Distinctive pro-inflammatory gene signatures induced in articular chondrocytes by oncostatin M and IL-6 are regulated by Suppressor of Cytokine Signaling-3

Osteoarthritis Cartilage. 2015 Oct;23(10):1743-54. doi: 10.1016/j.joca.2015.05.011. Epub 2015 Jun 2.

Abstract

Objective: To describe gene expression in murine chondrocytes stimulated with IL-6 family cytokines and the impact of deleting Suppressor of Cytokine Signaling-3 (SOCS-3) in this cell type.

Method: Primary chondrocytes were isolated from wild type and SOCS-3-deficient (Socs3(Δ/Δcol2)) mice and stimulated with oncostatin M (OSM), IL-6 plus the soluble IL-6 receptor (IL-6/sIL-6R), IL-11 or leukemia inhibitory factor (LIF) for 4 h. Total RNA was extracted and gene expression was evaluated by microarray analysis. Validation of the microarray results was performed using Taqman probes on RNA derived from chondrocytes stimulated for 1, 2, 4 or 8 h. Gene ontology was characterized using DAVID (database for annotation, visualization and integrated discovery).

Results: Multiple genes, including Bcl3, Junb, Tgm1, Angptl4 and Lrg1, were upregulated in chondrocytes stimulated with each gp130 cytokine. The gene transcription profile in response to OSM stimulation was pro-inflammatory and was highly correlated to IL-6/sIL-6R, rather than IL-11 or LIF. In the absence of SOCS-3, OSM and IL-6/sIL-6R stimulation induced an interferon (IFN)-like gene signature, including expression of IL-31ra and S100a9.

Conclusion: While each gp130 cytokine induced a transcriptional response in chondrocytes, OSM- and IL-6/sIL-6R were the most potent members of this cytokine family. SOCS-3 plays an important regulatory role in this cell type, as it does in hematopoietic cells. Our results provide new insights into a hierarchy of gp130-induced transcriptional responses in chondrocytes that is normally restrained by SOCS-3 and suggest therapeutic inhibition of OSM may have benefit over and above antagonism of IL-6 during inflammatory arthritis.

Keywords: Arthritis; Cartilage and chondrocytes; Cytokines; Inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiopoietin-Like Protein 4
  • Angiopoietins / genetics
  • Animals
  • B-Cell Lymphoma 3 Protein
  • Calgranulin B / drug effects
  • Calgranulin B / genetics
  • Cartilage, Articular / cytology
  • Chondrocytes / drug effects*
  • Chondrocytes / metabolism
  • Gene Expression Regulation / drug effects*
  • Glycoproteins / drug effects
  • Glycoproteins / genetics
  • Growth Inhibitors / pharmacology*
  • Inflammation / genetics
  • Interleukin-11 / pharmacology*
  • Interleukin-6 / pharmacology*
  • Leukemia Inhibitory Factor / pharmacology*
  • Mice
  • Mice, Knockout
  • Oncostatin M / pharmacology*
  • Proto-Oncogene Proteins / drug effects
  • Proto-Oncogene Proteins / genetics
  • RNA, Messenger / drug effects*
  • RNA, Messenger / metabolism
  • Receptors, Interleukin / drug effects
  • Receptors, Interleukin / genetics
  • Receptors, Interleukin-6
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins / genetics*
  • Transcription Factors / drug effects
  • Transcription Factors / genetics
  • Transglutaminases / drug effects
  • Transglutaminases / genetics
  • Up-Regulation

Substances

  • Angiopoietin-Like Protein 4
  • Angiopoietins
  • Angptl4 protein, mouse
  • B-Cell Lymphoma 3 Protein
  • Bcl3 protein, mouse
  • Calgranulin B
  • Glycoproteins
  • Growth Inhibitors
  • Il31ra protein, mouse
  • Interleukin-11
  • Interleukin-6
  • JunB protein, mouse
  • LRG1 protein, mouse
  • Leukemia Inhibitory Factor
  • Proto-Oncogene Proteins
  • RNA, Messenger
  • Receptors, Interleukin
  • Receptors, Interleukin-6
  • S100A9 protein, mouse
  • Socs3 protein, mouse
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Transcription Factors
  • Oncostatin M
  • Transglutaminases
  • transglutaminase 1