MyD88 primes macrophages for full-scale activation by interferon-gamma yet mediates few responses to Mycobacterium tuberculosis

J Exp Med. 2003 Oct 6;198(7):987-97. doi: 10.1084/jem.20030603. Epub 2003 Sep 29.

Abstract

Macrophages are activated from a resting state by a combination of cytokines and microbial products. Microbes are often sensed through Toll-like receptors signaling through MyD88. We used large-scale microarrays in multiple replicate experiments followed by stringent statistical analysis to compare gene expression in wild-type (WT) and MyD88-/- macrophages. We confirmed key results by quantitative reverse transcription polymerase chain reaction, Western blot, and enzyme-linked immunosorbent assay. Surprisingly, many genes, such as inducible nitric oxide synthase, IRG-1, IP-10, MIG, RANTES, and interleukin 6 were induced by interferon (IFN)-gamma from 5- to 100-fold less extensively in MyD88-/- macrophages than in WT macrophages. Thus, widespread, full-scale activation of macrophages by IFN-gamma requires MyD88. Analysis of the mechanism revealed that MyD88 mediates a process of self-priming by which resting macrophages produce a low level of tumor necrosis factor. This and other factors lead to basal activation of nuclear factor kappaB, which synergizes with IFN-gamma for gene induction. In contrast, infection by live, virulent Mycobacterium tuberculosis (Mtb) activated macrophages largely through MyD88-independent pathways, and macrophages did not need MyD88 to kill Mtb in vitro. Thus, MyD88 plays a dynamic role in resting macrophages that supports IFN-gamma-dependent activation, whereas macrophages can respond to a complex microbial stimulus, the tubercle bacillus, chiefly by other routes.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Antigens, Differentiation / physiology*
  • Gene Expression Regulation / drug effects
  • Interferon-gamma / pharmacology*
  • Interleukin-1 / biosynthesis
  • Macrophage Activation* / drug effects
  • Macrophages / metabolism*
  • Membrane Glycoproteins / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mycobacterium tuberculosis / physiology*
  • Myeloid Differentiation Factor 88
  • NF-kappa B / physiology
  • Receptors, Cell Surface / physiology
  • Receptors, Immunologic / physiology*
  • Toll-Like Receptors
  • Transcriptional Activation
  • Tumor Necrosis Factor-alpha / physiology

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, Differentiation
  • Interleukin-1
  • Membrane Glycoproteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • NF-kappa B
  • Receptors, Cell Surface
  • Receptors, Immunologic
  • Toll-Like Receptors
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma