Tumour heterogeneity and metastasis at single-cell resolution
Open accessAbstract
Tumours comprise a heterogeneous collection of cells with distinct genetic and phenotypic properties that can differentially promote progression, metastasis and drug resistance. Emerging single-cell technologies provide a new opportunity to profile individual cells within tumours and investigate what roles they play in these processes. This Review discusses key technological considerations for single-cell studies in cancer, new findings using single-cell technologies and critical open questions for future applications.
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Single-cell methods applied to cancer cells have described heterogeneity in transcriptomics, epigenomics, metabolomics, and proteomics.
“Indeed, single-cell methods applied to cancer cells have described heterogeneity in terms of transcriptomics, epigenomics, metabolomics, and proteomics,5,6”
From Dynamic IL-6R/STAT3 signaling leads to heterogeneity of metabolic phenotype in pancreatic ductal adenocarcinoma cells (2024) · cites this paper as [6]
The review describes transcriptomic, epigenetic and proteomic differences between cancer cells (opening section, page unavailable), and its diagnostics section reports heterogeneity detected by single-cell RNA-seq and mass cytometry. It does not describe single-cell metabolomic heterogeneity in cancer cells; searches for “metabolomics” and “metabolite” found no supporting passage. (LLM, conf=0.86)
Experimental — accuracy not yet measuredEvidence points to a substantial level of metabolic heterogeneity even in aggressive cancers.
“evidence points to a substantial level of metabolic heterogeneity even in aggressive cancers”
From Dynamic IL-6R/STAT3 signaling leads to heterogeneity of metabolic phenotype in pancreatic ductal adenocarcinoma cells (2024) · cites this paper as [6]
The Abstract describes pervasive heterogeneity in human cancers, supporting the general point. The section ‘Non-genetic heterogeneity and cellular differentiation’ mentions differences in metabolic state among cells in normal tissues, but does not establish substantial metabolic heterogeneity in aggressive cancers. (LLM, conf=0.83)
Experimental — accuracy not yet measuredDesynchronized dynamics would ration resources evenly, while maintaining a relatively normal bulk metabolic rate, as shown in primary tumors.
“Desynchronized dynamics would ration resources evenly, while maintaining a relatively “normal” bulk metabolic rate, as shown in primary tumors.”
From Dynamic IL-6R/STAT3 signaling leads to heterogeneity of metabolic phenotype in pancreatic ductal adenocarcinoma cells (2024) · cites this paper as [6]
The Non-genetic heterogeneity and cellular differentiation section (page unavailable) mentions differences in cellular metabolic state, but does not discuss desynchronized dynamics, even resource allocation, or a normal bulk metabolic rate in primary tumours. Searches for those terms and related concepts found no passage addressing the attributed claim. (LLM, conf=0.76)
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Cites
Signatures of mutational processes in human cancer
Initiative, A. P. C. G., Alexandrov, L. B., ICGC Breast Cancer Consortium, ICGC MMML-Seq Consortium, PedBrain, I., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., Behjati, S., Biankin, A. V., et al. (2013) · Nature · doi:10.1038/nature12477 · Cited by 9,660 · see citing works
Microenvironmental regulation of tumor progression and metastasis
Quail, D. F., & Joyce, J. A. (2013) · Nature Medicine · doi:10.1038/nm.3394 · Cited by 7,994 · see citing works
Vogelstein, B., Papadopoulos, N., Velculescu, V. E., Zhou, S., Diaz, L. A., & Kinzler, K. W. (2013) · Science · doi:10.1126/science.1235122 · Cited by 7,863 · see citing works
Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing
Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1113205 · Cited by 7,774 · see citing works
Verhaak, R. G. W., Hoadley, K. A., Purdom, E., Wang, V., Qi, Y., Wilkerson, M. D., Miller, C. R., Ding, L., Golub, T., Mesirov, J. P., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.020 · Cited by 7,575 · see citing works
Massively parallel digital transcriptional profiling of single cells
Zheng, G. X. Y., Terry, J. M., Belgrader, P., Ryvkin, P., Bent, Z. W., Wilson, R., Ziraldo, S. B., Wheeler, T. D., McDermott, G. P., Zhu, J., et al. (2017) · Nature Communications · doi:10.1038/ncomms14049 · Cited by 7,353 · see citing works
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · see citing works
Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma
Patel, A. P., Tirosh, I., Trombetta, J. J., Shalek, A. K., Gillespie, S. M., Wakimoto, H., Cahill, D. P., Nahed, B. V., Curry, W. T., Martuza, R. L., et al. (2014) · Science · doi:10.1126/science.1254257 · Cited by 5,063 · see citing works
Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq
Tirosh, I., Izar, B., Prakadan, S. M., Wadsworth, M. H., Treacy, D., Trombetta, J. J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al. (2016) · Science · doi:10.1126/science.aad0501 · Cited by 4,944 · see citing works
Full-length RNA-seq from single cells using Smart-seq2
Picelli, S., Faridani, O. R., Björklund, Å. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.006 · Cited by 4,137 · see citing works
Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells
Klein, A. M., Mazutis, L., Akartuna, I., Tallapragada, N., Veres, A., Li, V., Peshkin, L., Weitz, D. A., & Kirschner, M. W. (2015) · Cell · doi:10.1016/j.cell.2015.04.044 · Cited by 3,356 · see citing works
Simultaneous epitope and transcriptome measurement in single cells
Stoeckius, M., Hafemeister, C., Stephenson, W., Houck-Loomis, B., Chattopadhyay, P. K., Swerdlow, H., Satija, R., & Smibert, P. (2017) · Nature Methods · doi:10.1038/nmeth.4380 · Cited by 3,098 · see citing works
Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade
McGranahan, N., Furness, A. J. S., Rosenthal, R., Ramskov, S., Lyngaa, R., Saini, S. K., Jamal-Hanjani, M., Wilson, G. A., Birkbak, N. J., Hiley, C. T., et al. (2016) · Science · doi:10.1126/science.aaf1490 · Cited by 3,065 · see citing works
Spatially resolved, highly multiplexed RNA profiling in single cells
Chen, K. H., Boettiger, A. N., Moffitt, J. R., Wang, S., & Zhuang, X. (2015) · Science · doi:10.1126/science.aaa6090 · Cited by 2,969 · see citing works
Batlle, E., & Clevers, H. (2017) · Nature Medicine · doi:10.1038/nm.4409 · Cited by 2,769 · see citing works
Metastasis: from dissemination to organ-specific colonization
Nguyen, D. X., Bos, P. D., & Massagué, J. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2622 · Cited by 2,637 · see citing works
Tumour evolution inferred by single-cell sequencing
Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., Cook, K., Stepansky, A., Levy, D., Esposito, D., et al. (2011) · Nature · doi:10.1038/nature09807 · Cited by 2,598 · see citing works
Puram, S. V., Tirosh, I., Parikh, A. S., Patel, A. P., Yizhak, K., Gillespie, S., Rodman, C., Luo, C. L., Mroz, E. A., Emerick, K. S., et al. (2017) · Cell · doi:10.1016/j.cell.2017.10.044 · Cited by 2,557 · see citing works
Distant metastasis occurs late during the genetic evolution of pancreatic cancer
Yachida, S., Jones, S., Bozic, I., Antal, T., Leary, R., Fu, B., Kamiyama, M., Hruban, R. H., Eshleman, J. R., Nowak, M. A., et al. (2010) · Nature · doi:10.1038/nature09515 · Cited by 2,502 · see citing works
Circulating Tumor Cell Clusters Are Oligoclonal Precursors of Breast Cancer Metastasis
Aceto, N., Bardia, A., Miyamoto, D. T., Collier, M. D., Wittner, B. S., Spencer, J. A., Yu, M., Pely, A., Engstrom, A., Zhu, H., et al. (2014) · Cell · doi:10.1016/j.cell.2014.07.013 · Cited by 2,438 · see citing works
Massive genomic rearrangement acquired in a single catastrophic event during cancer development
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) · Cell · doi:10.1016/j.cell.2010.11.055 · Cited by 2,414 · see citing works
Smart-seq2 for sensitive full-length transcriptome profiling in single cells
Picelli, S., Björklund, Å. K., Faridani, O. R., Sagasser, S., Winberg, G., & Sandberg, R. (2013) · Nature Methods · doi:10.1038/nmeth.2639 · Cited by 2,358 · see citing works
Single-cell chromatin accessibility reveals principles of regulatory variation
Buenrostro, J. D., Wu, B., Litzenburger, U. M., Ruff, D., Gonzales, M. L., Snyder, M. P., Chang, H. Y., & Greenleaf, W. J. (2015) · Nature · doi:10.1038/nature14590 · Cited by 2,308 · see citing works
Data-Driven Phenotypic Dissection of AML Reveals Progenitor-like Cells that Correlate with Prognosis
Levine, J. H., Simonds, E. F., Bendall, S. C., Davis, K. L., Amir, E.-A. D., Tadmor, M. D., Litvin, O., Fienberg, H. G., Jager, A., Zunder, E. R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.047 · Cited by 2,303 · see citing works
Bendall, S. C., Simonds, E. F., Qiu, P., Amir, E.-A. D., Krutzik, P. O., Finck, R., Bruggner, R. V., Melamed, R., Trejo, A., Ornatsky, O. I., et al. (2011) · Science · doi:10.1126/science.1198704 · Cited by 2,279 · see citing works
The immune contexture in cancer prognosis and treatment
Fridman, W. H., Zitvogel, L., Sautès–Fridman, C., & Kroemer, G. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.101 · Cited by 2,263 · see citing works
Evolution of the Cancer Stem Cell Model
Kreso, A., & Dick, J. E. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.02.006 · Cited by 2,212 · see citing works
Metastatic colonization by circulating tumour cells
Massagué, J., & Obenauf, A. C. (2016) · Nature · doi:10.1038/nature17038 · Cited by 2,062 · see citing works
Intra-tumour heterogeneity: a looking glass for cancer?
