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      Cancer evolution: Darwin and beyond

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          Abstract

          Clinical and laboratory studies over recent decades have established branched evolution as a feature of cancer. However, while grounded in somatic selection, several lines of evidence suggest a Darwinian model alone is insufficient to fully explain cancer evolution. First, the role of macroevolutionary events in tumour initiation and progression contradicts Darwin's central thesis of gradualism. Whole‐genome doubling, chromosomal chromoplexy and chromothripsis represent examples of single catastrophic events which can drive tumour evolution. Second, neutral evolution can play a role in some tumours, indicating that selection is not always driving evolution. Third, increasing appreciation of the role of the ageing soma has led to recent generalised theories of age‐dependent carcinogenesis. Here, we review these concepts and others, which collectively argue for a model of cancer evolution which extends beyond Darwin. We also highlight clinical opportunities which can be grasped through targeting cancer vulnerabilities arising from non‐Darwinian patterns of evolution.

          Abstract

          Evolutionary concepts explaining cancer progression, the selective pressures acting on tumours, and their therapeutic implications are discussed in this comprehensive review.

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          Cancer statistics, 2018

          Kimberly D Miller, Rebecca L Siegel, Ahmedin Jemal (2018)
          Each year, the American Cancer Society estimates the numbers of new cancer cases and deaths that will occur in the United States and compiles the most recent data on cancer incidence, mortality, and survival. Incidence data, available through 2014, were collected by the Surveillance, Epidemiology, and End Results Program; the National Program of Cancer Registries; and the North American Association of Central Cancer Registries. Mortality data, available through 2015, were collected by the National Center for Health Statistics. In 2018, 1,735,350 new cancer cases and 609,640 cancer deaths are projected to occur in the United States. Over the past decade of data, the cancer incidence rate (2005-2014) was stable in women and declined by approximately 2% annually in men, while the cancer death rate (2006-2015) declined by about 1.5% annually in both men and women. The combined cancer death rate dropped continuously from 1991 to 2015 by a total of 26%, translating to approximately 2,378,600 fewer cancer deaths than would have been expected if death rates had remained at their peak. Of the 10 leading causes of death, only cancer declined from 2014 to 2015. In 2015, the cancer death rate was 14% higher in non-Hispanic blacks (NHBs) than non-Hispanic whites (NHWs) overall (death rate ratio [DRR], 1.14; 95% confidence interval [95% CI], 1.13-1.15), but the racial disparity was much larger for individuals aged <65 years (DRR, 1.31; 95% CI, 1.29-1.32) compared with those aged ≥65 years (DRR, 1.07; 95% CI, 1.06-1.09) and varied substantially by state. For example, the cancer death rate was lower in NHBs than NHWs in Massachusetts for all ages and in New York for individuals aged ≥65 years, whereas for those aged <65 years, it was 3 times higher in NHBs in the District of Columbia (DRR, 2.89; 95% CI, 2.16-3.91) and about 50% higher in Wisconsin (DRR, 1.78; 95% CI, 1.56-2.02), Kansas (DRR, 1.51; 95% CI, 1.25-1.81), Louisiana (DRR, 1.49; 95% CI, 1.38-1.60), Illinois (DRR, 1.48; 95% CI, 1.39-1.57), and California (DRR, 1.45; 95% CI, 1.38-1.54). Larger racial inequalities in young and middle-aged adults probably partly reflect less access to high-quality health care. CA Cancer J Clin 2018;68:7-30. © 2018 American Cancer Society.
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            Cancer Statistics, 2017.

            Rebecca L Siegel, Kimberly D Miller, Ahmedin Jemal (2017)
            Each year, the American Cancer Society estimates the numbers of new cancer cases and deaths that will occur in the United States in the current year and compiles the most recent data on cancer incidence, mortality, and survival. Incidence data were collected by the Surveillance, Epidemiology, and End Results Program; the National Program of Cancer Registries; and the North American Association of Central Cancer Registries. Mortality data were collected by the National Center for Health Statistics. In 2017, 1,688,780 new cancer cases and 600,920 cancer deaths are projected to occur in the United States. For all sites combined, the cancer incidence rate is 20% higher in men than in women, while the cancer death rate is 40% higher. However, sex disparities vary by cancer type. For example, thyroid cancer incidence rates are 3-fold higher in women than in men (21 vs 7 per 100,000 population), despite equivalent death rates (0.5 per 100,000 population), largely reflecting sex differences in the "epidemic of diagnosis." Over the past decade of available data, the overall cancer incidence rate (2004-2013) was stable in women and declined by approximately 2% annually in men, while the cancer death rate (2005-2014) declined by about 1.5% annually in both men and women. From 1991 to 2014, the overall cancer death rate dropped 25%, translating to approximately 2,143,200 fewer cancer deaths than would have been expected if death rates had remained at their peak. Although the cancer death rate was 15% higher in blacks than in whites in 2014, increasing access to care as a result of the Patient Protection and Affordable Care Act may expedite the narrowing racial gap; from 2010 to 2015, the proportion of blacks who were uninsured halved, from 21% to 11%, as it did for Hispanics (31% to 16%). Gains in coverage for traditionally underserved Americans will facilitate the broader application of existing cancer control knowledge across every segment of the population. CA Cancer J Clin 2017;67:7-30. © 2017 American Cancer Society.
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              Inflammation and cancer.

