Spatial genomics enables multi-modal study of clonal heterogeneity in tissues

Comprehensive molecular characterization of human colon and rectal cancer

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Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position

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Clonal heterogeneity and tumor evolution: past, present, and the future

McGranahan, N., & Swanton, C. (2017) · Cell · doi:10.1016/j.cell.2017.01.018 · Cited by 2,840 · see citing works

Slide-seq: A scalable technology for measuring genome-wide expression at high spatial resolution

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Tracking the Evolution of Non–Small-Cell Lung Cancer

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Concepts of extracellular matrix remodelling in tumour progression and metastasis

Winkler, J., Abisoye-Ogunniyan, A., Metcalf, K. J., & Werb, Z. (2020) · Nature Communications · doi:10.1038/s41467-020-18794-x · Cited by 2,296 · see citing works

Robust decomposition of cell type mixtures in spatial transcriptomics

Cable, D. M., Murray, E., Zou, L. S., Goeva, A., Macosko, E. Z., Chen, F., & Irizarry, R. A. (2022) · Nature Biotechnology · doi:10.1038/s41587-021-00830-w · Cited by 1,487 · see citing works

The Integrative Human Microbiome Project

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Evolution and impact of subclonal mutations in chronic lymphocytic leukemia

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Highly sensitive spatial transcriptomics at near-cellular resolution with Slide-seqV2

Stickels, R. R., Murray, E., Kumar, P., Li, J., Marshall, J. L., Di Bella, D. J., Arlotta, P., Macosko, E. Z., & Chen, F. (2021) · Nature Biotechnology · doi:10.1038/s41587-020-0739-1 · Cited by 1,295 · see citing works

The updated landscape of tumor microenvironment and drug repurposing

Jin, M.-Z., & Jin, W.-L. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00280-x · Cited by 1,262 · see citing works

Towards Practical, High-Capacity, Low-Maintenance Information Storage in Synthesized DNA

Goldman, N., Bertone, P., Chen, S., Dessimoz, C., LeProust, E. M., Sipos, B., & Birney, E. (2013) · Nature · doi:10.1038/nature11875 · Cited by 1,220 · see citing works

Somatic activation of the K-ras oncogene causes early onset lung cancer in mice

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The evolutionary history of 2,658 cancers

Gerstung, M., Jolly, C., Leshchiner, I., Dentro, S. C., Gonzalez, S., Rosebrock, D., Mitchell, T. J., Rubanova, Y., Anur, P., Yu, K., et al. (2020) · Nature · doi:10.1038/s41586-019-1907-7 · Cited by 1,057 · see citing works

Consensus molecular subtypes and the evolution of precision medicine in colorectal cancer

Dienstmann, R., Vermeulen, L., Guinney, J., Kopetz, S., Tejpar, S., & Tabernero, J. M. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2016.126 · Cited by 1,038 · 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

A Big Bang model of human colorectal tumor growth

Sottoriva, A., Kang, H., Ma, Z., Graham, T. A., Salomon, M. P., Zhao, J., Marjoram, P., Siegmund, K. D., Press, M. F., Shibata, D. K., et al. (2015) · Nature Genetics · doi:10.1038/ng.3214 · Cited by 1,010 · see citing works

Turning Cold into Hot: Firing up the Tumor Microenvironment

Duan, Q., Zhang, H., Zheng, J., & Zhang, L. (2020) · Trends in Cancer · doi:10.1016/j.trecan.2020.02.022 · Cited by 934 · see citing works

Single-Cell Exome Sequencing Reveals Single-Nucleotide Mutation Characteristics of a Kidney Tumor

Xu, X., Hou, Y., Yin, X., Bao, L., Tang, A., Song, L., Li, F., Tsang, S., Wu, K., Wu, H., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.025 · Cited by 667 · see citing works

Resolving genetic heterogeneity in cancer

Turajlic, S., Sottoriva, A., Graham, T. A., & Swanton, C. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0114-6 · Cited by 655 · see citing works

Circular ecDNA promotes accessible chromatin and high oncogene expression

Wu, S., Turner, K. M., Nguyen, N., Raviram, R., Erb, M. L., Santini, J., Luebeck, J., Rajkumar, U., Diao, Y., Li, B., et al. (2019) · Nature · doi:10.1038/s41586-019-1763-5 · Cited by 651 · see citing works

Mechanical compression drives cancer cells toward invasive phenotype

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53BP1, a Mediator of the DNA Damage Checkpoint

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Reengineering the Physical Microenvironment of Tumors to Improve Drug Delivery and Efficacy: From Mathematical Modeling to Bench to Bedside

Stylianopoulos, T., Munn, L. L., & Jain, R. K. (2018) · Trends in cancer · doi:10.1016/j.trecan.2018.02.005 · Cited by 570 · see citing works

Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition

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Lineage Tracing in Humans Enabled by Mitochondrial Mutations and Single-Cell Genomics

Ludwig, L. S., Lareau, C. A., Ulirsch, J. C., Christian, E., Muus, C., Li, L. H., Pelka, K., Ge, W. H., Oren, Y., Brack, A., et al. (2019) · Cell · doi:10.1016/j.cell.2019.01.022 · Cited by 534 · see citing works

Clinical implications of intratumor heterogeneity: challenges and opportunities

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Transforming growth factor-β employs HMGA2 to elicit epithelial–mesenchymal transition

Thuault, S., Valcourt, U., Petersen, M., Manfioletti, G., Heldin, C., & Moustakas, A. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200512110 · Cited by 500 · see citing works

Bisulfite-free direct detection of 5-methylcytosine and 5-hydroxymethylcytosine at base resolution

Liu, Y., Siejka-Zielińska, P., Velikova, G., Bi, Y., Yuan, F., Tomková, M., Bai, C., Chen, L., Schuster‐Böckler, B., & Song, C. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0041-2 · Cited by 474 · 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

Divergent modes of clonal spread and intraperitoneal mixing in high-grade serous ovarian cancer

McPherson, A., Roth, A. J. L., Laks, E., Masud, T., Bashashati, A., Zhang, A. W., Ha, G., Biele, J., Yap, D., Wan, A., et al. (2016) · Nature Genetics · doi:10.1038/ng.3573 · Cited by 331 · see citing works

Genetic and Clonal Dissection of Murine Small Cell Lung Carcinoma Progression by Genome Sequencing

McFadden, D. G., Papagiannakopoulos, T. Y., Taylor-Weiner, A. N., Stewart, C., Carter, S. L., Cibulskis, K., Bhutkar, A. J., McKenna, A., Dooley, A. L., Vernon, A. N., et al. (2014) · Cell · doi:10.1016/j.cell.2014.02.031 · Cited by 289 · see citing works

The delivery challenge: fulfilling the promise of therapeutic genome editing

van Haasteren, J., Li, J., Scheideler, O. J., Murthy, N., & Schaffer, D. V. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0565-5 · Cited by 285 · see citing works

HMGA2 Is a Driver of Tumor Metastasis

Morishita, A., Zaidi, M. R., Mitoro, A., Sankarasharma, D., Szabolcs, M. J., Okada, Y., D'Armiento, J. M., & Chada, K. K. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3848 · Cited by 257 · see citing works

Breast tumours maintain a reservoir of subclonal diversity during expansion

Minussi, D. C., Nicholson, M. D., Ye, H., Davis, A., Wang, K., Baker, T., Tarabichi, M., Sei, E., Du, H., Rabbani, M., et al. (2021) · Nature · doi:10.1038/s41586-021-03357-x · Cited by 256 · see citing works

Mechanism of RAD51-Dependent DNA Interstrand Cross-Link Repair

Long, D. T., Räschle, M., Joukov, V., & Walter, J. C. (2011) · Science · doi:10.1126/science.1204258 · Cited by 238 · see citing works

Recurrent Fusions in MYB and MYBL1 Define a Common, Transcription Factor–Driven Oncogenic Pathway in Salivary Gland Adenoid Cystic Carcinoma

Brayer, K. J., Frerich, C. A., Kang, H., & Ness, S. A. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0859 · Cited by 225 · see citing works

The role of Galectin-3 in modulating tumor growth and immunosuppression within the tumor microenvironment

Farhad, M. E., Rolig, A. S., & Redmond, W. L. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1434467 · Cited by 212 · 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

In situ genome sequencing resolves DNA sequence and structure in intact biological samples

Payne, A. C., Chiang, Z., Reginato, P., Mangiameli, S. M., Murray, E. M., Yao, C., Markoulaki, S., Earl, A., Labade, A. S., Jaenisch, R., et al. (2021) · Science · doi:10.1126/science.aay3446 · Cited by 198 · see citing works