Marusyk, A., Almendro, V., & Polyák, K. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3261 · Cited by 2,003 · see citing works
Pan-cancer patterns of somatic copy number alteration
Zack, T. I., Schumacher, S. E., Carter, S. L., Cherniack, A. D., Saksena, G., Tabak, B., Lawrence, M. S., Zhang, C., Wala, J. A., Mermel, C. H., et al. (2013) · Nature Genetics · doi:10.1038/ng.2760 · Cited by 1,843 · see citing works
Efficient tumour formation by single human melanoma cells
Quintana, E., Shackleton, M. J., Sabel, M. S., Fullen, D. R., Johnson, T. M., & Morrison, S. J. (2008) · Nature · doi:10.1038/nature07567 · Cited by 1,796 · see citing works
Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types
Jaitin, D. A., Kenigsberg, E., Keren-Shaul, H., Elefant, N., Paul, F., Zaretsky, I., Mildner, A., Cohen, N., Jung, S., Tanay, A., et al. (2014) · Science · doi:10.1126/science.1247651 · Cited by 1,795 · see citing works
Deep profiling of mouse splenic architecture with CODEX multiplexed imaging
Goltsev, Y., Samusik, N., Kennedy-Darling, J., Bhate, S., Hale, M., Vazquez, G., Black, S., & Nolan, G. P. (2018) · Cell · doi:10.1016/j.cell.2018.07.010 · Cited by 1,501 · see citing works
Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding
Rosenberg, A. B., Roco, C. M., Muscat, R. A., Kuchina, A., Sample, P., Yao, Z., Graybuck, L. T., Peeler, D. J., Mukherjee, S., Chen, W., et al. (2018) · Science · doi:10.1126/science.aam8999 · Cited by 1,422 · see citing works
Cao, J., Packer, J. S., Ramani, V., Cusanovich, D. A., Huynh, C., Daza, R., Qiu, X., Lee, C., Furlan, S. N., Steemers, F. J., et al. (2017) · doi:10.1101/104844 · Cited by 1,402 · see citing works
Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma
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) · Science · doi:10.1126/science.1239947 · Cited by 1,362 · see citing works
Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq
Treutlein, B., Brownfield, D. G., Wu, A. R., Neff, N. F., Mantalas, G. L., Espinoza, F. H., Desai, T. J., Krasnow, M. A., & Quake, S. R. (2014) · Nature · doi:10.1038/nature13173 · Cited by 1,342 · see citing works
Interactions between cancer stem cells and their niche govern metastatic colonization
Malanchi, I., Santamaria-Martínez, A., Susanto, E., Peng, H., Lehr, H.-A., Delaloye, J.-F., & Huelsken, J. (2012) · Nature · doi:10.1038/nature10694 · Cited by 1,339 · see citing works
Single-cell genome sequencing: current state of the science
Gawad, C., Koh, W., & Quake, S. R. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2015.16 · Cited by 1,334 · see citing works
Bandura, D. R., Baranov, V. I., Ornatsky, O. I., Antonov, A., Kinach, R., Lou, X., Pavlov, S., Vorobiev, S., Dick, J. E., & Tanner, S. D. (2009) · Analytical Chemistry · doi:10.1021/ac901049w · Cited by 1,295 · see citing works
Multiplex single-cell profiling of chromatin accessibility by combinatorial cellular indexing
Cusanovich, D. A., Daza, R., Adey, A., Pliner, H. A., Christiansen, L., Gunderson, K. L., Steemers, F. J., Trapnell, C., & Shendure, J. (2015) · Science · doi:10.1126/science.aab1601 · Cited by 1,248 · see citing works
Single-cell RNA-seq supports a developmental hierarchy in human oligodendroglioma
Tirosh, I., Venteicher, A. S., Hebert, C. M., Escalante, L. E., Patel, A. P., Yizhak, K., Fisher, J. M., Rodman, C., Mount, C., Filbin, M. G., et al. (2016) · Nature · doi:10.1038/nature20123 · Cited by 1,216 · see citing works
Gerlinger, M., Horswell, S. D., Larkin, J., Rowan, A., Salm, M., Varela, I., Fisher, R. A., McGranahan, N., Matthews, N., Santos, C. R., et al. (2014) · Nature Genetics · doi:10.1038/ng.2891 · Cited by 1,211 · see citing works
Systemic Spread Is an Early Step in Breast Cancer
Hüsemann, Y., Geigl, J. B., Schubert, F., Musiani, P., Meyer, M., Burghart, E., Forni, G., Eils, R., Fehm, T. N., Riethmüller, G., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2007.12.003 · Cited by 1,175 · see citing works
An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers
Roberts, S. A., Lawrence, M. S., Klimczak, L. J., Grimm, S. A., Fargo, D. C., Stojanov, P., Kieżun, A., Kryukov, G. V., Carter, S. L., Saksena, G., et al. (2013) · Nature Genetics · doi:10.1038/ng.2702 · Cited by 1,145 · see citing works
Genome remodelling in a basal-like breast cancer metastasis and xenograft
Ding, L., Ellis, M. J., Li, S., Larson, D. E., Chen, K., Wallis, J. W., Harris, C. C., McLellan, M. D., Fulton, R. S., Fulton, L., et al. (2010) · Nature · doi:10.1038/nature08989 · Cited by 1,134 · see citing works
Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity
Smallwood, S. A., Lee, H. J., Angermueller, C., Krueger, F., Saadeh, H., Peat, J., Andrews, S. R., Stegle, O., Reik, W., & Kelsey, G. (2014) · Nature Methods · doi:10.1038/nmeth.3035 · Cited by 1,125 · see citing works
Chemoresistance Evolution in Triple-Negative Breast Cancer Delineated by Single-Cell Sequencing
Kim, C. R., Gao, R., Sei, E., Brandt, R., Hartman, J., Hatschek, T., Crosetto, N., Foukakis, T., & Navin, N. E. (2018) · Cell · doi:10.1016/j.cell.2018.03.041 · Cited by 1,092 · see citing works
Biological and therapeutic impact of intratumor heterogeneity in cancer evolution
McGranahan, N., & Swanton, C. (2015) · Cancer Cell · doi:10.1016/j.ccell.2014.12.001 · Cited by 1,077 · see citing works
Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations
van den Brink, S. C., Sage, F., Vértesy, Á., Spanjaard, B., Peterson-Maduro, J., Baron, C. S., Robin, C., & van Oudenaarden, A. (2017) · Nature Methods · doi:10.1038/nmeth.4437 · Cited by 1,072 · see citing works
Massively parallel single-nucleus RNA-seq with DroNc-seq
Habib, N., Avraham-Davidi, I., Basu, A., Burks, T., Shekhar, K., Hofree, M., Choudhury, S. R., Aguet, F., Gelfand, E., Ardlie, K., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4407 · Cited by 1,069 · see citing works
Clonal evolution in breast cancer revealed by single nucleus genome sequencing
Wang, Y., Waters, J., Leung, M. L., Unruh, A., Roh, W., Shi, X., Chen, K., Scheet, P., Vattathil, S., Liang, H., et al. (2014) · Nature · doi:10.1038/nature13600 · Cited by 1,029 · see citing works
Darmanis, S., Sloan, S. A., Croote, D., Mignardi, M., Chernikova, S. B., Samghababi, P., Zhang, Y., Neff, N. F., Kowarsky, M., Caneda, C., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.030 · Cited by 1,004 · see citing works
Single-cell RNA-seq enables comprehensive tumour and immune cell profiling in primary breast cancer
Chung, W., Eum, H. H., Lee, H.-O., Lee, K.-M., Lee, H.-B., Kim, K.-T., Ryu, H. S., Kim, S., Lee, J. E., Park, Y. H., et al. (2017) · Nature Communications · doi:10.1038/ncomms15081 · Cited by 992 · see citing works
Decoupling genetics, lineages, and microenvironment in IDH-mutant gliomas by single-cell RNA-seq
Venteicher, A. S., Tirosh, I., Hebert, C. M., Yizhak, K., Neftel, C., Filbin, M. G., Hovestadt, V., Escalante, L. E., Shaw, M. L., Rodman, C., et al. (2017) · Science · doi:10.1126/science.aai8478 · Cited by 975 · see citing works
