Mastering the use of cellular barcoding to explore cancer heterogeneity (original) (raw)
Marusyk, A., Janiszewska, M. & Polyak, K. Intratumor heterogeneity: the Rosetta stone of therapy resistance. Cancer Cell37, 471–484 (2020). ArticleCASPubMedPubMed Central Google Scholar
Tabassum, D. P. & Polyak, K. Tumorigenesis: it takes a village. Nat. Rev. Cancer15, 473–483 (2015). ArticleCASPubMed Google Scholar
Curtis, C. et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature486, 346–352 (2012). ArticleCASPubMedPubMed Central Google Scholar
Kim, C. et al. Chemoresistance evolution in triple-negative breast cancer delineated by single-cell sequencing. Cell173, 879–893 e813 (2018). ArticleCASPubMedPubMed Central Google Scholar
Jia, Q., Chu, H., Jin, Z., Long, H. & Zhu, B. High-throughput single-cell sequencing in cancer research. Signal. Transduct. Target. Ther.7, 145 (2022). ArticlePubMedPubMed Central Google Scholar
Nam, A. S., Chaligne, R. & Landau, D. A. Integrating genetic and non-genetic determinants of cancer evolution by single-cell multi-omics. Nat. Rev. Genet.22, 3–18 (2021). ArticleCASPubMed Google Scholar
Merino, D. et al. Barcoding reveals complex clonal behavior in patient-derived xenografts of metastatic triple negative breast cancer. Nat. Commun.10, 766 (2019). ArticleCASPubMedPubMed Central Google Scholar
Naik, S. H., Schumacher, T. N. & Perie, L. Cellular barcoding: a technical appraisal. Exp. Hematol.42, 598–608 (2014). ArticlePubMed Google Scholar
Bystrykh, L. V. & Belderbos, M. E. Clonal analysis of cells with cellular barcoding: when numbers and sizes matter. Methods Mol. Biol.1516, 57–89 (2016). ArticleCASPubMed Google Scholar
Kebschull, J. M. & Zador, A. M. Cellular barcoding: lineage tracing, screening and beyond. Nat. Methods15, 871–879 (2018). ArticleCASPubMed Google Scholar
Klein, C. A. Parallel progression of primary tumours and metastases. Nat. Rev. Cancer9, 302–312 (2009). ArticleCASPubMed Google Scholar
Dagogo-Jack, I. & Shaw, A. T. Tumour heterogeneity and resistance to cancer therapies. Nat. Rev. Clin. Oncol.15, 81–94 (2018). ArticleCASPubMed Google Scholar
Livet, J. et al. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature450, 56–62 (2007). ArticleCASPubMed Google Scholar
Snippert, H. J. et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell143, 134–144 (2010). ArticleCASPubMed Google Scholar
Dumas, L., Clavreul, S., Michon, F. & Loulier, K. Multicolor strategies for investigating clonal expansion and tissue plasticity. Cell Mol. Life Sci.79, 141 (2022). ArticleCASPubMedPubMed Central Google Scholar
Baron, C. S. & van Oudenaarden, A. Unravelling cellular relationships during development and regeneration using genetic lineage tracing. Nat. Rev. Mol. Cell Biol.20, 753–765 (2019). ArticleCASPubMed Google Scholar
Wagner, D. E. & Klein, A. M. Lineage tracing meets single-cell omics: opportunities and challenges. Nat. Rev. Genet.21, 410–427 (2020). ArticleCASPubMedPubMed Central Google Scholar
Weber, K. et al. RGB marking facilitates multicolor clonal cell tracking. Nat. Med.17, 504–509 (2011). ArticleCASPubMed Google Scholar
Caiado, F. et al. Lineage tracing of acute myeloid leukemia reveals the impact of hypomethylating agents on chemoresistance selection. Nat. Commun.10, 4986 (2019). ArticlePubMedPubMed Central Google Scholar
Berthelet, J. et al. The site of breast cancer metastases dictates their clonal composition and reversible transcriptomic profile. Sci. Adv.https://doi.org/10.1126/sciadv.abf4408 (2021). This study uses optical barcoding to map clonal fate and interactions of 31 breast cancer clones in vitro and in vivo, in multiple organs and in response to targeted therapy. ArticlePubMedPubMed Central Google Scholar
Nguyen, L. V. et al. DNA barcoding reveals diverse growth kinetics of human breast tumour subclones in serially passaged xenografts. Nat. Commun.5, 5871 (2014). This study is one of the first to use genetic barcoding to investigate the frequency of tumour-initiating cells in retransplantation experiments using PDXs. ArticleCASPubMed Google Scholar
Naik, S. H. et al. Diverse and heritable lineage imprinting of early haematopoietic progenitors. Nature496, 229–232 (2013). ArticleCASPubMed Google Scholar
Jordan, C. T. & Lemischka, I. R. Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev.4, 220–232 (1990). ArticleCASPubMed Google Scholar
Walsh, C. & Cepko, C. L. Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science255, 434–440 (1992). ArticleCASPubMed Google Scholar
Elder, A. et al. Abundant and equipotent founder cells establish and maintain acute lymphoblastic leukaemia. Leukemia31, 2577–2586 (2017). ArticleCASPubMedPubMed Central Google Scholar
