Repeated social defeat increases the bactericidal activity of splenic macrophages through a Toll-like receptor-dependent pathway

Am J Physiol Regul Integr Comp Physiol. 2007 Sep;293(3):R1180-90. doi: 10.1152/ajpregu.00307.2007. Epub 2007 Jun 27.

Abstract

Phagocytes of the innate immune system, such as monocytes/macrophages, represent a first line of defense against invading microorganisms. Psychological stress is often thought to suppress the functioning of these cells, in part due to the immunosuppressive activity of stress-induced glucocorticoid hormones. However, exposure to the stressor social disruption (SDR) has been shown to increase cytokine production by monocytes/macrophages and to reduce their sensitivity to corticosterone. Thus, it was hypothesized that splenic monocytes/macrophages from socially stressed mice would be primed to be more physiologically active than cells from nonstressed controls. Flow cytometry was used to demonstrate that exposure to SDR significantly increased the expression of Toll-like receptors (TLR) 2 and 4 on the surface of splenic macrophages. In a follow-up experiment, exposure to SDR also increased the ability of these macrophages to kill Escherichia coli ex vivo and in vivo. However, SDR failed to increase the bactericidal activity of splenic macrophages from C3H/HeJ mice, which lack functional TLR4. In mice with functional TLR4, the stress-induced increase in bactericidal activity was associated with a significant increase in macrophage gene expression for inducible nitric oxide synthase and subunits of the NADPH oxidase complex, which are responsible for generating reactive nitrogen and oxygen intermediates, respectively. This stress-induced increase in gene expression was not evident in the TLR4-deficient mice. These data indicate that SDR increases TLR expression, which in turn enhances the bactericidal activity of splenic macrophages, in part by increasing pathways responsible for reactive oxygen and nitrogen intermediate production.

Publication types

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

MeSH terms

  • Animals
  • CD11b Antigen / biosynthesis
  • CD11b Antigen / genetics
  • Dominance-Subordination*
  • Escherichia coli / immunology
  • Escherichia coli Infections / immunology
  • Escherichia coli Infections / microbiology
  • Flow Cytometry
  • Macrophages / immunology*
  • Mice
  • Mice, Inbred C3H
  • NADPH Oxidases / biosynthesis
  • NADPH Oxidases / genetics
  • Nitric Oxide Synthase Type II / biosynthesis
  • Nitric Oxide Synthase Type II / genetics
  • Organ Size / physiology
  • Phagocytosis
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology*
  • Spleen / cytology*
  • Spleen / immunology*
  • Stress, Psychological / immunology
  • Toll-Like Receptor 2 / biosynthesis
  • Toll-Like Receptor 4 / biosynthesis
  • Toll-Like Receptors / physiology*

Substances

  • CD11b Antigen
  • Toll-Like Receptor 2
  • Toll-Like Receptor 4
  • Toll-Like Receptors
  • Nitric Oxide Synthase Type II
  • NADPH Oxidases