Inhibition of tumor growth by NK1.1+ cells and CD8+ T cells activated by IL-15 through receptor beta/common gamma signaling in trans

J Immunol. 2008 Dec 15;181(12):8237-47. doi: 10.4049/jimmunol.181.12.8237.

Abstract

IL-15 is an important cytokine involved in the survival and function of CD8(+) T cells and NK cells. IL-15 can be presented by IL-15Ralpha (IL-15RA) to bind with the shared IL-2/IL-15Rbeta and common gamma-chains, which activate signaling pathways on NK cells and CD8(+) T cells. In the present study, we characterized the function of trans-presented IL-15 on NK cells and CD8(+) T cells using TC-1 tumor cells transduced with a retrovirus encoding IL-15 linked to IL-15RA (IL-15/IL-15RA). We demonstrated that the expression of IL-15/IL-15RA on TC-1 cells led to increased percentages of tumor-infiltrating NK cells, NKT cells, and CD8(+) T cells, resulting in the inhibition of tumor growth in challenged mice. Additionally, in vivo Ab depletion experiments demonstrated that NK1.1(+) cells and CD8(+) T cells were important in this inhibition of tumor growth. Furthermore, this accumulation of immune cells and inhibition of tumor growth was abolished by a single amino acid mutation in the common gamma-chain binding site on IL-15. We also observed that IL-15/IL-15RA-transduced TC-1 cells led to the activation of STAT5 in NK and CD8(+) T cells in trans, which was abolished in the mutated IL-15/IL-15RA-transduced TC-1 cells. Taken together, our data suggest that common gamma-chain binding-dependent activation of the shared IL-15/IL-2Rbeta/common gamma signaling pathway may play an important role in the activation of NK cells and CD8(+) T cells, resulting in IL-15/IL-15RA trans-presentation-mediated inhibition of tumor growth.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigen Presentation / genetics
  • Antigens, Ly / biosynthesis*
  • Antigens, Ly / physiology
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / pathology
  • Cell Line, Tumor
  • Female
  • Growth Inhibitors / biosynthesis
  • Growth Inhibitors / physiology*
  • Interleukin Receptor Common gamma Subunit / genetics
  • Interleukin Receptor Common gamma Subunit / physiology*
  • Interleukin-15 / biosynthesis
  • Interleukin-15 / genetics
  • Interleukin-15 / metabolism
  • Interleukin-15 / physiology*
  • Interleukin-15 Receptor alpha Subunit / biosynthesis
  • Interleukin-15 Receptor alpha Subunit / genetics
  • Interleukin-15 Receptor alpha Subunit / metabolism
  • Interleukin-15 Receptor alpha Subunit / physiology
  • Interleukin-2 Receptor beta Subunit / physiology*
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Killer Cells, Natural / pathology
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • NK Cell Lectin-Like Receptor Subfamily B / biosynthesis*
  • NK Cell Lectin-Like Receptor Subfamily B / physiology
  • Ovarian Neoplasms / immunology
  • Ovarian Neoplasms / pathology
  • Ovarian Neoplasms / prevention & control*
  • Ovarian Neoplasms / virology
  • Retroviridae / genetics
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Transduction, Genetic

Substances

  • Antigens, Ly
  • Growth Inhibitors
  • Il2rb protein, mouse
  • Interleukin Receptor Common gamma Subunit
  • Interleukin-15
  • Interleukin-15 Receptor alpha Subunit
  • Interleukin-2 Receptor beta Subunit
  • Klrb1c protein, mouse
  • NK Cell Lectin-Like Receptor Subfamily B