Toll-like receptor 4 ligation enforces tolerogenic properties of oral mucosal Langerhans cells

J Allergy Clin Immunol. 2008 Feb;121(2):368-374.e1. doi: 10.1016/j.jaci.2007.09.045. Epub 2007 Nov 26.

Abstract

Background: Despite high bacterial colonization, acute infections are rare in the oral mucosa, implicating tolerogenic predominance. Bacterial antigens like LPSs are recognized by innate immunity receptors such as Toll-like receptor 4 (TLR4), associated with LPS receptor (CD14).

Objectives: Toll-like receptor 4 agonist monosphoryl lipid A has been successfully used as adjuvant in subcutaneous immunotherapy, suggesting reinforcement of allergen-specific tolerance. Recently sublingual immunotherapy (SLIT) has been shown to be an effective alternative to subcutaneous immunotherapy. We observed CD14 expression on human oral Langerhans cells (oLCs), representing a major target of SLIT. However, not much is known about TLR4 expression and its effect on oLCs.

Methods: Cell suspensions were obtained by trypsinization of human oral mucosa and analyzed by flow cytometry, RT-PCR, cytometric bead arrays, ELISA, and mixed lymphocyte reactions.

Results: We could show that oLCs express TLR4, and its ligation by monosphoryl lipid A upregulated expression of coinhibitory molecules B7-H1 and B7-H3 while surface expression of costimulatory molecule CD86 was concomitantly decreased. Furthermore, TLR4 ligation on oLCs increased their release of the anti-inflammatory cytokine IL-10 and decreased their stimulatory capacity toward T cells. Moreover, TLR4-ligation on oLCs induced IL-10, TGF-beta1, Forkhead box protein 3, IFN-gamma, and IL-2 production in T cells.

Conclusion: In view of these data, TLR4-ligation on oLCs might not only play a role in pathogen recognition for efficient immunity but also contribute to the tolerogenic state predominating in the oral cavity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / pharmacology*
  • Antigens, CD / metabolism
  • B7 Antigens
  • B7-2 Antigen / metabolism
  • B7-H1 Antigen
  • Cytokines / metabolism
  • Down-Regulation
  • Forkhead Transcription Factors / metabolism
  • Humans
  • Immune Tolerance / drug effects*
  • In Vitro Techniques
  • Interleukin-10 / metabolism
  • Langerhans Cells / immunology*
  • Langerhans Cells / metabolism
  • Lipid A / analogs & derivatives*
  • Lipid A / pharmacology
  • Mouth Mucosa / immunology*
  • Mouth Mucosa / metabolism
  • Receptors, Immunologic / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Th1 Cells / metabolism
  • Toll-Like Receptor 4 / antagonists & inhibitors*
  • Toll-Like Receptor 4 / metabolism
  • Transforming Growth Factor beta1 / metabolism
  • Up-Regulation

Substances

  • Adjuvants, Immunologic
  • Antigens, CD
  • B7 Antigens
  • B7-2 Antigen
  • B7-H1 Antigen
  • CD274 protein, human
  • CD276 protein, human
  • Cytokines
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Lipid A
  • Receptors, Immunologic
  • TLR4 protein, human
  • Toll-Like Receptor 4
  • Transforming Growth Factor beta1
  • Interleukin-10
  • monophosphoryl lipid A