Minocycline blocks asthma-associated inflammation in part by interfering with the T cell receptor-nuclear factor κB-GATA-3-IL-4 axis without a prominent effect on poly(ADP-ribose) polymerase

J Biol Chem. 2013 Jan 18;288(3):1458-68. doi: 10.1074/jbc.M112.419580. Epub 2012 Nov 26.

Abstract

Minocycline protects against asthma independently of its antibiotic function and was recently reported as a potent poly(ADP-ribose) polymerase (PARP) inhibitor. In an animal model of asthma, a single administration of minocycline conferred excellent protection against ovalbumin-induced airway eosinophilia, mucus hypersecretion, and Th2 cytokine production (IL-4/IL-5/IL-12(p70)/IL-13/GM-CSF) and a partial protection against airway hyperresponsiveness. These effects correlated with pronounced reduction in lung and sera allergen-specific IgE. A reduction in poly(ADP-ribose) immunoreactivity in the lungs of minocycline-treated/ovalbumin-challenged mice correlated with decreased oxidative DNA damage. The effect of minocycline on PARP may be indirect, as the drug failed to efficiently block direct PARP activation in lungs of N-methyl-N'-nitro-N-nitroso-guanidine-treated mice or H(2)O(2)-treated cells. Minocycline blocked allergen-specific IgE production in B cells potentially by modulating T cell receptor (TCR)-linked IL-4 production at the mRNA level but not through a modulation of the IL-4-JAK-STAT-6 axis, IL-2 production, or NFAT1 activation. Restoration of IL-4, ex vivo, rescued IgE production by minocycline-treated/ovalbumin-stimulated B cells. IL-4 blockade correlated with a preferential inhibition of the NF-κB activation arm of TCR but not GSK3, Src, p38 MAPK, or ERK1/2. Interestingly, the drug promoted a slightly higher Src and ERK1/2 phosphorylation. Inhibition of NF-κB was linked to a complete blockade of TCR-stimulated GATA-3 expression, a pivotal transcription factor for IL-4 expression. Minocycline also reduced TNF-α-mediated NF-κB activation and expression of dependent genes. These results show a potentially broad effect of minocycline but that it may block IgE production in part by modulating TCR function, particularly by inhibiting the signaling pathway, leading to NF-κB activation, GATA-3 expression, and subsequent IL-4 production.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Asthma / complications
  • Asthma / drug therapy*
  • Asthma / genetics
  • Asthma / immunology
  • GATA3 Transcription Factor / agonists
  • GATA3 Transcription Factor / genetics*
  • GATA3 Transcription Factor / immunology
  • Gene Expression Regulation / drug effects
  • Immunoglobulin E / genetics
  • Immunoglobulin E / immunology
  • Immunologic Factors / pharmacology
  • Immunologic Factors / therapeutic use*
  • Inflammation / complications
  • Inflammation / drug therapy*
  • Inflammation / genetics
  • Inflammation / immunology
  • Interleukin-4 / antagonists & inhibitors
  • Interleukin-4 / genetics*
  • Interleukin-4 / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Minocycline / pharmacology
  • Minocycline / therapeutic use*
  • NF-kappa B / agonists
  • NF-kappa B / genetics*
  • NF-kappa B / immunology
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases / genetics
  • Poly(ADP-ribose) Polymerases / immunology
  • Receptors, Antigen, T-Cell / antagonists & inhibitors
  • Receptors, Antigen, T-Cell / genetics*
  • Receptors, Antigen, T-Cell / immunology
  • Signal Transduction / drug effects

Substances

  • GATA3 Transcription Factor
  • Gata3 protein, mouse
  • Immunologic Factors
  • NF-kappa B
  • Receptors, Antigen, T-Cell
  • Interleukin-4
  • Immunoglobulin E
  • Parp1 protein, mouse
  • Poly (ADP-Ribose) Polymerase-1
  • Poly(ADP-ribose) Polymerases
  • Minocycline