Highly Multiplexed Subcellular RNA Sequencing in Situ
Lee, J. H., Daugharthy, E. R., Scheiman, J., Kalhor, R., Yang, J. L., Ferrante, T. C., Terry, R., Jeanty, S. S. F., Li, C., Amamoto, R., et al. (2014) · Science · doi:10.1126/science.1250212 · Cited by 973 · see citing works
Systemic Immunity Is Required for Effective Cancer Immunotherapy
Spitzer, M. H., Carmi, Y., Reticker-Flynn, N. E., Kwek, S. S., Madhireddy, D., Martins, M. M., Gherardini, P. F., Prestwood, T. R., Chabon, J., Bendall, S. C., et al. (2017) · Cell · doi:10.1016/j.cell.2016.12.022 · Cited by 963 · see citing works
Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain
Lake, B. B., Ai, R., Kaeser, G. E., Salathia, N. S., Yung, Y. C., Liu, R., Wildberg, A., Gao, D., Fung, H.-L., Chen, S., et al. (2016) · Science · doi:10.1126/science.aaf1204 · Cited by 957 · see citing works
Pollen, A. A., Nowakowski, T. J., Shuga, J., Wang, X., Leyrat, A. A., Lui, J. H., Li, N., Szpankowski, L., Fowler, B., Chen, P., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2967 · Cited by 920 · see citing works
Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells
Lawson, D. A., Bhakta, N. R., Kessenbrock, K., Prummel, K. D., Yu, Y., Takai, K., Zhou, A. Y., Eyob, H., Balakrishnan, S., Wang, C., et al. (2015) · Nature · doi:10.1038/nature15260 · Cited by 894 · see citing works
Self-citationSeq-Well: portable, low-cost RNA sequencing of single cells at high throughput
Gierahn, T. M., Wadsworth, M. H., Hughes, T. K., Bryson, B. D., Butler, A., Satija, R., Fortune, S. M., Love, J. C., & Shalek, A. K. (2017) · Nature Methods · doi:10.1038/nmeth.4179 · Cited by 855 · see citing works
Single-cell ChIP-seq reveals cell subpopulations defined by chromatin state
Rotem, A., Ram, O., Shoresh, N., Sperling, R. A., Goren, A., Weitz, D. A., & Bernstein, B. E. (2015) · Nature Biotechnology · doi:10.1038/nbt.3383 · Cited by 854 · see citing works
Collective Invasion in Breast Cancer Requires a Conserved Basal Epithelial Program
Cheung, K. J., Gabrielson, E. W., Werb, Z., & Ewald, A. J. (2013) · Cell · doi:10.1016/j.cell.2013.11.029 · Cited by 838 · see citing works
Self-citationMultiplexed quantification of proteins and transcripts in single cells
Peterson, V. M., Zhang, K. X., Kumar, N., Wong, J., Li, L., Wilson, D. C., Moore, R., McClanahan, T. K., Sadekova, S., & Klappenbach, J. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3973 · Cited by 832 · see citing works
Abkevich, V., Timms, K. M., Hennessy, B. T., Potter, J., Carey, M. S., Meyer, L. A., Smith‐McCune, K., Broaddus, R. R., Lu, K. H., Chen, J., et al. (2012) · British Journal of Cancer · doi:10.1038/bjc.2012.451 · Cited by 818 · see citing works
Defining cell types and states with single-cell genomics
Trapnell, C. (2015) · Genome Research · doi:10.1101/gr.190595.115 · Cited by 813 · see citing works
Subclonal diversification of primary breast cancer revealed by multiregion sequencing
Yates, L. R., Gerstung, M., Knappskog, S., Desmedt, C., Gundem, G., Loo, P. V., Aas, T., Alexandrov, L. B., Larsimont, D., Davies, H., et al. (2015) · Nature Medicine · doi:10.1038/nm.3886 · Cited by 812 · see citing works
Metastatic Latency and Immune Evasion through Autocrine Inhibition of WNT
Malladi, S., Macalinao, D. G., Jin, X., He, L., Basnet, H., Zou, Y., de Stanchina, E., & Massagué, J. (2016) · Cell · doi:10.1016/j.cell.2016.02.025 · Cited by 791 · see citing works
Evidence for APOBEC3B mutagenesis in multiple human cancers
Burns, M. B., Temiz, N. A., & Harris, R. S. (2013) · Nature Genetics · doi:10.1038/ng.2701 · Cited by 763 · see citing works
G&T-seq: parallel sequencing of single-cell genomes and transcriptomes
Macaulay, I. C., Haerty, W., Kumar, P., Li, Y. I., Hu, T. X., Teng, M. J., Goolam, M., Saurat, N., Coupland, P., Shirley, L. M., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3370 · Cited by 750 · see citing works
Early dissemination seeds metastasis in breast cancer
Hosseini, H., Obradović, M. M. S., Hoffmann, M., Harper, K. L., Sosa, M. S., Werner‐Klein, M., Nanduri, L. K., Werno, C., Ehrl, C., Maneck, M., et al. (2016) · Nature · doi:10.1038/nature20785 · Cited by 740 · see citing works
Parallel single-cell sequencing links transcriptional and epigenetic heterogeneity
Angermueller, C., Clark, S. J., Lee, H. J., Macaulay, I. C., Teng, M. J., Hu, T. X., Krueger, F., Smallwood, S. A., Ponting, C. P., Voet, T., et al. (2016) · Nature Methods · doi:10.1038/nmeth.3728 · Cited by 717 · see citing works
RNA-Seq of single prostate CTCs implicates noncanonical Wnt signaling in antiandrogen resistance
Miyamoto, D. T., Zheng, Y., Wittner, B. S., Lee, R. J., Zhu, H., Broderick, K. T., Desai, R. N., Fox, D. B., Brannigan, B. W., Trautwein, J., et al. (2015) · Science · doi:10.1126/science.aab0917 · Cited by 706 · see citing works
Single-cell dissection of transcriptional heterogeneity in human colon tumors
Dalerba, P. D., Tomer Kalisky, C., Sahoo, D., Rajendran, P. S., Rothenberg, M. E., Leyrat, A. A., Sim, S., Okamoto, J., Johnston, D. M., Qian, D., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.2038 · Cited by 693 · see citing works
Flow cytometric immunophenotyping for hematologic neoplasms
Craig, F. E., & Foon, K. A. (2008) · Blood · doi:10.1182/blood-2007-11-120535 · Cited by 676 · see citing works
Popova, T. G., Manié, É., Rieunier, G., Caux‐Moncoutier, V., Tirapo, C., Dubois, T., Delattre, O., Sigal‐Zafrani, B., Bollet, M. A., Longy, M., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1470 · Cited by 666 · see citing works
Clark, S. J., Argelaguet, R., Kapourani, C.-A., Stubbs, T. M., Lee, H. J., Alda-Catalinas, C., Krueger, F., Sanguinetti, G., Kelsey, G., Marioni, J. C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03149-4 · Cited by 657 · see citing works
Müller, S., Kohanbash, G., Liu, S. J., Alvarado, B., Carrera, D. A., Bhaduri, A., Watchmaker, P. B., Yagnik, G., Lullo, E. D., Malatesta, M., et al. (2017) · Genome biology · doi:10.1186/s13059-017-1362-4 · Cited by 655 · see citing works
Hou, Y., Guo, H., Cao, C., Li, X., Hu, B., Zhu, P., Wu, X., Wen, L., Tang, F., Huang, Y., et al. (2016) · Cell Research · doi:10.1038/cr.2016.23 · Cited by 647 · see citing works
Revealing the vectors of cellular identity with single-cell genomics
Wagner, A., Regev, A., & Yosef, N. (2016) · Nature Biotechnology · doi:10.1038/nbt.3711 · Cited by 632 · see citing works
Schmidt‐Kittler, O., Ragg, T., Daskalakis, A., Granzow, M., Ahr, A., Blankenstein, T. J. F., Kaufmann, M., Diebold, J., Arnholdt, H., Müller, P. E., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1331931100 · Cited by 631 · see citing works
Div-Seq: Single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons
Habib, N., Li, Y., Heidenreich, M., Swiech, L., Avraham-Davidi, I., Trombetta, J. J., Hession, C., Zhang, F., & Regev, A. (2016) · Science · doi:10.1126/science.aad7038 · Cited by 601 · see citing works
The significance of hematogenous tumor cell clumps in the metastatic process.
