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The impact of naturally occurring regulatory T cells (nTregs) on the suppression or induction of lung allergic responses in mice depends on the nuclear environment and the production of the pro-inflammatory cytokine interleukin 6 (IL-6). These activities were shown to be different in nTregs derived from wild-type (WT) and CD8-deficient mice (CD8 −/− ), with increased IL-6 levels in nTregs from CD8 −/−  mice in comparison to WT nTregs. Thus, identification of the molecular mechanisms regulating IL-6 production is critical to understanding the phenotypic plasticity of nTregs. Electrophoretic mobility shift assays (EMSA) were performed to determine transcription factor binding to four  Il-6  promoter loci using nuclear extracts from nTregs of WT and CD8 −/−  mice. Increased transcription factor binding for each of the  Il-6  loci was identified in CD8 −/−  compared to WT nTregs. The impact of transcription factor binding and a novel short tandem repeat (STR) on  Il-6  promoter activity was analyzed by luciferase reporter assays. The  Il-6  promoter regions closer to the transcription start site (TSS) were more relevant to the regulation of  Il-6  depending on NF-κB, c-Fos, and SP and USF family members. Two  Il-6  promoter loci were most critical for the inducibility by lipopolysaccharide (LPS) and tumor necrosis factor α (TNFα). A novel STR of variable length in the  Il-6  promoter was identified with diverging prevalence in nTregs from WT or CD8 −/−  mice. The predominant GT repeat in CD8 −/−  nTregs revealed the highest luciferase activity. These novel regulatory mechanisms controlling the transcriptional regulation of the  Il-6  promoter are proposed to contribute to nTregs plasticity and may be central to disease pathogenesis.

Plasticity of Naturally Occurring Regulatory T Cells in Allergic Airway Disease Is Modulated by the Transcriptional Activity of Il-6