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The Clonal Evolution of Tumor Cell Populations: Acquired genetic lability permits stepwise selection of variant sublines and underlies tumor progression.
Abstract
It is proposed that most neoplasms arise from a single cell of origin, and tumor progression results from acquired genetic variability within the original clone allowing sequential selection of more aggressive sublines. Tumor cell populations are apparently more genetically unstable than normal cells, perhaps from activation of specific gene loci in the neoplasm, continued presence of carcinogen, or even nutritional deficiencies within the tumor. The acquired genetic insta0ility and associated selection process, most readily recognized cytogenetically, results in advanced human malignancies being highly individual karyotypically and biologically. Hence, each patient's cancer may require individual specific therapy, and even this may be thwarted by emergence of a genetically variant subline resistant to the treatment. More research should be directed toward understanding and controlling the evolutionary process in tumors before it reaches the late stage usually seen in clinical cancer.
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“Mutations enabling rapid proliferation are selected positively in cancers because they accelerate the emergence of aggressive phenotypes through somatic evolution.1,2”
From Dynamic IL-6R/STAT3 signaling leads to heterogeneity of metabolic phenotype in pancreatic ductal adenocarcinoma cells (2024) · cites this paper as [2]
Citations
Cites
Mutation selection and the natural history of cancer
Cairns, J. (1975) · Nature · doi:10.1038/255197a0 · Cited by 1,592
Normal genetically mosaic mice produced from malignant teratocarcinoma cells.
Mintz, B., & Illmensee, K. (1975) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.72.9.3585 · Cited by 1,179
Handbuch der allgemeinen pathologie
(1973) · Experimental Gerontology · doi:10.1016/0531-5565(73)90021-1 · Cited by 794
Glucose-6-Phosphate Dehydrogenase Mosaicism: Utilization as a Cell Marker in the Study of Leiomyomas
Linder, D., & Gartler, S. M. (1965) · Science · doi:10.1126/science.150.3692.67 · Cited by 398
Differentiation of malignant to benign cells
Kauffman, S. A. (1971) · Journal of Theoretical Biology · doi:10.1016/0022-5193(71)90020-8 · Cited by 309
Suppression of malignancy in human cells
Stanbridge, E. J. (1976) · Nature · doi:10.1038/260017a0 · Cited by 307
Methodology in mammalian genetics
Burdette, W. J. (1963) · Holden-Day eBooks · doi:10.5962/bhl.title.6428 · Cited by 302
LEVAN, A., Levan, G., & Mitelman, F. (2009) · Hereditas · doi:10.1111/j.1601-5223.1977.tb01208.x · Cited by 263
The analysis of malignancy by cell fusion: I. hybrids between tumour cells and l cell derivatives
Klein, G., Bregula, U., Wiener, F., & Harris, H. (1971) · Journal of Cell Science · doi:10.1242/jcs.8.3.659 · Cited by 248
Neoplasia: a disease of cell differentiation.
Markert, C. L. (1968) · PubMed · Cited by 244
Research works printed but not linked: 24
- ALSAADI, A, SEQUENTIAL CYTOGENETIC CHANGES IN EVOLUTION OFTRANSPLANTED THYROID TUMORS IN METASTATIC CARCINOMA IN FICHER RAT, CANCER RESEARCH 27: 1831 (1967).
- BOYSE, E.A., CURRENT RES ONCOLOGY: 57 (1972).
- DIPAOLO, J.A., KARYOLOGICAL INSTABILITY OF NEOPLASTIC SOMATIC-CELLS, IN VITRO-JOURNAL OF THE TISSUE CULTURE ASSOCIATION 11: 89 (1975).
- FOLKMAN, J, S FUNDAMENTAL ASPECT: 331 (1975).
- FURTH, J, NATIONAL CANCER INSTITUTE MONOGRAPHS 2: 148 (1960).
- GERMAN, J, GENES WHICH INCREASE CHROMOSOMAL INSTABILITY IN SOMATIC CELLS AND PREDISPOSE TO CANCER, PROGRESS IN MEDICAL GENETICS 8: 61 (1972).
- GOLUB, S.H., CANCER COMPREHENSIVE 4: 259 (1975).
- GROUCHY, J.D., CHROMOSOMES CANCER: 287 (1974).
- HANDEN, D.G., CHROMOSOMES CANCER: 151 (1974).