Liotta, L. A., Saidel, M. G., & Kleinerman, J. I. (1976) · PubMed · Cited by 572 · see citing works
Somatic mutation in single human neurons tracks developmental and transcriptional history
Lodato, M. A., Woodworth, M. B., Lee, S., Evrony, G. D., Mehta, B. K., Karger, A., Lee, S., Chittenden, T. W., D’Gama, A. M., Cai, X., et al. (2015) · Science · doi:10.1126/science.aab1785 · Cited by 570 · see citing works
Mechanism of early dissemination and metastasis in Her2+ mammary cancer
Harper, K. L., Sosa, M. S., Entenberg, D. R., Hosseini, H., Cheung, J. F., Nobre, A. R., Avivar‐Valderas, A., Nagi, C., Girnius, N., Davis, R. J., et al. (2016) · Nature · doi:10.1038/nature20609 · Cited by 569 · see citing works
Self-citationPower analysis of single-cell RNA-sequencing experiments
Svensson, V., Natarajan, K. N., Ly, L.-H., Miragaia, R. J., Labalette, C., Macaulay, I. C., Cvejic, A., & Teichmann, S. A. (2017) · Nature Methods · doi:10.1038/nmeth.4220 · Cited by 568 · see citing works
Massively multiplex single-cell Hi-C
Ramani, V., Deng, X.-X., Qiu, R., Gunderson, K., Steemers, F. J., Disteche, C., Noble, W. S., Duan, Z., & Shendure, J. (2016) · Nature Methods · doi:10.1038/nmeth.4155 · Cited by 545 · see citing works
Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer
Lohr, J. G., Adalsteinsson, V. A., Cibulskis, K., Choudhury, A. D., Rosenberg, M. W., Cruz‐Gordillo, P., Francis, J. M., Zhang, C.-Z., Shalek, A. K., Satija, R., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2892 · Cited by 534 · see citing works
Lee, J. H., Daugharthy, E. R., Scheiman, J., Kalhor, R., Ferrante, T. C., Terry, R., Turczyk, B. M., Yang, J. L., Lee, H. S., Aach, J., et al. (2015) · Nature Protocols · doi:10.1038/nprot.2014.191 · Cited by 529 · see citing works
Integrated genome and transcriptome sequencing of the same cell
Dey, S. S., Kester, L., Spanjaard, B., Bienko, M., & van Oudenaarden, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3129 · Cited by 502 · see citing works
Heitzer, E., Auer, M., Gasch, C., Pichler, M., Ulz, P., Hoffmann, E. M., Lax, S., Waldispuehl‐Geigl, J., Mauermann, O., Lackner, C., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4140 · Cited by 497 · see citing works
The heterogeneity of human CD127+ innate lymphoid cells revealed by single-cell RNA sequencing
Björklund, Å. K., Forkel, M., Picelli, S., Kónya, V., Theorell, J., Friberg, D., Sandberg, R., & Mjösberg, J. (2016) · Nature Immunology · doi:10.1038/ni.3368 · Cited by 491 · see citing works
Ni, X., Zhuo, M., Su, Z., Duan, J., Gao, Y., Wang, Z., Zong, C., Bai, H., Chapman, A. R., Zhao, J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320659110 · Cited by 454 · see citing works
Comparative genomic hybridization, loss of heterozygosity, and DNA sequence analysis of single cells
Klein, C. A., Schmidt‐Kittler, O., Schardt, J., Pantel, K., Speicher, M. R., & Riethmüller, G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4494 · Cited by 450 · see citing works
RNA-sequencing from single nuclei
Grindberg, R. V., Yee-Greenbaum, J. L., McConnell, M. J., Novotny, M., O’Shaughnessy, A. L., Lambert, G. M., Araúzo-Bravo, M. J., Lee, J., Fishman, M., Robbins, G. E., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319700110 · Cited by 422 · see citing works
Single-Cell Whole-Genome Amplification and Sequencing: Methodology and Applications
Huang, L., Ma, F., Chapman, A. R., Lü, S., & Xie, X. S. (2015) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-090413-025352 · Cited by 419 · see citing works
Macrophages orchestrate breast cancer early dissemination and metastasis
Linde, N., Casanova-Acebes, M., Sosa, M. S., Mortha, A., Rahman, A. H., Farias, E., Harper, K. L., Tardio, E., Reyes-Torres, I., Jones, J. G., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02481-5 · Cited by 416 · see citing works
Multiclonal Invasion in Breast Tumors Identified by Topographic Single Cell Sequencing
Casasent, A. K., Schalck, A., Gao, R., Sei, E., Long, A., Pangburn, W., Casasent, T., Meric-Bernstam, F., Edgerton, M. E., & Navin, N. E. (2018) · Cell · doi:10.1016/j.cell.2017.12.007 · Cited by 411 · see citing works
Single-cell whole-genome analyses by Linear Amplification via Transposon Insertion (LIANTI)
Chen, C., Xing, D., Tan, L., Li, H., Zhou, G., Huang, L., & Xie, X. S. (2017) · Science · doi:10.1126/science.aak9787 · Cited by 386 · see citing works
Heppner, G. H. (1984) · PubMed · Cited by 374 · see citing works
Highly multiparametric analysis by mass cytometry
Ornatsky, O., Bandura, D. R., Baranov, V. I., Nitz, M., Winnik, M. A., & Tanner, S. D. (2010) · Journal of Immunological Methods · doi:10.1016/j.jim.2010.07.002 · Cited by 368 · see citing works
Tumor evolution: Linear, branching, neutral or punctuated?
Davis, A., Gao, R., & Navin, N. E. (2017) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2017.01.003 · Cited by 355 · see citing works
Genome-wide detection of DNase I hypersensitive sites in single cells and FFPE tissue samples
Jin, W., Tang, Q., Wan, M., Cui, K., Zhang, Y., Ren, G., Ni, B., Sklar, J., Przytycka, T. M., Childs, R., et al. (2015) · Nature · doi:10.1038/nature15740 · Cited by 332 · see citing works
Intratumoral Hypoxic Gradient Drives Stem Cells Distribution and MGMT Expression in Glioblastoma
Pistollato, F., Abbadi, S., Rampazzo, E., Persano, L., Puppa, A. D., Frasson, C., Sarto, E., Scienza, R., D’Avella, D., & Basso, G. (2010) · Stem Cells · doi:10.1002/stem.415 · Cited by 321 · see citing works
The evolution of tumour phylogenetics: principles and practice
Schwartz, R. S., & Schäffer, A. A. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2016.170 · Cited by 317 · see citing works
Carter, L., Rothwell, D. G., Mesquita, B., Smowton, C., Leong, H. S., Fernández‐Gutiérrez, F., Li, Y., Burt, D. J., Antonello, J., Morrow, C. J., et al. (2016) · Nature Medicine · doi:10.1038/nm.4239 · Cited by 308 · see citing works
Probing Meiotic Recombination and Aneuploidy of Single Sperm Cells by Whole-Genome Sequencing
Lü, S., Zong, C. C., Fan, W., Yang, M., Li, J., Chapman, A. R., Zhu, P., Hu, X., Xu, L., Yan, L., et al. (2012) · Science · doi:10.1126/science.1229112 · Cited by 294 · see citing works
Hayashi, T., Ozaki, H., Sasagawa, Y., Umeda, M., Danno, H., & Nikaido, I. (2018) · Nature Communications · doi:10.1038/s41467-018-02866-0 · Cited by 281 · see citing works
Dissecting the clonal origins of childhood acute lymphoblastic leukemia by single-cell genomics
Gawad, C., Koh, W. L. C., & Quake, S. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420822111 · Cited by 276 · see citing works
Transcriptomes of major renal collecting duct cell types in mouse identified by single-cell RNA-seq
Chen, L., Lee, J. W., Chou, C.-L., Nair, A. V., Battistone, M. A., Păunescu, T. G., Merkulova, M., Breton, S., Verlander, J. W., Wall, S. M., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710964114 · Cited by 267 · see citing works
Computational genomics tools for dissecting tumour–immune cell interactions
Hackl, H., Charoentong, P., Finotello, F., & Trajanoski, Z. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.67 · Cited by 266 · see citing works
Schardt, J., Meyer, M., Hartmann, C. H., Schubert, F., Schmidt‐Kittler, O., Fuhrmann, C., Polzer, B. M., Petronio, M., Eils, R., & Klein, C. A. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.08.003 · Cited by 255 · see citing works
Molecular profiling of single circulating tumor cells with diagnostic intention
Polzer, B. M., Medoro, G., Pasch, S., Fontana, F., Zorzino, L., Pestka, A., Andergassen, U., Meier-Stiegen, F., Czyż, Z. T., Alberter, B., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201404033 · Cited by 254 · see citing works
Single-cell DNA sequencing reveals a late-dissemination model in metastatic colorectal cancerPreprint
Leung, M. L., Davis, A., Gao, R., Casasent, T. D., Wang, Y., Sei, E., Vilar, E., Maru, D. M., Kopetz, S., & Navin, N. E. (2017) · Genome Research · doi:10.1101/gr.209973.116 · Cited by 222 · see citing works
Mroz, E. A., Tward, A. D., Pickering, C. R., Myers, J. N., Ferris, R. L., & Rocco, J. W. (2013) · Cancer · doi:10.1002/cncr.28150 · Cited by 220 · see citing works
Single-cell sequencing of the small-RNA transcriptome
