Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression

Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11918-23. doi: 10.1073/pnas.1001749107. Epub 2010 Jun 14.

Abstract

Regulatory T cells (Tregs) are thought to play a major role in pregnancy by inhibiting the maternal immune system and preventing fetal rejection. In decidual tissues, NK cells (dNK) reside in close contact with particular myelomonocytic CD14(+) (dCD14(+)) cells. Here we show that the interaction between dNK and dCD14(+) cells results in induction of Tregs. The interaction is mediated by soluble factors as shown by transwell experiments, and the prominent role of IFN-gamma is revealed by the effect of a neutralizing monoclonal antibody. Following interaction with dNK cells, dCD14(+) cells express indoleamine 2,3-dioxygenase (IDO), which, in turn, induces Tregs. Notably, unlike peripheral blood NK (pNK) cells, dNK cells are resistant to inhibition by the IDO metabolite L-kynurenine. "Conditioned" dCD14(+) cells also may induce Tregs through transforming growth factor-beta (TGF-beta) production or CTLA-4-mediated interactions, as indicated by the effect of specific neutralizing Abs. Remarkably, only the interaction between dNK and dCD14(+) cells results in Treg induction, whereas other coculture combinations involving either NK or CD14(+) cells isolated from peripheral blood are ineffective. Our study provides interesting clues to understanding how the crosstalk between decidual NK and CD14(+) cells may initiate a process that leads to Treg induction and immunosuppression. Along this line, it is conceivable that an impaired function of these cells may result in pregnancy failure.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD / metabolism
  • Base Sequence
  • CTLA-4 Antigen
  • Cell Communication / immunology
  • DNA Primers / genetics
  • Decidua / cytology*
  • Decidua / immunology*
  • Female
  • Humans
  • Immune Tolerance / immunology*
  • In Vitro Techniques
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / genetics
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Interferon-gamma / metabolism
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Kynurenine / metabolism
  • Lipopolysaccharide Receptors / metabolism
  • Myeloid Cells / immunology*
  • Myeloid Cells / metabolism
  • Pregnancy / immunology*
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Transforming Growth Factor beta / metabolism
  • Tryptophan / metabolism

Substances

  • Antigens, CD
  • CTLA-4 Antigen
  • CTLA4 protein, human
  • DNA Primers
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Lipopolysaccharide Receptors
  • Transforming Growth Factor beta
  • Kynurenine
  • Interferon-gamma
  • Tryptophan