Nguyen, L. V. et al. Clonal analysis via barcoding reveals diverse growth and differentiation of transplanted mouse and human mammary stem cells. Cell Stem Cell14, 253–263 (2014). ArticleCASPubMed Google Scholar
Seth, S. et al. Pre-existing functional heterogeneity of tumorigenic compartment as the origin of chemoresistance in pancreatic tumors. Cell Rep.26, 1518–1532 e1519 (2019). ArticleCASPubMed Google Scholar
Fennell, K. A. et al. Non-genetic determinants of malignant clonal fitness at single-cell resolution. Naturehttps://doi.org/10.1038/s41586-021-04206-7 (2021). This article describes the generation of a high-diversity transcribed library, which is used to study, over time, the non-genetic processes influencing clonal fitness in leukaemia. ArticlePubMed Google Scholar
Oren, Y. et al. Cycling cancer persister cells arise from lineages with distinct programs. Naturehttps://doi.org/10.1038/s41586-021-03796-6 (2021). This study describes the development of the Watermelon library, which enables the characterization of drug-resistant clones at single-cell resolution. ArticlePubMedPubMed Central Google Scholar
Gutierrez, C. et al. Multifunctional barcoding with ClonMapper enables high-resolution study of clonal dynamics during tumor evolution and treatment. Nat. Cancer2, 758–772 (2021). This study describes the use of a multifunctional library, ClonMapper, to combine lineage tracing, single-cell analysis and lineage recall to study the behaviour of leukaemia clones in response to chemotherapy. ArticleCASPubMedPubMed Central Google Scholar
Prasher, D. C., Eckenrode, V. K., Ward, W. W., Prendergast, F. G. & Cormier, M. J. Primary structure of the Aequorea victoria green-fluorescent protein. Gene111, 229–233 (1992). ArticleCASPubMed Google Scholar
Chudakov, D. M., Matz, M. V., Lukyanov, S. & Lukyanov, K. A. Fluorescent proteins and their applications in imaging living cells and tissues. Physiol. Rev.90, 1103–1163 (2010). ArticleCASPubMed Google Scholar
Kremers, G. J., Gilbert, S. G., Cranfill, P. J., Davidson, M. W. & Piston, D. W. Fluorescent proteins at a glance. J. Cell Sci.124, 157–160 (2011). ArticleCASPubMed Google Scholar
Weber, K., Bartsch, U., Stocking, C. & Fehse, B. A multicolor panel of novel lentiviral “gene ontology” (LeGO) vectors for functional gene analysis. Mol. Ther.16, 698–706 (2008). ArticleCASPubMed Google Scholar
Weber, K., Mock, U., Petrowitz, B., Bartsch, U. & Fehse, B. Lentiviral gene ontology (LeGO) vectors equipped with novel drug-selectable fluorescent proteins: new building blocks for cell marking and multi-gene analysis. Gene Ther.17, 511–520 (2010). ArticleCASPubMed Google Scholar
Weber, K., Thomaschewski, M., Benten, D. & Fehse, B. RGB marking with lentiviral vectors for multicolor clonal cell tracking. Nat. Protoc.7, 839–849 (2012). This article provides a highly detailed protocol for the use of red–green–blue labelling using LeGO vectors. ArticleCASPubMed Google Scholar
Gomez-Nicola, D., Riecken, K., Fehse, B. & Perry, V. H. In-vivo RGB marking and multicolour single-cell tracking in the adult brain. Sci. Rep.4, 7520 (2014). ArticleCASPubMedPubMed Central Google Scholar
Mohme, M. et al. Optical barcoding for single-clone tracking to study tumor heterogeneity. Mol. Ther.25, 621–633 (2017). This study provides one of the first demonstrations highlighting the power of LeGO vectors to study cancer heterogeneity. ArticleCASPubMedPubMed Central Google Scholar
Marusyk, A. & Polyak, K. Tumor heterogeneity: causes and consequences. Biochim. Biophys. Acta1805, 105–117 (2010). CASPubMed Google Scholar
Singh, S. K. et al. Identification of human brain tumour initiating cells. Nature432, 396–401 (2004). ArticleCASPubMed Google Scholar
Zhang, M. et al. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res.68, 4674–4682 (2008). ArticleCASPubMedPubMed Central Google Scholar
Echeverria, G. V. et al. High-resolution clonal mapping of multi-organ metastasis in triple negative breast cancer. Nat. Commun.9, 5079 (2018). ArticlePubMedPubMed Central Google Scholar
van der Heijden, M. et al. Spatiotemporal regulation of clonogenicity in colorectal cancer xenografts. Proc. Natl Acad. Sci. USA116, 6140–6145 (2019). ArticlePubMedPubMed Central Google Scholar
Nguyen, L. V. et al. Barcoding reveals complex clonal dynamics of de novo transformed human mammary cells. Nature528, 267–271 (2015). ArticleCASPubMed Google Scholar
Baldwin, L. A. et al. DNA barcoding reveals ongoing immunoediting of clonal cancer populations during metastatic progression and in response to immunotherapy. Preprint at bioRxivhttps://doi.org/10.1101/2021.01.11.426174 (2021).
