nature.com

Clonal evolution in cancer - Nature

  • ️Maley, Carlo C.
  • ️Wed Jan 18 2012
  • Jemal, A. et al. Cancer statistics, 2008. CA Cancer J. Clin. 58, 71–96 (2008).

    PubMed  Google Scholar 

  • Stratton, M. R. Exploring the genomes of cancer cells: progress and promise. Science 331, 1553–1558 (2011).

    ADS  CAS  PubMed  Google Scholar 

  • Nowell, P. C. The clonal evolution of tumor cell populations. Science 194, 23–28 (1976). The foundation paper that established the evolutionary theory of cancer.

    ADS  CAS  PubMed  Google Scholar 

  • Merlo, L. M., Pepper, J. W., Reid, B. J. & Maley, C. C. Cancer as an evolutionary and ecological process. Nature Rev. Cancer 6, 924–935 (2006).

    CAS  Google Scholar 

  • Pepper, J., Scott Findlay, C., Kassen, R., Spencer, S. & Maley, C. Cancer research meets evolutionary biology. Evol. Appl. 2, 62–70 (2009).

    PubMed  PubMed Central  Google Scholar 

  • Greaves, M. Cancer: The Evolutionary Legacy (Oxford Univ. Press, 2000).

    Google Scholar 

  • Sakr, W. A., Haas, G. P., Cassin, B. F., Pontes, J. E. & Crissman, J. D. The frequency of carcinoma and intraepithelial neoplasia of the prostate in young male patients. J. Urol. 150, 379–385 (1993).

    CAS  PubMed  Google Scholar 

  • Mori, H. et al. Chromosome translocations and covert leukemic clones are generated during normal fetal development. Proc. Natl Acad. Sci. USA 99, 8242–8247 (2002).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid, B. J., Li, X., Galipeau, P. C. & Vaughan, T. L. Barrett's oesophagus and oesophageal adenocarcinoma: time for a new synthesis. Nature Rev. Cancer 10, 87–101 (2010).

    CAS  Google Scholar 

  • Klein, C. A. Parallel progression of primary tumours and metastases. Nature Rev. Cancer 9, 302–312 (2009).

    CAS  Google Scholar 

  • Malaise, E. P., Chavaudra, N. & Tubiana, M. The relationship between growth rate, labelling index and histological type of human solid tumours. Eur. J. Cancer 9, 305–312 (1973).

    CAS  PubMed  Google Scholar 

  • Tsai, A. G. et al. Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity. Cell 135, 1130–1142 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bardelli, A. et al. Carcinogen-specific induction of genetic instability. Proc. Natl Acad. Sci. USA 98, 5770–5775 (2001).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Cahill, D. P., Kinzler, K. W., Vogelstein, B. & Lengauer, C. Genetic instability and Darwinian selection in tumors. Trends Cell Biol. 9, M57–M60 (1999).

    CAS  PubMed  Google Scholar 

  • Barcellos-Hoff, M. H., Park, C. & Wright, E. G. Radiation and the microenvironment – tumorigenesis and therapy. Nature Rev. Cancer 5, 867–875 (2005).

    CAS  Google Scholar 

  • Maley, C. C. et al. Selectively advantageous mutations and hitchhikers in neoplasms: p16 lesions are selected in Barrett's esophagus. Cancer Res. 64, 3414–3427 (2004).

    CAS  PubMed  Google Scholar 

  • Tao, Y. et al. Rapid growth of a hepatocellular carcinoma and the driving mutations revealed by cell-population genetic analysis of whole-genome data. Proc. Natl Acad. Sci. USA 108, 12042–12047 (2011).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Bignell, G. R. et al. Signatures of mutation and selection in the cancer genome. Nature 463, 893–898 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Youn, A. & Simon, R. Identifying cancer driver genes in tumor genome sequencing studies. Bioinformatics 27, 175–181 (2011).

    CAS  PubMed  Google Scholar 

  • Greenman, C., Wooster, R., Futreal, P. A., Stratton, M. R. & Easton, D. F. Statistical analysis of pathogenicity of somatic mutations in cancer. Genetics 173, 2187–2198 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bozic, I. et al. Accumulation of driver and passenger mutations during tumor progression. Proc. Natl Acad. Sci. USA 107, 18545–18550 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz, M., Zlotorynski, E. & Kerem, B. The molecular basis of common and rare fragile sites. Cancer Lett. 232, 13–26 (2006).

    CAS  PubMed  Google Scholar 

  • Loeb, L. A. Human cancers express mutator phenotypes: origin, consequences and targeting. Nature Rev. Cancer 11, 450–457 (2011).

