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.
Integrity signals
Registry
Cites
Statistics
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?
There is evidence that APOBEC-mediated mutagenesis fuels sub-clonal diversification and branched evolution.
“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]
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 · see citing works
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 · see citing works
Estimating the Dimension of a Model
Schwarz, G. (1978) · The Annals of Statistics · doi:10.1214/aos/1176344136 · Cited by 47,033 · see citing works
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr121 · Cited by 39,795 · see citing works
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 14,380 · see citing works
Siegel, R., Naishadham, D., & Jemal, A. (2013) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21166 · Cited by 11,825 · see citing works
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 10,838 · see citing works
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 · see citing works
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
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 · 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
Self-citationComprehensive genomic characterization defines human glioblastoma genes and core pathways
The Cancer Genome Atlas Research Network (2008) · Nature · doi:10.1038/nature07385 · Cited by 7,735 · see citing works
VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencingPreprint
Koboldt, D. C., Zhang, Q., Larson, D. E., Shen, D., McLellan, M. D., Lin, L., Miller, C. A., Mardis, E. R., Ding, L., & Wilson, R. K. (2012) · Genome Research · doi:10.1101/gr.129684.111 · Cited by 4,822 · see citing works
Comprehensive genomic characterization of squamous cell lung cancers
The Cancer Genome Atlas Research Network (2012) · Nature · doi:10.1038/nature11404 · Cited by 3,994 · see citing works
Self-citationEpidermal growth factor receptor mutations in lung cancer
Sharma, S. V., Bell, D. W., Settleman, J., & Haber, D. A. (2007) · Nature Reviews Cancer · doi:10.1038/nrc2088 · Cited by 3,170 · see citing works
Discovery and saturation analysis of cancer genes across 21 tumour types
Lawrence, M. S., Stojanov, P., Mermel, C. H., Robinson, J. T., Garraway, L. A., Golub, T. R., Meyerson, M., Gabriel, S. B., Lander, E. S., & Getz, G. (2014) · Nature · doi:10.1038/nature12912 · Cited by 3,096 · see citing works
Somatic mutations affect key pathways in lung adenocarcinoma
Ding, L., Getz, G., Wheeler, D. A., Mardis, E. R., McLellan, M. D., Cibulskis, K., Sougnez, C., Greulich, H., Muzny, D. M., Morgan, M. B., et al. (2008) · Nature · doi:10.1038/nature07423 · Cited by 2,681 · see citing works
The causes and consequences of genetic heterogeneity in cancer evolution
Burrell, R. A., McGranahan, N., Bartek, J., & Swanton, C. (2013) · Nature · doi:10.1038/nature12625 · Cited by 2,262 · see citing works
Self-citationAbsolute quantification of somatic DNA alterations in human cancer
Carter, S. L., Cibulskis, K., Helman, E., McKenna, A., Shen, H., Zack, T. I., Laird, P. W., Onofrio, R. C., Winckler, W., Weir, B. A., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2203 · Cited by 2,003 · see citing works
Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing
Ding, L., Ley, T. J., Larson, D. E., Miller, C. A., Koboldt, D. C., Welch, J. S., Ritchey, J. K., Young, M. A., Lamprecht, T., McLellan, M. D., et al. (2012) · Nature · doi:10.1038/nature10738 · Cited by 1,993 · see citing works
Ye, K., Schulz, M. H., Long, Q., Apweiler, R., & Ning, Z. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp394 · Cited by 1,978 · 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
The DNA damage response and cancer therapy
Lord, C. J., & Ashworth, A. (2012) · Nature · doi:10.1038/nature10760 · Cited by 1,843 · see citing works
Mapping the Hallmarks of Lung Adenocarcinoma with Massively Parallel Sequencing
Imielinski, M., Berger, A. H., Hammerman, P. S., Hernandez, B., Pugh, T. J., Hodis, E., Cho, J., Suh, J., Capelletti, M., Sivachenko, A., et al. (2012) · Cell · doi:10.1016/j.cell.2012.08.029 · Cited by 1,789 · see citing works
The landscape of cancer genes and mutational processes in breast cancer
Stephens, P. J., Tarpey, P. S., Davies, H. R., Loo, P. V., Greenman, C., Wedge, D. C., Nik‐Zainal, S., Martin, S., Varela, I., Bignell, G. R., et al. (2012) · Nature · doi:10.1038/nature11017 · Cited by 1,686 · see citing works
Self-citationThe Life History of 21 Breast Cancers
Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., Raine, K., Jones, D., Marshall, J., Ramakrishna, M., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.023 · Cited by 1,443 · see citing works
Self-citationPunctuated Evolution of Prostate Cancer Genomes
Baca, S. C., Prandi, D., Lawrence, M. S., Mosquera, J. M., Romanel, A., Drier, Y., Park, K., Kitabayashi, N., MacDonald, T. Y., Ghandi, M., et al. (2013) · Cell · doi:10.1016/j.cell.2013.03.021 · Cited by 1,300 · see citing works
Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma
Varela, I., Tarpey, P. S., Raine, K. M., Huang, D., Ong, C. K., Stephens, P., Davies, H. R., Jones, D., Lin, M., Teague, J. W., et al. (2011) · Nature · doi:10.1038/nature09639 · Cited by 1,278 · see citing works
