The DOI matches its Crossref record; 62 of the 62 references it cites were found in a registry or an index.
Spatial and temporal diversity in genomic instability processes defines lung cancer evolution
Open accessAbstract
Spatial and temporal dissection of the genomic changes occurring during the evolution of human non–small cell lung cancer (NSCLC) may help elucidate the basis for its dismal prognosis. We sequenced 25 spatially distinct regions from seven operable NSCLCs and found evidence of branched evolution, with driver mutations arising before and after subclonal diversification. There was pronounced intratumor heterogeneity in copy number alterations, translocations, and mutations associated with APOBEC cytidine deaminase activity. Despite maintained carcinogen exposure, tumors from smokers showed a relative decrease in smoking-related mutations over time, accompanied by an increase in APOBEC-associated mutations. In tumors from former smokers, genome-doubling occurred within a smoking-signature context before subclonal diversification, which suggested that a long period of tumor latency had preceded clinical detection. The regionally separated driver mutations, coupled with the relentless and heterogeneous nature of the genome instability processes, are likely to confound treatment success in NSCLC.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“While the full extent to which mutational processes account for unique combinations of somatic genomic alterations in NSCLC is currently unknown, there is evidence that APOBEC-mediated mutagenesis fuels sub-clonal diversification and branched evolution78, 79.”
From Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy (2019) · cites this paper as [79]
Citations
Cites
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607
Estimating the Dimension of a Model
Schwarz, G. (1978) · The Annals of Statistics · doi:10.1214/aos/1176344136 · Cited by 47,033
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr121 · Cited by 40,166
ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data
Wang, K., Li, M., & Hakonarson, H. H. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq603 · Cited by 14,724
Siegel, R., Naishadham, D., & Jemal, A. (2013) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21166 · Cited by 11,825
Circos: An information aesthetic for comparative genomicsPreprint
Krzywinski, M. I., Schein, J. E., Birol, İ., Connors, J. M., Gascoyne, R. D., Horsman, D. E., Jones, S. J. M., & Marra, M. A. (2009) · Genome Research · doi:10.1101/gr.092759.109 · Cited by 11,073
Mutations of the BRAF gene in human cancer
Davies, H., Bignell, G. R., Cox, C., Stephens, P., Edkins, S., Clegg, S., Teague, J., Woffendin, H., Garnett, M. J., Bottomley, W., et al. (2002) · Nature · doi:10.1038/nature00766 · Cited by 10,674
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
Self-citation<tt>BLAT</tt> —The <tt>BLAST</tt> -Like Alignment Tool
Kent, W. J. (2002) · Genome Research · doi:10.1101/gr.229202 · Cited by 8,480
Flagged first, then by citations
Research works printed but not linked: 1
- Soria J. C., Cruz C., Bahleda R., Delord J. P., Horn L., Herbst R. S., Spigel D., Mokatrin A., Fine G., Gettinger S., Clinical activity, safety and biomarkers of PD-L1 blockade in non-small cell lung cancer (NSCLC). Eur. J. Cancer 49 (suppl. 2), 3408 (2013).
Cited by
Sorted by citations
Tumour heterogeneity and resistance to cancer therapies
Dagogo-Jack, I., & Shaw, A. T. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.166 · Cited by 3,846
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
Self-citationClonal 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
Self-citationThe PI3K Pathway in Human Disease
Fruman, D. A., Chiu, H., Hopkins, B. D., Bagrodia, S., Cantley, L. C., & Abraham, R. T. (2017) · Cell · doi:10.1016/j.cell.2017.07.029 · Cited by 2,749
Liquid biopsies come of age: Towards implementation of circulating tumour DNA
Wan, J. C. M., Massie, C., Garcia-Corbacho, J., Mouliere, F., Brenton, J. D., Caldas, C., Pacey, S., Baird, R., & Rosenfeld, N. (2017) · Nature Reviews Cancer · doi:10.1038/nrc.2017.7 · Cited by 2,809
Tracking the Evolution of Non–Small-Cell Lung Cancer
Jamal-Hanjani, M., Wilson, G. A., McGranahan, N., Birkbak, N. J., Watkins, T. B. K., Veeriah, S., Shafi, S., Johnson, D. H., Mitter, R., Rosenthal, R., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1616288 · Cited by 2,349
Self-citationComprehensive genomic profiles of small cell lung cancer
George, J., Lim, J. S., Jang, S. J., Cun, Y., Ozretić, L., Kong, G., Leenders, F., Lu, X. L., Fernandez‐Cuesta, L., Bosco, G., et al. (2015) · Nature · doi:10.1038/nature14664 · Cited by 2,362
Artificial intelligence in cancer imaging: Clinical challenges and applications
Bi, W. L., Hosny, A., Schabath, M. B., Giger, M. L., Birkbak, N. J., Mehrtash, A., Allison, T., Arnaout, O., Abbosh, C., Dunn, I. F., et al. (2019) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21552 · Cited by 1,846
Self-citationThe evolutionary significance of polyploidy
de Peer, Y. V., Mizrachi, E., & Marchal, K. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.26 · Cited by 1,786
Distinct patterns of somatic genome alterations in lung adenocarcinomas and squamous cell carcinomas
Cancer Genome Atlas Research Network, Campbell, J. D., Alexandrov, A., Kim, J., Wala, J., Berger, A. H., Pedamallu, C. S., Shukla, S. A., Guo, G., Brooks, A. N., et al. (2016) · Nature Genetics · doi:10.1038/ng.3564 · Cited by 1,200
Rosenthal, R., McGranahan, N., Herrero, J., Taylor, B. S., & Swanton, C. (2016) · Genome biology · doi:10.1186/s13059-016-0893-4 · Cited by 1,178
Self-citationBiological 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
Self-citationGridelli, C., Rossi, A., Carbone, D. P., Guarize, J., Karachaliou, N., Mok, T. S. K., Petrella, F., Spaggiari, L., & Rosell, R. (2015) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2015.9 · Cited by 1,162
Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy
Skoulidis, F., & Heymach, J. V. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-019-0179-8 · Cited by 1,019
High-Spatial-Resolution Multi-Omics Sequencing via Deterministic Barcoding in Tissue
Liu, Y., Yang, M., Deng, Y., Su, G., Enninful, A., Guo, C. C., Tebaldi, T., Zhang, D., Kim, D., Bai, Z., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.026 · Cited by 966
Hata, A. N., Niederst, M. J., Archibald, H. L., Gomez-Caraballo, M., Siddiqui, F. M., Mulvey, H. E., Maruvka, Y. E., Ji, F., Bhang, H.-E. C., Krishnamurthy Radhakrishna, V., et al. (2016) · Nature Medicine · doi:10.1038/nm.4040 · Cited by 985
Skoulidis, F., Byers, L. A., Diao, L., Papadimitrakopoulou, V. A., Tong, P., Izzo, J., Behrens, C., Kadara, H., Parra, E. R., Canales, J. R., et al. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-14-1236 · Cited by 936
Cancer Stem Cells: Basic Concepts and Therapeutic Implications
Nassar, D., & Blanpain, C. (2016) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044438 · Cited by 904
