Coordinate expression of cytokines and chemokines by NK cells during murine cytomegalovirus infection

J Immunol. 2004 Mar 1;172(5):3119-31. doi: 10.4049/jimmunol.172.5.3119.

Abstract

Cytokines and chemokines activate and direct effector cells during infection. We previously identified a functional group of five cytokines and chemokines, namely, IFN-gamma, activation-induced T cell-derived and chemokine-related cytokine/lymphotactin, macrophage-inflammatory protein 1alpha, macrophage-inflammatory protein 1beta, and RANTES, coexpressed in individual activated NK cells, CD8(+) T cells, and CD4(+) Th1 cells in vitro and during in vivo infections. However, the stimuli during infection were not known. In murine CMV (MCMV) infection, the DAP12/KARAP-associated Ly49H NK cell activation receptor is crucial for resistance through recognition of MCMV-encoded m157 but NK cells also undergo in vivo nonspecific responses to uncharacterized stimuli. In this study, we show that Ly49H ligation by m157 resulted in a coordinated release of all five cytokines/chemokines from Ly49H(+) NK cells. Whereas other cytokines also triggered the release of these cytokines/chemokines, stimulation was not confined to the Ly49H(+) population. At the single-cell level, the production of the five mediators showed strong positive correlation with each other. Interestingly, NK cells were a major source of these five cytokines/chemokines in vitro and in vivo, whereas infected macrophages produced only limited amounts of macrophage-inflammatory protein 1alpha, macrophage-inflammatory protein1beta, and RANTES. These findings suggest that both virus-specific and nonspecific NK cells play crucial roles in activating and directing other inflammatory cells during MCMV infection.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antigens, Ly / immunology
  • Antigens, Ly / metabolism
  • Antigens, Ly / physiology
  • Cells, Cultured
  • Chemokine CCL4
  • Chemokine CCL5 / biosynthesis
  • Chemokines / biosynthesis*
  • Chemokines, C
  • Coculture Techniques
  • Cytokines / biosynthesis*
  • Cytokines / physiology
  • Herpesviridae Infections / immunology*
  • Herpesviridae Infections / metabolism
  • Interferon-gamma / biosynthesis
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Killer Cells, Natural / virology*
  • Lectins, C-Type
  • Lymphocyte Activation / immunology
  • Lymphokines / biosynthesis
  • Macrophage Inflammatory Proteins / biosynthesis
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / virology
  • Mice
  • Mice, Inbred C57BL
  • Mice, SCID
  • Muromegalovirus / immunology*
  • NK Cell Lectin-Like Receptor Subfamily A
  • Receptors, NK Cell Lectin-Like
  • Sialoglycoproteins / biosynthesis

Substances

  • Antigens, Ly
  • Chemokine CCL4
  • Chemokine CCL5
  • Chemokines
  • Chemokines, C
  • Cytokines
  • Klra8 protein, mouse
  • Lectins, C-Type
  • Lymphokines
  • Macrophage Inflammatory Proteins
  • NK Cell Lectin-Like Receptor Subfamily A
  • Receptors, NK Cell Lectin-Like
  • Sialoglycoproteins
  • Xcl1 protein, mouse
  • lymphotactin
  • Interferon-gamma