MUC1-C Induces the LIN28B→LET-7→HMGA2 Axis to Regulate Self-Renewal in NSCLC

Mol Cancer Res. 2015 Mar;13(3):449-60. doi: 10.1158/1541-7786.MCR-14-0363. Epub 2014 Nov 3.

Abstract

The LIN28B→let-7 pathway contributes to regulation of the epithelial-mesenchymal transition (EMT) and stem cell self-renewal. The oncogenic MUC1-C transmembrane protein is aberrantly overexpressed in lung and other carcinomas; however, there is no known association between MUC1-C and the LIN28B→let-7 pathway. Here in non-small cell lung cancer (NSCLC), silencing MUC1-C downregulates the RNA-binding protein LIN28B and coordinately increases the miRNA let-7. Targeting MUC1-C function with a dominant-negative mutant or a peptide inhibitor provided confirming evidence that MUC1-C induces LIN28B→let-7 signaling. Mechanistically, MUC1-C promotes NF-κB p65 chromatin occupancy of the LIN28B first intron and activates LIN28B transcription, which is associated with suppression of let-7. Consistent with let-7-mediated inhibition of HMGA2 transcripts, targeting of MUC1-C also decreases HMGA2 expression. HMGA2 has been linked to stemness, and functions as a competing endogenous RNA (ceRNA) of let-7-mediated regulation of the TGFβ coreceptor TGFBR3. Accordingly, targeting MUC1-C suppresses HMGA2 mRNA and protein, which is associated with decreases in TGFBR3, reversal of the EMT phenotype, and inhibition of self-renewal capacity. These findings support a model in which MUC1-C activates the ⇑LIN28B→⇓let-7→⇑HMGA2 axis in NSCLC and thereby promotes EMT traits and stemness.

Implications: A novel pathway is defined in which MUC1-C drives LIN28B→let-7→HMGA2 signaling, EMT, and self-renewal in NSCLC.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Carcinoma, Non-Small-Cell Lung / genetics*
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Line, Tumor
  • Epithelial-Mesenchymal Transition
  • Gene Expression Regulation, Neoplastic
  • HMGA2 Protein / genetics
  • HMGA2 Protein / metabolism
  • Humans
  • Lung Neoplasms / genetics*
  • MicroRNAs / genetics*
  • Mucin-1 / chemistry
  • Mucin-1 / genetics*
  • RNA-Binding Proteins / genetics*
  • Signal Transduction

Substances

  • HMGA2 Protein
  • LIN28B protein, human
  • MUC1 protein, human
  • MicroRNAs
  • Mucin-1
  • RNA-Binding Proteins
  • mirnlet7 microRNA, human