Functional relevance of protein glycosylation to the pro-inflammatory effects of extracellular matrix metalloproteinase inducer (EMMPRIN) on monocytes/macrophages

PLoS One. 2015 Feb 6;10(2):e0117463. doi: 10.1371/journal.pone.0117463. eCollection 2015.

Abstract

Background and objective: Extracellular matrix metalloproteinase inducer (EMMPRIN) is an important pro-inflammatory protein involved in the cellular functions of monocytes/macrophages. We have hypothesized that high-level heterogeneousness of protein glycosylation of EMMPRIN may have functional relevance to its biological effects and affect the inflammatory activity of monocytes/macrophages.

Methods: The glycosylation patterns of EMMPRIN expressed by monocytes/macrophages (THP-1 cells) in response to different extracellular stimuli were observed, and the structures of different glycosylation forms were identified. After the purification of highly- and less-glycosylated proteins respectively, the impacts of different glycosylation forms on the pro-inflammatory effects of EMMPRIN were examined in various aspects, such as cell adhesion to endothelial cells, cell migrations, cytokine expression, and activation of inflammatory signalling pathway.

Results: 1) It was mainly the highly-glycosylated form of EMMPRIN (HG-EMMPRIN) that increased after being exposed to inflammatory signals (PMA and H2O2). 2) Glycosylation of EMMPRIN in monocytes/macrophages led to N-linked-glycans being added to the protein, with the HG form containing complex-type glycans and the less-glycosylated form (LG) the simple type. 3) Only the HG-EMMPRIN but not the LG-EMMPRIN exhibited pro-inflammatory effects and stimulated inflammatory activities of the monocytes/macrophages (i.e., activation of ERK1/2 and NF-κB pathway, enhanced monocyte-endothelium adhesion, cell migration and matrix metalloproteinase -9 expression).

Conclusions: Post-transcriptional glycosylation represents an important mechanism that determines the biological effects of EMMPRIN in monocytes/macrophages. Glycosylation of EMMPRIN may serve as a potential target for regulating the inflammatory activities of monocytes/macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Basigin / chemistry
  • Basigin / isolation & purification
  • Basigin / metabolism*
  • Cell Adhesion / drug effects
  • Cell Line
  • Cell Movement / drug effects
  • Glycosylation / drug effects
  • Humans
  • Hydrogen Peroxide / toxicity
  • Macrophages / cytology
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Matrix Metalloproteinase 9 / metabolism
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • NF-kappa B / metabolism
  • Signal Transduction / drug effects
  • Tetradecanoylphorbol Acetate / toxicity

Substances

  • NF-kappa B
  • Basigin
  • Hydrogen Peroxide
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Matrix Metalloproteinase 9
  • Tetradecanoylphorbol Acetate

Grants and funding

This work was supported by Natural Science Foundation of China (grant numbers 81000114 (GH), 81200163 (PJ), 81330006 (HB) and 81270282(PJ) [www.nsfc.gov.cn]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.