Inflammatory monocytes activate memory CD8(+) T and innate NK lymphocytes independent of cognate antigen during microbial pathogen invasion

Immunity. 2012 Sep 21;37(3):549-62. doi: 10.1016/j.immuni.2012.05.029. Epub 2012 Aug 30.

Abstract

Memory CD8(+) T cells induced upon immunization exhibit improved functional features that contribute to protection of immunized hosts. Although both cognate antigen recognition and inflammation are important for memory CD8(+) T cell reactivation, the relative contribution of these factors and the cell types providing these signals in vivo are poorly defined. Here, we show that Ly6C(+)CCR2(+) inflammatory monocytes, a subset of monocytes, largely orchestrate memory CD8(+) T and NK lymphocytes activation by differentiating into interleukin-18 (IL-18)- and IL-15-producing cells in an inflammasome and type I interferon-IRF3-dependent manner. Memory CD8(+) T cells became potent effector cells by sensing inflammation from monocytes independently of their cognate antigen. Like NK cells, they underwent rapid mobilization, upregulated intense and sustained effector functions during bacterial, viral, and parasitic infections, and contributed to innate responses and protection in vivo. Thus, inflammatory monocyte-derived IL-18 and IL-15 are critical to initiate memory CD8(+) T and NK lymphocytes differentiation into antimicrobial effector cells.

Publication types

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

MeSH terms

  • Animals
  • Antigens / immunology*
  • Antigens, Ly / immunology
  • Antigens, Ly / metabolism
  • Bacterial Infections / immunology
  • Bacterial Infections / microbiology
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • Female
  • Flow Cytometry
  • Immunologic Memory / immunology*
  • Inflammation / immunology
  • Interleukin-15 / genetics
  • Interleukin-15 / immunology
  • Interleukin-15 / metabolism
  • Interleukin-18 / immunology
  • Interleukin-18 / metabolism
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Listeria monocytogenes / immunology
  • Malaria / immunology
  • Malaria / parasitology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Monocytes / immunology*
  • Monocytes / metabolism
  • Plasmodium berghei / immunology
  • Receptors, CCR2 / genetics
  • Receptors, CCR2 / immunology
  • Receptors, CCR2 / metabolism
  • Streptococcus pneumoniae / immunology

Substances

  • Antigens
  • Antigens, Ly
  • Ccr2 protein, mouse
  • Interleukin-15
  • Interleukin-18
  • Ly-6C antigen, mouse
  • Receptors, CCR2