YB-1 orchestrates onset and resolution of renal inflammation via IL10 gene regulation

J Cell Mol Med. 2017 Dec;21(12):3494-3505. doi: 10.1111/jcmm.13260. Epub 2017 Jun 30.

Abstract

The Y-box-binding protein (YB)-1 plays a non-redundant role in both systemic and local inflammatory response. We analysed YB-1-mediated expression of the immune regulatory cytokine IL-10 in both LPS and sterile inflammation induced by unilateral renal ischaemia-reperfusion (I/R) and found an important role of YB-1 not only in the onset but also in the resolution of inflammation in kidneys. Within a decisive cis-regulatory region of the IL10 gene locus, the fourth intron, we identified and characterized an operative YB-1 binding site via gel shift experiments and reporter assays in immune and different renal cells. In vivo, YB-1 phosphorylated at serine 102 localized to the fourth intron, which was paralleled by enhanced IL-10 mRNA expression in mice following LPS challenge and in I/R. Mice with half-maximal expression of YB-1 (Yb1+/- ) had diminished IL-10 expression upon LPS challenge. In I/R, Yb1+/- mice exhibited ameliorated kidney injury/inflammation in the early-phase (days 1 and 5), however showed aggravated long-term damage (day 21) with increased expression of IL-10 and other known mediators of renal injury and inflammation. In conclusion, these data support the notion that there are context-specific decisions concerning YB-1 function and that a fine-tuning of YB-1, for example, via a post-translational modification regulates its activity and/or localization that is crucial for systemic processes such as inflammation.

Keywords: LPS; IL-10; YB-1; fourth intron; ischaemia-reperfusion; renal fibrosis; renal inflammation.

MeSH terms

  • Animals
  • Base Sequence
  • Binding Sites
  • Electrophoretic Mobility Shift Assay
  • Exons
  • Gene Expression Regulation*
  • Heterozygote
  • Homozygote
  • Inflammation
  • Interleukin-10 / genetics*
  • Interleukin-10 / metabolism
  • Introns
  • Kidney / metabolism*
  • Kidney / pathology
  • Lipopolysaccharides
  • Male
  • Mice
  • Mice, Transgenic
  • Protein Binding
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism
  • Reperfusion Injury / genetics*
  • Reperfusion Injury / metabolism
  • Reperfusion Injury / pathology
  • Signal Transduction
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • IL10 protein, mouse
  • Lipopolysaccharides
  • RNA, Messenger
  • Transcription Factors
  • YB-1 protein, mouse
  • Interleukin-10