PD-1 deficiency results in the development of fatal myocarditis in MRL mice

Int Immunol. 2010 Jun;22(6):443-52. doi: 10.1093/intimm/dxq026. Epub 2010 Apr 21.

Abstract

The deficiency of programmed cell death 1 (PD-1, Pdcd1), a negative immuno-receptor belonging to the CD28/cytotoxic T lymphocyte antigen 4 (CTLA-4) family, can support various tissue-specific autoimmune conditions. Here, we analyzed the effect of PD-1 deficiency in MRL mice that is genetically predisposed to systemic autoimmunity. MRL-Pdcd1(-)(/-) mice developed a fatal myocarditis, which is reminiscent of CTLA-4-deficient (Ctla4(-)(/-)) mice. Massive infiltration of CD4(+) and CD8(+) T cells and myeloid cells was found in hearts of MRL-Pdcd1(-)(/-) mice concomitant with the production of high-titer auto-antibodies against cardiac myosin. In contrast to Ctla4(-)(/-) mice in which most of the CD4(+) T cells are non-specifically activated and invade various organs, T cells in the heart but not in the spleen and lymph nodes are activated in MRL-Pdcd1(-)(/-) mice, suggesting that myocarditis is mediated by antigen-specific autoimmune response. Heart infiltrating myeloid cells strongly suppressed the allogenic response of T cells in vitro, suggesting that these Mac1(+)Gr1(+) myeloid cells are phenotypically similar to myeloid suppressor cells, which can be found in tumor-bearing hosts. These findings unravel the hidden heart-specific autoimmune predisposition of MRL mice and provide MRL-Pdcd1(-)(/-) mice as a useful animal model of lymphocytic myocarditis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / genetics
  • Antigens, Differentiation / genetics*
  • Antigens, Differentiation / metabolism
  • Autoantibodies / biosynthesis
  • Autoantibodies / genetics
  • Autoantibodies / immunology
  • CTLA-4 Antigen
  • Cardiac Myosins / immunology
  • Genetic Predisposition to Disease
  • Immune Tolerance
  • Inflammation
  • Lymphocyte Culture Test, Mixed
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred MRL lpr
  • Mice, Knockout
  • Myeloid Cells / metabolism*
  • Myeloid Cells / pathology
  • Myocarditis / genetics
  • Myocarditis / immunology
  • Myocarditis / metabolism*
  • Organ Specificity
  • Programmed Cell Death 1 Receptor
  • T-Lymphocytes / metabolism*
  • T-Lymphocytes / pathology

Substances

  • Antigens, CD
  • Antigens, Differentiation
  • Autoantibodies
  • CTLA-4 Antigen
  • Ctla4 protein, mouse
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Cardiac Myosins