Autocrine production of IFN-gamma by macrophages controls their recruitment to kidney and the development of glomerulonephritis in MRL/lpr mice

J Immunol. 2002 Jul 15;169(2):1058-67. doi: 10.4049/jimmunol.169.2.1058.

Abstract

Anti-DNA autoantibody production is a key factor in lupus erythematosus development; nonetheless, the link between glomerular anti-DNA autoantibody deposition and glomerulonephritis development is not understood. To study the inflammatory and destructive processes in kidney, we used IFN-gamma(+/-) MRL/lpr mice which produce high anti-DNA Ab levels but are protected from kidney disease. The results showed that defective macrophage recruitment to IFN-gamma(+/-) mouse kidney was not caused by decreased levels of monocyte chemoattractant protein-1, a chemokine that controls macrophage migration to MRL/lpr mouse kidney. To determine which IFN-gamma-producing cell type orchestrates the inflammation pathway in kidney, we transferred IFN-gamma(+/+) monocyte/macrophages or T cells to IFN-gamma(-/-) mice, which do not develop anti-DNA autoantibodies. The data demonstrate that IFN-gamma production by infiltrating macrophages, and not by T cells, is responsible for adhesion molecule up-regulation, macrophage accumulation, and inflammation in kidney, even in the absence of autoantibody deposits. Therefore, in addition to monocyte chemoattractant protein-1, macrophage-produced IFN-gamma controls macrophage migration to kidney; the degree of IFN-gamma production by macrophages also regulates glomerulonephritis development. Our findings establish the level of IFN-gamma secretion by macrophages as a link between anti-DNA autoantibody deposition and glomerulonephritis development, outline the pathway of the inflammatory process, and suggest potential treatment for disease even after autoantibody development.

Publication types

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

MeSH terms

  • Animals
  • Autoantibodies / biosynthesis
  • Autocrine Communication / genetics
  • Autocrine Communication / immunology*
  • Cell Adhesion Molecules / biosynthesis
  • Cell Movement / genetics
  • Cell Movement / immunology*
  • Chemokine CCL2 / biosynthesis
  • Down-Regulation / genetics
  • Down-Regulation / immunology
  • Genetic Carrier Screening
  • Glomerulonephritis / etiology
  • Glomerulonephritis / genetics
  • Glomerulonephritis / immunology*
  • Glomerulonephritis / pathology*
  • Interferon-gamma / biosynthesis*
  • Interferon-gamma / deficiency
  • Interferon-gamma / genetics
  • Interferon-gamma / physiology
  • Kidney / immunology*
  • Kidney / pathology
  • Kidney Glomerulus / immunology
  • Kidney Glomerulus / metabolism
  • Kidney Glomerulus / pathology
  • Lung / immunology
  • Lung / pathology
  • Lupus Nephritis / genetics
  • Lupus Nephritis / immunology
  • Lupus Nephritis / pathology
  • Macrophages / immunology*
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred MRL lpr
  • Mice, Knockout
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Up-Regulation / genetics
  • Up-Regulation / immunology

Substances

  • Autoantibodies
  • Cell Adhesion Molecules
  • Chemokine CCL2
  • Interferon-gamma