MSH3-deficiency initiates EMAST without oncogenic transformation of human colon epithelial cells

PLoS One. 2012;7(11):e50541. doi: 10.1371/journal.pone.0050541. Epub 2012 Nov 27.

Abstract

Background/aim: Elevated microsatellite instability at selected tetranucleotide repeats (EMAST) is a genetic signature in certain cases of sporadic colorectal cancer and has been linked to MSH3-deficiency. It is currently controversial whether EMAST is associated with oncogenic properties in humans, specifically as cancer development in Msh3-deficient mice is not enhanced. However, a mutator phenotype is different between species as the genetic positions of repetitive sequences are not conserved. Here we studied the molecular effects of human MSH3-deficiency.

Methods: HCT116 and HCT116+chr3 (both MSH3-deficient) and primary human colon epithelial cells (HCEC, MSH3-wildtype) were stably transfected with an EGFP-based reporter plasmid for the detection of frameshift mutations within an [AAAG]17 repeat. MSH3 was silenced by shRNA and changes in protein expression were analyzed by shotgun proteomics. Colony forming assay was used to determine oncogenic transformation and double strand breaks (DSBs) were assessed by Comet assay.

Results: Despite differential MLH1 expression, both HCT116 and HCT116+chr3 cells displayed comparable high mutation rates (about 4×10(-4)) at [AAAG]17 repeats. Silencing of MSH3 in HCECs leads to a remarkable increased frameshift mutations in [AAAG]17 repeats whereas [CA]13 repeats were less affected. Upon MSH3-silencing, significant changes in the expression of 202 proteins were detected. Pathway analysis revealed overexpression of proteins involved in double strand break repair (MRE11 and RAD50), apoptosis, L1 recycling, and repression of proteins involved in metabolism, tRNA aminoacylation, and gene expression. MSH3-silencing did not induce oncogenic transformation and DSBs increased 2-fold.

Conclusions: MSH3-deficiency in human colon epithelial cells results in EMAST, formation of DSBs and significant changes of the proteome but lacks oncogenic transformation. Thus, MSH3-deficiency alone is unlikely to drive human colon carcinogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Colon / cytology
  • Colon / metabolism*
  • Colon / pathology*
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / pathology*
  • DNA Breaks, Double-Stranded
  • DNA-Binding Proteins / deficiency*
  • DNA-Binding Proteins / metabolism
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Humans
  • Male
  • Microsatellite Instability*
  • Microsatellite Repeats / genetics*
  • MutS Homolog 3 Protein

Substances

  • DNA-Binding Proteins
  • MSH3 protein, human
  • MutS Homolog 3 Protein

Grants and funding

This study was supported by the Austrian Science Fund (FWF grant P18270) and the Christian Doppler Research Association. The financial support by the Federal Ministry of Economy, Family and Youth, and the National Foundation for Research, Technology and Development is gratefully acknowledged. CG received research support from AOP Orphan Pharmaceuticals, Biogena Naturstoffe GmbH, and Shire Pharmaceuticals. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.