Requirement of IFN-gamma-mediated indoleamine 2,3-dioxygenase expression in the modulation of lymphocyte proliferation by human adipose-derived stem cells

Tissue Eng Part A. 2009 Oct;15(10):2795-806. doi: 10.1089/ten.TEA.2008.0630.

Abstract

Human adipose-derived mesenchymal stem cells (hASCs) are mesenchymal stem cells (MSCs) with reduced immunogenicity and capability to modulate immune responses. Whereas the immunosuppressive activity of bone marrow-MSCs has received considerable attention during the last few years, the specific mechanisms underlying hASC-mediated immunosuppression have been poorly studied. Recent studies comparing both cell types have reported differences at transcriptional and proteomic levels, suggesting that hASCs and bone marrow-MSCs, while having similarities, are quite different. This suggests that different mechanisms of immunosuppression may apply. Here, we report that hASCs inhibit peripheral blood mononuclear cells (PBMCs), and CD4(+) and CD8(+) T cell proliferation in both cell-cell contact and transwell conditions, which is accompanied by a reduction of proinflammatory cytokines. We demonstrate that hASCs do not constitutively express immunomodulatory factors. Conditioned supernatants from hASCs stimulated by IFN-gamma, PBMCs, or activated PBMCs highly inhibited PBMC proliferation, indicating that inhibitory factors are released upon hASC activation. Many factors have been involved in MSC-mediated immunosuppression, including IFN-gamma, IL-10, hepatocyte growth factor, prostaglandin E2, transforming growth factor-beta1, indoleamine 2,3-dioxygenase (IDO), nitric oxide, and IL-10. Using pharmacological inhibitors, neutralizing antibodies, and genetically modified hASCs that constitutively express or silence IDO enzyme, we demonstrate that, in the case of hASCs, the IFN-gamma/IDO axis is essential. Taken together, our data support the key role of IDO in the therapeutic use of hASC on immunomediated diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipocytes / cytology*
  • CD4-Positive T-Lymphocytes / cytology
  • CD8-Positive T-Lymphocytes / cytology
  • Cell Proliferation
  • Dinoprostone / metabolism
  • Flow Cytometry
  • Hepatocyte Growth Factor / metabolism
  • Humans
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism*
  • Interferon-gamma / metabolism*
  • Interleukin-10 / metabolism
  • Leukocytes, Mononuclear / cytology
  • Lymphocytes / cytology*
  • Lymphocytes / immunology
  • Mesenchymal Stem Cells / cytology*
  • Nitric Oxide / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Tissue Engineering
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Transforming Growth Factor beta1
  • Interleukin-10
  • Nitric Oxide
  • Hepatocyte Growth Factor
  • Interferon-gamma
  • Dinoprostone