IL-15.IL-15Rα complex shedding following trans-presentation is essential for the survival of IL-15 responding NK and T cells

Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8565-70. doi: 10.1073/pnas.1405514111. Epub 2014 May 27.

Abstract

Interleukin (IL)-15 and its specific receptor chain, IL-15Rα, support the development of various effector cells, including NK and CD8 T cells via a mechanism called trans-presentation. Whereas the dynamic of trans-presentation has been shown to involve the recycling of IL-15Rα by presenting cells, the way responding cells integrate, or take advantage of this process has not been evaluated yet. To address this question, we set up a trans-presentation model using a membrane-bound IL-15.IL-15Rα fusion protein, and found that IL-15 is detectable within responding cells following IL-15 trans-presentation. The role of the proteolytic cleavage of IL-15Rα in this process was investigated by generating an uncleavable form of IL-15Rα. We showed that IL-15 entry into responding cells necessitates the cleavage of IL-15.IL-15Rα complex from the surface of IL-15 presenting cells, and observed that IL-15Rα cleavage is associated with a decrease of the duration of Stat5 signaling. Once separated from presenting cells, responding cells are able to recycle IL-15.IL-15Rα complexes via intracellular compartments, for residual proliferation in a time-limited manner. These studies define an unprecedented cytokine pathway in which the IL-15.IL-15Rα complex cleaved from presenting cells allows responding cells to internalize, store and use IL-15.IL-15Rα complex for their own proliferation and survival.

Keywords: IL-2Rβ; autocrine; cell–cell interaction; lymphocyte; synapse.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigen Presentation / immunology
  • Cell Communication / immunology
  • Cell Line
  • Cell Line, Tumor
  • Cell Proliferation
  • Cell Survival / immunology
  • Coculture Techniques
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Flow Cytometry
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Interleukin-15 / genetics
  • Interleukin-15 / immunology*
  • Interleukin-15 / metabolism
  • Interleukin-15 Receptor alpha Subunit / genetics
  • Interleukin-15 Receptor alpha Subunit / immunology*
  • Interleukin-15 Receptor alpha Subunit / metabolism
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Microscopy, Fluorescence
  • Protein Binding / immunology
  • Protein Transport / immunology
  • STAT5 Transcription Factor / immunology
  • STAT5 Transcription Factor / metabolism
  • Signal Transduction / immunology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism

Substances

  • Interleukin-15
  • Interleukin-15 Receptor alpha Subunit
  • STAT5 Transcription Factor