BCL9L Dysfunction Impairs Caspase-2 Expression Permitting Aneuploidy Tolerance in Colorectal Cancer

Cancer Cell. 2017 Jan 9;31(1):79-93. doi: 10.1016/j.ccell.2016.11.001.

Abstract

Chromosomal instability (CIN) contributes to cancer evolution, intratumor heterogeneity, and drug resistance. CIN is driven by chromosome segregation errors and a tolerance phenotype that permits the propagation of aneuploid genomes. Through genomic analysis of colorectal cancers and cell lines, we find frequent loss of heterozygosity and mutations in BCL9L in aneuploid tumors. BCL9L deficiency promoted tolerance of chromosome missegregation events, propagation of aneuploidy, and genetic heterogeneity in xenograft models likely through modulation of Wnt signaling. We find that BCL9L dysfunction contributes to aneuploidy tolerance in both TP53-WT and mutant cells by reducing basal caspase-2 levels and preventing cleavage of MDM2 and BID. Efforts to exploit aneuploidy tolerance mechanisms and the BCL9L/caspase-2/BID axis may limit cancer diversity and evolution.

Keywords: BCL9L; BID; aneuploidy tolerance; caspase-2; chromosomal instability; chromosome segregation errors; colorectal cancer evolution; intratumor heterogeneity; mitotic checkpoint; p53.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Aneuploidy*
  • Animals
  • BH3 Interacting Domain Death Agonist Protein / physiology
  • Caspase 2 / analysis
  • Caspase 2 / physiology*
  • Chromosome Segregation
  • Colorectal Neoplasms / genetics*
  • Cysteine Endopeptidases / analysis
  • Cysteine Endopeptidases / physiology*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • HCT116 Cells
  • Humans
  • Mice
  • Middle Aged
  • Mutation
  • Proto-Oncogene Proteins c-mdm2 / physiology
  • Transcription Factors / genetics
  • Transcription Factors / physiology*
  • Tumor Suppressor Protein p53 / physiology

Substances

  • BCL9L protein, human
  • BH3 Interacting Domain Death Agonist Protein
  • BID protein, human
  • DNA-Binding Proteins
  • TP53 protein, human
  • Transcription Factors
  • Tumor Suppressor Protein p53
  • MDM2 protein, human
  • Proto-Oncogene Proteins c-mdm2
  • CASP2 protein, human
  • Caspase 2
  • Cysteine Endopeptidases