Loss of a single Hic1 allele accelerates polyp formation in Apc(Δ716) mice

Oncogene. 2011 Jun 9;30(23):2659-69. doi: 10.1038/onc.2010.633. Epub 2011 Feb 7.

Abstract

Adenomatous polyposis coli (APC) gene mutations have been implicated in familial and sporadic gastrointestinal (GI) cancers. APC mutations are associated with autosomal dominant inheritance of disease in humans. Similarly, mice that contain a single mutant APC gene encoding a protein truncated at residue 716 (Apc(Δ716)) develop multiple polyps throughout the GI tract as early as 4 weeks after birth. Inactivation of another tumor suppressor gene, Hypermethylated in Cancer 1 (HIC1), often occurs in human colon cancers, among others, via CpG island hypermethylation. Homozygous deletion of Hic1 in mice results in major developmental defects and embryonic lethality. Hic1 heterozygotes have previously been shown to develop tumors of a variety of tissue types. We now report that loss of a single Hic1 allele can promote crypt hyperplasia and neoplasia of the GI tract, and Hic1(+/-), Apc(+/Δ716) double heterozygotes (DH) develop increased numbers of polyps throughout the GI tract at 60 days. Hic1 expression is absent in polyps from DH mice, with concomitant increased expression of two transcriptional repression targets of Hic1, Sirt1 and Sox9. Together, our data suggest that loss of a gene frequently silenced via epigenetic mechanisms, Hic1, can cooperate with loss of a gene mutated in GI cancer, Apc, to promote tumorigenesis in an in vivo model of multiple intestinal neoplasia.

Publication types

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

MeSH terms

  • Adenomatous Polyposis Coli / genetics*
  • Adenomatous Polyposis Coli / metabolism
  • Adenomatous Polyposis Coli / pathology
  • Adenomatous Polyposis Coli Protein / genetics*
  • Adenomatous Polyposis Coli Protein / metabolism
  • Animals
  • Cells, Cultured
  • CpG Islands / genetics
  • DNA Methylation
  • Embryo, Mammalian / cytology
  • Female
  • Fibroblasts / metabolism
  • Gene Expression Regulation, Neoplastic
  • HCT116 Cells
  • Heterozygote
  • Humans
  • Hyperplasia
  • Immunohistochemistry
  • Intestine, Small / metabolism*
  • Intestine, Small / pathology
  • Kruppel-Like Transcription Factors / genetics*
  • Kruppel-Like Transcription Factors / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Reverse Transcriptase Polymerase Chain Reaction
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism
  • Sirtuin 1 / genetics
  • Sirtuin 1 / metabolism

Substances

  • Adenomatous Polyposis Coli Protein
  • Hic1 protein, mouse
  • Kruppel-Like Transcription Factors
  • SOX9 Transcription Factor
  • Sox9 protein, mouse
  • Sirt1 protein, mouse
  • Sirtuin 1