CREMα suppresses spleen tyrosine kinase expression in normal but not systemic lupus erythematosus T cells

Arthritis Rheum. 2012 Mar;64(3):799-807. doi: 10.1002/art.33375.

Abstract

Objective: T cells from patients with systemic lupus erythematosus (SLE) display increased amounts of spleen tyrosine kinase (Syk), which is involved in the aberrant CD3/T cell receptor-mediated signaling process, and increased amounts of CREMα, which suppresses the production of interleukin-2. Syk expression can be suppressed by CREMα. This study was undertaken to investigate why CREMα fails to suppress Syk expression in SLE T cells.

Methods: CREMα was overexpressed in healthy T cells by transfection with CREMα expression vector, and Syk expression and phosphorylation were measured. A newly identified cAMP response element (CRE) site on the SYK promoter was characterized by chromatin immunoprecipitation (ChIP) and electrophoretic mobility shift assay. The CREMα-mediated repression of Syk expression was further evaluated by analyzing SYK promoter activity. T cells from SLE patients and healthy individuals were subjected to ChIP to evaluate CREMα binding and histone H3 acetylation.

Results: Increased CREMα levels suppressed Syk expression by direct binding to a CRE site of the SYK promoter in T cells from healthy individuals but failed to do so in T cells from SLE patients. The failure of CREMα to suppress Syk expression in SLE T cells was due to weaker binding to the CRE site of the SYK promoter compared to healthy T cells because the promoter site is hypoacetylated in SLE T cells and therefore of limited access to transcription factors.

Conclusion: Our findings indicate that epigenetic alteration of the SYK promoter in SLE T cells results in the inability of the transcriptional repressor CREMα to bind and suppress the expression of Syk, resulting in aberrant T cell signaling.

Publication types

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

MeSH terms

  • Acetylation
  • Acetyltransferases / metabolism
  • Base Sequence
  • Chromatin / metabolism
  • Chromatin Immunoprecipitation / methods
  • Cyclic AMP Response Element Modulator / chemistry
  • Cyclic AMP Response Element Modulator / genetics
  • Cyclic AMP Response Element Modulator / metabolism*
  • Electrophoretic Mobility Shift Assay
  • Epigenesis, Genetic
  • Gene Expression Regulation
  • Gene Silencing
  • Histones / metabolism
  • Humans
  • Lupus Erythematosus, Systemic / genetics
  • Lupus Erythematosus, Systemic / immunology
  • Lupus Erythematosus, Systemic / metabolism*
  • Molecular Sequence Data
  • Protein-Tyrosine Kinases / metabolism*
  • Signal Transduction
  • Spleen / enzymology*
  • T-Lymphocytes / metabolism*
  • Transfection

Substances

  • Chromatin
  • Histones
  • Cyclic AMP Response Element Modulator
  • Acetyltransferases
  • Protein-Tyrosine Kinases