TRF2 inhibits a cell-extrinsic pathway through which natural killer cells eliminate cancer cells

Nat Cell Biol. 2013 Jul;15(7):818-28. doi: 10.1038/ncb2774. Epub 2013 Jun 23.

Abstract

Dysfunctional telomeres suppress tumour progression by activating cell-intrinsic programs that lead to growth arrest. Increased levels of TRF2, a key factor in telomere protection, are observed in various human malignancies and contribute to oncogenesis. We demonstrate here that a high level of TRF2 in tumour cells decreased their ability to recruit and activate natural killer (NK) cells. Conversely, a reduced dose of TRF2 enabled tumour cells to be more easily eliminated by NK cells. Consistent with these results, a progressive upregulation of TRF2 correlated with decreased NK cell density during the early development of human colon cancer. By screening for TRF2-bound genes, we found that HS3ST4--a gene encoding for the heparan sulphate (glucosamine) 3-O-sulphotransferase 4--was regulated by TRF2 and inhibited the recruitment of NK cells in an epistatic relationship with TRF2. Overall, these results reveal a TRF2-dependent pathway that is tumour-cell extrinsic and regulates NK cell immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Blotting, Western
  • Breast Neoplasms / immunology
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / prevention & control*
  • Cell Adhesion
  • Cell Proliferation
  • Colonic Neoplasms / immunology
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / prevention & control*
  • DNA Primers / chemistry
  • Discoidin Domain Receptor 1
  • Female
  • Flow Cytometry
  • HeLa Cells
  • Humans
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Killer Cells, Natural / pathology
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Lymphocytes, Tumor-Infiltrating / pathology
  • Melanoma, Experimental / immunology
  • Melanoma, Experimental / metabolism
  • Melanoma, Experimental / prevention & control*
  • Mice
  • Mice, Nude
  • RNA, Messenger / genetics
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sulfotransferases / genetics
  • Sulfotransferases / metabolism*
  • Telomeric Repeat Binding Protein 2 / antagonists & inhibitors
  • Telomeric Repeat Binding Protein 2 / genetics
  • Telomeric Repeat Binding Protein 2 / metabolism*
  • Tumor Cells, Cultured

Substances

  • DNA Primers
  • RNA, Messenger
  • RNA, Small Interfering
  • Telomeric Repeat Binding Protein 2
  • DDR1 protein, human
  • Discoidin Domain Receptor 1
  • Receptor Protein-Tyrosine Kinases
  • Sulfotransferases
  • heparitin sulfotransferase