              Lisa M Coussens, Zena Werb (2002)
              Recent data have expanded the concept that inflammation is a critical component of tumour progression. Many cancers arise from sites of infection, chronic irritation and inflammation. It is now becoming clear that the tumour microenvironment, which is largely orchestrated by inflammatory cells, is an indispensable participant in the neoplastic process, fostering proliferation, survival and migration. In addition, tumour cells have co-opted some of the signalling molecules of the innate immune system, such as selectins, chemokines and their receptors for invasion, migration and metastasis. These insights are fostering new anti-inflammatory therapeutic approaches to cancer development.
              Article 0 comments Cited 1925 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Kevin Litchfield: k.litchfield@ucl.ac.uk
                Charles Swanton: charles.swanton@crick.ac.uk
                Journal
                Journal ID (nlm-ta): EMBO J
                Journal ID (iso-abbrev): EMBO J
                Journal ID (doi): 10.1002/(ISSN)1460-2075
                Journal ID (publisher-id): EMBJ
                Journal ID (hwp): embojnl
                Title: The EMBO Journal
                Publisher: John Wiley and Sons Inc. (Hoboken )
                ISSN (Print): 0261-4189
                ISSN (Electronic): 1460-2075
                Publication date (Electronic): 30 August 2021
                Publication date (Print): 15 September 2021
                Publication date PMC-release: 30 August 2021
                Volume: 40
                Issue: 18 ( doiID: 10.1002/embj.v40.18 )
                Electronic Location Identifier: e108389
                Affiliations
                [ 1 ] Cancer Research UK Lung Cancer Centre of Excellence University College London Cancer Institute London UK
                [ 2 ] Cancer Evolution and Genome Instability Laboratory The Francis Crick Institute London UK
                Author notes
                [*] [* ] Corresponding author. Tel: +44 207679 6500; E‐mail: k.litchfield@ 123456ucl.ac.uk

                Corresponding author. Tel: +44 203796 2047; E‐mail: charles.swanton@ 123456crick.ac.uk

                Author information
                https://orcid.org/0000-0001-7191-4887
                Article
                Publisher ID: EMBJ2021108389
                DOI: 10.15252/embj.2021108389
                PMC ID: 8441388
                PubMed ID: 34459009
                SO-VID: 186be688-3f78-4f6b-86e6-6c8f965daa00
                Copyright © © 2021 The Authors. Published under the terms of the CC BY 4.0 license
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date revision received : 04 June 2021
                Date received : 02 April 2021
                Date accepted : 25 June 2021
                Page count
                Figures: 4, Tables: 0, Pages: 20, Words: 18914
                Funding
                Funded by: UK Medical Research Council
                Award ID: MR/V033077/1
                Funded by: Rosetrees Trust and Cotswold Trust
                Award ID: A2437
                Funded by: Royal Marsden Cancer Charity
                Funded by: Melanoma Research Alliance and Cancer Research UK
                Award ID: C69256/A30194
                Funded by: Royal Society Napier Research
                Award ID: RP150154
                Funded by: Cancer Research UK
                Award ID: FC001169
                Funded by: UK Medical Research Council
                Award ID: FC001169
                Funded by: Wellcome Trust
                Award ID: FC001169
                Funded by: Cancer Research UK (TRACERx, PEACE and CRUK Cancer Immunotherapy Catalyst Network)
                Funded by: Cancer Research UK Lung Cancer Centre of Excellence
                Award ID: C11496/A30025
                Funded by: Rosetrees Trust, Butterfield and Stoneygate Trusts
                Funded by: NovoNordisk Foundation
                Award ID: ID16584
                Funded by: Royal Society Professorship Enhancement Award
                Award ID: RP/EA/180007
                Funded by: National Institute for Health Research (NIHR) Biomedical Research Centre at University College London Hospitals
                Funded by: Cancer Research UK‐University College London Experimental Cancer Medicine Centre
                Funded by: Breast Cancer Research Foundation
                Award ID: BCRF 20‐157
                Funded by: Stand Up To Cancer‐LUNGevity‐American Lung Association Lung Cancer Interception Dream Team Translational Research Grant
                Award ID: SU2C‐AACR‐DT23‐17
                Funded by: ERC Advanced Grant (PROTEUS) from the European Research Council under the European Union’s Horizon 2020 research and innovation programme
                Award ID: 835297
                Categories
                Subject: Review
                Subject: Reviews
                Series title: Cancer Reviews 2021 series
                Custom metadata
                source-schema-version-number 2.0
                cover-date 15 September 2021
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.7 mode:remove_FC converted:15.09.2021

                ScienceOpen disciplines: Molecular biology
                Keywords: cancer,cancer evolution,cancer therapy,tumour heterogeneity
                Data availability:
                ScienceOpen disciplines: Molecular biology
                Keywords: cancer, cancer evolution, cancer therapy, tumour heterogeneity

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