STAT5 Is a Key Regulator in NK Cells and Acts as a Molecular Switch from Tumor Surveillance to Tumor Promotion

Cancer Discov. 2016 Apr;6(4):414-29. doi: 10.1158/2159-8290.CD-15-0732. Epub 2016 Feb 12.

Abstract

Natural killer (NK) cells are tightly regulated by the JAK-STAT signaling pathway and cannot survive in the absence of STAT5. We now report that STAT5-deficient NK cells can be rescued by overexpression of BCL2. Our experiments define STAT5 as a master regulator of NK-cell proliferation and lytic functions. Although NK cells are generally responsible for killing tumor cells, the rescued STAT5-deficient NK cells promote tumor formation by producing enhanced levels of the angiogenic factor VEGFA. The importance of VEGFA produced by NK cells was verified by experiments with a conditional knockout of VEGFA in NK cells. We show that STAT5 normally represses the transcription of VEGFA in NK cells, in both mice and humans. These findings reveal that STAT5-directed therapies may have negative effects: In addition to impairing NK-cell-mediated tumor surveillance, they may even promote tumor growth by enhancing angiogenesis.

Significance: The importance of the immune system in effective cancer treatment is widely recognized. We show that the new signal interceptors targeting the JAK-STAT5 pathway may have dangerous side effects that must be taken into account in clinical trials: inhibiting JAK-STAT5 has the potential to promote tumor growth by enhancing NK-cell-mediated angiogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation
  • Cell Proliferation
  • Cell Survival / genetics
  • Cell Transformation, Neoplastic / immunology*
  • Cell Transformation, Neoplastic / metabolism*
  • Cytotoxicity, Immunologic
  • Disease Models, Animal
  • Gene Expression
  • Gene Knockout Techniques
  • Humans
  • Immunologic Surveillance*
  • Killer Cells, Natural / cytology
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism*
  • Lymphocyte Activation
  • Mice
  • Mice, Transgenic
  • Neoplasms / immunology*
  • Neoplasms / metabolism*
  • Neoplasms / mortality
  • Neoplasms / pathology
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • STAT5 Transcription Factor / deficiency
  • STAT5 Transcription Factor / metabolism*
  • Vascular Endothelial Growth Factor A / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Proto-Oncogene Proteins c-bcl-2
  • STAT5 Transcription Factor
  • Vascular Endothelial Growth Factor A