MCM7 amplification and overexpression are associated with prostate cancer progression

Ren, B., Yu, G., Tseng, G. C., Cieply, K. M., Gavel, T., Nelson, J., Michalopoulos, G. K., Yu, Y., & Luo, J.-H. (2005) · Oncogene · doi:10.1038/sj.onc.1209134 · Cited by 190 · see citing works

Erratum: Consensus molecular subtypes and the evolution of precision medicine in colorectal cancer

Dienstmann, R., Vermeulen, L., Guinney, J., Kopetz, S., Tejpar, S., & Tabernero, J. M. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2017.24 · Cited by 183 · see citing works

Plag1 and Plagl2 are oncogenes that induce acute myeloid leukemia in cooperation with Cbfb-MYH11

Landrette, S. F., Kuo, Y., Hensen, K., van Doorn-Khosrovani, S. B. V. W., Perrat, P. N., de Ven, W. J. M. V., Delwel, R., & Castilla, L. H. (2004) · Blood · doi:10.1182/blood-2004-09-3630 · Cited by 130 · see citing works

Ubiquitinated Fancd2 recruits Fan1 to stalled replication forks to prevent genome instability

Lachaud, C., Moreno, A., Marchesi, F., Toth, R. L., Blow, J. J., & Rouse, J. W. (2016) · Science · doi:10.1126/science.aad5634 · Cited by 119 · see citing works

Lineage tracing reveals multipotent stem cells maintain human adenomas and the pattern of clonal expansion in tumor evolution

Humphries, A., Cereser, B., Gay, L. J., Miller, D. S. J., Das, B., Gutteridge, A., Elia, G., Nye, E. L., Jeffery, R. E., Poulsom, R., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220353110 · Cited by 98 · see citing works

Selection of metastasis competent subclones in the tumour interior

Zhao, Y., Fu, X., Lopez, J. I., Rowan, A., Au, L., Fendler, A., Hazell, S., Xu, H., Horswell, S., Shepherd, S. T. C., et al. (2021) · Nature Ecology & Evolution · doi:10.1038/s41559-021-01456-6 · Cited by 95 · see citing works

Integrative single-cell analysis of allele-specific copy number alterations and chromatin accessibility in cancer

Wu, C.-Y., Lau, B. T., Kim, H. S., Sathe, A., Grimes, S. M., Ji, H. P., & Zhang, N. R. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00911-w · Cited by 70 · see citing works

Harnessing Tumor Evolution to Circumvent Resistance

McNamara, K. L., & Curtis, C. N. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.05.007 · Cited by 66 · see citing works

Prom1 Function in Development, Intestinal Inflammation, and Intestinal Tumorigenesis

Karim, B. O., Rhee, K., Liu, G., Yun, K., & Brant, S. R. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00323 · Cited by 33 · see citing works

Many private mutations originate from the first few divisions of a human colorectal adenoma

Kang, H., Salomon, M. P., Sottoriva, A., Zhao, J., Toy, M., Press, M. F., Curtis, C. N., Marjoram, P., Siegmund, K. D., & Shibata, D. K. (2015) · The Journal of Pathology · doi:10.1002/path.4581 · Cited by 32 · see citing works

The technological landscape and applications of single-cell multi-omics

Baysoy, A., Bai, Z., Satija, R., & Fan, R. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00615-w · Cited by 1,037 · see citing works

Breast cancer: pathogenesis and treatments

Xiong, X., Zheng, L., Ding, Y., Chen, Y., Cai, Y., Wang, L., Huang, L., Liu, C., Shao, Z., & Yu, K. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-02108-4 · Cited by 1,098 · see citing works

Spatially resolved multi-omics deciphers bidirectional tumor-host interdependence in glioblastoma

Ravi, V. M., Will, P., Kueckelhaus, J., Sun, N., Joseph, K., Salié, H., Vollmer, L., Kuliešiūtė, U., von Ehr, J., Benotmane, J. K., et al. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.05.009 · Cited by 671 · see citing works

The dawn of spatial omics

Bressan, D., Battistoni, G., & Hannon, G. J. (2023) · Science · doi:10.1126/science.abq4964 · Cited by 606 · see citing works

