A polymorphic enhancer near GREM1 influences bowel cancer risk through differential CDX2 and TCF7L2 binding

Cell Rep. 2014 Aug 21;8(4):983-90. doi: 10.1016/j.celrep.2014.07.020. Epub 2014 Aug 14.

Abstract

A rare germline duplication upstream of the bone morphogenetic protein antagonist GREM1 causes a Mendelian-dominant predisposition to colorectal cancer (CRC). The underlying disease mechanism is strong, ectopic GREM1 overexpression in the intestinal epithelium. Here, we confirm that a common GREM1 polymorphism, rs16969681, is also associated with CRC susceptibility, conferring ∼20% differential risk in the general population. We hypothesized the underlying cause to be moderate differences in GREM1 expression. We showed that rs16969681 lies in a region of active chromatin with allele- and tissue-specific enhancer activity. The CRC high-risk allele was associated with stronger gene expression, and higher Grem1 mRNA levels increased the intestinal tumor burden in Apc(Min) mice. The intestine-specific transcription factor CDX2 and Wnt effector TCF7L2 bound near rs16969681, with significantly higher affinity for the risk allele, and CDX2 overexpression in CDX2/GREM1-negative cells caused re-expression of GREM1. rs16969681 influences CRC risk through effects on Wnt-driven GREM1 expression in colorectal tumors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • CDX2 Transcription Factor
  • Cell Line, Tumor
  • Colonic Neoplasms / genetics*
  • Enhancer Elements, Genetic
  • Gene Expression Regulation, Neoplastic
  • Genetic Association Studies
  • Genetic Predisposition to Disease
  • Homeodomain Proteins / metabolism*
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Mice, Transgenic
  • Organ Specificity
  • Polymorphism, Single Nucleotide
  • Risk
  • Transcription Factor 7-Like 2 Protein / metabolism*

Substances

  • CDX2 Transcription Factor
  • CDX2 protein, human
  • GREM1 protein, human
  • Homeodomain Proteins
  • Intercellular Signaling Peptides and Proteins
  • TCF7L2 protein, human
  • Transcription Factor 7-Like 2 Protein