    CAS  Google Scholar 

  • Weisenberger, D. J. et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nature Genet 38, 787–793 (2006).

    CAS  PubMed  Google Scholar 

  • Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011). This paper consolidates the common phenotypes that evolve in neoplastic cells of all types.

    Article  CAS  PubMed  Google Scholar 

  • Siegmund, K. D., Marjoram, P., Woo, Y. J., Tavare, S. & Shibata, D. Inferring clonal expansion and cancer stem cell dynamics from DNA methylation patterns in colorectal cancers. Proc. Natl Acad. Sci. USA 106, 4828–4833 (2009).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Varley, K. E., Mutch, D. G., Edmonston, T. B., Goodfellow, P. J. & Mitra, R. D. Intra-tumor heterogeneity of MLH1 promoter methylation revealed by deep single molecule bisulfite sequencing. Nucleic Acids Res. 37, 4603–4612 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aktipis, C. A., Kwan, V. S. Y., Johnson, K. A., Neuberg, S. L. & Maley, C. C. Overlooking evolution: a systematic analysis of cancer relapse and therapeutic resistance research. PLoS ONE 6, e261000 10.1371/journal.pone.0026100 (2011).

    Article  CAS  Google Scholar 

  • Beerenwinkel, N. et al. Genetic progression and the waiting time to cancer. PLoS Comput. Biol. 3, e225 (2007).

    ADS  MathSciNet  PubMed  PubMed Central  Google Scholar 

  • de Visser, J. A. & Rozen, D. E. Clonal interference and the periodic selection of new beneficial mutations in Escherichia coli . Genetics 172, 2093–2100 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leedham, S. J. et al. Individual crypt genetic heterogeneity and the origin of metaplastic glandular epithelium in human Barrett's oesophagus. Gut 57, 1041–1048 (2008).

    CAS  PubMed  Google Scholar 

  • Navin, N. et al. Tumour evolution inferred by single-cell sequencing. Nature 472, 90–94 (2011). Single-cell sequencing revealed the clonal structure of two breast cancers.

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson, K. et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 469, 356–361 (2011). Single-cell genetic analyses and xenografts revealed the clonal architecture within acute lymphoblastic leukaemia stem-cell populations and demonstrated repeated independent acquisition of copy number changes within the same neoplasm.

    ADS  CAS  PubMed  Google Scholar 

  • Tsao, J. L. et al. Colorectal adenoma and cancer divergence. Evidence of multilineage progression. Am. J. Pathol. 154, 1815–1824 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maley, C. C. et al. Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nature Genet. 38, 468–473 (2006).

    CAS  PubMed  Google Scholar 

  • Sidransky, D. et al. Clonal expansion of p53 mutant cells is associated with brain tumour progression. Nature 355, 846–847 (1992).

    ADS  CAS  PubMed  Google Scholar 

  • Yachida, S. et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467, 1114–1117 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould, S. J. & Eldredge, N. Punctuated equilibrium comes of age. Nature 366, 223–227 (1993).

    ADS  CAS  PubMed  Google Scholar 

  • Stephens, P. J. et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144, 27–40 (2011).

    MathSciNet  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell, P. J. et al. Subclonal phylogenetic structures in cancer revealed by ultra-deep sequencing. Proc. Natl Acad. Sci. USA 105, 13081–13086 (2008). Deep sequencing revealed rare (frequency <0.001) intermediate genotypes between the common clones in leukaemias (using immunoglobulin rearrangements as surrogate mutations).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Aguirre-Ghiso, J. A. Models, mechanisms and clinical evidence for cancer dormancy. Nature Rev. Cancer 7, 834–846 (2007).

    CAS  Google Scholar 

  • Isoda, T. et al. Immunologically silent cancer clone transmission from mother to offspring. Proc. Natl Acad. Sci. USA 106, 17882–17885 (2009).

    ADS  PubMed  PubMed Central  Google Scholar 

  • Welsh, J. S. Contagious cancer. Oncologist 16, 1–4 (2011).

    PubMed  PubMed Central  Google Scholar 

  • Gatenby, R. A. & Gillies, R. J. A microenvironmental model of carcinogenesis. Nature Rev. Cancer 8, 56–61 (2008).

    CAS  Google Scholar 

  • Bierie, B. & Moses, H. L. Tumour microenvironment: TGFβ: the molecular Jekyll and Hyde of cancer. Nature Rev. Cancer 6, 506–520 (2006).

