Myeloid cells, BAFF, and IFN-gamma establish an inflammatory loop that exacerbates autoimmunity in Lyn-deficient mice

J Exp Med. 2010 Aug 2;207(8):1757-73. doi: 10.1084/jem.20100086. Epub 2010 Jul 12.

Abstract

Autoimmunity is traditionally attributed to altered lymphoid cell selection and/or tolerance, whereas the contribution of innate immune cells is less well understood. Autoimmunity is also associated with increased levels of B cell-activating factor of the TNF family (BAFF; also known as B lymphocyte stimulator), a cytokine that promotes survival of self-reactive B cell clones. We describe an important role for myeloid cells in autoimmune disease progression. Using Lyn-deficient mice, we show that overproduction of BAFF by hyperactive myeloid cells contributes to inflammation and autoimmunity in part by acting directly on T cells to induce the release of IFN-gamma. Genetic deletion of IFN-gamma or reduction of BAFF activity, achieved by either reducing myeloid cell hyperproduction or by treating with an anti-BAFF monoclonal antibody, reduced disease development in lyn(-/-) mice. The increased production of IFN-gamma in lyn(-/-) mice feeds back on the myeloid cells to further stimulate BAFF release. Expression of BAFF receptor on T cells was required for their full activation and IFN-gamma release. Overall, our data suggest that the reciprocal production of BAFF and IFN-gamma establishes an inflammatory loop between myeloid cells and T cells that exacerbates autoimmunity in this model. Our findings uncover an important pathological role of BAFF in autoimmune disorders.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antibodies, Monoclonal / immunology
  • Antibodies, Monoclonal / pharmacology
  • Autoantibodies / blood
  • Autoantibodies / immunology
  • Autoimmunity / genetics
  • Autoimmunity / immunology*
  • B-Cell Activating Factor / blood
  • B-Cell Activating Factor / genetics
  • B-Cell Activating Factor / immunology
  • B-Cell Activating Factor / metabolism*
  • B-Cell Activation Factor Receptor / genetics
  • B-Lymphocytes / cytology
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • Cell Proliferation / drug effects
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Gene Expression / genetics
  • Gene Expression / immunology
  • Inflammation / immunology
  • Interferon-gamma / blood
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism*
  • Interferon-gamma / pharmacology
  • Lymphocyte Activation / drug effects
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Macrophages / cytology
  • Macrophages / immunology
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Immunological
  • Myeloid Cells / cytology
  • Myeloid Cells / drug effects
  • Myeloid Cells / immunology*
  • Myeloid Cells / metabolism
  • Nephritis / genetics
  • Nephritis / immunology
  • Nephritis / metabolism
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins c-hck / genetics
  • Spleen / cytology
  • Spleen / metabolism
  • Spleen / pathology
  • Splenomegaly / genetics
  • Splenomegaly / immunology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / transplantation
  • src-Family Kinases / genetics*

Substances

  • Antibodies, Monoclonal
  • Autoantibodies
  • B-Cell Activating Factor
  • B-Cell Activation Factor Receptor
  • Proto-Oncogene Proteins
  • Tnfrsf13c protein, mouse
  • Tnfsf13b protein, mouse
  • Interferon-gamma
  • Hck protein, mouse
  • Proto-Oncogene Proteins c-hck
  • lyn protein-tyrosine kinase
  • proto-oncogene proteins c-fgr
  • src-Family Kinases