Wagenblast, E. et al. A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis. Nature520, 358–362 (2015). ArticleCASPubMedPubMed Central Google Scholar
Iacobuzio-Donahue, C. A. et al. Cancer biology as revealed by the research autopsy. Nat. Rev. Cancer19, 686–697 (2019). ArticleCASPubMed Google Scholar
Paget, S. The distribution of secondary growths in cancer of the breast. Lancet133, 571–573 (1889). Article Google Scholar
Lin, D. S. et al. DiSNE movie visualization and assessment of clonal kinetics reveal multiple trajectories of dendritic cell development. Cell Rep.22, 2557–2566 (2018). ArticleCASPubMed Google Scholar
Tian, L. et al. Clonal multi-omics reveals Bcor as a negative regulator of emergency dendritic cell development. Immunity54, 1338–1351 e1339 (2021). ArticleCASPubMed Google Scholar
Maetzig, T. et al. Lentiviral fluorescent genetic barcoding for multiplex fate tracking of leukemic cells. Mol. Ther. Methods Clin. Dev.6, 54–65 (2017). ArticleCASPubMedPubMed Central Google Scholar
Garcia-Bermudez, J. et al. Squalene accumulation in cholesterol auxotrophic lymphomas prevents oxidative cell death. Nature567, 118–122 (2019). ArticleCASPubMedPubMed Central Google Scholar
Akimov, Y., Bulanova, D., Timonen, S., Wennerberg, K. & Aittokallio, T. Improved detection of differentially represented DNA barcodes for high-throughput clonal phenomics. Mol. Syst. Biol.16, e9195 (2020). ArticleCASPubMedPubMed Central Google Scholar
Walens, A. et al. Adaptation and selection shape clonal evolution of tumors during residual disease and recurrence. Nat. Commun.11, 5017 (2020). ArticleCASPubMedPubMed Central Google Scholar
Rehman, S. K. et al. Colorectal cancer cells enter a diapause-like DTP state to survive chemotherapy. Cell184, 226–242 e221 (2021). ArticleCASPubMed Google Scholar
Jin, X. et al. A metastasis map of human cancer cell lines. Nature588, 331–336 (2020). This study uses the multiplexing capability of genetic barcoding to generate a ‘metastasis map’ for 500 cancer cell lines. ArticleCASPubMedPubMed Central Google Scholar
Alemany, A., Florescu, M., Baron, C. S., Peterson-Maduro, J. & van Oudenaarden, A. Whole-organism clone tracing using single-cell sequencing. Nature556, 108–112 (2018). ArticleCASPubMed Google Scholar
McKenna, A. et al. Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science353, aaf7907 (2016). ArticlePubMedPubMed Central Google Scholar
Frieda, K. L. et al. Synthetic recording and in situ readout of lineage information in single cells. Nature541, 107–111 (2017). ArticleCASPubMed Google Scholar
Raj, B. et al. Simultaneous single-cell profiling of lineages and cell types in the vertebrate brain. Nat. Biotechnol.36, 442–450 (2018). ArticleCASPubMedPubMed Central Google Scholar
Simeonov, K. P. et al. Single-cell lineage tracing of metastatic cancer reveals selection of hybrid EMT states. Cancer Cell39, 1150–1162 e1159 (2021). ArticleCASPubMedPubMed Central Google Scholar
Lamprecht, S. et al. Multicolor lineage tracing reveals clonal architecture and dynamics in colon cancer. Nat. Commun.8, 1406 (2017). ArticlePubMedPubMed Central Google Scholar
Tiede, S. et al. Multi-color clonal tracking reveals intra-stage proliferative heterogeneity during mammary tumor progression. Oncogene40, 12–27 (2021). ArticleCASPubMed Google Scholar
Kalhor, R., Mali, P. & Church, G. M. Rapidly evolving homing CRISPR barcodes. Nat. Methods14, 195–200 (2017). ArticleCASPubMed Google Scholar
Pei, W. et al. Using Cre-recombinase-driven Polylox barcoding for in vivo fate mapping in mice. Nat. Protoc.14, 1820–1840 (2019). ArticleCASPubMed Google Scholar
