miR-155 drives telomere fragility in human breast cancer by targeting TRF1

Cancer Res. 2014 Aug 1;74(15):4145-56. doi: 10.1158/0008-5472.CAN-13-2038. Epub 2014 May 29.

Abstract

Telomeres consist of DNA tandem repeats that recruit the multiprotein complex shelterin to build a chromatin structure that protects chromosome ends. Although cancer formation is linked to alterations in telomere homeostasis, there is little understanding of how shelterin function is limited in cancer cells. Using a small-scale screening approach, we identified miR-155 as a key regulator in breast cancer cell expression of the shelterin component TERF1 (TRF1). miR-155 targeted a conserved sequence motif in the 3'UTR of TRF1, resulting in its translational repression. miR-155 was upregulated commonly in breast cancer specimens, as associated with reduced TRF1 protein expression, metastasis-free survival, and relapse-free survival in estrogen receptor-positive cases. Modulating miR-155 expression in cells altered TRF1 levels and TRF1 abundance at telomeres. Compromising TRF1 expression by elevating miR-155 increased telomere fragility and altered the structure of metaphase chromosomes. In contrast, reducing miR-155 levels improved telomere function and genomic stability. These results implied that miR-155 upregulation antagonizes telomere integrity in breast cancer cells, increasing genomic instability linked to poor clinical outcome in estrogen receptor-positive disease. Our work argued that miRNA-dependent regulation of shelterin function has a clinically significant impact on telomere function, suggesting the existence of "telo-miRNAs" that have an impact on cancer and aging.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Base Sequence
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / metabolism
  • Cell Culture Techniques
  • Female
  • HCT116 Cells
  • HeLa Cells
  • Humans
  • MCF-7 Cells
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Molecular Sequence Data
  • Sequence Homology, Nucleic Acid
  • Telomere / genetics*
  • Telomere / metabolism
  • Telomeric Repeat Binding Protein 1 / genetics*
  • Telomeric Repeat Binding Protein 1 / metabolism
  • Transfection

Substances

  • 3' Untranslated Regions
  • MIRN155 microRNA, human
  • MicroRNAs
  • Telomeric Repeat Binding Protein 1