MicroRNA-455-3p modulates cartilage development and degeneration through modification of histone H3 acetylation

Biochim Biophys Acta. 2016 Dec;1863(12):2881-2891. doi: 10.1016/j.bbamcr.2016.09.010. Epub 2016 Sep 13.

Abstract

Histone acetylation regulated by class I histone deacetylases (HDACs) plays a pivotal role in matrix-specific gene transcription and cartilage development. While we previously demonstrated that microRNA (miR)-455-3p is upregulated during chondrogenesis and can enhance early chondrogenesis, the mechanism underlying this process remains largely unclear. In this study, we characterized the effect of miR-455-3p on histone H3 acetylation and its role during cartilage development and degeneration. We observed that miR-455-3p was highly expressed in proliferating and pre-hypertrophic chondrocytes, while HDAC2 and HDAC8 were primarily expressed in hypertrophic chondrocytes. Meanwhile, miR-455-3p suppressed the activity of reporter constructs containing the 3'-untranslated regions of HDAC2/8, inhibited HDAC2/8 expression and promoted histone H3 acetylation at the collagen 2 (COL2A1) promoter in human SW1353 chondrocyte-like cells. Treatment with the HDAC inhibitor trichostatin A (TSA) resulted in increased expression of cartilage-specific genes and promoted glycosaminoglycan deposition. Moreover, TSA inhibited matrix metalloproteinase 13 (Mmp13) expression and promoted nuclear translocation of SOX9 in interleukin-1-treated primary mouse chondrocytes. Lastly, knockdown of HDAC2/3/8 increased SRY (sex-determining region Y)-box 9 (SOX9) and decreased Runt-related transcription factor 2 (RUNX2) expression. Taken together, these findings suggest that miR-455-3p plays a critical role during chondrogenesis by directly targeting HDAC2/8 and promoting histone H3 acetylation, which raises possibilities of using miR-455-3p to influence chondrogenesis and cartilage degeneration.

Keywords: Cartilage-specific genes; Chondrogenesis; Class I HDACs; Histone acetylation; miR-455-3p.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions
  • Acetylation / drug effects
  • Animals
  • Base Sequence
  • Binding Sites
  • Cartilage / cytology
  • Cartilage / metabolism
  • Cell Line, Tumor
  • Chondrocytes / cytology
  • Chondrocytes / drug effects
  • Chondrocytes / metabolism*
  • Chondrogenesis / drug effects
  • Chondrogenesis / genetics*
  • Collagen Type II / genetics
  • Collagen Type II / metabolism
  • Core Binding Factor Alpha 1 Subunit / genetics
  • Core Binding Factor Alpha 1 Subunit / metabolism
  • Histone Deacetylase 2 / antagonists & inhibitors
  • Histone Deacetylase 2 / genetics
  • Histone Deacetylase 2 / metabolism
  • Histone Deacetylase Inhibitors / pharmacology
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism
  • Histones / genetics
  • Histones / metabolism*
  • Humans
  • Hydroxamic Acids / pharmacology
  • Interleukin-1 / pharmacology
  • Matrix Metalloproteinase 13 / genetics
  • Matrix Metalloproteinase 13 / metabolism
  • Mice
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Primary Cell Culture
  • Protein Processing, Post-Translational*
  • Repressor Proteins / antagonists & inhibitors
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • SOX9 Transcription Factor / antagonists & inhibitors
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism
  • Signal Transduction

Substances

  • 3' Untranslated Regions
  • COL2A1 protein, human
  • Collagen Type II
  • Core Binding Factor Alpha 1 Subunit
  • Histone Deacetylase Inhibitors
  • Histones
  • Hydroxamic Acids
  • Interleukin-1
  • MIRN455 microRNA, human
  • MIRN455 microRNA, mouse
  • MicroRNAs
  • Repressor Proteins
  • Runx2 protein, mouse
  • SOX9 Transcription Factor
  • Sox9 protein, mouse
  • trichostatin A
  • MMP13 protein, human
  • Matrix Metalloproteinase 13
  • HDAC2 protein, human
  • HDAC8 protein, human
  • Histone Deacetylase 2
  • Histone Deacetylases