Weber, T. S. et al. Site-specific recombinatorics: in situ cellular barcoding with the Cre Lox system. BMC Syst. Biol.10, 43 (2016). ArticlePubMedPubMed Central Google Scholar
Bowling, S. et al. An engineered CRISPR-Cas9 mouse line for simultaneous readout of lineage histories and gene expression profiles in single cells. Cell181, 1410–1422 e1427 (2020). ArticleCASPubMedPubMed Central Google Scholar
Yu, C. et al. High-throughput identification of genotype-specific cancer vulnerabilities in mixtures of barcoded tumor cell lines. Nat. Biotechnol.34, 419–423 (2016). ArticleCASPubMedPubMed Central Google Scholar
Patwardhan, G. A. et al. Treatment scheduling effects on the evolution of drug resistance in heterogeneous cancer cell populations. NPJ Breast Cancer7, 60 (2021). ArticleCASPubMedPubMed Central Google Scholar
Hata, A. N. et al. Tumor cells can follow distinct evolutionary paths to become resistant to epidermal growth factor receptor inhibition. Nat. Med.22, 262–269 (2016). ArticleCASPubMedPubMed Central Google Scholar
Bhang, H. E. et al. Studying clonal dynamics in response to cancer therapy using high-complexity barcoding. Nat. Med.21, 440–448 (2015). ArticleCASPubMed Google Scholar
Hinohara, K. et al. KDM5 histone demethylase activity links cellular transcriptomic heterogeneity to therapeutic resistance. Cancer Cell34, 939–953 e939 (2018). ArticleCASPubMedPubMed Central Google Scholar
Marine, J. C., Dawson, S. J. & Dawson, M. A. Non-genetic mechanisms of therapeutic resistance in cancer. Nat. Rev. Cancer20, 743–756 (2020). ArticleCASPubMed Google Scholar
Kaufman, T. et al. Visual barcodes for clonal-multiplexing of live microscopy-based assays. Nat. Commun.13, 2725 (2022). In this study, fluorescent proteins targeted to specific locations are used to increase the multiplexing potential of optical barcoding. ArticleCASPubMedPubMed Central Google Scholar
Roh, V. et al. 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, 2208–2222 e2207 (2018). ArticleCASPubMed Google Scholar
Maetzig, T., Morgan, M. & Schambach, A. Fluorescent genetic barcoding for cellular multiplex analyses. Exp. Hematol.67, 10–17 (2018). ArticleCASPubMed Google Scholar
Askary, A. et al. In situ readout of DNA barcodes and single base edits facilitated by in vitro transcription. Nat. Biotechnol.38, 66–75 (2020). ArticleCASPubMed Google Scholar
Eyler, C. E. et al. Single-cell lineage analysis reveals genetic and epigenetic interplay in glioblastoma drug resistance. Genome Biol.21, 174 (2020). ArticleCASPubMedPubMed Central Google Scholar
Al’Khafaji, A. M., Deatherage, D. & Brock, A. Control of lineage-specific gene expression by functionalized gRNA barcodes. ACS Synth. Biol.7, 2468–2474 (2018). ArticlePubMedPubMed Central Google Scholar
Umkehrer, C. et al. Isolating live cell clones from barcoded populations using CRISPRa-inducible reporters. Nat. Biotechnol.39, 174–178 (2021). This article describes the development of a CaTCH high-diversity library, which is used to study the fate of melanoma clones in response to targeted therapy and retrieve the clones of interest. ArticleCASPubMed Google Scholar
Fehse, B., Kustikova, O. S., Bubenheim, M. & Baum, C. Pois(s)on–it’s a question of dose. Gene Ther.11, 879–881 (2004). ArticleCASPubMed Google Scholar
Ludwig, L. S. et al. Lineage tracing in humans enabled by mitochondrial mutations and single-cell genomics. Cell176, 1325–1339 e1322 (2019). ArticleCASPubMedPubMed Central Google Scholar