- KLEIN, G, METHODOLOGY MAMMALIA: 407 (1963).
- KNUDSON, A.G., HEREDITY AND CANCER IN MAN, PROGRESS IN MEDICAL GENETICS 9: 113 (1973).
- MAKINO, S, ANN N Y ACAD SCI 64: 818 (1956).
- Miller, E. C., The Molecular Biology of Cancer: 377 (1974).
- NOWELL, P.C., CANCER COMPREHENSIVE 1: 3 (1975).
- NOWELL, P.C., CHROMOSOMES CANCER J: 267 (1974).
- ODELL, W, TXB ENDOCRINOLOGY: 1105 (1974).
- Oksala, T., Chromosomes and Cancer: 239 (1974).
- Pedersen, B., Proceedings of the Fourth International Congress on Human Genetics: 166 (1972).
- Pitot, H. C., Molecular Biology of Cancer: 523 (1974).
- Robbins, J. C., Cancer: A Comprehensive Treatise 4: 3 (1975).
- RUBIN, H, SCIENCE 191: 241 (1976). · DOI
- STICH, H.F., CANADIAN CANCER CONFERENCE 5: 99 (1963).
- WOLMAN, S.R., CANCER COMPREHENSIVE 3: 155 (1975).
- Yosida, T. H., Handbuch der Allgemeinen Pathologic: 677 (1975).
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A genetic model for colorectal tumorigenesis
Fearon, E. R., & Vogelstein, B. (1990) · Cell · doi:10.1016/0092-8674(90)90186-i · Cited by 12,132
Vogelstein, B., Papadopoulos, N., Velculescu, V. E., Zhou, S., Diaz, L. A., & Kinzler, K. W. (2013) · Science · doi:10.1126/science.1235122 · Cited by 7,863
Age-related clonal hematopoiesis associated with adverse outcomes
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The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited
Fidler, I. J. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1098 · Cited by 4,686
The landscape of somatic copy-number alteration across human cancers
Beroukhim, R., Mermel, C. H., Porter, D., Wei, G., Raychaudhuri, S., Donovan, J., Barretina, J., Boehm, J. S., Dobson, J., Urashima, M., et al. (2010) · Nature · doi:10.1038/nature08822 · Cited by 4,017
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 hematopoiesis and blood-cancer risk inferred from blood DNA sequence
Genovese, G., Kähler, A. K., Handsaker, R. E., Lindberg, J., Rose, S. A., Bakhoum, S. F., Chambert, K., Mick, E., Neale, B. M., Fromer, M., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1409405 · Cited by 3,531
Cancer stem cells in solid tumours: accumulating evidence and unresolved questions
Visvader, J. E., & Lindeman, G. J. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2499 · Cited by 3,501
Immunogenic cell death and DAMPs in cancer therapy
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Greaves, M., & Maley, C. C. (2012) · Nature · doi:10.1038/nature10762 · Cited by 3,162
Emerging Biological Principles of Metastasis
Lambert, A. W., Pattabiraman, D. R., & Weinberg, R. A. (2017) · Cell · doi:10.1016/j.cell.2016.11.037 · Cited by 3,191
Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability
Colotta, F., Allavena, P., Sica, A., Garlanda, C., & Mantovani, A. (2009) · Carcinogenesis · doi:10.1093/carcin/bgp127 · Cited by 2,960
A view on drug resistance in cancer
Vasan, N., Baselga, J., & Hyman, D. M. (2019) · Nature · doi:10.1038/s41586-019-1730-1 · Cited by 2,770
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
Hsieh, J. J., Purdue, M. P., Signoretti, S., Swanton, C., Albiges, L., Schmidinger, M., Heng, D. Y., Larkin, J., & Ficarra, V. (2017) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2017.9 · Cited by 2,426
Tumour evolution inferred by single-cell sequencing
Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., Cook, K., Stepansky, A., Levy, D., Esposito, D., et al. (2011) · Nature · doi:10.1038/nature09807 · Cited by 2,598
Roodman, G. D. (2004) · New England Journal of Medicine · doi:10.1056/nejmra030831 · Cited by 2,752
Hartwell, L. H., & Kastan, M. B. (1994) · Science · doi:10.1126/science.7997877 · Cited by 2,539
Plasminogen Activators, Tissue Degradation, and Cancer
Danø, K., Andreasen, P. A., Grøndahl-Hansen, J., Kristensen, P., Nielsen, L. S., & Skriver, L. (1985) · Advances in cancer research · doi:10.1016/s0065-230x(08)60028-7 · Cited by 2,535
Genomic instability — an evolving hallmark of cancer
Negrini, S., Gorgoulis, V. G., & Halazonetis, T. D. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2858 · Cited by 2,397
Tumour heterogeneity and cancer cell plasticity
Meacham, C. E., & Morrison, S. J. (2013) · Nature · doi:10.1038/nature12624 · Cited by 2,526
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
Evolution of the Cancer Stem Cell Model
Kreso, A., & Dick, J. E. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.02.006 · Cited by 2,304
TRANSFORMING GROWTH FACTOR-β REGULATION OF IMMUNE RESPONSES
Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A.-K. L., & Flavell, R. A. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.24.021605.090737 · Cited by 2,264
Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry
Giesen, C., Wang, H. A. O., Schapiro, D., Zivanovic, N., Jacobs, A., Hattendorf, B., Schüffler, P. J., Grolimund, D., Buhmann, J. M., Brandt, S., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2869 · Cited by 1,951
Intra-tumour heterogeneity: a looking glass for cancer?