Faridani, O. R., Abdullayev, I., Hagemann-Jensen, M., Schell, J. P., Lanner, F., & Sandberg, R. (2016) · Nature Biotechnology · doi:10.1038/nbt.3701 · Cited by 219 · see citing works
Meier, B., Cooke, S. L., Weiss, J., Bailly, A., Alexandrov, L. B., Marshall, J., Raine, K. M., Maddison, M., Anderson, E. L., Stratton, M. R., et al. (2014) · Genome Research · doi:10.1101/gr.175547.114 · Cited by 182 · see citing works
IFNγ-Dependent Tissue-Immune Homeostasis Is Co-opted in the Tumor Microenvironment
Nirschl, C. J., Suárez‐Fariñas, M., Izar, B., Prakadan, S. M., Dannenfelser, R., Tirosh, I., Liu, Y., Zhu, Q., Devi, K. S. P., Carroll, S. L., et al. (2017) · Cell · doi:10.1016/j.cell.2017.06.016 · Cited by 182 · see citing works
Separation and parallel sequencing of the genomes and transcriptomes of single cells using G&T-seq
Macaulay, I. C., Teng, M. J., Haerty, W., Kumar, P., Ponting, C. P., & Voet, T. (2016) · Nature Protocols · doi:10.1038/nprot.2016.138 · Cited by 171 · see citing works
Experimental Considerations for Single-Cell RNA Sequencing Approaches
Nguyen, Q. H., Pervolarakis, N., Nee, K., & Kessenbrock, K. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00108 · Cited by 170 · see citing works
Self-citationPestrin, M., Salvianti, F., Galardi, F., Luca, F. D., Turner, N. H., Malorni, L., Pazzagli, M., Leo, A. D., & Pinzani, P. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.12.001 · Cited by 167 · see citing works
Mooijman, D., Dey, S. S., Boisset, J.-C., Crosetto, N., & van Oudenaarden, A. (2016) · Nature Biotechnology · doi:10.1038/nbt.3598 · Cited by 165 · see citing works
Lih, C., Harrington, R. D., Sims, D. J., Harper, K. N., Bouk, C. H., Datta, V., Yau, J., Singh, R. R., Routbort, M. J., Luthra, R., et al. (2017) · Journal of Molecular Diagnostics · doi:10.1016/j.jmoldx.2016.10.007 · Cited by 159 · see citing works
Zhu, C., Gao, Y., Guo, H., Xia, B., Song, J., Wu, X., Zeng, H., Kee, K., Tang, F., & Yi, C. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.02.013 · Cited by 159 · see citing works
Pistollato, F., Rampazzo, E., Persano, L., Abbadi, S., Frasson, C., Denaro, L., D’Avella, D., Panchision, D. M., Puppa, A. D., Scienza, R., et al. (2010) · Stem Cells · doi:10.1002/stem.518 · Cited by 148 · see citing works
Deep profiling of mouse splenic architecture with CODEX multiplexed imagingPreprint
Goltsev, Y., Samusik, N., Kennedy‐Darling, J., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/203166 · Cited by 148 · see citing works
Shah, S., Lubeck, E., Zhou, W., & Cai, L. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.008 · Cited by 146 · see citing works
Hypoxia Contributes to Melanoma Heterogeneity by Triggering HIF1α-Dependent Phenotype Switching
Widmer, D. S., Hoek, K. S., Cheng, P. F., Eichhoff, O. M., Biedermann, T., Raaijmakers, M. I. G., Hemmi, S., Dummer, R., & Levesque, M. P. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2013.115 · Cited by 139 · see citing works
Redmond, D., Poran, A., & Elemento, O. (2016) · Genome Medicine · doi:10.1186/s13073-016-0335-7 · Cited by 139 · see citing works
Quantitative analysis of gene expression in a single cell by qPCR
Taniguchi, K., Kajiyama, T., & Kambara, H. (2009) · Nature Methods · doi:10.1038/nmeth.1338 · Cited by 136 · see citing works
PIK3CA Mutations in In situ and Invasive Breast Carcinomas
Miron, A., Varadi, M., Carrasco, D. R., Li, H., Luongo, L., Kim, H. J., Park, S. Y., Cho, E. Y., Lewis, G., Kehoe, S. M., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-08-2660 · Cited by 133 · see citing works
An Automated Microwell Platform for Large-Scale Single Cell RNA-Seq
Yuan, J., & Sims, P. A. (2016) · Scientific Reports · doi:10.1038/srep33883 · Cited by 128 · see citing works
Single-Cell Transcriptomics Bioinformatics and Computational Challenges
Poirion, O., Zhu, X., Ching, T. H., & Garmire, L. X. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00163 · Cited by 125 · see citing works
Discovery of biclonal origin and a novel oncogene SLC12A5 in colon cancer by single-cell sequencing
Yu, C., Yu, J. Q., Yao, X., Wu, W. K. K., Lu, Y., Tang, S., Li, X., Bao, L., Li, X., Hou, Y., et al. (2014) · Cell Research · doi:10.1038/cr.2014.43 · Cited by 121 · see citing works
Single cell analysis of cancer genomes
Loo, P. V., & Voet, T. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.12.004 · Cited by 116 · see citing works
Nanogrid single-nucleus RNA sequencing reveals phenotypic diversity in breast cancer
Gao, R., Kim, C. R., Sei, E., Foukakis, T., Crosetto, N., Chan, L., Srinivasan, M., Zhang, H., Meric‐Bernstam, F., & Navin, N. E. (2017) · Nature Communications · doi:10.1038/s41467-017-00244-w · Cited by 116 · see citing works
Tumor Heterogeneity—A ‘Contemporary Concept’ Founded on Historical Insights and Predictions
Welch, D. R. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-3024 · Cited by 113 · see citing works
Riethmüller, G., & Klein, C. A. (2001) · Seminars in Cancer Biology · doi:10.1006/scbi.2001.0386 · Cited by 112 · see citing works
SNES: single nucleus exome sequencing
Leung, M. L., Wang, Y., Waters, J., & Navin, N. E. (2015) · Genome Biology · doi:10.1186/s13059-015-0616-2 · Cited by 112 · see citing works
Behbehani, G. K., Samusik, N., Bjornson, Z. B., Fantl, W. J., Medeiros, B. C., & Nolan, G. P. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0298 · Cited by 106 · see citing works
Technical Variations in Low-Input RNA-seq Methodologies
Bhargava, V., Head, S. R., Ordoukhanian, P. T., Mercola, M. A., & Subramaniam, S. (2014) · Scientific Reports · doi:10.1038/srep03678 · Cited by 85 · see citing works
Hypoxia drives transient site-specific copy gain and drug-resistant gene expressionPreprint
Black, J. C., Atabakhsh, E., Kim, J., Biette, K. M., Rechem, C. V., Ladd, B., Burrowes, P. D., Donado, C. A., Mattoo, H., Kleinstiver, B. P., et al. (2015) · Genes & Development · doi:10.1101/gad.259796.115 · Cited by 83 · see citing works
Comparison of whole genome amplification techniques for human single cell exome sequencing
Borgström, E., Paterlini, M., Mold, J. E., Frisen, J., & Lundeberg, J. (2017) · PLOS ONE · doi:10.1371/journal.pone.0171566 · Cited by 77 · see citing works
Dense transcript profiling in single cells by image correlation decoding
Coskun, A. F., & Cai, L. (2016) · Nature Methods · doi:10.1038/nmeth.3895 · Cited by 74 · see citing works
A Targetable EGFR-Dependent Tumor-Initiating Program in Breast Cancer
Savage, P., Blanchet-Cohen, A., Revil, T., Badescu, D., Saleh, S. M. I., Wang, Y.-C., Zuo, D., Liu, L., Bertos, N., Muñoz-Ramos, V., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.015 · Cited by 73 · see citing works
Mitra, A., Mukherjee, U. K., Harding, T., Jang, J. S., Stessman, H. A. F., Li, Y., Abyzov, A. S., Jen, J., Kumar, S. K., Rajkumar, S. V., et al. (2015) · Leukemia · doi:10.1038/leu.2015.361 · Cited by 71 · see citing works
Characterizing heterogeneity in leukemic cells using single-cell gene expression analysis
Saadatpour, A., Guo, G., Orkin, S. H., & Yuan, G. (2014) · Genome biology · doi:10.1186/s13059-014-0525-9 · Cited by 59 · see citing works
Salehi, S., Steif, A., Roth, A. J. L., Aparicio, S. A. J. R., Bouchard‐Côté, A., & Shah, S. P. (2017) · Genome biology · doi:10.1186/s13059-017-1169-3 · Cited by 59 · see citing works
A brief review of single-cell transcriptomic technologies
Tomer Kalisky, C., Oriel, S., Bar-Lev, T. H., Ben-Haim, N., Trink, A., Wineberg, Y., Kanter, I., Gilad, S., & Pyne, S. (2017) · Briefings in Functional Genomics · doi:10.1093/bfgp/elx019 · Cited by 54 · see citing works
Han, L. G., Wu, H., Zhu, H., Kim, K., Marjani, S. L., Riester, M., Euskirchen, G. M., Zi, X., Yang, J., Han, J., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx026 · Cited by 53 · see citing works
Highly multiplexed targeted DNA sequencing from single nuclei
Leung, M. L., Wang, Y., Kim, C. R., Gao, R., Jiang, J., Sei, E., & Navin, N. E. (2016) · Nature Protocols · doi:10.1038/nprot.2016.005 · Cited by 51 · see citing works
Ferrell, P. B., Diggins, K. E., Polikowsky, H. G., Mohan, S. R., Seegmiller, A. C., & Irish, J. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0153207 · Cited by 45 · see citing works
Succession of transiently active tumor‐initiating cell clones in human pancreatic cancer xenografts
