Epigenetic loss of heterozygosity of Apc and an inflammation-associated mutational signature detected in Lrig1+/--driven murine colonic adenomas

BMC Cancer. 2020 Feb 14;20(1):126. doi: 10.1186/s12885-020-6616-y.

Abstract

Background: The loss of a single copy of adenomatous polyposis coli (Apc) in leucine-rich repeats and immunoglobulin-like domains 1 (Lrig1)-expressing colonic progenitor cells induces rapid growth of adenomas in mice with high penetrance and multiplicity. The tumors lack functional APC, and a genetic loss of heterozygosity of Apc was previously observed.

Methods: To identify genomic features of early tumorigenesis, and to profile intertumoral genetic heterogeneity, tumor exome DNA (n = 9 tumors) and mRNA (n = 5 tumors) sequences were compared with matched nontumoral colon tissue. Putative somatic mutations were called after stringent variant filtering. Somatic signatures of mutational processes were determined and splicing patterns were observed.

Results: The adenomas were found to be genetically heterogeneous and unexpectedly hypermutated, displaying a strong bias toward G:C > A:T mutations. A genetic loss of heterozygosity of Apc was not observed, however, an epigenetic loss of heterozygosity was apparent in the tumor transcriptomes. Complex splicing patterns characterized by a loss of intron retention were observed uniformly across tumors.

Conclusion: This study demonstrates that early tumors originating from intestinal stem cells with reduced Lrig1 and Apc expression are highly mutated and genetically heterogeneous, with an inflammation-associated mutational signature and complex splicing patterns that are uniform across tumors.

Keywords: Adenoma; Colorectal cancer; Intestinal stem cells; Lgr5; Lrig1; Mutations.

MeSH terms

  • Animals
  • Cell Transformation, Neoplastic / genetics
  • Colonic Neoplasms / genetics*
  • Disease Models, Animal
  • Epigenesis, Genetic*
  • Exome
  • Gene Expression Profiling
  • Gene Silencing
  • Genes, APC*
  • Humans
  • Loss of Heterozygosity*
  • Membrane Glycoproteins / genetics*
  • Mice
  • Mutation*
  • Nerve Tissue Proteins / genetics*
  • Transcriptome

Substances

  • Lrig1 protein, mouse
  • Membrane Glycoproteins
  • Nerve Tissue Proteins

Grants and funding