Burkholderia pseudomallei-induced expression of suppressor of cytokine signaling 3 and cytokine-inducible src homology 2-containing protein in mouse macrophages: a possible mechanism for suppression of the response to gamma interferon stimulation

Infect Immun. 2005 Nov;73(11):7332-9. doi: 10.1128/IAI.73.11.7332-7339.2005.

Abstract

Burkholderia pseudomallei, the causative agent of melioidosis, is a facultative intracellular gram-negative bacterium that is able to survive and multiply in macrophages. Previously, we reported that B. pseudomallei was able to escape macrophage killing by interfering with the expression of inducible nitric oxide synthase (iNOS). In the present study, we extended this finding and demonstrated that B. pseudomallei was able to activate the expression of suppressor of cytokine signaling 3 (SOCS3) and cytokine-inducible Src homology 2-containing protein (CIS) but not SOCS1 in a mouse macrophage cell line (RAW 264.7). The expression of SOCS3 and CIS in B. pseudomallei-infected macrophages directly correlated with a decreased gamma interferon (IFN-gamma) signaling response, as indicated by a reduction in Y701-STAT-1 phosphorylation (pY701-STAT-1). Moreover, a reduction in the expression of IFN-gamma-induced proteins, such as interferon regulatory factor 1 (IRF-1), was observed in B. pseudomallei-infected macrophages that were treated with IFN-gamma. Since pY701-STAT-1 and IRF-1 are essential transcription factors for regulating iNOS expression, the failure to activate these factors could also result in depression of iNOS expression and a loss of macrophage killing capacity. Taken together, the data indicate that the activation of SOCS3 and CIS expression in B. pseudomallei-infected macrophages interfered with IFN-gamma signaling, thus allowing the bacteria to escape killing by these phagocytic cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Burkholderia pseudomallei / physiology*
  • Cell Line
  • Immediate-Early Proteins / biosynthesis*
  • Immediate-Early Proteins / genetics
  • Interferon Regulatory Factor-1 / metabolism
  • Interferon-gamma / physiology*
  • Macrophages / metabolism*
  • Mice
  • Nitric Oxide Synthase Type II / metabolism
  • Phosphorylation
  • Protein Subunits
  • STAT1 Transcription Factor / metabolism
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins / biosynthesis*
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Up-Regulation*

Substances

  • Immediate-Early Proteins
  • Interferon Regulatory Factor-1
  • Protein Subunits
  • STAT1 Transcription Factor
  • Socs3 protein, mouse
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • cytokine inducible SH2-containing protein
  • Interferon-gamma
  • Nitric Oxide Synthase Type II