Polyclonality overcomes fitness barriers in Apc-driven tumorigenesis

Nature. 2024 Oct;634(8036):1196-1203. doi: 10.1038/s41586-024-08053-0. Epub 2024 Oct 30.

Abstract

Loss-of-function mutations in the tumour suppressor APC are an initial step in intestinal tumorigenesis1,2. APC-mutant intestinal stem cells outcompete their wild-type neighbours through the secretion of Wnt antagonists, which accelerates the fixation and subsequent rapid clonal expansion of mutants3-5. Reports of polyclonal intestinal tumours in human patients and mouse models appear at odds with this process6,7. Here we combine multicolour lineage tracing with chemical mutagenesis in mice to show that a large proportion of intestinal tumours have a multiancestral origin. Polyclonal tumours retain a structure comprising subclones with distinct Apc mutations and transcriptional states, driven predominantly by differences in KRAS and MYC signalling. These pathway-level changes are accompanied by profound differences in cancer stem cell phenotypes. Of note, these findings are confirmed by introducing an oncogenic Kras mutation that results in predominantly monoclonal tumour formation. Further, polyclonal tumours have accelerated growth dynamics, suggesting a link between polyclonality and tumour progression. Together, these findings demonstrate the role of interclonal interactions in promoting tumorigenesis through non-cell autonomous pathways that are dependent on the differential activation of oncogenic pathways between clones.

MeSH terms

  • Adenomatous Polyposis Coli Protein* / genetics
  • Adenomatous Polyposis Coli Protein* / metabolism
  • Animals
  • Cell Lineage*
  • Cell Transformation, Neoplastic* / genetics
  • Cell Transformation, Neoplastic* / pathology
  • Clone Cells* / metabolism
  • Clone Cells* / pathology
  • Disease Progression
  • Female
  • Genes, APC
  • Genetic Fitness* / genetics
  • Humans
  • Intestinal Neoplasms / genetics
  • Intestinal Neoplasms / metabolism
  • Intestinal Neoplasms / pathology
  • Loss of Function Mutation / genetics
  • Male
  • Mice
  • Mutation*
  • Neoplastic Stem Cells* / metabolism
  • Neoplastic Stem Cells* / pathology
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Proto-Oncogene Proteins p21(ras) / metabolism
  • Signal Transduction
  • Transcription, Genetic

Substances

  • Adenomatous Polyposis Coli Protein
  • adenomatous polyposis coli protein, mouse
  • Hras protein, mouse
  • Proto-Oncogene Proteins c-myc
  • Proto-Oncogene Proteins p21(ras)
  • Myc protein, mouse