The expanding vistas of spatial transcriptomics

Tian, L., Chen, F., & Macosko, E. Z. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01448-2 · Cited by 539 · see citing works

Deep Visual Proteomics defines single-cell identity and heterogeneity

Mund, A., Coscia, F., Kriston, A., Hollandi, R., Kovács, F., Brunner, A.-D., Migh, E., Schweizer, L., Santos, A., Bzorek, M., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01302-5 · Cited by 562 · see citing works

Spatial profiling technologies illuminate the tumor microenvironment

Elhanani, O., Ben-Uri, R., & Keren, L. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.01.010 · Cited by 526 · see citing works

Artificial intelligence in histopathology: enhancing cancer research and clinical oncology

Shmatko, A., Ghaffari Laleh, N., Gerstung, M., & Kather, J. N. (2022) · Nature Cancer · doi:10.1038/s43018-022-00436-4 · Cited by 446 · see citing works

Tumor heterogeneity reshapes the tumor microenvironment to influence drug resistance

Zhang, A., Miao, K., Sun, H., & Deng, C. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.72534 · Cited by 368 · see citing works

Spatially resolved clonal copy number alterations in benign and malignant tissue

Erickson, A. M., He, M., Berglund, E., Marklund, M., Mirzazadeh, R., Schultz, N., Kvastad, L., Andersson, A., Bergenstråhle, L., Bergenstråhle, J., et al. (2022) · Nature · doi:10.1038/s41586-022-05023-2 · Cited by 307 · see citing works

Profiling cell identity and tissue architecture with single-cell and spatial transcriptomics

Gulati, G. S., D'Silva, J. P., Liu, Y., Wang, L., & Newman, A. M. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00768-2 · Cited by 328 · see citing works

BANKSY unifies cell typing and tissue domain segmentation for scalable spatial omics data analysis

Singhal, V., Chou, N., Lee, J., Yue, Y., Liu, J., Chock, W. K., Lin, L., Chang, Y.-C., Teo, E. M. L., Aow, J., et al. (2024) · Nature Genetics · doi:10.1038/s41588-024-01664-3 · Cited by 282 · see citing works

Big data in basic and translational cancer research

Jiang, P., Sinha, S., Aldape, K., Hannenhalli, S., Sahinalp, C., & Ruppin, E. (2022) · Nature Reviews Cancer · doi:10.1038/s41568-022-00502-0 · Cited by 254 · see citing works

Spatiotemporal omics for biology and medicine

Liu, L., Chen, A., Li, Y., Mulder, J., Heyn, H., & Xu, X. (2024) · Cell · doi:10.1016/j.cell.2024.07.040 · Cited by 239 · see citing works

Slide-tags enables single-nucleus barcoding for multimodal spatial genomics

Russell, A. J. C., Weir, J. A., Nadaf, N. M., Shabet, M., Kumar, V., Kambhampati, S., Raichur, R., Marrero, G. J., Liu, S., Balderrama, K. S., et al. (2024) · Nature · doi:10.1038/s41586-023-06837-4 · Cited by 225 · see citing works

CellCharter reveals spatial cell niches associated with tissue remodeling and cell plasticity

Varrone, M., Tavernari, D., Santamaria‐Martínez, A., Walsh, L. A., & Ciriello, G. (2023) · Nature Genetics · doi:10.1038/s41588-023-01588-4 · Cited by 210 · see citing works

Spatial multi-omics: deciphering technological landscape of integration of multi-omics and its applications

Liu, X., Peng, T., Xu, M., Lin, S., Hu, B., Chu, T., Liu, B., Xu, Y., Ding, W., Li, L., et al. (2024) · Journal of Hematology & Oncology · doi:10.1186/s13045-024-01596-9 · Cited by 229 · see citing works

Systematic comparison of sequencing-based spatial transcriptomic methods

You, Y., Fu, Y., Li, L., Zhang, Z., Jia, S., Lu, S., Ren, W., Liu, Y., Xu, Y., Liu, X., et al. (2024) · Nature Methods · doi:10.1038/s41592-024-02325-3 · Cited by 220 · see citing works

Spatial biology of cancer evolution

Seferbekova, Z., Lomakin, A., Yates, L. R., & Gerstung, M. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00553-x · Cited by 210 · see citing works

Advances in molecular pathology and therapy of non-small cell lung cancer

Huang, Q., Li, Y., Huang, Y., Wu, J., Bao, W., Xue, C., Li, X., Dong, S., Dong, Z., & Hu, S. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02243-6 · Cited by 197 · see citing works

