β-Catenin regulates deiodinase levels and thyroid hormone signaling in colon cancer cells

Gastroenterology. 2012 Oct;143(4):1037-47. doi: 10.1053/j.gastro.2012.06.042. Epub 2012 Jul 3.

Abstract

Background & aims: Activation of the β-catenin/T-cell factor (TCF) complex occurs in most colon tumors, and its actions correlate with the neoplastic phenotype of intestinal epithelial cells. Type 3 deiodinase (D3), the selenoenzyme that inactivates thyroid hormone (3,5,3' triiodothyronine [T3]), is frequently expressed by tumor cells, but little is known about its role in the regulation of T3 signaling in cancer cells.

Methods: We measured D3 expression in 6 colon cancer cell lines and human tumors and correlated it with the activity of the β-catenin/TCF complex. We also determined the effects of D3 loss on local thyroid hormone signaling and colon tumorigenesis.

Results: We show that D3 is a direct transcriptional target of the β-catenin/TCF complex; its expression was higher in human intestinal adenomas and carcinomas than in healthy intestinal tissue. Experimental attenuation of β-catenin reduced D3 levels and induced type 2 deiodinase (the D3 antagonist that converts 3,5,3',5' tetraiodothyronine into active T3) thereby increasing T3-dependent transcription. In the absence of D3, excess T3 reduced cell proliferation and promoted differentiation in cultured cells and in xenograft mouse models. This occurred via induction of E-cadherin, which sequestered β-catenin at the plasma membrane and promoted cell differentiation.

Conclusions: Deiodinases are at the interface between the β-catenin and the thyroid hormone pathways. Their synchronized regulation of intracellular T3 concentration is a hitherto unrecognized route by which the multiple effects of β-catenin are generated and may be targeted to reduce the oncogenic effects of β-catenin in intestinal cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoma / enzymology*
  • Adenoma / genetics
  • Adenoma / pathology
  • Animals
  • Caco-2 Cells
  • Cadherins / drug effects
  • Cadherins / metabolism
  • Carcinoma / enzymology*
  • Carcinoma / genetics
  • Carcinoma / pathology
  • Cell Differentiation / drug effects
  • Cell Proliferation / drug effects
  • Colon / enzymology
  • Colonic Neoplasms / enzymology*
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / pathology
  • Female
  • Gene Expression Regulation
  • HCT116 Cells
  • Humans
  • Iodide Peroxidase / genetics
  • Iodide Peroxidase / metabolism*
  • Iodothyronine Deiodinase Type II
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Plasmids
  • RNA, Messenger / metabolism
  • Transcription Factor 7-Like 2 Protein / genetics
  • Transcription Factor 7-Like 2 Protein / metabolism
  • Transfection
  • Transplantation, Heterologous
  • Triiodothyronine / metabolism*
  • Triiodothyronine / pharmacology
  • Wnt Signaling Pathway*
  • beta Catenin / metabolism*

Substances

  • Cadherins
  • RNA, Messenger
  • TCF7L2 protein, human
  • Transcription Factor 7-Like 2 Protein
  • beta Catenin
  • Triiodothyronine
  • iodothyronine deiodinase type III
  • Iodide Peroxidase