Mutational landscape and clonal architecture in grade II and III gliomas
Suzuki, H., Aoki, K., Chiba, K., Sato, Y., Shiozawa, Y., Shiraishi, Y., Shimamura, T., Niida, A., Motomura, K., Ohka, F., et al. (2015) · Nature Genetics · doi:10.1038/ng.3273 · Cited by 831
Tumour evolution in hepatocellular carcinoma
Craig, A. J., von Felden, J., García‐Lezana, T., Sarcognato, S., & Villanueva, A. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0229-4 · Cited by 842
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 833
Self-citationChang, M. T., Asthana, S., Gao, S. P., Lee, B. H., Chapman, J. S., Kandoth, C., Gao, J., Socci, N. D., Solit, D. B., Olshen, A. B., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3391 · Cited by 808
High-intensity sequencing reveals the sources of plasma circulating cell-free DNA variants
Razavi, P., Li, B. T., Brown, D. N., Jung, B., Hubbell, E. A., Shen, R., Abida, W. M., Juluru, K., de Bruijn, I., Hou, C., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0652-7 · Cited by 808
Self-citationPascual, J., Attard, G., Bidard, F.-C., Curigliano, G., De Mattos-Arruda, L., Diehn, M., Italiano, A., Lindberg, J., Merker, J. D., Montagut, C., et al. (2022) · Annals of Oncology · doi:10.1016/j.annonc.2022.05.520 · Cited by 783
Pham, D., Tan, X., Balderson, B., Xu, J., Grice, L. F., Yoon, S., Willis, E. F., Tran, M., Lam, P. Y., Raghubar, A. M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-43120-6 · Cited by 757
Kumar, A., Coleman, I. M., Morrissey, C. M., Zhang, X., True, L. D., Gulati, R., Etzioni, R., Bolouri, H., Montgomery, B., White, T. A., et al. (2016) · Nature Medicine · doi:10.1038/nm.4053 · Cited by 747
Neoantigen vaccine: an emerging tumor immunotherapy
Miao, P., Mo, Y., Wang, Y., Wu, P., Zhang, Y., Xiong, F., Guo, C. J., Wu, S., Li, Y., Li, X., et al. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1055-6 · Cited by 711
Lanman, R. B., Mortimer, S. A., Zill, O. A., Sebisanovic, D., Lopez, R., Blau, S., Collisson, E. A., Divers, S. G., Hoon, D. S. B., Kopetz, E. S., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0140712 · Cited by 695
Clonal status of actionable driver events and the timing of mutational processes in cancer evolution
McGranahan, N., Favero, F., de Bruin, E. C., Birkbak, N. J., Szallasi, Z., & Swanton, C. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa1408 · Cited by 685
Self-citationChabon, J. J., Simmons, A. D., Lovejoy, A. F., Esfahani, M. S., Newman, A. M., Haringsma, H. J., Kurtz, D. M., Stehr, H., Scherer, F., Karlovich, C., et al. (2016) · Nature Communications · doi:10.1038/ncomms11815 · Cited by 657
Comprehensive Transcriptional Analysis of Early-Stage Urothelial Carcinoma
Hedegaard, J., Lamy, P., Nordentoft, I., Ferran Algaba, B., Høyer, S., Ulhøi, B. P., Vang, S., Reinert, T., Hermann, G. G., Mogensen, K., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.05.004 · Cited by 641
Identification of neutral tumor evolution across cancer types
Williams, M. J., Werner, B., Barnes, C. P., Graham, T. A., & Sottoriva, A. (2016) · Nature Genetics · doi:10.1038/ng.3489 · Cited by 624
Genomic correlates of response to immune checkpoint blockade in microsatellite-stable solid tumors
Miao, D., Margolis, C. A., Vokes, N. I., Liu, D., Taylor-Weiner, A., Wankowicz, S. M., Adeegbe, D., Keliher, D., Schilling, B., Tracy, A., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0200-2 · Cited by 620
Metastasis as an evolutionary process
Turajlic, S., & Swanton, C. (2016) · Science · doi:10.1126/science.aaf2784 · Cited by 661
Self-citationHendriks, L. E. L., Remón, J., Finn, C. F., Garassino, M. C., Heymach, J. V., Kerr, K. M., Tan, D. S. W., Veronesi, G., & Reck, M. (2024) · Nature Reviews Disease Primers · doi:10.1038/s41572-024-00551-9 · Cited by 690
