Single-Chromosomal Gains Can Function as Metastasis Suppressors and Promoters in Colon Cancer

Dev Cell. 2020 Feb 24;52(4):413-428.e6. doi: 10.1016/j.devcel.2020.01.034.

Abstract

High levels of cancer aneuploidy are frequently associated with poor prognosis. To examine the relationship between aneuploidy and cancer progression, we analyzed a series of congenic cell lines that harbor single extra chromosomes. We found that across 13 different trisomic cell lines, 12 trisomies suppressed invasiveness or were largely neutral, while a single trisomy increased metastatic behavior by triggering a partial epithelial-mesenchymal transition. In contrast, we discovered that chromosomal instability activates cGAS/STING signaling but strongly suppresses invasiveness. By analyzing patient copy-number data, we demonstrate that specific aneuploidies are associated with distinct outcomes, and the acquisition of certain aneuploidies is in fact linked with a favorable prognosis. Thus, aneuploidy is not a uniform driver of malignancy, and different aneuploidies can uniquely influence tumor progression. At the same time, the gain of a single chromosome is capable of inducing a profound cell state transition, thereby linking genomic plasticity, phenotypic plasticity, and metastasis.

Keywords: EMT; aneuploidy; cGAS/STING; chromosome missegregation; copy number variation; metastasis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aneuploidy*
  • Animals
  • Apoptosis
  • Cell Movement*
  • Cell Proliferation
  • Chromosomal Instability*
  • Chromosomes, Human, Pair 5 / genetics*
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / pathology*
  • Colonic Neoplasms / prevention & control*
  • Epithelial-Mesenchymal Transition*
  • Female
  • Humans
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Nude
  • Neoplasm Invasiveness
  • Nucleotidyltransferases / genetics
  • Nucleotidyltransferases / metabolism
  • Tumor Cells, Cultured
  • Xenograft Model Antitumor Assays

Substances

  • Membrane Proteins
  • STING1 protein, human
  • Nucleotidyltransferases
  • cGAS protein, human