MyD88-dependent SHIP1 regulates proinflammatory signaling pathways in dendritic cells after monophosphoryl lipid A stimulation of TLR4

J Immunol. 2011 Apr 1;186(7):3858-65. doi: 10.4049/jimmunol.1001034. Epub 2011 Feb 21.

Abstract

We previously showed that monophosphoryl lipid A (MLA) activates TLR4 in dendritic cells (DCs) in a Toll/IL-1R domain-containing adaptor inducing IFN-β (TRIF)-biased manner: MLA produced from Salmonella minnesota Re595 induced signaling events and expression of gene products that were primarily TRIF dependent, whereas MyD88-dependent signaling was impaired. Moreover, when tested in TRIF-intact/MyD88-deficient DCs, synthetic MLA of the Escherichia coli chemotype (sMLA) showed the same activity as its diphosphoryl, inflammatory counterpart (synthetic diphosphoryl lipid A), indicating that TRIF-mediated signaling is fully induced by sMLA. Unexpectedly, we found that the transcript level of one proinflammatory cytokine was increased in sMLA-treated cells by MyD88 deficiency to the higher level induced by synthetic diphosphoryl lipid A, which suggested MyD88 may paradoxically help restrain proinflammatory signaling by TRIF-biased sMLA. In this article, we demonstrate that sMLA induces MyD88 recruitment to TLR4 and activates the anti-inflammatory lipid phosphatase SHIP1 in an MyD88-dependent manner. At the same time, MyD88-dependent signaling activity at the level of IL-1R-associated kinase 1 is markedly reduced. Increased SHIP1 activity is associated with reductions in sMLA-induced IκB kinase α/β and IFN regulatory factor 3 activation and with restrained expression of their downstream targets, endothelin-1 and IFN-β, respectively. Results of this study identify a pattern that is desirable in the context of vaccine adjuvant design: TRIF-biased sMLA can stimulate partial MyD88 activity, with MyD88-dependent SHIP1 helping to reduce proinflammatory signaling in DCs.

Publication types

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

MeSH terms

  • Adjuvants, Immunologic / antagonists & inhibitors
  • Adjuvants, Immunologic / metabolism
  • Adjuvants, Immunologic / physiology*
  • Animals
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / microbiology
  • Bone Marrow Cells / pathology
  • Dendritic Cells / immunology*
  • Dendritic Cells / microbiology
  • Dendritic Cells / pathology
  • Escherichia coli / immunology
  • Inflammation Mediators / antagonists & inhibitors
  • Inflammation Mediators / metabolism
  • Inflammation Mediators / physiology*
  • Inositol Polyphosphate 5-Phosphatases
  • Lipid A / analogs & derivatives*
  • Lipid A / physiology
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Myeloid Differentiation Factor 88 / deficiency
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / physiology*
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases
  • Phosphoric Monoester Hydrolases / deficiency
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / physiology*
  • Salmonella / immunology
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Toll-Like Receptor 4 / agonists
  • Toll-Like Receptor 4 / metabolism*
  • Toll-Like Receptor 4 / physiology

Substances

  • Adjuvants, Immunologic
  • Inflammation Mediators
  • Lipid A
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • diphosphoryl lipid A
  • Phosphoric Monoester Hydrolases
  • Inositol Polyphosphate 5-Phosphatases
  • Inpp5d protein, mouse
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases
  • monophosphoryl lipid A