Overcoming therapy resistance in EGFR-mutant lung cancer
Passaro, A., Jänne, P. A., Mok, T., & Peters, S. (2021) · Nature Cancer · doi:10.1038/s43018-021-00195-8 · Cited by 565
Characterizing genetic intra-tumor heterogeneity across 2,658 human cancer genomes
Dentro, S. C., Leshchiner, I., Haase, K., Tarabichi, M., Wintersinger, J., Deshwar, A. G., Yu, K., Rubanova, Y., Macintyre, G., Demeulemeester, J., et al. (2021) · Cell · doi:10.1016/j.cell.2021.03.009 · Cited by 533
Self-citationSchiavon, G., Hrebien, S., García-Murillas, I., Cutts, R. J., Pearson, A., Tarazona, N., Fenwick, K., Kozarewa, I., López‐Knowles, E., Ribas, R., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aac7551 · Cited by 602
Blakely, C. M., Watkins, T. B. K., Wu, W., Gini, B., Chabon, J. J., McCoach, C. E., McGranahan, N., Wilson, G. A., Birkbak, N. J., Olivas, V. R., et al. (2017) · Nature Genetics · doi:10.1038/ng.3990 · Cited by 571
Self-citationSpatial maps of prostate cancer transcriptomes reveal an unexplored landscape of heterogeneity
Berglund, E., Maaskola, J., Schultz, N., Friedrich, S., Marklund, M., Bergenstråhle, J., Tarish, F., Tanoglidi, A., Vicković, S., Larsson, L., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04724-5 · Cited by 558
Intra-tumour diversification in colorectal cancer at the single-cell level
Roerink, S. F., Sasaki, N., Lee-Six, H., Young, M. D., Alexandrov, L. B., Behjati, S., Mitchell, T. J., Großmann, S., Lightfoot, H. W., Egan, D. A., et al. (2018) · Nature · doi:10.1038/s41586-018-0024-3 · Cited by 558
Self-citationTranslational Implications of Tumor Heterogeneity
Jamal‐Hanjani, M., Quezada, S. A., Larkin, J., & Swanton, C. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-1429 · Cited by 567
Self-citationEnhancing the accuracy of next-generation sequencing for detecting rare and subclonal mutations
Salk, J. J., Schmitt, M. W., & Loeb, L. A. (2018) · Nature Reviews Genetics · doi:10.1038/nrg.2017.117 · Cited by 551
Enabling Technologies for Personalized and Precision Medicine
Ho, D., Quake, S. R., McCabe, E. R. B., Chng, W. J., Chow, E. K., Ding, X., Gelb, B. D., Ginsburg, G. S., Hassenstab, J., Ho, C.-M., et al. (2020) · Trends in Biotechnology · doi:10.1016/j.tibtech.2019.12.021 · Cited by 517
Timing the Landmark Events in the Evolution of Clear Cell Renal Cell Cancer: TRACERx Renal
Mitchell, T. J., Turajlic, S., Rowan, A., Nicol, D. L., Farmery, J. H. R., O’Brien, T., Martincorena, I., Tarpey, P. S., Angelopoulos, N., Yates, L. R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.02.020 · Cited by 522
Self-citationAn evolutionary perspective on field cancerization
Curtius, K., Wright, N. A., & Graham, T. A. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2017.102 · Cited by 540
Genomic landscape of lung adenocarcinoma in East Asians
Chen, J., Yang, H., Teo, A. S. M., Amer, L. B., Sherbaf, F. G., Tan, C. Q., Alvarez, J. J. S., Lu, B., Lim, J. Q., Takano, A. M., et al. (2020) · Nature Genetics · doi:10.1038/s41588-019-0569-6 · Cited by 517
Comparing and contrasting predictive biomarkers for immunotherapy and targeted therapy of NSCLC
Camidge, D. R., Doebele, R. C., & Kerr, K. M. (2019) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0173-9 · Cited by 520
Spatially resolved transcriptomics and beyond
Crosetto, N., Bienko, M., & van Oudenaarden, A. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3832 · Cited by 509
Lee, J. J.-K., Lee, J., Kim, S., Kim, S., Youk, J., Park, S., An, Y., Keam, B., Kim, D., Heo, D. S., et al. (2017) · Journal of Clinical Oncology · doi:10.1200/jco.2016.71.9096 · Cited by 516
Self-citationGenomic and phenotypic heterogeneity in prostate cancer
