Cited by 6,471Cancer Genomics and DiagnosticsCancer Cells and MetastasisEvolution and Genetic Dynamics

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The Clonal Evolution of Tumor Cell Populations: Acquired genetic lability permits stepwise selection of variant sublines and underlies tumor progression.

Nowell, Peter C.·1976·Science

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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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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
Chromosomes and cancer
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

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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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Devilee, P., Cleton-Jansen, A., & Cornelisse, C. J. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02416-7 · Cited by 106
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Waghorne, C. G., Thomas, M., Lagarde, A., Kerbel, R. S., & Breitman, M. L. (1988) · PubMed · Cited by 102
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Williams, G. M. (2001) · Toxicology · doi:10.1016/s0300-483x(01)00442-5 · Cited by 101
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Characterizing genetic intra-tumor heterogeneity across 2,658 human cancer genomesPreprint
Dentro, S. C., Leshchiner, I., Haase, K., Tarabichi, M., Wintersinger, J. A., Deshwar, A. G., Yu, K., Rubanova, Y., Macintyre, G., Demeulemeester, J., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/312041 · Cited by 103
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Deakin, J. E., Bender, H. S., Pearse, A., Rens, W., O’Brien, P. C. M., Ferguson-Smith, M. A., Cheng, Y., Morris, K., Taylor, R. L., Stuart, A. B., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002483 · Cited by 98
Behavior of seeds and soil in the mechanism of metastasis: A deeper understanding
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Kadara, H. N., Scheet, P. A., Wistuba, I. I., & Spira, A. E. (2016) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-15-0400 · Cited by 102
Cell population heterogeneity and evolution towards drug resistance in cancer: Biological and mathematical assessment, theoretical treatment optimisation
Chisholm, R. H., Lorenzi, T., & Clairambault, J. (2016) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2016.06.009 · Cited by 99
Functional variomics and network perturbation: connecting genotype to phenotype in cancer
Yi, S. S., Lin, S., Li, Y., Zhao, W., Mills, G. B., & Sahni, N. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.8 · Cited by 105
Differing Roles of Hyaluronan Molecular Weight on Cancer Cell Behavior and Chemotherapy Resistance
Price, Z. K., Lokman, N. A., & Ricciardelli, C. (2018) · Cancers · doi:10.3390/cancers10120482 · Cited by 100
EMT and Stemness—Key Players in Pancreatic Cancer Stem Cells
Rodríguez-Aznar, E., Wiesmüller, L., Sáinz, B., & Hermann, P. C. (2019) · Cancers · doi:10.3390/cancers11081136 · Cited by 99
Cancer genome sequencing: The challenges ahead
Heng, H. H. (2007) · BioEssays · doi:10.1002/bies.20610 · Cited by 99
Intestinal metaplasia: A premalignant lesion involved in gastric carcinogenesis
Busuttil, R. A., & Boussioutas, A. (2009) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2008.05774.x · Cited by 96
Molecular interactions in the Vogelstein model of colorectal carcinoma
Arends, J. W. (2000) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(200003)190:4 · Cited by 184
The evolving concept of tumor microenvironments
Laconi, E. (2007) · BioEssays · doi:10.1002/bies.20606 · Cited by 103
Sialic Acid Metabolism: A Key Player in Breast Cancer Metastasis Revealed by Metabolomics
Teoh, S. T., Ogrodzinski, M. P., Ross, C. R., Hunter, K. W., & Lunt, S. Y. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00174 · Cited by 100
Somatic mitochondrial mutation in gastric cancer.
Burgart, L. J., Zheng, J., Shu, Q., Strickler, J. G., & Shibata, D. K. (1995) · Europe PMC (PubMed Central) · Cited by 98
Radiologically Defined Ecological Dynamics and Clinical Outcomes in Glioblastoma Multiforme: Preliminary Results
Zhou, M., Hall, L., Goldgof, D., Russo, R., Balagurunathan, Y., Gillies, R., & Gatenby, R. (2014) · Translational Oncology · doi:10.1593/tlo.13730 · Cited by 97
Challenges and opportunities in the proteomic characterization of clear cell renal cell carcinoma (ccRCC): A critical step towards the personalized care of renal cancers
Li, Q. K., Pavlovich, C. P., Zhang, H., Kinsinger, C. R., & Chan, D. W. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.06.004 · Cited by 98
Phylodynamics for cell biologists
Stadler, T., Pybus, O. G., & Stumpf, M. P. H. (2021) · Science · doi:10.1126/science.aah6266 · Cited by 91
Crypt dynamics and colorectal cancer: advances in mathematical modelling
van Leeuwen, I. M. M., Byrne, H. M., Jensen, O. E., & King, J. R. (2006) · Cell Proliferation · doi:10.1111/j.1365-2184.2006.00378.x · Cited by 95
Evidence for the involvement of pim‐2, a new common proviral insertion site, in progression of lymphomas.
Breuer, M., Cuypers, H., & Berns, A. (1989) · EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03434.x · Cited by 102
Novel clinico–genome network modeling for revolutionizing genotype–phenotype-based personalized cancer care
Roukos, D. H. (2009) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.09.69 · Cited by 97
Chromosomal instability and its relationship to other end points of genomic instability.
Limoli, C. L., Kaplan, M. I., Corcoran, J., Meyers, M., Boothman, D. A., & Morgan, W. F. (1997) · PubMed · Cited by 97
Evolutionary Mechanisms and Diversity in Cancer
Heng, H. H., Stevens, J. B., Bremer, S. W., Liu, G., Abdallah, B. Y., & Ye, C. J. (2011) · Advances in cancer research · doi:10.1016/b978-0-12-387688-1.00008-9 · Cited by 96

Authors: Nowell, P. C.
Affiliations: School of Medicine, University of Pennsylvania, Philadelphia 19174.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 1976-10
Volume: 194
Issue: 4260
Pages: 23-28
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.959840
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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The Clonal Evolution of Tumor Cell Populations: Acquired genetic lability permits stepwise selection of variant sublines and underlies tumor progression.

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