Self-citationAllele-specific copy number analysis of tumors
Loo, P. V., Nord, S., Lingjærde, O. C., Russnes, H. G., Rye, I. H., Sun, W., Weigman, V., Marynen, P., Zetterberg, A., Naume, B., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009843107 · Cited by 1,231 · see citing works
Somatic<i>SF3B1</i>Mutation in Myelodysplasia with Ring Sideroblasts
Papaemmanuil, E., Cazzola, M., Boultwood, J., Malcovati, L., Vyas, P., Bowen, D., Pellagatti, A., Wainscoat, J. S., Hellstrom-Lindberg, E., Gambacorti-Passerini, C., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1103283 · Cited by 1,222 · see citing works
Self-citationGerlinger, 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
Self-citationAn 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
Genomic Landscape of Non-Small Cell Lung Cancer in Smokers and Never-Smokers
Govindan, R., Ding, L., Griffith, M., Subramanian, J., Dees, N. D., Kanchi, K., Maher, C. A., Fulton, R. S., Fulton, L., Wallis, J. W., et al. (2012) · Cell · doi:10.1016/j.cell.2012.08.024 · Cited by 1,144 · see citing works
Characterizing the cancer genome in lung adenocarcinoma
Weir, B. A., Woo, M. S., Getz, G., Perner, S., Ding, L., Beroukhim, R., Lin, W. M., Province, M. A., Kraja, A., Johnson, L. A., et al. (2007) · Nature · doi:10.1038/nature06358 · Cited by 1,105 · see citing works
A small-cell lung cancer genome with complex signatures of tobacco exposure
Pleasance, E., Stephens, P. J., O’Meara, S., McBride, D. J., Meynert, A. M., Jones, D., Lin, M., Beare, D. M., Lau, K. W., Greenman, C., et al. (2009) · Nature · doi:10.1038/nature08629 · Cited by 1,067 · see citing works
Self-citationDiverse somatic mutation patterns and pathway alterations in human cancers
Kan, Z., Jaiswal, B. S., Stinson, J., Janakiraman, V., Bhatt, D., Stern, H. M., Yue, P., Haverty, P. M., Bourgon, R., Zheng, J., et al. (2010) · Nature · doi:10.1038/nature09208 · Cited by 1,018 · see citing works
Acquired Resistance and Clonal Evolution in Melanoma during BRAF Inhibitor Therapy
Shi, H., Hugo, W., Kong, X., Hong, A., Koya, R. C., Moriceau, G., Chodon, T., Guo, R., Johnson, D. B., Dahlman, K. B., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0642 · Cited by 982 · see citing works
Heterogeneity of genomic evolution and mutational profiles in multiple myeloma
Bolli, N., Avet-Loiseau, H., Wedge, D. C., Van Loo, P., Alexandrov, L. B., Martincorena, I., Dawson, K. J., Iorio, F., Nik-Zainal, S., Bignell, G. R., et al. (2014) · Nature Communications · doi:10.1038/ncomms3997 · Cited by 875 · see citing works
Self-citationPhosphatidylinositol 3-kinase mutations identified in human cancer are oncogenic
Kang, S., Bader, A. G., & Vogt, P. K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408864102 · Cited by 827 · see citing works
dbNSFP: A lightweight database of human nonsynonymous SNPs and their functional predictions
Liu, X., Jian, X., & Boerwinkle, E. (2011) · Human Mutation · doi:10.1002/humu.21517 · Cited by 816 · see citing works
Davoli, T., Xu, A. W., Mengwasser, K. E., Sack, L. M., Yoon, J. C., Park, P. J., & Elledge, S. J. (2013) · Cell · doi:10.1016/j.cell.2013.10.011 · Cited by 815 · 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
Management of non-small-cell lung cancer: recent developments
Reck, M., Heigener, D. F., Mok, T. S. K., Soria, J., & Rabe, K. F. (2013) · The Lancet · doi:10.1016/s0140-6736(13)61502-0 · Cited by 714 · see citing works
Sequence-specific error profile of Illumina sequencers
Nakamura, K., Oshima, T., Morimoto, T., Ikeda, S., Yoshikawa, H., Shiwa, Y., Ishikawa, S., Linak, M. C., Hirai, A. M., Takahashi, H., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr344 · Cited by 593 · see citing works
McKernan, K. J., Peckham, H. E., Costa, G. L., McLaughlin, S. F., Fu, Y., Tsung, E. F., Clouser, C. R., Duncan, C., Ichikawa, J. K., Lee, C. C., et al. (2009) · Genome Research · doi:10.1101/gr.091868.109 · Cited by 529 · see citing works
Self-citationThe mutation spectrum revealed by paired genome sequences from a lung cancer patient
Lee, W., Jiang, Z., Liu, J., Haverty, P. M., Guan, Y., Stinson, J., Yue, P., Zhang, Y., Pant, K. P., Bhatt, D., et al. (2010) · Nature · doi:10.1038/nature09004 · Cited by 486 · see citing works
CREST maps somatic structural variation in cancer genomes with base-pair resolution
Wang, J., Mullighan, C. G., Easton, J. B., Roberts, S., Heatley, S. L., Ma, J., Rusch, M., Chen, K., Harris, C. C., Ding, L., et al. (2011) · Nature Methods · doi:10.1038/nmeth.1628 · Cited by 485 · see citing works
Chromosomal Instability Confers Intrinsic Multidrug Resistance
Lee, A. J. X., Endesfelder, D., Rowan, A., Walther, A., Birkbak, N. J., Futreal, P. A., Downward, J., Szállási, Z., Tomlinson, I. P. M., Howell, M. T., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-3604 · Cited by 466 · see citing works
Self-citationDewhurst, S. M., McGranahan, N., Burrell, R. A., Rowan, A., Gronroos, E. C., Endesfelder, D., Joshi, T., Mouradov, D., Gibbs, P., Ward, R. L., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0285 · Cited by 450 · see citing works
Self-citationEnd-joining, translocations and cancer
Bunting, S. F., & Nussenzweig, A. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3537 · Cited by 359 · see citing works