Haffner, M. C., Zwart, W. T., Roudier, M. P., True, L. D., Nelson, W. G., Epstein, J. I., Marzo, A. M. D., Nelson, P. S., & Yegnasubramanian, S. (2020) · Nature Reviews Urology · doi:10.1038/s41585-020-00400-w · Cited by 544
APOBEC Enzymes: Mutagenic Fuel for Cancer Evolution and Heterogeneity
Swanton, C., McGranahan, N., Starrett, G. J., & Harris, R. S. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0344 · Cited by 492
Self-citationLiquid Biopsies, What We Do Not Know (Yet)
Bardelli, A., & Pantel, K. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.01.002 · Cited by 482
Piotrowska, Z., Niederst, M. J., Karlovich, C., Wakelee, H. A., Neal, J. W., Mino-Kenudson, M. A., Fulton, L. E., Hata, A. N., Lockerman, E. L., Kalsy, A., et al. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0399 · Cited by 467
Odegaard, J. I., Vincent, J. J., Mortimer, S., Vowles, J. V., Ulrich, B. C., Banks, K. C., Fairclough, S. R., Zill, O. A., Sikora, M., Mokhtari, R. B., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-3831 · Cited by 437
Self-citationSpatial genomic heterogeneity in multiple myeloma revealed by multi-region sequencing
Rasche, L., Chavan, S. S., Stephens, O. W., Patel, P. H., Tytarenko, R., Ashby, C., Bauer, M., Stein, C., Deshpande, S., Wardell, C., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00296-y · Cited by 417
Chan, K., Roberts, S. A., Klimczak, L. J., Sterling, J. F., Saini, N., Malc, E. P., Kim, J., Kwiatkowski, D. J., Fargo, D. C., Mieczkowski, P. A., et al. (2015) · Nature Genetics · doi:10.1038/ng.3378 · Cited by 414
Evolutionary Determinants of Cancer
Greaves, M. F. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0439 · Cited by 432
Makohon-Moore, A. P., Zhang, M., Reiter, J. G., Bozic, I., Allen, B., Kundu, D., Chatterjee, K., Wong, F., Jiao, Y., Kohutek, Z. A., et al. (2017) · Nature Genetics · doi:10.1038/ng.3764 · Cited by 403
Lung Cancers: Molecular Characterization, Clonal Heterogeneity and Evolution, and Cancer Stem Cells
Testa, U., Castelli, G., & Pelosi, E. (2018) · Cancers · doi:10.3390/cancers10080248 · Cited by 417
Genomic alterations in lung adenocarcinoma
Devarakonda, S. H. K., Morgensztern, D., & Govindan, R. (2015) · The Lancet Oncology · doi:10.1016/s1470-2045(15)00077-7 · Cited by 423
Spatial and Temporal Heterogeneity in High-Grade Serous Ovarian Cancer: A Phylogenetic Analysis
Schwarz, R. F., Ng, C. K. Y., Cooke, S. L., Newman, S., Temple, J., Piskorz, A., Gale, D. G., Sayal, K., Murtaza, M., Baldwin, P., et al. (2015) · PLoS Medicine · doi:10.1371/journal.pmed.1001789 · Cited by 403
Determinants and clinical implications of chromosomal instability in cancer
Sansregret, L., Vanhaesebroeck, B., & Swanton, C. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.198 · Cited by 411
Self-citationLindskrog, S. V., Prip, F., Lamy, P., Taber, A., Groeneveld, C. S., Birkenkamp‐Demtröder, K., Jensen, J. B., Strandgaard, T., Nordentoft, I., Christensen, E., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22465-w · Cited by 389
Tracking the origins and drivers of subclonal metastatic expansion in prostate cancer
Hong, M. K. H., Macintyre, G., Wedge, D. C., Loo, P. V., Patel, K., Lunke, S., Alexandrov, L. B., Sloggett, C., Cmero, M., Marass, F., et al. (2015) · Nature Communications · doi:10.1038/ncomms7605 · Cited by 367
Self-citationSala, E., Mema, E., Himoto, Y., Veeraraghavan, H., Brenton, J. D., Snyder, A., Weigelt, B., & Vargas, H. A. (2016) · Clinical Radiology · doi:10.1016/j.crad.2016.09.013 · Cited by 369
Ling, S., Hu, Z., Yang, Z., Yang, F., Li, Y., Lin, P., Chen, K., Dong, L., Cao, L., Tao, Y., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1519556112 · Cited by 355
