Extracellular microRNAs exhibit sequence-dependent stability and cellular release kinetics

RNA Biol. 2019 May;16(5):696-706. doi: 10.1080/15476286.2019.1582956. Epub 2019 Mar 5.

Abstract

Multiple studies have described extracellular microRNAs (ex-miRNAs) as being remarkably stable despite the hostile extracellular environment, when stored at 4ºC or lower. Here we show that many ex-miRNAs are rapidly degraded when incubated at 37ºC in the presence of serum (thereby simulating physiologically relevant conditions). Stability varied widely between miRNAs, with half-lives ranging from ~1.5 hours to more than 13 hours. Notably, ex-miRNA half-lives calculated in two different biofluids (murine serum and C2C12 mouse myotube conditioned medium) were highly similar, suggesting that intrinsic sequence properties are a determining factor in miRNA stability. By contrast, ex-miRNAs associated with extracellular vesicles (isolated by size exclusion chromatography) were highly stable. The release of ex-miRNAs from C2C12 myotubes was measured over time, and mathematical modelling revealed miRNA-specific release kinetics. While some ex-miRNAs reached the steady state in cell culture medium within 24 hours, the extracellular level of miR-16 did not reach equilibrium, even after 3 days in culture. These findings are indicative of miRNA-specific release and degradation kinetics with implications for the utility of ex-miRNAs as biomarkers, and for the potential of ex-miRNAs to transfer gene regulatory information between cells.

Keywords: Extracellular microRNA; ex-miRNA; half-life; kinetics; miRNA; microRNA; serum.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Culture Media, Conditioned / chemistry
  • Extracellular Vesicles / genetics*
  • Female
  • Humans
  • Mice
  • MicroRNAs / chemistry*
  • MicroRNAs / genetics*
  • Muscle Fibers, Skeletal / chemistry
  • Muscle Fibers, Skeletal / cytology
  • Preservation, Biological
  • RNA Stability
  • Serum / chemistry
  • Temperature

Substances

  • Culture Media, Conditioned
  • MicroRNAs

Grants and funding

This work was supported by the John Fell Fund, University of Oxford [AVD00160];Medical Research Council [1371292];