    CAS  PubMed  Google Scholar 

  • Lathia, J. D., Heddleston, J. M., Venere, M. & Rich, J. N. Deadly teamwork: neural cancer stem cells and the tumor microenvironment. Cell Stem Cell 8, 482–485 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cairns, J. Mutation selection and the natural history of cancer. Nature 255, 197–200 (1975). This paper identified natural selection as a driving force in carcinogenesis and identified tissue architecture as a cancer suppressor, and posited an immortal strand of DNA in tissue stem cells.

    ADS  CAS  PubMed  Google Scholar 

  • Anderson, A. R., Weaver, A. M., Cummings, P. T. & Quaranta, V. Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell 127, 905–915 (2006).

    CAS  PubMed  Google Scholar 

  • Chen, J., Sprouffske, K., Huang, Q. & Maley, C. C. Solving the puzzle of metastasis: the evolution of cell migration in neoplasms. PLoS ONE 6, e17933 (2011).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazzone, M. et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136, 839–851 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert, L. A. & Hemann, M. T. DNA damage-mediated induction of a chemoresistant niche. Cell 143, 355–366 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones, S. et al. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl Acad. Sci. USA 105, 4283–4288 (2008).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding, L. et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 464, 999–1005 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Sprouffske, K., Pepper, J. W. & Maley, C. C. Accurate reconstruction of the temporal order of mutations in neoplastic progression. Cancer Prev. Res. 4, 1135–1144 (2011).

    Google Scholar 

  • Greaves, M. F., Maia, A. T., Wiemels, J. L. & Ford, A. M. Leukemia in twins: lessons in natural history. Blood 102, 2321–2333 (2003).

    CAS  PubMed  Google Scholar 

  • Bateman, C. M. et al. Acquisition of genome-wide copy number alterations in monozygotic twins with acute lymphoblastic leukemia. Blood 115, 3553–3558 (2010).

    CAS  PubMed  Google Scholar 

  • Oosterhuis, J. W. & Looijenga, L. H. Testicular germ-cell tumours in a broader perspective. Nature Rev. Cancer 5, 210–222 (2005).

    CAS  Google Scholar 

  • Grant, P. R. & Grant, B. R. How and Why Species Multiply (Princeton Univ. Press, 2008).

    MATH  Google Scholar 

  • Durinck, S. et al. Temporal dissection of tumorigenesis in primary cancers. Cancer Discov. 1, 137–143 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Garcia, I., Sole, R. V. & Costa, J. Metapopulation dynamics and spatial heterogeneity in cancer. Proc. Natl Acad. Sci. USA 99, 13085–13089 (2002).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark, J. et al. Complex patterns of ETS gene alteration arise during cancer development in the human prostate. Oncogene 27, 1993–2003 (2008).

    CAS  PubMed  Google Scholar 

  • Navin, N. et al. Inferring tumor progression from genomic heterogeneity. Genome Res. 20, 68–80 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allred, D. C. et al. Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin. Cancer Res. 14, 370–378 (2008).

    CAS  PubMed  Google Scholar 

  • Park, S. Y., Gonen, M., Kim, H. J., Michor, F. & Polyak, K. Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype. J. Clin. Invest. 120, 636–644 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Merlo, L. M. et al. A comprehensive survey of clonal diversity measures in Barrett's esophagus as biomarkers of progression to esophageal adenocarcinoma. Cancer Prev. Res. 3, 1388–1397 (2010).

    Google Scholar 

  • Dick, J. E. Stem cell concepts renew cancer research. Blood 112, 4793–4807 (2008).

    CAS  PubMed  Google Scholar 

  • Reya, T., Morrison, S. J., Clarke, M. F. & Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105–111 (2001).

    ADS  CAS  PubMed  Google Scholar 

  • Greaves, M. Cancer stem cells renew their impact. Nature Med. 17, 1046–1048 (2011).

    CAS  PubMed  Google Scholar 

  • Rosen, J. M. & Jordan, C. T. The increasing complexity of the cancer stem cell paradigm. Science 324, 1670–1673 (2009).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Greaves, M. Cancer stem cells: back to Darwin? Semin. Cancer Biol. 20, 65–70 (2010).

    PubMed  Google Scholar 

  • Gupta, P. B. et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138, 645–659 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jamieson, C. H. et al. Granulocyte–macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med. 351, 657–667 (2004).

    CAS  PubMed  Google Scholar 

  • Akala, O. O. et al. Long-term haematopoietic reconstitution by Trp53−/−p164−/−p19Arf−/− multipotent progenitors. Nature 453, 228–232 (2008).

    ADS  CAS  PubMed  Google Scholar 

  • Krivtsov, A. V. et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL–AF9. Nature 442, 818–822 (2006).