Diverse Mechanisms of Somatic Structural Variations in Human Cancer Genomes
Yang, L., Luquette, L. J., Gehlenborg, N., Xi, R., Haseley, P. S., Hsieh, C.-H., Zhang, C., Ren, X., Protopopov, A. I., Chin, L., et al. (2013) · Cell · doi:10.1016/j.cell.2013.04.010 · Cited by 338 · see citing works
Self-citationCopynumber: Efficient algorithms for single- and multi-track copy number segmentation
Nilsen, G., Liestøl, K., Loo, P. V., Vollan, H. K. M., Brodtkorb, M., Rueda, O. M., Chin, S., Russell, R., Baumbusch, L. O., Caldas, C., et al. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-591 · Cited by 302 · see citing works
Mad2-induced chromosome instability leads to lung tumour relapse after oncogene withdrawal
Sotillo, R., Schvartzman, J. M., Socci, N. D., & Benezra, R. (2010) · Nature · doi:10.1038/nature08803 · Cited by 273 · see citing works
Chromothripsis and beyond: rapid genome evolution from complex chromosomal rearrangementsPreprint
Zhang, C.-Z., Leibowitz, M. L., & Pellman, D. (2013) · Genes & Development · doi:10.1101/gad.229559.113 · Cited by 241 · see citing works
Lineage-Specific Dependency of Lung Adenocarcinomas on the Lung Development Regulator TTF-1
Tanaka, H., Yanagisawa, K., Shinjo, K., Taguchi, A., Maeno, K., Tomida, S., Shimada, Y., Osada, H., Kosaka, T., Matsubara, H., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4774 · Cited by 216 · see citing works
Malhotra, A., Lindberg, M. R., Faust, G. G., Leibowitz, M. L., Clark, R. A., Layer, R. M., Quinlan, A. R., & Hall, I. M. (2013) · Genome Research · doi:10.1101/gr.143677.112 · Cited by 171 · see citing works
Bengtsson, H. L., Wirapati, P., & Speed, T. P. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp371 · Cited by 136 · see citing works
Yau, C., Mouradov, D., Jorissen, R. N., Colella, S., Mirza, G. K., Steers, G., Harris, A. L., Ragoussis, J., Sieber, O. M., & Holmes, C. C. (2010) · Genome biology · doi:10.1186/gb-2010-11-9-r92 · Cited by 129 · see citing works
TIGRA: A targeted iterative graph routing assembler for breakpoint assemblyPreprint
Chen, K., Chen, L., Fan, X., Wallis, J. W., Ding, L., & Weinstock, G. M. (2013) · Genome Research · doi:10.1101/gr.162883.113 · Cited by 90 · see citing works
On the origin of G→T transversions in lung cancer
Pfeifer, G. P., & Hainaut, P. L. (2003) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(03)00013-7 · Cited by 86 · see citing works
Bengtsson, H. L., Neuvial, P., & Speed, T. P. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-245 · Cited by 54 · see citing works
Ortiz-Estévez, M., Aramburu, A., Bengtsson, H. L., Neuvial, P., & Rubio, Á. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts248 · Cited by 19 · see citing works
Flagged first, then by citations
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 · 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
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 2,322 · see citing works
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 · see citing works
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 1,738 · see citing works
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 · see citing works
Rosenthal, R., McGranahan, N., Herrero, J., Taylor, B. S., & Swanton, C. (2016) · Genome biology · doi:10.1186/s13059-016-0893-4 · Cited by 1,217 · see citing works
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 · see citing works
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 1,121 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 869 · see citing works
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 · see citing works
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 825 · 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
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 · see citing works
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 795 · see citing works
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 · see citing works
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 716 · see citing works
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 732 · see citing works
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 701 · see citing works
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 · see citing works
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 · see citing works
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 647 · see citing works
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 639 · see citing works
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 628 · see citing works
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 · see citing works
Metastasis as an evolutionary process
Turajlic, S., & Swanton, C. (2016) · Science · doi:10.1126/science.aaf2784 · Cited by 661 · see citing works
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 672 · see citing works
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 · see citing works
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 · see citing works
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 589 · see citing works
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 · see citing works
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 550 · see citing works