Ball, C., Oppel, F., Ehrenberg, K. R., Dubash, T. D., Dieter, S., Hoffmann, C. M., Abel, U., Herbst, F., Koch, M., Werner, J., et al. (2017) · EMBO Molecular Medicine · doi:10.15252/emmm.201607354 · Cited by 41 · see citing works
Quantitative Transcriptomics using Designed Primer-based Amplification
Bhargava, V., Ko, P., Willems, E., Mercola, M. A., & Subramaniam, S. (2013) · Scientific Reports · doi:10.1038/srep01740 · Cited by 40 · see citing works
Chromosome-scale mega-haplotypes enable digital karyotyping of cancer aneuploidy
Bell, J., Lau, B. T., Greer, S., Wood-Bouwens, C. M., Xia, L. C., Connolly, I. D., Gephart, M. H., & Ji, H. P. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx712 · Cited by 31 · see citing works
Ahn, R. S., Taravati, K., Lai, K., Lee, K. M., Nititham, J., Gupta, R., Chang, D. S., Arron, S. T., Rosenblum, M. D., & Liao, W. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-01468-y · Cited by 18 · see citing works
Genotyping tumor clones from single-cell data
Navin, N. E., & Chen, K. (2016) · Nature Methods · doi:10.1038/nmeth.3903 · Cited by 14 · see citing works
High-throughput single-cell DNA sequencing of AML tumors with droplet microfluidicsPreprint
Pellegrino, M., Sciambi, A., Treusch, S., Durruthy-Durruthy, R., Gokhale, K., Jacob, J. P., Chen, T. X., Oldham, W. M., Matthews, J. A., Kantarjian, H. M., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/203158 · Cited by 3 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- [53]Miron A PIK3CA mutations in in situ and invasive breastcarcinomas. Cancer Res. 70, 5674– 5678 (2010). 20551053 PMC2905503
- [111]Tirosh I Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189– 196 (2016). 27124452 PMC4944528
- [115]Klein AM Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells. Cell 161, 1187– 1201 (2015). 26000487 PMC4441768
- [122]Cao J Comprehensive single-cell transcriptional profiling of a multicellular organism. Science 357, 661– 667 (2017). 28818938 PMC5894354
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Martínez-Jiménez, F., Muiños, F., Sentís, I., Deu-Pons, J., Reyes-Salazar, I., Arnedo-Pac, C., Mularoni, L., Pich, O., Bonet, J., Kranas, H., et al. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0290-x · Cited by 1,278 · see citing works
Macrophage diversity in cancer revisited in the era of single-cell omics
Ma, R., Black, A., & Qian, B. (2022) · Trends in Immunology · doi:10.1016/j.it.2022.04.008 · Cited by 706 · see citing works
Defining the Hallmarks of Metastasis
Welch, D. R., & Hurst, D. R. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-0458 · Cited by 695 · see citing works
Lüönd, F., Tiede, S., & Christofori, G. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01328-7 · Cited by 442 · see citing works
Emergence of a High-Plasticity Cell State during Lung Cancer Evolution
Marjanovic, N. D., Hofree, M., Chan, J. E., Canner, D. A., Wu, K., Trakala, M., Hartmann, G. G., Smith, O. C. G., Kim, J. Y., Evans, K. V., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.06.012 · Cited by 388 · see citing works
Comprehensive analysis of spatial architecture in primary liver cancer
Wu, R. T., Guo, W., Qiu, X., Wang, S., Sui, C., Lian, Q., Wu, J., Shan, Y., Zhao, Y., Yang, S., et al. (2021) · Science Advances · doi:10.1126/sciadv.abg3750 · Cited by 378 · see citing works
Role of m6A RNA methylation in cardiovascular disease (Review)
Qin, Y., Li, L., Luo, E., Hou, J., Yan, G., Wang, D., Qiao, Y., & Tang, C. (2020) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2020.4746 · Cited by 331 · see citing works
Advances in PET imaging of cancer
Schwenck, J., Sonanini, D., Cotton, J. M., Rammensee, H., la Fougère, C., Zender, L., & Pichler, B. J. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00576-4 · Cited by 322 · see citing works
The single-cell sequencing: new developments and medical applications
Tang, X., Huang, Y., Lei, J., Luo, H., & Zhu, X. M. (2019) · Cell & Bioscience · doi:10.1186/s13578-019-0314-y · Cited by 300 · see citing works
Davis, R. T., Blake, K., Ma, D., Gabra, M. B. I., Hernandez, G. A., Phung, A. T., Yang, Y., Maurer, D., Lefebvre, A. E. Y. T., Alshetaiwi, H. S., et al. (2020) · Nature Cell Biology · doi:10.1038/s41556-020-0477-0 · Cited by 298 · see citing works
Self-citationThe CRUK IMAXT Grand Challenge Team, O’Flanagan, C. H., Campbell, K. R., Zhang, A. W., Kabeer, F., Lim, J. L., Biele, J., Eirew, P. D., Lai, D., McPherson, A., et al. (2019) · Genome biology · doi:10.1186/s13059-019-1830-0 · Cited by 265 · see citing works
Single‐Cell Analysis Using Droplet Microfluidics
Matuła, K., Rivello, F., & Huck, W. T. S. (2019) · Advanced Biosystems · doi:10.1002/adbi.201900188 · Cited by 276 · see citing works
Open-ST: High-resolution spatial transcriptomics in 3D
Schott, M., León-Periñán, D., Splendiani, E., Strenger, L., Licha, J. R., Pentimalli, T. M., Schallenberg, S., Alles, J., Tagliaferro, S. S., Boltengagen, A., et al. (2024) · Cell · doi:10.1016/j.cell.2024.05.055 · Cited by 239 · see citing works
Intratumoral Heterogeneity: More Than Just Mutations
Hinohara, K., & Polyák, K. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.03.003 · Cited by 231 · see citing works
Metabolic Reprogramming of Cancer Cells during Tumor Progression and Metastasis
Ohshima, K., & Morii, E. (2021) · Metabolites · doi:10.3390/metabo11010028 · Cited by 230 · see citing works
Epigenomic State Transitions Characterize Tumor Progression in Mouse Lung Adenocarcinoma
LaFave, L. M., Kartha, V. K., Ma, S., Meli, K., Priore, I. S. D., Lareau, C. A., Naranjo, S., Westcott, P. M. K., Duarte, F. M., Sankar, V., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.06.006 · Cited by 207 · see citing works
Glial and myeloid heterogeneity in the brain tumour microenvironment
Andersen, B. M., Akl, C. F., Wheeler, M. A., Chiocca, E. A., Reardon, D. A., & Quintana, F. J. (2021) · Nature reviews. Cancer · doi:10.1038/s41568-021-00397-3 · Cited by 211 · see citing works
Multiomic Analysis of Lung Tumors Defines Pathways Activated in Neuroendocrine Transformation
Quintanal-Villalonga, A., Taniguchi, H., Zhan, Y. A., Hasan, M., Chavan, S. S., Meng, F., Uddin, F., Manoj, P., Donoghue, M. T. A., Won, H. H., et al. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-1863 · Cited by 190 · see citing works
Oxidative Metabolism Drives Immortalization of Neural Stem Cells during Tumorigenesis
Bonnay, F., Veloso, A., Steinmann, V., Köcher, T., Abdusselamoglu, M. D., Bajaj, S., Rivelles, E., Landskron, L., Esterbauer, H., Zinzen, R. P., et al. (2020) · Cell · doi:10.1016/j.cell.2020.07.039 · Cited by 191 · see citing works
Metal-free bioorthogonal click chemistry in cancer theranostics
Wu, D., Yang, K., Zhang, Z., Feng, Y., Rao, L., Chen, X. S., & Yu, G. (2022) · Chemical Society Reviews · doi:10.1039/d1cs00451d · Cited by 177 · see citing works
Cancer Stem Cells and Epithelial-to-Mesenchymal Transition in Cancer Metastasis
Celià-Terrassa, T., & Jolly, M. K. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a036905 · Cited by 163 · see citing works
Liu, Y., Ge, J., Chen, Y., Liu, T., Chen, L., Liu, C., Ma, D., Chen, Y., Cai, Y., Xu, Y., et al. (2023) · Advanced Science · doi:10.1002/advs.202205395 · Cited by 164 · see citing works
Clinical application and mechanism of traditional Chinese medicine in treatment of lung cancer
Su, X., Wang, J., Che, H., Wang, C., Jiang, H., Lei, X., Zhao, W., Kuang, H., & Wang, Q. (2020) · Chinese Medical Journal · doi:10.1097/cm9.0000000000001141 · Cited by 155 · see citing works
Fast and precise single-cell data analysis using a hierarchical autoencoder
Tran, D., Nguyen, H., Tran, B., La Vecchia, C., Luu, H. N., & Nguyen, T. (2021) · Nature Communications · doi:10.1038/s41467-021-21312-2 · Cited by 145 · see citing works
Cell and Nucleus Shape as an Indicator of Tissue Fluidity in Carcinoma
Grosser, S., Lippoldt, J., Oswald, L., Merkel, M., Sussman, D. M., Renner, F., Gottheil, P., Morawetz, E. W., Fuhs, T., Xie, X., et al. (2021) · Physical Review X · doi:10.1103/physrevx.11.011033 · Cited by 137 · see citing works
Cancer cell cycle heterogeneity as a critical determinant of therapeutic resistance
Maleki, E. H., Bahrami, A. R., & Matin, M. M. (2023) · Genes & Diseases · doi:10.1016/j.gendis.2022.11.025 · Cited by 133 · see citing works
