981–87
    [Google Scholar]
  155. Walens A, Lin J, Damrauer JS, McKinney B, Lupo R et al. 2020. Adaptation and selection shape clonal evolution of tumors during residual disease and recurrence. Nat. Commun. 11:5017
    [Google Scholar]
  156. Walsh C, Cepko CL. 1992. Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 255:5043434–40
    [Google Scholar]
  157. Wang R, Zhang R, Khodaveridan A, Yosef N. 2021. Theoretical guarantees for phylogeny inference from single-cell lineage tracing. bioRxiv 10.1101/2021.11.21.469464. https://doi.org/10.1101/2021.11.21.469464
  158. Wang S, Herriges MJ, Hurley K, Kotton DN, Klein AM. 2022. CoSpar identifies early cell fate biases from single-cell transcriptomic and lineage information. Nat. Biotechnol. 40:1066–77
    [Google Scholar]
  159. Weinreb C, Rodriguez-Fraticelli A, Camargo FD, Klein AM. 2020. Lineage tracing on transcriptional landscapes links state to fate during differentiation. Science 367:6479aaw3381
    [Google Scholar]
  160. Weissman TA, Pan YA. 2015. Brainbow: new resources and emerging biological applications for multicolor genetic labeling and analysis. Genetics 199:2293–306
    [Google Scholar]
  161. Williams MJ, Werner B, Heide T, Curtis C, Barnes C et al. 2018. Quantification of subclonal selection in cancer from bulk sequencing data. Nat. Genet. 50:6895–903
    [Google Scholar]
  162. Winters IP, Chiou S, Paulk NK, McFarland CD, Lalgudi PV et al. 2017. Multiplexed in vivo homology-directed repair and tumor barcoding enables parallel quantification of Kras variant oncogenicity. Nat. Commun. 8:2053
    [Google Scholar]
  163. Woodworth MB, Girskis KM, Walsh CA. 2017. Building a lineage from single cells: genetic techniques for cell lineage tracking. Nat. Rev. Genet. 18:4230–44
    [Google Scholar]
  164. Wroblewska A, Dhainaut M, Ben-Zvi B, Rose SA, Park ES et al. 2018. Protein barcodes enable high-dimensional single-cell CRISPR screens. Cell 175:41141–55.e16
    [Google Scholar]
  165. Yachida S, Jones S, Bozic I, Antal T, Leary R et al. 2010. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467:73191114–17
    [Google Scholar]
  166. Yang D, Jones MG, Naranjo S, Rideout WM 3rd, Min KH et al. 2022. Lineage tracing reveals the phylodynamics, plasticity, and paths of tumor evolution. Cell 185:111905–23.e25
    [Google Scholar]
  167. Yang J, Antin P, Berx G, Blanpain C, Brabletz T et al. 2020. Guidelines and definitions for research on epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 21:6341–52
    [Google Scholar]
  168. Yao Z, Mich JK, Ku S, Menon V, Krostag A et al. 2017. A single-cell roadmap of lineage bifurcation in human ESC models of embryonic brain development. Cell Stem Cell 20:120–34
    [Google Scholar]
  169. Yates LR, Knappskog S, Wedge D, Ramery JHR, Gonzalez S et al. 2017. Genomic evolution of breast cancer metastasis and relapse. Cancer Cell 32:2169–84.e7
    [Google Scholar]
  170. Yu M, Bardia A, Wittner BS, Sott SL, Smas ME et al. 2013. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339:6119580–84
    [Google Scholar]
  171. Zafar H, Lin C, Bar-Joseph Z. 2020. Single-cell lineage tracing by integrating CRISPR-Cas9 mutations with transcriptomic data. Nat. Commun. 11:3055
    [Google Scholar]
  172. Zhang W, Bado IL, Hu J, Wan Y, Wu L et al. 2021. The bone microenvironment invigorates metastatic seeds for further dissemination. Cell 184:92471–86.e20
    [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-061421-123301
Loading
/content/journals/10.1146/annurev-cancerbio-061421-123301
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error