Marusyk, A., Almendro, V., & Polyák, K. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3261 · Cited by 2,058
Merlo, A., Herman, J. G., Mao, L., Lee, D. J., Gabrielson, E. W., Burger, P. C., Baylin, S. B., & Sidransky, D. (1995) · Nature Medicine · doi:10.1038/nm0795-686 · Cited by 1,992
Alterations in DNA Methylation: A Fundamental Aspect of Neoplasia
Baylln, S. B., Herman, J. G., Graff, J. R., Vertino, P. M., & Issa, J. J. (1997) · Advances in cancer research · doi:10.1016/s0065-230x(08)60702-2 · Cited by 1,919
The cancer stem cell: premises, promises and challenges
Clevers, H. C. (2011) · Nature Medicine · doi:10.1038/nm.2304 · Cited by 1,990
The multistep nature of cancer
Vogelstein, B., & Kinzler, K. W. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90209-z · Cited by 1,858
High burden and pervasive positive selection of somatic mutations in normal human skin
Martincorena, I., Roshan, A., Gerstung, M., Ellis, P., Van Loo, P., McLaren, S., Wedge, D. C., Fullam, A., Alexandrov, L. B., Tubio, J. M., et al. (2015) · Science · doi:10.1126/science.aaa6806 · Cited by 1,770
The pathogenesis of cancer metastasis
Poste, G. H., & Fidler, I. J. (1980) · Nature · doi:10.1038/283139a0 · Cited by 1,739
Identification of a Chromosome 18q Gene that Is Altered in Colorectal Cancers
Fearon, E. R., Cho, K. R., Nigro, J. M., Kern, S. E., Simons, J. W., Ruppert, J. M., Hamilton, S. R., Preisinger, A. C., Thomas, G., Kinzler, K. W., et al. (1990) · Science · doi:10.1126/science.2294591 · Cited by 1,760
Addiction to Oncogenes--the Achilles Heal of Cancer
Weinstein, I. B. (2002) · Science · doi:10.1126/science.1073096 · Cited by 1,764
Universal Patterns of Selection in Cancer and Somatic Tissues
Martincorena, I., Raine, K. M., Gerstung, M., Dawson, K. J., Haase, K., Van Loo, P., Davies, H., Stratton, M. R., & Campbell, P. J. (2017) · Cell · doi:10.1016/j.cell.2017.09.042 · Cited by 1,523
Cancer as an evolutionary and ecological process
Merlo, L. M. F., Pepper, J. W., Reid, B. J., & Maley, C. C. (2006) · Nature reviews. Cancer · doi:10.1038/nrc2013 · Cited by 1,743
Divergent clonal evolution of castration-resistant neuroendocrine prostate cancer
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Immune evasion in cancer: mechanistic basis and therapeutic strategies
Vinay, D. S., Ryan, E. P., Pawelec, G., Talib, W. H., Stagg, J., Elkord, E., Lichtor, T., Decker, W. K., Whelan, R. L., Kumara, H. M. C. S., et al. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.03.004 · Cited by 1,625
Tumor heterogeneity: Causes and consequences
Marusyk, A., & Polyák, K. (2009) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2009.11.002 · Cited by 1,646
The origin and evolution of mutations in acute myeloid leukemia
Welch, J. S., Ley, T. J., Link, D. C., Miller, C. A., Larson, D. E., Koboldt, D. C., Wartman, L. D., Lamprecht, T. L., Liu, F., Xia, J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.06.023 · Cited by 1,575
Endogenous DNA damage as a source of genomic instability in cancer
Tubbs, A., & Nussenzweig, A. (2017) · Cell · doi:10.1016/j.cell.2017.01.002 · Cited by 1,452
Metabolite profiling identifies a key role for glycine in rapid cancer cell proliferation
Jain, M., Nilsson, R., Sharma, S., Madhusudhan, N., Kitami, T., Souza, A. L., Kafri, R., Kirschner, M. W., Clish, C. B., & Mootha, V. K. (2012) · Science · doi:10.1126/science.1218595 · Cited by 1,403
A mechanism linking extra centrosomes to chromosomal instability
Ganem, N. J., Godinho, S. A., & Pellman, D. S. (2009) · Nature · doi:10.1038/nature08136 · Cited by 1,427
