Type I IFN induces IL-10 production in an IL-27-independent manner and blocks responsiveness to IFN-γ for production of IL-12 and bacterial killing in Mycobacterium tuberculosis-infected macrophages

J Immunol. 2014 Oct 1;193(7):3600-12. doi: 10.4049/jimmunol.1401088. Epub 2014 Sep 3.

Abstract

Tuberculosis, caused by the intracellular bacterium Mycobacterium tuberculosis, currently causes ∼1.4 million deaths per year, and it therefore remains a leading global health problem. The immune response during tuberculosis remains incompletely understood, particularly regarding immune factors that are harmful rather than protective to the host. Overproduction of the type I IFN family of cytokines is associated with exacerbated tuberculosis in both mouse models and in humans, although the mechanisms by which type I IFN promotes disease are not well understood. We have investigated the effect of type I IFN on M. tuberculosis-infected macrophages and found that production of host-protective cytokines such as TNF-α, IL-12, and IL-1β is inhibited by exogenous type I IFN, whereas production of immunosuppressive IL-10 is promoted in an IL-27-independent manner. Furthermore, much of the ability of type I IFN to inhibit cytokine production was mediated by IL-10. Additionally, type I IFN compromised macrophage activation by the lymphoid immune response through severely disrupting responsiveness to IFN-γ, including M. tuberculosis killing. These findings describe important mechanisms by which type I IFN inhibits the immune response during tuberculosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Interferon Type I / genetics
  • Interferon Type I / immunology*
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology*
  • Interleukin-10 / genetics
  • Interleukin-10 / immunology*
  • Interleukin-12 / genetics
  • Interleukin-12 / immunology*
  • Interleukin-1beta / immunology
  • Interleukins / genetics
  • Interleukins / immunology*
  • Macrophage Activation / immunology
  • Macrophages / immunology*
  • Macrophages / microbiology
  • Macrophages / pathology
  • Mice
  • Mice, Knockout
  • Mycobacterium tuberculosis / immunology*
  • Tuberculosis / genetics
  • Tuberculosis / immunology*
  • Tuberculosis / pathology
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • IL10 protein, mouse
  • IL1B protein, mouse
  • Il27 protein, mouse
  • Interferon Type I
  • Interleukin-1beta
  • Interleukins
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Interleukin-12
  • Interferon-gamma