Novel Quantification of Extracellular Vesicles with Unaltered Surface Membranes Using an Internalized Oligonucleotide Tracer and Applied Pharmacokinetic Multiple Compartment Modeling

Pharm Res. 2021 Oct;38(10):1677-1695. doi: 10.1007/s11095-021-03102-z. Epub 2021 Oct 20.

Abstract

Purpose: We developed an accessible method for labeling small extracellular vesicles (sEVs) without disrupting endogenous ligands. Using labeled sEVs administered to conscious rats, we developed a multiple compartment pharmacokinetic model to identify potential differences in the disposition of sEVs from three different cell types.

Methods: Crude sEVs were labeled with a non-homologous oligonucleotide and isolated from cell culture media using a commercial reagent. Jugular vein catheters were used to introduce EVs to conscious rats (n = 30) and to collect blood samples. Digital PCR was leveraged to allow for quantification over a wide dynamic range. Non-linear mixed effects analysis with first order conditional estimation - extended least squares (FOCE ELS) was used to estimate population-level parameters with associated intra-animal variability.

Results: 86.5% ± 1.5% (mean ± S.E.) of EV particles were in the 45-195 nm size range and demonstrated protein and lipid markers of endosomal origin. Incorporated oligonucleotide was stable in blood and detectable over five half-lives. Data were best described by a three-compartment model with one elimination from the central compartment. We performed an observation-based simulated posterior predictive evaluation with prediction-corrected visual predictive check. Covariate and bootstrap analyses identified cell type having an influence on peripheral volumes (V2 and V3) and clearance (Cl3).

Conclusions: Our method relies upon established laboratory techniques, can be tailored to a variety of biological questions regarding the pharmacokinetic disposition of extracellular vesicles, and will provide a complementary approach for the of study EV ligand-receptor interactions in the context of EV uptake and targeted therapeutics.

Keywords: droplet digital PCR (ddPCR); exosomes; extracellular vesicles; pharmacokinetics; tracer miRNA.

MeSH terms

  • Animals
  • Base Sequence
  • Biological Transport
  • Caenorhabditis elegans / genetics
  • Extracellular Vesicles / metabolism*
  • Humans
  • Ligands
  • Lipids / chemistry
  • Male
  • MicroRNAs
  • Models, Biological
  • Nanoparticles / metabolism*
  • Oligonucleotides / metabolism
  • Oligonucleotides / pharmacokinetics*
  • Rats
  • Rats, Sprague-Dawley
  • Single Molecule Imaging

Substances

  • Ligands
  • Lipids
  • MicroRNAs
  • Oligonucleotides