Metastatic consequences of immune escape from NK cell cytotoxicity by human breast cancer stem cells

Cancer Res. 2014 Oct 15;74(20):5746-57. doi: 10.1158/0008-5472.CAN-13-2563. Epub 2014 Aug 27.

Abstract

Breast cancer stem-like cells (BCSC) are crucial for metastasis but the underlying mechanisms remain elusive. Here, we report that tumor-infiltrating natural killer (NK) cells failed to limit metastasis and were not associated with improved therapeutic outcome of BCSC-rich breast cancer. Primary BCSCs were resistant to cytotoxicity mediated by autologous/allogeneic NK cells due to reduced expression of MICA and MICB, two ligands for the stimulatory NK cell receptor NKG2D. Furthermore, the downregulation of MICA/MICB in BCSCs was mediated by aberrantly expressed oncogenic miR20a, which promoted the resistance of BCSC to NK cell cytotoxicity and resultant lung metastasis. The breast cancer cell differentiation-inducing agent, all-trans retinoic acid, restored the miR20a-MICA/MICB axis and sensitized BCSC to NK cell-mediated killing, thereby reducing immune escape-associated BCSC metastasis. Together, our findings reveal a novel mechanism for immune escape of human BCSC and identify the miR20a-MICA/MICB signaling axis as a therapeutic target to limit metastatic breast cancer.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Breast Neoplasms / immunology*
  • Breast Neoplasms / pathology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Histocompatibility Antigens Class I / metabolism
  • Humans
  • K562 Cells
  • Killer Cells, Natural / immunology*
  • Lung Neoplasms / immunology*
  • Lung Neoplasms / secondary
  • Mice, Inbred NOD
  • Mice, SCID
  • MicroRNAs / metabolism
  • Middle Aged
  • Neoplasm Transplantation
  • Neoplastic Stem Cells / immunology*
  • Neoplastic Stem Cells / pathology
  • RNA Interference
  • Tumor Escape*
  • Young Adult

Substances

  • Histocompatibility Antigens Class I
  • MHC class I-related chain A
  • MICB antigen
  • MIRN20a microRNA, human
  • MicroRNAs