Stem cells in cancer initiation and progression
Bajaj, J., Diaz, E., & Reya, T. (2019) · Journal of Cell Biology · doi:10.1083/jcb.201911053 · Cited by 105 · see citing works
Single cell profiling of primary and paired metastatic lymph node tumors in breast cancer patients
Liu, T., Liu, C., Yan, M., Zhang, L., Zhang, J., Xiao, M., Li, Z., Wei, X., & Zhang, H. (2022) · Nature Communications · doi:10.1038/s41467-022-34581-2 · Cited by 121 · see citing works
Wang, H., Mei, Y., Luo, C., Huang, Q., Wang, Z., Lu, G.-M., Qin, L., Sun, Z., Huang, C.-W., Yang, Z.-W., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-4796 · Cited by 116 · see citing works
Dynamic single-cell phenotyping of immune cells using the microfluidic platform DropMap
Bounab, Y., Eyer, K., Dixneuf, S., Rybczynska, M., Chauvel, C., Mistretta, M., Tran, T., Aymerich, N., Chenon, G., Llitjos, J., et al. (2020) · Nature Protocols · doi:10.1038/s41596-020-0354-0 · Cited by 111 · see citing works
Circulating Tumor Cells as a Tool for Assessing Tumor Heterogeneity
Gabriel, M. T., Heymann, M., & Heymann, D. (2019) · Theranostics · doi:10.7150/thno.34337 · Cited by 111 · see citing works
Commander, R., Wei, C., Sharma, A., Mouw, J. K., Burton, L. J., Summerbell, E. R., Mahboubi, D., Peterson, R. J., Konen, J. M., Zhou, W., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15219-7 · Cited by 111 · see citing works
Kondo, H., Ratcliffe, C. D. H., Hooper, S., Ellis, J., MacRae, J. I., Hennequart, M., Dunsby, C. W., Anderson, K. I., & Sahai, E. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108750 · Cited by 109 · see citing works
Maximizing transcription of nucleic acids with efficient T7 promoters
Conrad, T., Plumbom, I., Alcobendas, M., Vidal, R. O., & Sauer, S. (2020) · Communications Biology · doi:10.1038/s42003-020-01167-x · Cited by 109 · see citing works
Chakraborty, P., George, J. T., Tripathi, S., Levine, H., & Jolly, M. K. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00220 · Cited by 105 · see citing works
Sun, H., Cao, S., Mashl, R. J., Mo, C.-K., Zaccaria, S., Wendl, M. C., Davies, S. R., Bailey, M. H., Primeau, T. M., Hoog, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25177-3 · Cited by 102 · see citing works
Moving pan-cancer studies from basic research toward the clinic
Chen, F., Wendl, M. C., Wyczalkowski, M. A., Bailey, M. H., Li, Y., & Ding, L. (2021) · Nature Cancer · doi:10.1038/s43018-021-00250-4 · Cited by 107 · see citing works
Quantification of tumor heterogeneity: from data acquisition to metric generation
Kashyap, A., Rapsomaniki, M., Barros, V., Khartchenko, A. F., Martinelli, A. L., Foncubierta–Rodríguez, A., Gabrani, M., Rosen‐Zvi, M., & Kaigala, G. V. (2021) · Trends in biotechnology · doi:10.1016/j.tibtech.2021.11.006 · Cited by 104 · see citing works
Limia, C. M., Sauzay, C., Urra, H., Hetz, C. A., Chevet, É., & Avril, T. (2019) · Cancers · doi:10.3390/cancers11050631 · Cited by 102 · see citing works
Hypoxia-driven intratumor heterogeneity and immune evasion
Terry, S., Engelsen, A. S. T., Buart, S., El‐Sayed, W., Venkatesh, G. H., & Chouaı̈b, S. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.07.004 · Cited by 100 · see citing works
Radiological tumour classification across imaging modality and histology
Wu, J., Li, C., Gensheimer, M. F., Padda, S. K., Kato, F., Shirato, H., Wei, Y., Schönlieb, C., Price, S. J., Jaffray, D. A., et al. (2021) · Nature Machine Intelligence · doi:10.1038/s42256-021-00377-0 · Cited by 98 · see citing works
Vera, J. C., Sun, J., Lin, Y. T., Drnevich, J., Ke, R., & Brooke, C. B. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008671 · Cited by 97 · see citing works
Multiplex protein imaging in tumour biology
de Souza, N., Zhao, S., & Bodenmiller, B. (2024) · Nature reviews. Cancer · doi:10.1038/s41568-023-00657-4 · Cited by 93 · see citing works
Frank, M. H., Wilson, B. J., Gold, J. S., & Frank, N. Y. (2021) · Gastroenterology · doi:10.1053/j.gastro.2020.12.080 · Cited by 98 · see citing works
Levayer, R. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.05.004 · Cited by 93 · see citing works
In Situ Single Cell Proteomics Reveals Circulating Tumor Cell Heterogeneity during Treatment
Khondakar, K. R., Dey, S., Wuethrich, A., Wang, J., Behren, A., Antaw, F., Wang, Y., Sina, A. A. I., & Trau, M. (2021) · ACS Nano · doi:10.1021/acsnano.0c10008 · Cited by 92 · see citing works
Ling, Y., Zhong, J., Weng, Z., Lin, G., Liu, C., Pan, C., Yang, H., Wei, X., Xie, X., Wei, X., et al. (2022) · Clinical and Translational Medicine · doi:10.1002/ctm2.1074 · Cited by 92 · see citing works
Organ-Specificity of Breast Cancer Metastasis
Ibragimova, M. K., Tsyganov, M. M., Kravtsova, E. A., Tsydenova, I. A., & Литвяков, Н. В. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115625 · Cited by 92 · see citing works
Breast cancers, mammary stem cells, and cancer stem cells, characteristics, and hypotheses
Taurin, S., & Alkhalifa, H. (2020) · Neoplasia · doi:10.1016/j.neo.2020.09.009 · Cited by 90 · see citing works
Over a century of cancer research: Inconvenient truths and promising leads
Sonnenschein, C., & Soto, A. M. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000670 · Cited by 86 · see citing works
Single-cell mapping of DNA G-quadruplex structures in human cancer cells
Hui, W. W. I., Simeone, A., Zyner, K. G., Tannahill, D., & Balasubramanian, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-02943-3 · Cited by 85 · see citing works
Breast Cancer Heterogeneity and Response to Novel Therapeutics
Baliu‐Piqué, M., Pandiella, A., & Ocaña, A. (2020) · Cancers · doi:10.3390/cancers12113271 · Cited by 86 · see citing works
Mechano‐Responsive Leapfrog Micelles Enable Interactive Apoptotic and Ferroptotic Cancer Therapy
Li, Y., Qin, Y., Shang, Y., Li, Y., Liu, F., Luo, J., Zhu, J., Guo, X., Wang, Z., & Zhao, Y. (2022) · Advanced Functional Materials · doi:10.1002/adfm.202112000 · Cited by 85 · see citing works
Wu, W., Liu, Y., Zeng, S., Han, Y., & Shen, H. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01166-3 · Cited by 81 · see citing works
Leshchiner, I., Livitz, D. G., Gainor, J. F., Rosebrock, D., Spiro, O., Martinez, A. Z., Mroz, E. A., Lin, J. J., Stewart, C., Kim, J., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/508127 · Cited by 79 · see citing works
Estimation of tumor cell total mRNA expression in 15 cancer types predicts disease progression
Cao, S., Wang, J. R., Ji, S., Peng, Y., Dai, Y., Guo, S., Montierth, M. D., Shen, J. P., Zhao, X. H., Chen, J., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01342-x · Cited by 80 · see citing works
Addressing Patient Specificity in the Engineering of Tumor Models
Bray, L. J., Hutmacher, D. W., & Bock, N. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00217 · Cited by 76 · see citing works
Li, J., Wang, H., Wang, Y., Gong, X., Xu, X., Sha, X., Zhang, A., Zhang, Z., & Li, Y. (2020) · Advanced Materials · doi:10.1002/adma.202002380 · Cited by 73 · see citing works
Bock, N., Forouz, F., Hipwood, L., Clegg, J., Jeffery, P. L., Gough, M., van Wyngaard, T., Pyke, C., Adams, M. N., Bray, L. J., et al. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15010261 · Cited by 73 · see citing works
Deep Profiling of Cellular Heterogeneity by Emerging Single‐Cell Proteomic Technologies
Yang, L., George, J., & Wang, J. (2019) · PROTEOMICS · doi:10.1002/pmic.201900226 · Cited by 70 · see citing works
Single-Cell RNA Sequencing: Technological Progress and Biomedical Application in Cancer Research
Xu, C., Zheng, Y., & Xu, K. (2023) · Molecular Biotechnology · doi:10.1007/s12033-023-00777-0 · Cited by 74 · see citing works
Neitzel, C., Demuth, P., Wittmann, S., & Fahrer, J. (2020) · Cancers · doi:10.3390/cancers12071731 · Cited by 68 · see citing works
Single cell metabolomics using mass spectrometry: Techniques and data analysis
Liu, R., & Yang, Z. (2020) · Analytica Chimica Acta · doi:10.1016/j.aca.2020.11.020 · Cited by 68 · see citing works
Heterogeneity of Circulating Tumor Cells in Breast Cancer: Identifying Metastatic Seeds
Menyailo, M. E., Tretyakova, M. S., & Denisov, E. V. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051696 · Cited by 67 · see citing works