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 371
Spatial Heterogeneity in the Tumor Microenvironment
Yuan, Y. (2016) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a026583 · Cited by 342
Refining the treatment of NSCLC according to histological and molecular subtypes
Thomas, A., Liu, S. V., Subramaniam, D. S., & Giaccone, G. (2015) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2015.90 · Cited by 323
Intra-tumor heterogeneity of cancer cells and its implications for cancer treatment
Sun, X., & Yu, Q. (2015) · Acta Pharmacologica Sinica · doi:10.1038/aps.2015.92 · Cited by 322
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 329
The evolution of lung cancer and impact of subclonal selection in TRACERx
Frankell, A. M., Dietzen, M., Bakir, M. A., Lim, E. L., Karasaki, T., Ward, S., Veeriah, S., Colliver, E., Huebner, A., Bunkum, A., et al. (2023) · Nature · doi:10.1038/s41586-023-05783-5 · Cited by 329
Self-citationMetabolic interventions in the immune response to cancer
O’Sullivan, D., Sanin, D. E., Pearce, E. J., & Pearce, E. L. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0140-9 · Cited by 320
Heterogeneity of the tumor immune microenvironment and its clinical relevance
Jia, Q., Wang, A., Yuan, Y., Zhu, B., & Long, H. (2022) · Experimental Hematology and Oncology · doi:10.1186/s40164-022-00277-y · Cited by 332
Pan-cancer analysis of intratumor heterogeneity as a prognostic determinant of survival
Morris, L. G. T., Riaz, N., Desrichard, A., Şenbabaoğlu, Y., Hakimi, A. A., Makarov, V., Reis-Filho, J. S., & Chan, T. A.-T. (2016) · Oncotarget · doi:10.18632/oncotarget.7067 · Cited by 307
Parkinson, C., Gale, D. G., Piskorz, A., Biggs, H., Hodgkin, C., Addley, H. C., Freeman, S., Moyle, P., Sala, E., Sayal, K., et al. (2016) · PLoS Medicine · doi:10.1371/journal.pmed.1002198 · Cited by 299
Therapy-induced mutations drive the genomic landscape of relapsed acute lymphoblastic leukemia
Li, B., Brady, S. W., Ma, X., Shen, S., Zhang, Y., Li, Y., Szlachta, K. A., Dong, L., Liu, Y., Yang, F., et al. (2019) · Blood · doi:10.1182/blood.2019002220 · Cited by 291
Simpson, S., Dunning, M., de Brot, S., Grau‐Roma, L., Mongan, N. P., & Rutland, C. S. (2017) · Acta veterinaria Scandinavica · doi:10.1186/s13028-017-0341-9 · Cited by 304
Lee, G., Lee, H. Y., Park, H., Schiebler, M. L., van Beek, E. J. R., Ohno, Y., Seo, J. B., & Leung, A. N. C. (2016) · European Journal of Radiology · doi:10.1016/j.ejrad.2016.09.005 · Cited by 281
Polytherapy and Targeted Cancer Drug Resistance
Chatterjee, N., & Bivona, T. G. (2019) · Trends in cancer · doi:10.1016/j.trecan.2019.02.003 · Cited by 277
Clinical Implications of Genomic Discoveries in Lung Cancer
Swanton, C., & Govindan, R. (2016) · New England Journal of Medicine · doi:10.1056/nejmra1504688 · Cited by 274
Self-citationThe Role of Aneuploidy in Cancer EvolutionPreprint
Sansregret, L., & Swanton, C. (2016) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a028373 · Cited by 272
Self-citationCytokinesis defects and cancer
Lens, S. M. A., & Medema, R. H. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0084-6 · Cited by 276
Clonal expansion in non-cancer tissues
Kakiuchi, N., & Ogawa, S. (2021) · Nature Reviews Cancer · doi:10.1038/s41568-021-00335-3 · Cited by 252
Schultheis, A. M., Ng, C. K. Y., Filippo, M. R. D., Piscuoglio, S., Macedo, G. S., Gatius, S., Perez‐Mies, B., Soslow, R. A., Lim, R. S., Viale, A. J., et al. (2015) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djv427 · Cited by 257
Hao, J., Lin, D., Dinh, H. Q., Mayakonda, A., Jiang, Y., Chen, C., Jiang, Y., Lü, C., Shi, Z., Xu, X., et al. (2016) · Nature Genetics · doi:10.1038/ng.3683 · Cited by 259