Integration of whole transcriptome spatial profiling with protein markers

Ben‐Chetrit, N., Niu, X., Swett, A. D., Sotelo, J., Jiao, M. S., Stewart, C. M., Potenski, C. J., Mielinis, P., Roelli, P., Stoeckius, M., et al. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01536-3 · Cited by 212 · see citing works

Spatially resolved transcriptomics: a comprehensive review of their technological advances, applications, and challenges

Cheng, M., Jiang, Y., Xu, J., Mentis, A. A., Wang, S., Zheng, H., Sahu, S. K., Liu, L., & Xu, X. (2023) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2023.03.011 · Cited by 190 · see citing works

Spatial genomics maps the structure, nature and evolution of cancer clones

Lomakin, A., Svedlund, J., Strell, C., Gatarić, M., Shmatko, A., Rukhovich, G. D., Park, J. S., Ju, Y. S., Dentro, S. C., Kleshchevnikov, V., et al. (2022) · Nature · doi:10.1038/s41586-022-05425-2 · Cited by 206 · see citing works

Clinical application of advanced multi-omics tumor profiling: Shaping precision oncology of the future

Akhoundova, D., & Rubin, M. A. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.08.011 · Cited by 188 · see citing works

Spatial transcriptomics reveals discrete tumour microenvironments and autocrine loops within ovarian cancer subclones

Denisenko, E., de Kock, L., Tan, A. L. Y., Beasley, A. B., Beilin, M., Jones, M. E., Hou, R., Muirí, D. Ó., Bilic, S., Mohan, G. R. K. A., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47271-y · Cited by 164 · see citing works

Cell type-specific inference of differential expression in spatial transcriptomics

Cable, D. M., Murray, E. M., Shanmugam, V., Zhang, S., Zou, L. S., Diao, M., Chen, H., Macosko, E. Z., Irizarry, R. A., & Chen, F. (2022) · Nature Methods · doi:10.1038/s41592-022-01575-3 · Cited by 164 · see citing works

Spatial Transcriptomic Technologies

Chen, T.-Y., You, L., Hardillo, J. A., & Chien, M. (2023) · Cells · doi:10.3390/cells12162042 · Cited by 153 · see citing works

Estimation of cell lineages in tumors from spatial transcriptomics data

Ru, B., Huang, J., Zhang, Y., Aldape, K., & Jiang, P. (2023) · Nature Communications · doi:10.1038/s41467-023-36062-6 · Cited by 136 · see citing works

Spatial oncology: Translating contextual biology to the clinic

Gong, D. H., Arbesfeld-Qiu, J. M., Perrault, E. N., Bae, J. W., & Hwang, W. L. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.09.001 · Cited by 133 · see citing works

Spatial omics technologies at multimodal and single cell/subcellular level

Park, J., Kim, J., Lewy, T., Rice, C. M., Elemento, O., Rendeiro, A. F., & Mason, C. E. (2022) · Genome biology · doi:10.1186/s13059-022-02824-6 · Cited by 125 · see citing works

SODB facilitates comprehensive exploration of spatial omics data

Yuan, Z., Pan, W., Zhao, X., Zhao, F., Xu, Z., Li, X., Zhao, Y. C., Zhang, M. Q., & Yao, J. (2023) · Nature Methods · doi:10.1038/s41592-023-01773-7 · Cited by 112 · see citing works

Mapping epigenetic modifications by sequencing technologies

Chen, X., Xu, H., Shu, X., & Song, C.-X. (2025) · Cell Death & Differentiation · doi:10.1038/s41418-023-01213-1 · Cited by 105 · see citing works

Single-cell multi-omics in cancer immunotherapy: from tumor heterogeneity to personalized precision treatment

Le, J., Dian, Y., Zhao, D., Guo, Z., Luo, Z., Chen, X., Zeng, F., & Deng, G. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02426-3 · Cited by 109 · see citing works

Alignment of spatial genomics data using deep Gaussian processes

Jones, A., Townes, F. W., Li, D., & Engelhardt, B. E. (2023) · Nature Methods · doi:10.1038/s41592-023-01972-2 · Cited by 85 · see citing works

Spatial multi-omics reveals cell-type-specific nuclear compartments

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