Metastasis Results from Preexisting Variant Cells Within a Malignant Tumor
Fidler, I. J., & Kripke, M. L. (1977) · Science · doi:10.1126/science.887927 · Cited by 1,426
The impact of translocations and gene fusions on cancer causation
Mitelman, F., Johansson, B., & Mertens, F. (2007) · Nature Reviews Cancer · doi:10.1038/nrc2091 · Cited by 1,400
Somatic mutation in cancer and normal cells
Martincorena, I., & Campbell, P. J. (2015) · Science · doi:10.1126/science.aab4082 · Cited by 1,396
The evolutionary history of lethal metastatic prostate cancer
ICGC Prostate UK Group, Gundem, G., Loo, P. V., Kremeyer, B., Alexandrov, L. B., Tubío, J. M. C., Papaemmanuil, E., Brewer, D. S., Kallio, H. M. L., Högnäs, G., et al. (2015) · Nature · doi:10.1038/nature14347 · Cited by 1,358
Tumor Microsatellite Instability and Clinical Outcome in Young Patients with Colorectal Cancer
Gryfe, R., Kim, H., Hsieh, E., Aronson, M. D., Holowaty, E. J., Bull, S. B., Redston, M. S., & Gallinger, S. (2000) · New England Journal of Medicine · doi:10.1056/nejm200001133420201 · Cited by 1,396
Jass, J. R. (2006) · Histopathology · doi:10.1111/j.1365-2559.2006.02549.x · Cited by 1,416
Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53
Livingstone, L. R., White, A., Sprouse, J., Livanos, E., Jacks, T., & Tlsty, T. D. (1992) · Cell · doi:10.1016/0092-8674(92)90243-6 · Cited by 1,328
Lessons from the Cancer Genome
Garraway, L. A., & Lander, E. S. (2013) · Cell · doi:10.1016/j.cell.2013.03.002 · Cited by 1,377
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Tumour heterogeneity in the clinic
Bedard, P. L., Hansen, A. R., Ratain, M. J., & Siu, L. L. (2013) · Nature · doi:10.1038/nature12627 · Cited by 1,231
Braakhuis, B. J. M., Tabor, M. P., Kummer, J. A., Leemans, C. R., & Brakenhoff, R. H. (2003) · PubMed · Cited by 1,208
On the Origin of Cancer Metastasis
Seyfried, T. N., & Huysentruyt, L. C. (2012) · Critical Reviews™ in Oncogenesis · doi:10.1615/critrevoncog.v18.i1-2.40 · Cited by 1,218
AACR Centennial Series: The Biology of Cancer Metastasis: Historical Perspective
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Shackleton, M. J., Quintana, E., Fearon, E. R., & Morrison, S. J. (2009) · Cell · doi:10.1016/j.cell.2009.08.017 · Cited by 1,204
Ovarian cancer: strategies for overcoming resistance to chemotherapy
Agarwal, R., & Kaye, S. B. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1123 · Cited by 1,165
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
Biological and therapeutic impact of intratumor heterogeneity in cancer evolution
McGranahan, N., & Swanton, C. (2015) · Cancer Cell · doi:10.1016/j.ccell.2014.12.001 · Cited by 1,077
Cancer Stem Cells: Impact, Heterogeneity, and Uncertainty
Magee, J. A., Piskounova, E., & Morrison, S. J. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.03.003 · Cited by 1,136
Lung cancer: Biology and treatment options
Lemjabbar‐Alaoui, H., Hassan, O. U., Yang, Y., & Buchanan, P. C. (2015) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2015.08.002 · Cited by 1,067
T and Tn, General Carcinoma Autoantigens
Springer, G. F. (1984) · Science · doi:10.1126/science.6729450 · Cited by 1,009
PyClone: statistical inference of clonal population structure in cancer
Roth, A. J. L., Khattra, J. S., Yap, D., Wan, A. N. C., Laks, E., Biele, J., Ha, G., Aparicio, S. A. J. R., Bouchard‐Côté, A., & Shah, S. P. (2014) · Nature Methods · doi:10.1038/nmeth.2883 · Cited by 1,002
Cancer heterogeneity: implications for targeted therapeutics