Functions and consequences of AID/APOBEC-mediated DNA and RNA deamination
Pecori, R., Giorgio, S. D., Lorenzo, J. P., & Papavasiliou, F. N. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00459-8 · Cited by 262
The evolution of non-small cell lung cancer metastases in TRACERx
Bakir, M. A., Huebner, A., Martínez‐Ruiz, C., Grigoriadis, K., Watkins, T. B. K., Pich, O., Moore, D. A., Veeriah, S., Ward, S., Laycock, J., et al. (2023) · Nature · doi:10.1038/s41586-023-05729-x · Cited by 263
Self-citationCancer evolution: Darwin and beyond
Vendramin, R., Litchfield, K., & Swanton, C. (2021) · The EMBO Journal · doi:10.15252/embj.2021108389 · Cited by 269
Self-citationThe Evolutionary Landscape of Localized Prostate Cancers Drives Clinical Aggression
Espiritu, S. M. G., Liu, L., Rubanova, Y., Bhandari, V., Holgersen, E. M., Szyca, L., Fox, N. S., Chua, M. L. K., Yamaguchi, T. N., Heisler, L. E., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.029 · Cited by 251
Cancer Evolution and the Limits of Predictability in Precision Cancer Medicine
Lipinski, K. A., Barber, L. J., Davies, M. N., Ashenden, M., Sottoriva, A., & Gerlinger, M. (2016) · Trends in cancer · doi:10.1016/j.trecan.2015.11.003 · Cited by 256
Self-citationTracking the Genomic Evolution of Esophageal Adenocarcinoma through Neoadjuvant Chemotherapy
Murugaesu, N., Wilson, G. A., Birkbak, N. J., Watkins, T. B. K., McGranahan, N., Kumar, S., Abbassi‐Ghadi, N., Salm, M., Mitter, R., Horswell, S. D., et al. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0412 · Cited by 246
Self-citationGenomic and immune profiling of pre-invasive lung adenocarcinoma
Chen, H., Carrot‐Zhang, J., Zhao, Y., Hu, H., Freeman, S. S., Yu, S. J., Ha, G., Taylor, A. M., Berger, A. C., Westlake, L. C., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13460-3 · Cited by 246
Paweletz, C. P., Sacher, A. G., Raymond, C. K., Alden, R. S., O’Connell, A., Mach, S. L., Kuang, Y., Gandhi, L., Kirschmeier, P. T., English, J. M., et al. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-1627-t · Cited by 243
Choi, W., Ochoa, A. E., McConkey, D. J., Aine, M., Höglund, M., Kim, W. Y., Real, F. X., Kiltie, A. E., Milsom, I., Dyrskjøt, L., et al. (2017) · European Urology · doi:10.1016/j.eururo.2017.03.010 · Cited by 236
Rodak, O., Peris‐Díaz, M. D., Olbromski, M., Podhorska‐Okołów, M., & Dzięgiel, P. (2021) · Cancers · doi:10.3390/cancers13184705 · Cited by 250
Fast and scalable inference of multi-sample cancer lineages
Popic, V., Salari, R., Hajirasouliha, I., Kashef-Haghighi, D., West, R. B., & Batzoglou, S. (2015) · Genome biology · doi:10.1186/s13059-015-0647-8 · Cited by 231
Patient-derived micro-organospheres enable clinical precision oncology
Ding, S., Hsu, C., Wang, Z., Natesh, N. R., Millen, R., Negrete, M., Giroux, N., Rivera, G. O., Dohlman, A., Bose, S., et al. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2022.04.006 · Cited by 228
Zheng, D., Ye, X.-R., Zhang, M. Z., Sun, Y., Wang, J. Y., Ni, J., Zhang, H. P., Zhang, L., Luo, J., Zhang, J., et al. (2016) · Scientific Reports · doi:10.1038/srep20913 · Cited by 229
Metadata
- Authors
- de Bruin, E. C., McGranahan, N., Mitter, R., Salm, M., Wedge, D. C., Yates, L., Jamal-Hanjani, M., Shafi, S., Murugaesu, N., Rowan, A. J., Grönroos, E., Muhammad, M. A., Horswell, S., Gerlinger, M., Varela, I., Jones, D., Marshall, J., Voet, T., Van Loo, P., Rassl, D. M., Rintoul, R. C., Janes, S. M., Lee, S.-M., Forster, M., Ahmad, T., Lawrence, D., Falzon, M., Capitanio, A., Harkins, T. T., Lee, C. C., Tom, W., Teefe, E., Chen, S.-C., Begum, S., Rabinowitz, A., Phillimore, B., Spencer-Dene, B., Stamp, G., Szallasi, Z., Matthews, N., Stewart, A., Campbell, P., & Swanton, C.
