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Prostate cancer evolution from multilineage primary to single lineage metastases with implications for liquid biopsy

Author

Listed:
  • D. J. Woodcock

    (University of Oxford)

  • E. Riabchenko

    (Tampere University and Tays Cancer Center)

  • S. Taavitsainen

    (Tampere University and Tays Cancer Center)

  • M. Kankainen

    (University of Helsinki and Helsinki University Hospital)

  • G. Gundem

    (Memorial Sloan Kettering Cancer Center)

  • D. S. Brewer

    (University of East Anglia)

  • P. Ellonen

    (University of Helsinki)

  • M. Lepistö

    (University of Helsinki)

  • Y. A. Golubeva

    (NCI, FNLCR, Leidos Biomedical Research, Inc)

  • A. C. Warner

    (Frederick National Laboratory for Cancer Research)

  • T. Tolonen

    (Tampere University and Tays Cancer Center
    Tampere University Hospital)

  • J. Jasu

    (Tampere University and Tays Cancer Center)

  • W. B. Isaacs

    (Johns Hopkins University School of Medicine)

  • M. R. Emmert-Buck

    (National Cancer Institute, National Institutes of Health
    Avoneaux Medical Institute)

  • M. Nykter

    (Tampere University and Tays Cancer Center)

  • T. Visakorpi

    (Tampere University and Tays Cancer Center
    Tampere University Hospital)

  • G. S. Bova

    (Tampere University and Tays Cancer Center)

  • D. C. Wedge

    (University of Oxford
    Oxford NIHR Biomedical Research Centre
    University of Manchester)

Abstract

The evolutionary progression from primary to metastatic prostate cancer is largely uncharted, and the implications for liquid biopsy are unexplored. We infer detailed reconstructions of tumor phylogenies in ten prostate cancer patients with fatal disease, and investigate them in conjunction with histopathology and tumor DNA extracted from blood and cerebrospinal fluid. Substantial evolution occurs within the prostate, resulting in branching into multiple spatially intermixed lineages. One dominant lineage emerges that initiates and drives systemic metastasis, where polyclonal seeding between sites is common. Routes to metastasis differ between patients, and likely genetic drivers of metastasis distinguish the metastatic lineage from the lineage that remains confined to the prostate within each patient. Body fluids capture features of the dominant lineage, and subclonal expansions that occur in the metastatic phase are non-uniformly represented. Cerebrospinal fluid analysis reveals lineages not detected in blood-borne DNA, suggesting possible clinical utility.

Suggested Citation

  • D. J. Woodcock & E. Riabchenko & S. Taavitsainen & M. Kankainen & G. Gundem & D. S. Brewer & P. Ellonen & M. Lepistö & Y. A. Golubeva & A. C. Warner & T. Tolonen & J. Jasu & W. B. Isaacs & M. R. Emmer, 2020. "Prostate cancer evolution from multilineage primary to single lineage metastases with implications for liquid biopsy," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18843-5
    DOI: 10.1038/s41467-020-18843-5
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    Cited by:

    1. Udit Singhal & Srinivas Nallandhighal & Jeffrey J. Tosoian & Kevin Hu & Trinh M. Pham & Judith Stangl-Kremser & Chia-Jen Liu & Razeen Karim & Komal R. Plouffe & Todd M. Morgan & Marcin Cieslik & Rober, 2024. "Integrative multi-region molecular profiling of primary prostate cancer in men with synchronous lymph node metastasis," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    2. A. M. Mahedi Hasan & Paolo Cremaschi & Daniel Wetterskog & Anuradha Jayaram & Stephen Q. Wong & Scott Williams & Anupama Pasam & Anna Trigos & Blanca Trujillo & Emily Grist & Stefanie Friedrich & Osva, 2023. "Copy number architectures define treatment-mediated selection of lethal prostate cancer clones," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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