Fisher, R. A., Pusztai, L., & Swanton, C. (2013) · British Journal of Cancer · doi:10.1038/bjc.2012.581 · Cited by 972
Intratumor Heterogeneity: Evolution through Space and Time
Swanton, C. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-2217 · Cited by 931
DePinho, R. A. (2000) · Nature · doi:10.1038/35041694 · Cited by 951
Tumor microenvironmental physiology and its implications for radiation oncology
Vaupel, P. W. (2004) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2004.04.008 · Cited by 966
A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity.
Nishikawa, R., Ji, X.-D., Harmon, R. C., Lazar, C. S., Gill, G. N., Cavenee, W. K., & Huang, H. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.16.7727 · Cited by 936
Biological Diversity in Metastatic Neoplasms: Origins and Implications
Fidler, I. J., & Hart, I. R. (1982) · Science · doi:10.1126/science.7112116 · Cited by 926
Cancer Epigenetics: Tumor Heterogeneity, Plasticity of Stem-like States, and Drug Resistance
Easwaran, H., Tsai, H.-C., & Baylin, S. B. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.015 · Cited by 915
DNA Mismatch Repair: Functions and Mechanisms
Iyer, R. R., Pluciennik, A., Burdett, V., & Modrich, P. L. (2005) · Chemical Reviews · doi:10.1021/cr0404794 · Cited by 935
Rausch, T., Jones, D. T. W., Zapatka, M., Stütz, A. M., Zichner, T., Weischenfeldt, J., Jäger, N., Remke, M., Shih, D., Northcott, P. A., et al. (2012) · Cell · doi:10.1016/j.cell.2011.12.013 · Cited by 865
Evolution of high mutation rates in experimental populations of E. coli
Sniegowski, P. D., Gerrish, P. J., & Lenski, R. E. (1997) · Nature · doi:10.1038/42701 · Cited by 879
c-Myc Can Induce DNA Damage, Increase Reactive Oxygen Species, and Mitigate p53 Function
Vafa, O., Wade, M., Kern, S., Beeche, M., Pandita, T. K., Hampton, G. M., & Wahl, G. M. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00520-8 · Cited by 876
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Turner, K. M., Deshpande, V., Beyter, D., Koga, T., Rusert, J. M., Lee, C., Li, B., Arden, K. C., Ren, B., Nathanson, D. A., et al. (2017) · Nature · doi:10.1038/nature21356 · Cited by 835
Tumour-initiating cells: challenges and opportunities for anticancer drug discovery
Zhou, B. S., Zhang, H., Damelin, M. I., Geles, K. G., Grindley, J. C., & Dirks, P. B. (2009) · Nature Reviews Drug Discovery · doi:10.1038/nrd2137 · Cited by 846
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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
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Fidler, I. J. (1978) · PubMed · Cited by 818
Genetic variegation of clonal architecture and propagating cells in leukaemia
Anderson, K., Lutz, C., van Delft, F. W., Bateman, C. M., Guo, Y., Colman, S., Kempski, H. M., Moorman, A. V., Titley, I., Swansbury, J. G., et al. (2010) · Nature · doi:10.1038/nature09650 · Cited by 803
The Biology of Cancer Invasion and Metastasis
Fidler, I. J., Gersten, D. M., & Hart, I. R. (1978) · Advances in cancer research · doi:10.1016/s0065-230x(08)60648-x · Cited by 799
Genetic determinants of cancer metastasis
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DNA repair, genome stability and cancer: a historical perspective
Jeggo, P. A., Pearl, L. H., & Carr, A. M. (2015) · Nature reviews. Cancer · doi:10.1038/nrc.2015.4 · Cited by 781
Pan-cancer analysis of the extent and consequences of intratumor heterogeneity
Andor, N., Graham, T. A., Jansen, M., Xia, L. C., Aktipis, A., Petritsch, C. K., Ji, H. P., & Maley, C. C. (2015) · Nature Medicine · doi:10.1038/nm.3984 · Cited by 766
Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells
Hartwell, L. H. (1992) · Cell · doi:10.1016/0092-8674(92)90586-2 · Cited by 770
Loeb, L. A., Loeb, K. R., & Anderson, J. P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0334858100 · Cited by 762
Clonal evolution of glioblastoma under therapy
Wang, J., Cazzato, E., Ladewig, E., Frattini, V., Rosenbloom, D. I. S., Zairis, S., Abate, F., Liu, Z., Elliott, O., Shin, Y.-J., et al. (2016) · Nature Genetics · doi:10.1038/ng.3590 · Cited by 720
Tumor Morphology and Phenotypic Evolution Driven by Selective Pressure from the Microenvironment
Anderson, A. R. A., Weaver, A. M., Cummings, P. T., & Quaranta, V. (2006) · Cell · doi:10.1016/j.cell.2006.09.042 · Cited by 764
Genetic instability and darwinian selection in tumours
Cahill, D. P., Kinzler, K. W., Vogelstein, B., & Lengauer, C. (1999) · Trends in Cell Biology · doi:10.1016/s0962-8924(99)01661-x · Cited by 747
How nucleotide excision repair protects against cancer
Friedberg, E. C. (2001) · Nature Reviews Cancer · doi:10.1038/35094000 · Cited by 730
Rajagopalan, H., & Lengauer, C. (2004) · Nature · doi:10.1038/nature03099 · Cited by 731
A microenvironmental model of carcinogenesis
Gatenby, R. A., & Gillies, R. J. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2255 · Cited by 741
Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity
Vermeulen, L., Todaro, M., Melo, F. D. S. E., Sprick, M. R., Kemper, K., Pérez‐Alea, M., Richel, D. J., Stassi, G., & Medema, J. P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805706105 · Cited by 741
Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia
Jan, M., Snyder, T. M., Corces-Zimmerman, M. R., Vyas, P., Weissman, I. L., Quake, S. R., & Majeti, R. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004315 · Cited by 721
Defining the mode of tumour growth by clonal analysis
Driessens, G., Beck, B., Caauwe, A., Simons, B. D., & Blanpain, C. (2012) · Nature · doi:10.1038/nature11344 · Cited by 718
Defining the Hallmarks of Metastasis
Welch, D. R., & Hurst, D. R. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-0458 · Cited by 722
Genetic clonal diversity predicts progression to esophageal adenocarcinoma
Maley, C. C., Galipeau, P. C., Finley, J. C., Wongsurawat, V. J., Li, X., Sanchez, C. A., Paulson, T. G., Blount, P. L., Risques, R., Rabinovitch, P. S., et al. (2006) · Nature Genetics · doi:10.1038/ng1768 · Cited by 687
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
“Peter Nowell posited almost 40 years ago that “each patient's cancer may require individual specific therapy, and even this may be thwarted by emergence of a genetically variant subline [subclone] resistant to the treatment” [62].”
Background
Metadata
- Authors
- Nowell, P. C.
- Affiliations
- School of Medicine, University of Pennsylvania, Philadelphia 19174.
- Venue
- Science
- Published
- 1976-10
- Volume
- 194
- Issue
- 4260
- Pages
- 23-28
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1967304777
- Cited by
- 6,471
- References
- 52
- Citations by year
- 2026: 117 · 2025: 163 · 2024: 183 · 2023: 201 · 2022: 209 · 2021: 282 · 2020: 287 · 2019: 259 · 2018: 304 · 2017: 332 · 2016: 263 · 2015: 261 · 2014: 241 · 2013: 233 · 2012: 200
- FWCI
- 16.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- clonal evolution, tumor progression, karyotypic heterogeneity, tumor cell populations, treatment resistance, carcinogen exposure, precision oncology
- MeSH terms
- Carcinogens, Chromosomes, Clone Cells, Karyotyping, Models, Biological, Mutation, Neoplasms
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