Yang, Q., Xiao, Y., Yin, Y., Li, G., & Peng, J. (2019) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.9b00413 · Cited by 66 · see citing works
SPARSim single cell: a count data simulator for scRNA-seq data
Baruzzo, G., Patuzzi, I., & Camillo, B. D. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz752 · Cited by 61 · see citing works
Disordered chromatin packing regulates phenotypic plasticity
Virk, R. K. A., Wu, W., Almassalha, L. M., Bauer, G. M., Li, Y., VanDerway, D., Frederick, J., Zhang, D., Eshein, A., Roy, H. K., et al. (2020) · Science Advances · doi:10.1126/sciadv.aax6232 · Cited by 61 · see citing works
Long Non-Coding RNA: Dual Effects on Breast Cancer Metastasis and Clinical Applications
Huang, Q.-Y., Liu, G., Qian, X., Tang, L.-B., Huang, Q.-Y., & Xiong, L. (2019) · Cancers · doi:10.3390/cancers11111802 · Cited by 63 · see citing works
Targeting of cancer stem cells by differentiation therapy
Arima, Y., Nobusue, H., & Saya, H. (2020) · Cancer Science · doi:10.1111/cas.14504 · Cited by 63 · see citing works
Stashko, C., Hayward, M.-K., Northey, J. J., Pearson, N., Ironside, A. J., Lakins, J. N., Oria, R., Goyette, M.-A., Mayo, L. N., Russnes, H. G., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39085-1 · Cited by 62 · see citing works
Nanobody Conjugates for Targeted Cancer Therapy and Imaging
Kang, W., Ding, C., Zheng, D., Ma, X., Yi, L., Tong, X., Wu, C., Xue, C., Yu, Y., & Zhou, Q. (2021) · Technology in Cancer Research & Treatment · doi:10.1177/15330338211010117 · Cited by 62 · see citing works
Preedy, M. K., White, M., & Tergaonkar, V. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06559-z · Cited by 64 · see citing works
Spatiotemporal pH Heterogeneity as a Promoter of Cancer Progression and Therapeutic Resistance
Korenchan, D. E., & Flavell, R. R. (2019) · Cancers · doi:10.3390/cancers11071026 · Cited by 61 · see citing works
Koberstein, J. N., Stewart, M. L., Smith, C. B., Tarasov, A. I., Ashcroft, F. M., Stork, P. A., & Goodman, R. H. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204407119 · Cited by 60 · see citing works
Zheng, X., Yu, C., & Xu, M. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.678333 · Cited by 59 · see citing works
Mezawa, Y., & Orimo, A. (2021) · FEBS Journal · doi:10.1111/febs.15851 · Cited by 59 · see citing works
Zhu, Z., Jiang, L., & Ding, X. (2023) · Cancers · doi:10.3390/cancers15164164 · Cited by 58 · see citing works
A review of computational strategies for denoising and imputation of single-cell transcriptomic data
Patruno, L., Maspero, D., Craighero, F., Angaroni, F., Antoniotti, M., & Graudenzi, A. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa222 · Cited by 53 · see citing works
Evolution of core archetypal phenotypes in progressive high grade serous ovarian cancer
Nath, A., Cosgrove, P. A., Mirsafian, H., Christie, E. L., Pflieger, L. T., Copeland, B., Majumdar, S., Cristea, M. C., Han, E. S., Lee, S. J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23171-3 · Cited by 56 · see citing works
Spatial proteomics for understanding the tissue microenvironment
Mao, Y., Wang, X., Huang, P., & Tian, R. (2021) · The Analyst · doi:10.1039/d1an00472g · Cited by 53 · see citing works
From Chaos to Opportunity: Decoding Cancer Heterogeneity for Enhanced Treatment Strategies
Ottaiano, A., Ianniello, M., Santorsola, M., Ruggiero, R., Sirica, R., Sabbatino, F., Perri, F., Cascella, M., Marzo, M. D., Berretta, M., et al. (2023) · Biology · doi:10.3390/biology12091183 · Cited by 56 · see citing works
Spatial intra-tumor heterogeneity is associated with survival of lung adenocarcinoma patients
Wu, H., Temko, D., Maliga, Z., Moreira, A. L., Sei, E., Minussi, D. C., Dean, J., Lee, C., Xu, Q., Hochart, G., et al. (2022) · Cell Genomics · doi:10.1016/j.xgen.2022.100165 · Cited by 51 · see citing works
Nanopore approaches for single-molecule temporal omics: promises and challenges
Li, M., Jiang, J., Li, J., Niu, H., Ying, Y., Tian, R., & Long, Y. (2024) · Nature Methods · doi:10.1038/s41592-024-02492-3 · Cited by 56 · see citing works
Pang, L., Ding, J., Ge, Y., Fan, J., & Fan, S. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.9b01084 · Cited by 53 · see citing works
CyTOF: An Emerging Technology for Single‐Cell Proteomics in the Mouse
Tracey, L. J., An, Y., & Justice, M. J. (2021) · Current Protocols · doi:10.1002/cpz1.118 · Cited by 53 · see citing works
Pitfalls in Cancer Biomarker Discovery and Validation with Emphasis on Circulating Tumor DNA
Ren, A. H., Fiala, C., Diamandis, E. P., & Kulasingam, V. (2020) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-20-0074 · Cited by 52 · see citing works
Chen, Z.-C., Huang, Y.-W., Hu, Z.-Y., Zhao, M.-N., Bian, Y.-Y., Chen, Z., Zheng, Y.-S., Bi, G.-S., Pang, Y., Zhan, C., et al. (2021) · Oncogenesis · doi:10.1038/s41389-021-00359-2 · Cited by 38 · see citing works
Spatial Transcriptomics for Tumor Heterogeneity Analysis
Li, Q., Zhang, X., & Ke, R. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.906158 · Cited by 52 · see citing works
Interrogation of Phenotypic Plasticity between Epithelial and Mesenchymal States in Breast Cancer
Bhatia, S., Monkman, J. H., Blick, T., Pinto, C., Waltham, M. C., Nagaraj, S. H., & Thompson, E. W. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8060893 · Cited by 52 · see citing works
Nanobodies as non-invasive imaging tools
Rashidian, M., & Ploegh, H. L. (2020) · Immuno-Oncology Technology · doi:10.1016/j.iotech.2020.07.001 · Cited by 51 · see citing works
Scalable co-sequencing of RNA and DNA from individual nuclei
Olsen, T. R., Talla, P., Sagatelian, R., Furnari, J. L., Bruce, J. N., Canoll, P., Zha, S., & Sims, P. A. (2025) · Nature Methods · doi:10.1038/s41592-024-02579-x · Cited by 50 · see citing works
Ge, L., Jin, X., Ma, D., Wang, Z.-Y., Liu, C., Zhou, C., Zhao, S., Yu, T., Liu, X., Di, G. H., et al. (2024) · Cell Research · doi:10.1038/s41422-023-00909-w · Cited by 49 · see citing works
Targeting Epigenetics in Lung CancerPreprint
Chao, Y. L., & Pecot, C. V. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a038000 · Cited by 47 · see citing works
Huang, P., Kong, Q., Gao, W., Chu, B., Li, H., Mao, Y., Cai, Z., Xu, R., & Tian, R. (2020) · Analytica Chimica Acta · doi:10.1016/j.aca.2020.06.049 · Cited by 46 · see citing works
Li, J., Lin, P., Tan, Y., & Cheng, J. (2019) · Biomedical Optics Express · doi:10.1364/boe.10.004329 · Cited by 46 · see citing works
Tumor biology and multidisciplinary strategies of oligometastasis in gastrointestinal cancers
Zhao, Y., Li, J., Li, D., Wang, Z., Zhao, J., Wu, X., Sun, Q., Lin, P. P., Plum, P. S., Damanakis, A. I., et al. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.08.026 · Cited by 47 · see citing works
Connecting Metabolic Rewiring With Phenotype Switching in Melanoma
Falletta, P., Goding, C. R., & Vivas, Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.930250 · Cited by 44 · see citing works
- Authors
- Lawson, D. A., Kessenbrock, K., Davis, R. T., Pervolarakis, N., & Werb, Z.
- Affiliations
- University of California, Irvine (US)
- University of California, San Francisco (US)
- Corresponding author
- Lawson, Devon A.
- Kessenbrock, Kai
- Venue
- Nature Cell Biology
- Published
- 2018-11-26
- Volume
- 20
- Issue
- 12
- Pages
- 1349-1360
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC6477686
- OpenAlex
- W2900850487
- Cited by
- 606
- References
- 157
- Citations by year
- 2026: 51 · 2025: 78 · 2024: 89 · 2023: 74 · 2022: 90 · 2021: 98 · 2020: 76 · 2019: 48 · 2018: 1 · 2015: 1
- FWCI
- 5.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Cancer Institute (R00CA181490, U01CA199315, K22CA190511, U54CA217378, T32CA009054)
- National Institute of Biomedical Imaging and Bioengineering (T32EB009418)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- tumor heterogeneity, metastasis, single-cell technologies, single-cell profiling, tumor progression, drug resistance, tumor cell subpopulations
- MeSH terms
- Humans, Neoplastic Cells, Circulating, Neoplasm Metastasis, Neoplasms, Biomarkers, Tumor, Gene Expression Regulation, Neoplastic, Genetic Heterogeneity, Single-Cell Analysis, Tumor Microenvironment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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