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 554 · see citing works
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 549 · see citing works
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 536 · see citing works
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 · see citing works
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 502 · see citing works
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 533 · see citing works
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 511 · see citing works
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 514 · see citing works
Spatially resolved transcriptomics and beyond
Crosetto, N., Bienko, M., & van Oudenaarden, A. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3832 · Cited by 509 · see citing works
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 506 · see citing works
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 520 · see citing works
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 480 · see citing works
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 · see citing works
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 459 · see citing works
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 · see citing works
Self-citationChan, 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 · see citing works
Evolutionary Determinants of Cancer
Greaves, M. F. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0439 · Cited by 411 · see citing works
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 · see citing works
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 406 · see citing works
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 398 · see citing works
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 · see citing works
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 396 · see citing works
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 · see citing works
Lindskrog, 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 384 · see citing works
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 · see citing works
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 · see citing works
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 · 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
Spatial Heterogeneity in the Tumor Microenvironment
Yuan, Y. (2016) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a026583 · Cited by 342 · see citing works
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 320 · see citing works
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 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
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 322 · see citing works
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 314 · see citing works
Heterogeneity of the tumor immune microenvironment and its clinical relevance
Jia, Q., Wang, A., Yuan, Y.-X., Zhu, B., & Long, H.-X. (2022) · Experimental Hematology & Oncology · doi:10.1186/s40164-022-00277-y · Cited by 236 · see citing works
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 297 · see citing works
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 · see citing works
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 289 · see citing works
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 294 · see citing works
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 277 · see citing works
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 271 · see citing works
Clinical Implications of Genomic Discoveries in Lung Cancer
Swanton, C., & Govindan, R. (2016) · New England Journal of Medicine · doi:10.1056/nejmra1504688 · Cited by 271 · see citing works
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 264 · see citing works
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 266 · see citing works
Clonal expansion in non-cancer tissues
Kakiuchi, N., & Ogawa, S. (2021) · Nature Reviews Cancer · doi:10.1038/s41568-021-00335-3 · Cited by 252 · see citing works
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 · see citing works
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 257 · see citing works
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 254 · see citing works
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 259 · see citing works
Self-citationCancer evolution: Darwin and beyond
Vendramin, R., Litchfield, K., & Swanton, C. (2021) · The EMBO Journal · doi:10.15252/embj.2021108389 · Cited by 253 · see citing works
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 250 · see citing works
Cancer Evolution and the Limits of Predictability in Precision Cancer Medicine
Lipiński, K., Barber, L., Davies, M., Ashenden, M., Sottoriva, A., & Gerlinger, M. (2016) · Trends in Cancer · doi:10.1016/j.trecan.2015.11.003 · Cited by 248 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 234 · see citing works
Rodak, O., Peris‐Díaz, M. D., Olbromski, M., Podhorska‐Okołów, M., & Dzięgiel, P. (2021) · Cancers · doi:10.3390/cancers13184705 · Cited by 237 · see citing works
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 · see citing works
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 · see citing works
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 224 · see citing works
- 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