Advanced Intestinal Cancers often Maintain a Multi-Ancestral Architecture

PLoS One. 2016 Feb 26;11(2):e0150170. doi: 10.1371/journal.pone.0150170. eCollection 2016.

Abstract

A widely accepted paradigm in the field of cancer biology is that solid tumors are uni-ancestral being derived from a single founder and its descendants. However, data have been steadily accruing that indicate early tumors in mice and humans can have a multi-ancestral origin in which an initiated primogenitor facilitates the transformation of neighboring co-genitors. We developed a new mouse model that permits the determination of clonal architecture of intestinal tumors in vivo and ex vivo, have validated this model, and then used it to assess the clonal architecture of adenomas, intramucosal carcinomas, and invasive adenocarcinomas of the intestine. The percentage of multi-ancestral tumors did not significantly change as tumors progressed from adenomas with low-grade dysplasia [40/65 (62%)], to adenomas with high-grade dysplasia [21/37 (57%)], to intramucosal carcinomas [10/23 (43%]), to invasive adenocarcinomas [13/19 (68%)], indicating that the clone arising from the primogenitor continues to coexist with clones arising from co-genitors. Moreover, neoplastic cells from distinct clones within a multi-ancestral adenocarcinoma have even been observed to simultaneously invade into the underlying musculature [2/15 (13%)]. Thus, intratumoral heterogeneity arising early in tumor formation persists throughout tumorigenesis.

Publication types

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

MeSH terms

  • Adenocarcinoma / genetics
  • Adenocarcinoma / pathology*
  • Adenoma / genetics
  • Adenoma / pathology*
  • Animals
  • Carcinoma in Situ / genetics
  • Carcinoma in Situ / pathology*
  • Cell Lineage
  • Cell Transformation, Neoplastic* / genetics
  • Clone Cells / pathology
  • Disease Models, Animal
  • Disease Progression
  • Evolution, Molecular
  • Fatty Acid-Binding Proteins / genetics
  • Female
  • Gene Expression Regulation, Neoplastic
  • Genes, APC
  • Genes, Reporter
  • Integrases / genetics
  • Intestinal Mucosa / pathology
  • Intestinal Neoplasms / genetics
  • Intestinal Neoplasms / pathology*
  • Luminescent Proteins / analysis
  • Luminescent Proteins / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Models, Biological
  • Mosaicism
  • Neoplasm Invasiveness
  • Neoplastic Stem Cells / pathology*
  • RNA, Untranslated / genetics
  • Rats
  • Transgenes
  • Tumor Microenvironment

Substances

  • Fabp1 protein, rat
  • Fatty Acid-Binding Proteins
  • Gt(ROSA)26Sor non-coding RNA, mouse
  • Luminescent Proteins
  • RNA, Untranslated
  • Cre recombinase
  • Integrases