DC-SIGN(+) Macrophages Control the Induction of Transplantation Tolerance

Immunity. 2015 Jun 16;42(6):1143-58. doi: 10.1016/j.immuni.2015.05.009. Epub 2015 Jun 9.

Abstract

Tissue effector cells of the monocyte lineage can differentiate into different cell types with specific cell function depending on their environment. The phenotype, developmental requirements, and functional mechanisms of immune protective macrophages that mediate the induction of transplantation tolerance remain elusive. Here, we demonstrate that costimulatory blockade favored accumulation of DC-SIGN-expressing macrophages that inhibited CD8(+) T cell immunity and promoted CD4(+)Foxp3(+) Treg cell expansion in numbers. Mechanistically, that simultaneous DC-SIGN engagement by fucosylated ligands and TLR4 signaling was required for production of immunoregulatory IL-10 associated with prolonged allograft survival. Deletion of DC-SIGN-expressing macrophages in vivo, interfering with their CSF1-dependent development, or preventing the DC-SIGN signaling pathway abrogated tolerance. Together, the results provide new insights into the tolerogenic effects of costimulatory blockade and identify DC-SIGN(+) suppressive macrophages as crucial mediators of immunological tolerance with the concomitant therapeutic implications in the clinic.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cells, Cultured
  • Forkhead Transcription Factors / metabolism
  • Graft Rejection / etiology
  • Graft Rejection / prevention & control*
  • Heart Transplantation*
  • Immune Tolerance
  • Interleukin-10 / metabolism
  • Lectins, C-Type / genetics
  • Lectins, C-Type / metabolism*
  • Macrophage Colony-Stimulating Factor / metabolism
  • Macrophages / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Targeted Therapy
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Signal Transduction
  • T-Lymphocytes, Regulatory / immunology*
  • Toll-Like Receptor 4 / metabolism
  • Transplantation Tolerance
  • Up-Regulation

Substances

  • Cell Adhesion Molecules
  • DC-specific ICAM-3 grabbing nonintegrin
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Lectins, C-Type
  • Receptors, Cell Surface
  • Toll-Like Receptor 4
  • Interleukin-10
  • Macrophage Colony-Stimulating Factor

Associated data

  • GEO/GSE68648