Epithelial-mesenchymal transition leads to NK cell-mediated metastasis-specific immunosurveillance in lung cancer

J Clin Invest. 2018 Apr 2;128(4):1384-1396. doi: 10.1172/JCI97611. Epub 2018 Feb 26.

Abstract

During epithelial-mesenchymal transition (EMT) epithelial cancer cells transdifferentiate into highly motile, invasive, mesenchymal-like cells, giving rise to disseminating tumor cells. Few of these disseminated cells successfully metastasize. Immune cells and inflammation in the tumor microenvironment were shown to drive EMT, but few studies investigated the consequences of EMT for tumor immunosurveillance. In addition to initiating metastasis, we demonstrate that EMT confers increased susceptibility to natural killer (NK) cells and contributes, in part, to the inefficiency of the metastatic process. Depletion of NK cells allowed spontaneous metastasis without affecting primary tumor growth. EMT-induced modulation of E-cadherin and cell adhesion molecule 1 (CADM1) mediated increased susceptibility to NK cytotoxicity. Higher CADM1 expression correlates with improved patient survival in 2 lung and 1 breast adenocarcinoma patient cohorts and decreased metastasis. Our observations reveal a novel NK-mediated, metastasis-specific immunosurveillance in lung cancer and present a window of opportunity for preventing metastasis by boosting NK cell activity.

Keywords: Immunology; Immunotherapy; Lung cancer; NK cells; Oncology.

Publication types

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

MeSH terms

  • A549 Cells
  • Animals
  • Carcinoma, Lewis Lung / genetics
  • Carcinoma, Lewis Lung / immunology*
  • Carcinoma, Lewis Lung / pathology
  • Cell Adhesion Molecule-1 / genetics
  • Cell Adhesion Molecule-1 / immunology
  • Epithelial-Mesenchymal Transition / genetics
  • Epithelial-Mesenchymal Transition / immunology*
  • Female
  • Humans
  • Immunity, Cellular*
  • Immunologic Surveillance*
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / pathology
  • Lung Neoplasms / genetics
  • Lung Neoplasms / immunology*
  • Lung Neoplasms / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / immunology
  • Tumor Microenvironment / immunology*

Substances

  • CADM1 protein, human
  • Cadm1 protein, mouse
  • Cell Adhesion Molecule-1
  • Neoplasm Proteins