Macrophage-derived dendritic cells have strong Th1-polarizing potential mediated by beta-chemokines rather than IL-12

J Immunol. 2000 Oct 15;165(8):4388-96. doi: 10.4049/jimmunol.165.8.4388.

Abstract

Monocyte-derived dendritic cells (MDDCs) activate naive T lymphocytes to induce adaptive immunity, effecting Th1 polarization through IL-12. However, little is known about other potential DC Th1 polarizing mechanisms, or how T cell polarization may be affected by DCs differentiating in, or exposed to, a proinflammatory environment. Macrophages (MPhis) are DC precursors abundant in inflamed tissues, lymph nodes, and tumors. Thus we studied the T cell-activating and -polarizing properties of MPhi-derived DCs (PhiDCs). Monocytes were cultured in MPhi-CSF (M-CSF) to produce MPhis, which were then differentiated into DCs following culture with GM-CSF plus IL-4. PhiDCs activated a significant allogeneic MLR and were significantly better than MDDCs in activating T cells with superantigen. Most strikingly, PhiDCs elicited up to 9-fold more IFN-gamma from naive or Ag-specific T cells compared with MDDCs (with equivalent IL-4 secretion), despite producing up to 9-fold less IL-12. Neutralization of MDDC, but not PhiDC IL-12 significantly inhibited T cell IFN-gamma induction. PhiDCs produced up to 12-fold more beta-chemokines (macrophage-inflammatory protein-1alpha, -1beta, and RANTES) than MDDCs. Ab blockade of CCR5, but not CXC chemokine receptor 4, inhibited T cell IFN-gamma induction by PhiDCs significantly greater than by MDDCs. Thus DCs differentiating from MPhis induce T cell IFN-gamma through beta-chemokines with little or no requirement for IL-12. Myeloid DCs arising from distinct precursor cells may have differing properties, including different mechanisms of Th1 polarization. These data are the first reports of IFN-gamma induction through chemokines by DCs.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Antigens, CD / biosynthesis
  • Antigens, Surface / biosynthesis
  • Apoptosis / immunology
  • B7-1 Antigen / biosynthesis
  • B7-2 Antigen
  • CD36 Antigens / biosynthesis
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Differentiation / immunology
  • Cell Polarity / immunology*
  • Cells, Cultured
  • Chemokines, CC / metabolism
  • Chemokines, CC / physiology*
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Drug Synergism
  • Enterotoxins / immunology
  • Epitopes, T-Lymphocyte / immunology
  • Granulocyte-Macrophage Colony-Stimulating Factor / pharmacology
  • Histocompatibility Antigens Class I / biosynthesis
  • Humans
  • Integrins / biosynthesis
  • Intercellular Adhesion Molecule-1 / biosynthesis
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / metabolism
  • Interleukin-10 / metabolism
  • Interleukin-12 / biosynthesis
  • Interleukin-12 / metabolism
  • Interleukin-12 / physiology*
  • Interleukin-4 / pharmacology
  • Leukocyte Common Antigens / biosynthesis
  • Lipopolysaccharide Receptors / biosynthesis
  • Lipopolysaccharides / pharmacology
  • Lymphocyte Activation
  • Macrophage Colony-Stimulating Factor / pharmacology
  • Macrophages / cytology
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Membrane Glycoproteins / biosynthesis
  • Myeloid Cells / immunology
  • Myeloid Cells / metabolism
  • Receptors, CCR5 / physiology
  • Receptors, Vitronectin / biosynthesis
  • Staphylococcus aureus / immunology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Th1 Cells / immunology*

Substances

  • Antigens, CD
  • Antigens, Surface
  • B7-1 Antigen
  • B7-2 Antigen
  • CD36 Antigens
  • CD86 protein, human
  • Chemokines, CC
  • Enterotoxins
  • Epitopes, T-Lymphocyte
  • Histocompatibility Antigens Class I
  • Integrins
  • Lipopolysaccharide Receptors
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Receptors, CCR5
  • Receptors, Vitronectin
  • integrin alphaVbeta5
  • Intercellular Adhesion Molecule-1
  • Interleukin-10
  • Interleukin-12
  • Interleukin-4
  • enterotoxin B, staphylococcal
  • Macrophage Colony-Stimulating Factor
  • Interferon-gamma
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Leukocyte Common Antigens