Exposure to cigarette smoke suppresses IL-15 generation and its regulatory NK cell functions in poly I:C-augmented human PBMCs

Mol Immunol. 2009 Sep;46(15):3108-16. doi: 10.1016/j.molimm.2009.06.009. Epub 2009 Jul 9.

Abstract

Both NK cells and IL-15 play crucial roles in innate immunity against viral infections and cancer. Cigarette smoke is known to increase susceptibility to infections and certain cancers. Interleukin (IL)-15 plays an important role in immune responses by regulating proliferation, survival and functions of NK cells. Here, we examined the impact of cigarette smoke on IL-15 production and IL-15 mediated NK cell functions in human PBMCs. We report that cigarette smoke significantly suppresses the induction of IL-15 by poly I:C in human PBMCs. Serum IL-15 levels among smokers was significantly lower than non-smokers. In contrast to a profound increases in intracellular IL-15/IL-15Ralpha in poly I:C-treated PBMCs, exposure of PBMCs to smoke-conditioned media (SCM) diminished the IL-15/IL-15Ralpha production. We examined if inhibition of IL-15 production could lead to less NK cell activation. Interestingly, SCM-treated PBMCs had diminished up-regulation of NK cell activation marker, CD69, but not NKG2D compared with controls after poly I:C stimulation. We then confirmed by using IL-15 neutralizing antibody as well as exogenous IL-15 that the ploy I:C-induced NK cells activation was IL-15 mediated. More importantly, cigarette smoke significantly impaired NK cell cytolytic potential to kill K562 cancer cells which was found to be IL-15 mediated. The inhibition of IL-15 and its regulatory NK cell activities were linked to attenuated STAT3 and STAT5, but not ERK1/2 phosphorylations. We demonstrate, for the first time, that cigarette smoke compromises IL-15 production and as a result NK cell function which could link to the higher incidence of cancers or viral infections observed among smokers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD / drug effects
  • Antigens, CD / immunology
  • Antigens, CD / metabolism
  • Antigens, Differentiation, T-Lymphocyte / drug effects
  • Antigens, Differentiation, T-Lymphocyte / immunology
  • Antigens, Differentiation, T-Lymphocyte / metabolism
  • Culture Media, Conditioned / pharmacology
  • Cytotoxicity, Immunologic / drug effects
  • Cytotoxicity, Immunologic / immunology
  • Extracellular Signal-Regulated MAP Kinases / immunology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Humans
  • Interferon Inducers / pharmacology
  • Interleukin-15 / antagonists & inhibitors*
  • Interleukin-15 / blood
  • Interleukin-15 Receptor alpha Subunit / antagonists & inhibitors
  • Interleukin-15 Receptor alpha Subunit / immunology
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology*
  • Lectins, C-Type
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / immunology*
  • NK Cell Lectin-Like Receptor Subfamily K / drug effects
  • NK Cell Lectin-Like Receptor Subfamily K / immunology
  • NK Cell Lectin-Like Receptor Subfamily K / metabolism
  • Nicotiana / adverse effects*
  • Phosphorylation / drug effects
  • Phosphorylation / immunology
  • Poly I-C / pharmacology
  • STAT3 Transcription Factor / antagonists & inhibitors
  • STAT3 Transcription Factor / immunology
  • STAT3 Transcription Factor / metabolism
  • STAT5 Transcription Factor / antagonists & inhibitors
  • STAT5 Transcription Factor / immunology
  • STAT5 Transcription Factor / metabolism
  • Smoke / adverse effects*
  • Smoking / adverse effects*
  • Smoking / blood
  • Smoking / immunology

Substances

  • Antigens, CD
  • Antigens, Differentiation, T-Lymphocyte
  • CD69 antigen
  • Culture Media, Conditioned
  • Interferon Inducers
  • Interleukin-15
  • Interleukin-15 Receptor alpha Subunit
  • KLRK1 protein, human
  • Lectins, C-Type
  • NK Cell Lectin-Like Receptor Subfamily K
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • STAT5 Transcription Factor
  • Smoke
  • Extracellular Signal-Regulated MAP Kinases
  • Poly I-C