Classifying the evolutionary and ecological features of neoplasms

Carlo Maley, C Athena Aktipis, Trevor A. Graham, Andrea Sottoriva, Amy M. Boddy, Michalina Janiszewska, Ariosto S. Silva, Marco Gerlinger, Yinyin Yuan, Kenneth J. Pienta, Karen Anderson, Robert Gatenby, Charles Swanton, David Posada, Chung I. Wu, Joshua D. Schiffman, E. Shelley Hwang, Kornelia Polyak, Alexander R.A. Anderson, Joel S. Brown & 2 others Mel Greaves, Darryl Shibata

    Research output: Contribution to journalReview article

    46 Citations (Scopus)

    Abstract

    Neoplasms change over time through a process of cell-level evolution, driven by genetic and epigenetic alterations. However, the ecology of the microenvironment of a neoplastic cell determines which changes provide adaptive benefits. There is widespread recognition of the importance of these evolutionary and ecological processes in cancer, but to date, no system has been proposed for drawing clinically relevant distinctions between how different tumours are evolving. On the basis of a consensus conference of experts in the fields of cancer evolution and cancer ecology, we propose a framework for classifying tumours that is based on four relevant components. These are the diversity of neoplastic cells (intratumoural heterogeneity) and changes over time in that diversity, which make up an evolutionary index (Evo-index), as well as the hazards to neoplastic cell survival and the resources available to neoplastic cells, which make up an ecological index (Eco-index). We review evidence demonstrating the importance of each of these factors and describe multiple methods that can be used to measure them. Development of this classification system holds promise for enabling clinicians to personalize optimal interventions based on the evolvability of the patient's tumour. The Evo-A nd Eco-indices provide a common lexicon for communicating about how neoplasms change in response to interventions, with potential implications for clinical trials, personalized medicine and basic cancer research.

    Original languageEnglish (US)
    Pages (from-to)605-619
    Number of pages15
    JournalNature Reviews Cancer
    Volume17
    Issue number10
    DOIs
    StatePublished - Oct 1 2017

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    Neoplasms
    Ecology
    Precision Medicine
    Molecular Evolution
    Epigenomics
    Cell Survival
    Clinical Trials
    Research

    ASJC Scopus subject areas

    • Oncology
    • Cancer Research

    Cite this

    Maley, C., Aktipis, C. A., Graham, T. A., Sottoriva, A., Boddy, A. M., Janiszewska, M., ... Shibata, D. (2017). Classifying the evolutionary and ecological features of neoplasms. Nature Reviews Cancer, 17(10), 605-619. https://doi.org/10.1038/nrc.2017.69

    Classifying the evolutionary and ecological features of neoplasms. / Maley, Carlo; Aktipis, C Athena; Graham, Trevor A.; Sottoriva, Andrea; Boddy, Amy M.; Janiszewska, Michalina; Silva, Ariosto S.; Gerlinger, Marco; Yuan, Yinyin; Pienta, Kenneth J.; Anderson, Karen; Gatenby, Robert; Swanton, Charles; Posada, David; Wu, Chung I.; Schiffman, Joshua D.; Hwang, E. Shelley; Polyak, Kornelia; Anderson, Alexander R.A.; Brown, Joel S.; Greaves, Mel; Shibata, Darryl.

    In: Nature Reviews Cancer, Vol. 17, No. 10, 01.10.2017, p. 605-619.

    Research output: Contribution to journalReview article

    Maley, C, Aktipis, CA, Graham, TA, Sottoriva, A, Boddy, AM, Janiszewska, M, Silva, AS, Gerlinger, M, Yuan, Y, Pienta, KJ, Anderson, K, Gatenby, R, Swanton, C, Posada, D, Wu, CI, Schiffman, JD, Hwang, ES, Polyak, K, Anderson, ARA, Brown, JS, Greaves, M & Shibata, D 2017, 'Classifying the evolutionary and ecological features of neoplasms' Nature Reviews Cancer, vol. 17, no. 10, pp. 605-619. https://doi.org/10.1038/nrc.2017.69
    Maley, Carlo ; Aktipis, C Athena ; Graham, Trevor A. ; Sottoriva, Andrea ; Boddy, Amy M. ; Janiszewska, Michalina ; Silva, Ariosto S. ; Gerlinger, Marco ; Yuan, Yinyin ; Pienta, Kenneth J. ; Anderson, Karen ; Gatenby, Robert ; Swanton, Charles ; Posada, David ; Wu, Chung I. ; Schiffman, Joshua D. ; Hwang, E. Shelley ; Polyak, Kornelia ; Anderson, Alexander R.A. ; Brown, Joel S. ; Greaves, Mel ; Shibata, Darryl. / Classifying the evolutionary and ecological features of neoplasms. In: Nature Reviews Cancer. 2017 ; Vol. 17, No. 10. pp. 605-619.
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