- Affiliations
- Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London WC1E 6BT, UK.
- Cancer Research UK (GB)
- Wellcome Sanger Institute (GB)
- University of Cambridge (GB)
- Cancer Research UK London Research Institute, London WC2A 3LY, UK.
- Universidad de Cantabria (ES)
- Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK.
- Papworth Hospital NHS Foundation Trust (GB)
- University College London (GB)
- Thermo Fisher Scientific (United States) (US)
- Technical University of Denmark, 2800 Kongens Lyngby, Denmark.
- Corresponding author
- McGranahan, Nicholas
- Mitter, Richard
- Salm, Max
- Wedge, David C.
- Yates, Lucy
- Swanton, Charles
- ORCID
- McGranahan, Nicholas
- Mitter, Richard
- Salm, Max
- Wedge, David C.
- Yates, Lucy
- Murugaesu, Nirupa
- Rowan, Andrew J.
- Horswell, Stuart
- Gerlinger, Marco
- Varela, Ignacio
- Jones, David
- Voet, Thierry
- Rassl, Doris M.
- Rintoul, Robert C.
- Janes, Sam M.
- Lee, Siow-Ming
- Forster, Martin
- Lawrence, David
- Falzon, Mary
- Capitanio, Arrigo
- Harkins, Timothy T.
- Lee, Clarence C.
- Teefe, Enock
- Begum, Sharmin
- Rabinowitz, Adam
- Stamp, Gordon
- Matthews, Nik
- Campbell, Peter
- Swanton, Charles
- Venue
- Science
- Published
- 2014-10-10
- Volume
- 346
- Issue
- 6206
- Pages
- 251-256
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2108371618
- Cited by
- 1,117
- References
- 62
- Citations by year
- 2026: 38 · 2025: 43 · 2024: 59 · 2023: 82 · 2022: 82 · 2021: 86 · 2020: 99 · 2019: 113 · 2018: 111 · 2017: 145 · 2016: 131 · 2015: 119 · 2014: 9
- FWCI
- 43.17
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- other-oa
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- UCrea (University of Cantabria) (acceptedVersion, other-oa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- Prostate Cancer Foundation
- Breast Cancer Research Foundation
- Wellcome Trust (091730, 105104, 088340)
- Cancer Research UK (259303, A11590, A4688, A17786, 17001, A19310, 17786, 18377)
- National Institute for Health and Care Research (CL-2011-18-001)
- Academy of Medical Sciences (AMS-SGCL7-Murugaesu)
- University College London
- European Commission (259303)
- Rosetrees Trust (M35-F1-CD1)
- Fonds Wetenschappelijk Onderzoek
- Ministerio de Economía y Competitividad
- Vlaamse regering
- National Institutes of Health
- Medical Research Council
- NIHR Cambridge Biomedical Research Centre
- National Cancer Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- non-small cell lung cancer, tumor evolution, intratumoral heterogeneity, driver mutations, copy number alterations, chromosomal translocation, APOBEC mutational signature, genome doubling, tumor latency, carcinogen exposure, genomic instability
- MeSH terms
- APOBEC-1 Deaminase, Carcinogens, Carcinoma, Non-Small-Cell Lung, Cytidine Deaminase, Humans, Lung Neoplasms, Mutation, Neoplasm Recurrence, Local, Prognosis, Smoking, Translocation, Genetic, Tumor Cells, Cultured, Gene Dosage, Genetic Heterogeneity, Evolution, Molecular, Genomic Instability
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 ›
Are you an author, or do you see a problem with this page? Request a review
