MicroRNA-92a-3p Regulates Aggrecanase-1 and Aggrecanase-2 Expression in Chondrogenesis and IL-1β-Induced Catabolism in Human Articular Chondrocytes

Cell Physiol Biochem. 2017;44(1):38-52. doi: 10.1159/000484579. Epub 2017 Nov 3.

Abstract

Background/aims: Aggrecanase-1 (ADAMTS-4) and aggrecanase-2 (ADAMTS-5) are secreted enzymes belonging to the ADAMTS (a disintegrin and metalloproteinase with thrombospondin motifs) family that play significant roles in the progression of osteoarthritis (OA). Here, we aimed to determine whether the expression of ADAMTS-4/5 in chondrogenesis and inflammation is regulated by microRNA-92a-3p (miR-92a-3p).

Methods: MiR-92a-3p and ADAMTS-4/5 expressions were determined by quantitative polymerase chain reaction (qPCR). To investigate the repressive effect of miR-92a-3p on ADAMTS-4/5 expression, chondrogenic human mesenchymal stem cells (hMSCs) and human chondrocytes were transfected with mature miR-92a-3p or an antisense inhibitor (anti-miR-92a-3p), respectively. ADAMTS-4/5 protein production was quantified by enzyme-linked immunosorbent assay (ELISA), and miR-92a-3p involvement in IL-1β-mediated catabolic effects was examined by immunoblotting. The roles of activated MAP kinases (MAPK) and nuclear factor (NF)-κB were evaluated by using specific inhibitors. Interaction between miR-92a-3p and its putative binding site in the 3'-untranslated region (3'-UTR) of ADAMTS-4/5 mRNA was confirmed by luciferase reporter assay.

Results: miR-92a-3p expression was elevated in chondrogenic hMSCs, with significantly lower expression in OA cartilage than in normal cartilage. Stimulation with IL-1β significantly reduced miR-92a-3p expression in primary human chondrocytes (PHCs). Transfection of chondrocytes with miR-92a-3p downregulated IL-1β-induced ADAMTS-4/5 expression, and the activity of a reporter construct containing the 3'-UTR of human ADAMTS-4/5 mRNA. MiR-92a-3p expression was suppressed upon IL-1β-induced activation of MAPK and NF-κB in chondrocytes.

Conclusion: MiR-92a-3p is an important regulator of ADAMTS-4/5 in human chondrocytes and may contribute to the development of OA.

Keywords: Aggrecanase-1; Aggrecanase-2; Chondrocytes; Chondrogenesis; Mirna-92a-3p; Osteoarthritis.

MeSH terms

  • ADAMTS4 Protein / antagonists & inhibitors
  • ADAMTS4 Protein / genetics
  • ADAMTS4 Protein / metabolism*
  • ADAMTS5 Protein / antagonists & inhibitors
  • ADAMTS5 Protein / genetics
  • ADAMTS5 Protein / metabolism*
  • Adult
  • Aged
  • Antagomirs / metabolism
  • Bone Marrow Cells / cytology
  • Cartilage, Articular / metabolism
  • Cartilage, Articular / pathology
  • Cells, Cultured
  • Chondrocytes / cytology
  • Chondrocytes / drug effects
  • Chondrocytes / metabolism
  • Chondrogenesis / drug effects*
  • Chondrogenesis / genetics*
  • Female
  • Gene Expression / drug effects
  • Humans
  • Interleukin-1beta / pharmacology*
  • Male
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / drug effects
  • Mesenchymal Stem Cells / metabolism
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Middle Aged
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / metabolism
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / metabolism
  • Osteoarthritis, Knee / genetics
  • Osteoarthritis, Knee / metabolism
  • Osteoarthritis, Knee / pathology

Substances

  • Antagomirs
  • Interleukin-1beta
  • MIRN92 microRNA, human
  • MicroRNAs
  • NF-kappa B
  • Mitogen-Activated Protein Kinases
  • ADAMTS5 Protein
  • ADAMTS4 Protein