Natural Killer Cells Control Tumor Growth by Sensing a Growth Factor

Cell. 2018 Jan 25;172(3):534-548.e19. doi: 10.1016/j.cell.2017.11.037. Epub 2017 Dec 21.

Abstract

Many tumors produce platelet-derived growth factor (PDGF)-DD, which promotes cellular proliferation, epithelial-mesenchymal transition, stromal reaction, and angiogenesis through autocrine and paracrine PDGFRβ signaling. By screening a secretome library, we found that the human immunoreceptor NKp44, encoded by NCR2 and expressed on natural killer (NK) cells and innate lymphoid cells, recognizes PDGF-DD. PDGF-DD engagement of NKp44 triggered NK cell secretion of interferon gamma (IFN)-γ and tumor necrosis factor alpha (TNF-α) that induced tumor cell growth arrest. A distinctive transcriptional signature of PDGF-DD-induced cytokines and the downregulation of tumor cell-cycle genes correlated with NCR2 expression and greater survival in glioblastoma. NKp44 expression in mouse NK cells controlled the dissemination of tumors expressing PDGF-DD more effectively than control mice, an effect enhanced by blockade of the inhibitory receptor CD96 or CpG-oligonucleotide treatment. Thus, while cancer cell production of PDGF-DD supports tumor growth and stromal reaction, it concomitantly activates innate immune responses to tumor expansion.

Keywords: NK cell; NKp44; PDGF-D; cancer; cell cycle; cytokines; growth factor; immunosurveillance; innate lymphoid cells.

Publication types

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

MeSH terms

  • Animals
  • Brain Neoplasms / immunology*
  • Brain Neoplasms / pathology
  • CHO Cells
  • Cell Cycle Checkpoints*
  • Cells, Cultured
  • Cricetinae
  • Cricetulus
  • Female
  • Glioblastoma / immunology*
  • Glioblastoma / pathology
  • Humans
  • Immunity, Innate
  • Interferon-gamma / metabolism
  • Killer Cells, Natural / immunology*
  • MCF-7 Cells
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Natural Cytotoxicity Triggering Receptor 2 / metabolism
  • Platelet-Derived Growth Factor / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Natural Cytotoxicity Triggering Receptor 2
  • Platelet-Derived Growth Factor
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma