Trp53 negatively regulates autoimmunity via the STAT3-Th17 axis

FASEB J. 2011 Jul;25(7):2387-98. doi: 10.1096/fj.10-175299. Epub 2011 Apr 6.

Abstract

Emerging evidence suggests that the tumor suppressor p53 is also a crucial regulator for many physiological processes. Previous observations indicate that p53 suppresses inflammation by inhibiting inflammatory antigen-presenting cells. To investigate the potential role of p53 in autoimmune effector T cells, we generated p53(null)CD45.1 mice by crossing p53(null)CD45.2 and CD45.1 mice. We demonstrate that p53(null)CD45.1 mice spontaneously developed autoimmunity, with a significant increase in IL-17-producing Th17 effectors in their lymph nodes (4.7 ± 1.0%) compared to the age-matched counterparts (1.9 ± 0.8% for p53(null)CD45.2, 1.1 ± 0.2% for CD45.1, and 0.5 ± 0.1% for CD45.2 mice). Likewise, p53(null)CD45.1 mice possess highly elevated serum levels of inflammatory cytokines IL-17 and IL-6. This enhanced Th17 response results largely from an increased sensitivity of p53(null)CD45.1 T cells to IL-6-induced STAT3 phosphorylation. Administration of STAT3 inhibitor S31-201 (IC50 of 38.0 ± 7.2 μM for IL-6-induced STAT3 phosphorylation), but not PBS control, to p53(null)CD45.1 mice suppressed Th17 effectors and alleviated autoimmune pathology. This is the first report revealing that p53 activity in T cells suppresses autoimmunity by controlling Th17 effectors. This study suggests that p53 serves as a guardian of immunological functions and that the p53-STAT3-Th17 axis might be a therapeutic target for autoimmunity.

Publication types

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

MeSH terms

  • Animals
  • Autoimmunity / immunology*
  • Blotting, Western
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • Cytokines / immunology
  • Cytokines / metabolism
  • Female
  • Flow Cytometry
  • Interleukin-17 / immunology*
  • Interleukin-17 / metabolism
  • Interleukin-6 / immunology
  • Interleukin-6 / metabolism
  • Interleukin-6 / pharmacology
  • Leukocyte Common Antigens / genetics
  • Leukocyte Common Antigens / immunology
  • Leukocyte Common Antigens / metabolism
  • Lymphoid Tissue / immunology
  • Lymphoid Tissue / metabolism
  • Male
  • Mice
  • Mice, Congenic
  • Mice, Knockout
  • NF-kappa B / immunology
  • NF-kappa B / metabolism
  • Phosphorylation / drug effects
  • STAT3 Transcription Factor / antagonists & inhibitors
  • STAT3 Transcription Factor / immunology*
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / immunology
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Th17 Cells / immunology
  • Th17 Cells / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / immunology*
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Cytokines
  • Interleukin-17
  • Interleukin-6
  • NF-kappa B
  • STAT3 Transcription Factor
  • Tumor Suppressor Protein p53
  • Leukocyte Common Antigens
  • Ptprc protein, mouse