    ADS  CAS  PubMed  Google Scholar 

  • Olivier, M. & Taniere, P. Somatic mutations in cancer prognosis and prediction: lessons from TP53 and EGFR genes. Curr. Opin. Oncol. 23, 88–92 (2011).

    CAS  PubMed  Google Scholar 

  • Mizuno, H., Spike, B. T., Wahl, G. M. & Levine, A. J. Inactivation of p53 in breast cancers correlates with stem cell transcriptional signatures. Proc. Natl Acad. Sci. USA 107, 22745–22750 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Cicalese, A. et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138, 1083–1095 (2009).

    CAS  PubMed  Google Scholar 

  • Quintana, E. et al. Efficient tumour formation by single human melanoma cells. Nature 456, 593–598 (2008). New xenograft methods revealed that cancer stem cells are common cell types in melanoma.

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Pece, S. et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140, 62–73 (2010).

    CAS  PubMed  Google Scholar 

  • Notta, F. et al. Evolution of human BCR–ABL1 lymphoblastic leukaemia-initiating cells. Nature 469, 362–367 (2011).

    ADS  CAS  PubMed  Google Scholar 

  • Clappier, E. et al. Clonal selection in xenografted human T cell acute lymphoblastic leukemia recapitulates gain of malignancy at relapse. J. Exp. Med. 208, 653–661 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frank, N. Y., Schatton, T. & Frank, M. H. The therapeutic promise of the cancer stem cell concept. J. Clin. Invest. 120, 41–50 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa, F. et al. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nature Biotechnol. 25, 1315–1321 (2007).

    CAS  Google Scholar 

  • Marusyk, A. & Polyak, K. Tumor heterogeneity: causes and consequences. Biochim. Biophys. Acta 1805, 105–117 (2010).

    CAS  PubMed  Google Scholar 

  • Piccirillo, S. G. M. et al. Distinct pools of cancer stem-like cells coexist within human glioblastomas and display different tumorigenicity and independent genomic evolution. Oncogene 28, 1807–1811 (2009).

    CAS  PubMed  Google Scholar 

  • Solit, D. & Sawyers, C. L. How melanomas bypass new therapy. Nature 468, 902–903 (2010).

    ADS  CAS  PubMed  Google Scholar 

  • Goff, D. & Jamieson, C. Cycling toward elimination of leukemic stem cells. Cell Stem Cell 6, 296–297 (2010).

    CAS  PubMed  Google Scholar 

  • Sharma, S. V. et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69–80 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chin, L., Andersen, J. N. & Futreal, P. A. Cancer genomics: from discovery science to personalized medicine. Nature Med. 17, 297–303 (2011).

    CAS  PubMed  Google Scholar 

  • Sawyers, C. L. Shifting paradigms: the seeds of oncogene addiction. Nature Med. 15, 1158–1161 (2009).

    CAS  PubMed  Google Scholar 

  • Graham, S. M. et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro . Blood 99, 319–325 (2002).

    CAS  PubMed  Google Scholar 

  • Turke, A. B. et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 17, 77–88 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ashworth, A., Lord, C. J. & Reis-Filho, J. S. Genetic interactions in cancer progression and treatment. Cell 145, 30–38 (2011).

    CAS  PubMed  Google Scholar 

  • Zhang, B. et al. Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate. Cancer Cell 17, 427–442 (2010).

    PubMed  PubMed Central  Google Scholar 

  • Duy, C. et al. BCL6 enables Ph+ acute lymphoblastic leukaemia cells to survive BCR–ABL1 kinase inhibition. Nature 473, 384–388 (2011).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Pienta, K. J., McGregor, N., Axelrod, R. & Axelrod, D. E. Ecological therapy for cancer: defining tumors using an ecosystem paradigm suggests new opportunities for novel cancer treatments. Trans. Oncol. 1, 158–164 10.1593/tlo.08178 (2008).

    Article  Google Scholar 

  • Calabrese, C. et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11, 69–82 (2007).

    CAS  PubMed  Google Scholar 

  • Bissell, M. J. & Hines, W. C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nature Med. 17, 320–329 (2011).

    CAS  PubMed  Google Scholar 

  • Wargo, A. R., Huijben, S., de Roode, J. C., Shepherd, J. & Read, A. F. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc. Natl Acad. Sci. USA 104, 19914–19919 (2007).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Gatenby, R. A., Silva, A. S., Gillies, R. J. & Frieden, B. R. Adaptive therapy. Cancer Res. 69, 4894–4903 (2009). Dosing to maintain tumour size prolonged survival far longer than high-dose therapy in a mouse xenograft model.

    CAS  PubMed  PubMed Central  Google Scholar