Mitogen-inducible gene-6 is a multifunctional adaptor protein with tumor suppressor-like activity in papillary thyroid cancer

J Clin Endocrinol Metab. 2011 Mar;96(3):E554-65. doi: 10.1210/jc.2010-1800. Epub 2010 Dec 29.

Abstract

Context: Low tumoral expression of mitogen-inducible gene-6 (Mig-6) is associated with papillary thyroid cancer (PTC) recurrence after thyroidectomy.

Objective: We hypothesize that Mig-6 behaves as a tumor suppressor in PTC.

Design: Mig-6 expression and promoter methylation status were compared in 31 PTC specimens with matched normal thyroid tissue from the same patient. The impact of Mig-6 loss and gain of function on nuclear factor κ-light-chain-enhancer of activated B cells (NF-κB) activation, global tyrosine kinase phosphorylation, and cellular invasion was determined in vitro.

Results: Mig-6 protein was abundant in all normal thyroid specimens, whereas 77% of PTC had low Mig-6 expression. Mig-6 promoter methylation was found in 79% of PTC with low Mig-6 expression. Low Mig-6 expression in PTC specimens was associated with low NF-κB activity but high levels of epidermal growth factor receptor (EGFR) and ERK phosphorylation. Mig-6 expression inversely correlated with PTC size but had no association with other clinicopathological variables including age, extrathyroidal extension, lymphovascular invasion, or histological subtype. Mig-6 knockdown in thyroid cancer cell lines resulted in EGFR phosphorylation and diminished NF-κB activity, whereas Mig-6 overexpression had the opposite effects. Mig-6 knockdown activated ErbB2, Met, and Src phosphorylation. Furthermore, Mig-6 regulated ERK phosphorylation independent from its effects on EGFR. Mig-6 knockdown promoted cellular proliferation, as determined by clonogenic survival. Lastly, Mig-6 knockdown increased matrix metalloproteinase-2 and -9 activities and increased cellular invasion.

Conclusions: Mig-6 has tumor suppressor-like activity in PTC. In vivo studies are required to confirm that Mig-6 is a putative tumor suppressor in PTC, and future studies should investigate the utility of Mig-6 as a diagnostic marker.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Blotting, Western
  • Carcinoma
  • Carcinoma, Papillary / genetics*
  • Carcinoma, Papillary / pathology
  • Cell Line, Tumor
  • Cell Nucleus / chemistry
  • Cells, Cultured
  • Cytosol / chemistry
  • DNA, Neoplasm / genetics
  • DNA, Neoplasm / isolation & purification
  • Diffusion Chambers, Culture
  • Down-Regulation
  • ErbB Receptors / metabolism
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Genes, Tumor Suppressor / physiology*
  • Humans
  • NF-kappa B / genetics
  • Neoplasm Invasiveness / genetics
  • Phosphorylation
  • Reverse Transcriptase Polymerase Chain Reaction
  • Thyroid Cancer, Papillary
  • Thyroid Neoplasms / genetics
  • Thyroid Neoplasms / pathology
  • Tumor Stem Cell Assay
  • Tumor Suppressor Proteins / genetics*

Substances

  • Adaptor Proteins, Signal Transducing
  • DNA, Neoplasm
  • ERRFI1 protein, human
  • NF-kappa B
  • Tumor Suppressor Proteins
  • ErbB Receptors
  • Extracellular Signal-Regulated MAP Kinases