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Minimal barriers to invasion during human colorectal tumor growth

Author

Listed:
  • Marc D. Ryser

    (Duke University Medical Center
    Duke University
    Duke Cancer Institute)

  • Diego Mallo

    (Arizona State University)

  • Allison Hall

    (Duke University Medical Center)

  • Timothy Hardman

    (Duke University Medical Center)

  • Lorraine M. King

    (Duke University Medical Center)

  • Sergei Tatishchev

    (University of Southern California Keck School of Medicine)

  • Inmaculada C. Sorribes

    (Duke University)

  • Carlo C. Maley

    (Arizona State University)

  • Jeffrey R. Marks

    (Duke Cancer Institute
    Duke University Medical Center)

  • E. Shelley Hwang

    (Duke Cancer Institute
    Duke University Medical Center)

  • Darryl Shibata

    (University of Southern California Keck School of Medicine)

Abstract

Intra-tumoral heterogeneity (ITH) could represent clonal evolution where subclones with greater fitness confer more malignant phenotypes and invasion constitutes an evolutionary bottleneck. Alternatively, ITH could represent branching evolution with invasion of multiple subclones. The two models respectively predict a hierarchy of subclones arranged by phenotype, or multiple subclones with shared phenotypes. We delineate these modes of invasion by merging ancestral, topographic, and phenotypic information from 12 human colorectal tumors (11 carcinomas, 1 adenoma) obtained through saturation microdissection of 325 small tumor regions. The majority of subclones (29/46, 60%) share superficial and invasive phenotypes. Of 11 carcinomas, 9 show evidence of multiclonal invasion, and invasive and metastatic subclones arise early along the ancestral trees. Early multiclonal invasion in the majority of these tumors indicates the expansion of co-evolving subclones with similar malignant potential in absence of late bottlenecks and suggests that barriers to invasion are minimal during colorectal cancer growth.

Suggested Citation

  • Marc D. Ryser & Diego Mallo & Allison Hall & Timothy Hardman & Lorraine M. King & Sergei Tatishchev & Inmaculada C. Sorribes & Carlo C. Maley & Jeffrey R. Marks & E. Shelley Hwang & Darryl Shibata, 2020. "Minimal barriers to invasion during human colorectal tumor growth," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-14908-7
    DOI: 10.1038/s41467-020-14908-7
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    Cited by:

    1. Xiaodong Liu & Ke Zhang & Neslihan A. Kaya & Zhe Jia & Dafei Wu & Tingting Chen & Zhiyuan Liu & Sinan Zhu & Axel M. Hillmer & Torsten Wuestefeld & Jin Liu & Yun Shen Chan & Zheng Hu & Liang Ma & Li Ji, 2024. "Tumor phylogeography reveals block-shaped spatial heterogeneity and the mode of evolution in Hepatocellular Carcinoma," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Jonas Langerud & Ina A. Eilertsen & Seyed H. Moosavi & Solveig M. K. Klokkerud & Henrik M. Reims & Ingeborg F. Backe & Merete Hektoen & Ole H. Sjo & Marine Jeanmougin & Sabine Tejpar & Arild Nesbakken, 2024. "Multiregional transcriptomics identifies congruent consensus subtypes with prognostic value beyond tumor heterogeneity of colorectal cancer," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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