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Transient commensal clonal interactions can drive tumor metastasis

Author

Listed:
  • Suha Naffar-Abu Amara

    (Harvard Medical School)

  • Hendrik J. Kuiken

    (Harvard Medical School)

  • Laura M. Selfors

    (Harvard Medical School)

  • Timothy Butler

    (Oregon Health & Science University Portland
    Cancer, Ageing and Somatic Mutation, Wellcome Trust Sanger Institute)

  • Marco L. Leung

    (University of Texas MD Anderson Cancer Center
    Children’s Hospital of Philadelphia)

  • Cheuk T. Leung

    (Harvard Medical School
    University of Minnesota Medical School)

  • Elaine P. Kuhn

    (Harvard Medical School
    Dartmouth-Hitchcock Medical Center)

  • Teodora Kolarova

    (Harvard Medical School
    University of Washington)

  • Carina Hage

    (Harvard Medical School
    Roche Innovation Center Munich, Roche Pharmaceutical Research and Early Development, Nonnenwald 2)

  • Kripa Ganesh

    (Harvard Medical School
    Meyer Cancer Center, Weill Cornell Medicine
    Weill Cornell Medicine)

  • Richard Panayiotou

    (Harvard Medical School)

  • Rosemary Foster

    (Vincent Center for Reproductive Biology and Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Massachusetts General Hospital
    Harvard Medical School)

  • Bo R. Rueda

    (Vincent Center for Reproductive Biology and Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Massachusetts General Hospital
    Harvard Medical School)

  • Athena Aktipis

    (Arizona State University)

  • Paul Spellman

    (Oregon Health & Science University Portland)

  • Tan A. Ince

    (Weill Cornell Medicine
    New York Presbyterian-Brooklyn Methodist Hospital)

  • Joanne Xiu

    (Caris Life Sciences)

  • Matthew Oberley

    (Caris Life Sciences)

  • Zoran Gatalica

    (Caris Life Sciences
    University of Oklahoma Health Sciences Center)

  • Nicholas Navin

    (University of Texas MD Anderson Cancer Center)

  • Gordon B. Mills

    (Oregon Health and Science University Knight Cancer Institute)

  • Rodrick T. Bronson

    (Rodent Histopathology Core, Harvard Medical School)

  • Joan S. Brugge

    (Harvard Medical School)

Abstract

The extent and importance of functional heterogeneity and crosstalk between tumor cells is poorly understood. Here, we describe the generation of clonal populations from a patient-derived ovarian clear cell carcinoma model which forms malignant ascites and solid peritoneal tumors upon intraperitoneal transplantation in mice. The clonal populations are engineered with secreted Gaussia luciferase to monitor tumor growth dynamics and tagged with a unique DNA barcode to track their fate in multiclonal mixtures during tumor progression. Only one clone, CL31, grows robustly, generating exclusively malignant ascites. However, multiclonal mixtures form large solid peritoneal metastases, populated almost entirely by CL31, suggesting that transient cooperative interclonal interactions are sufficient to promote metastasis of CL31. CL31 uniquely harbors ERBB2 amplification, and its acquired metastatic activity in clonal mixtures is dependent on transient exposure to amphiregulin, which is exclusively secreted by non-tumorigenic clones. Amphiregulin enhances CL31 mesothelial clearance, a prerequisite for metastasis. These findings demonstrate that transient, ostensibly innocuous tumor subpopulations can promote metastases via “hit-and-run” commensal interactions.

Suggested Citation

  • Suha Naffar-Abu Amara & Hendrik J. Kuiken & Laura M. Selfors & Timothy Butler & Marco L. Leung & Cheuk T. Leung & Elaine P. Kuhn & Teodora Kolarova & Carina Hage & Kripa Ganesh & Richard Panayiotou & , 2020. "Transient commensal clonal interactions can drive tumor metastasis," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19584-1
    DOI: 10.1038/s41467-020-19584-1
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    Cited by:

    1. Rena Emond & Jason I. Griffiths & Vince Kornél Grolmusz & Aritro Nath & Jinfeng Chen & Eric F. Medina & Rachel S. Sousa & Timothy Synold & Frederick R. Adler & Andrea H. Bild, 2023. "Cell facilitation promotes growth and survival under drug pressure in breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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