Visualization of self-delivering hydrophobically modified siRNA cellular internalization

Nucleic Acids Res. 2017 Jan 9;45(1):15-25. doi: 10.1093/nar/gkw1005. Epub 2016 Nov 28.

Abstract

siRNAs are a new class of therapeutic modalities with promising clinical efficacy that requires modification or formulation for delivery to the tissue and cell of interest. Conjugation of siRNAs to lipophilic groups supports efficient cellular uptake by a mechanism that is not well characterized. Here we study the mechanism of internalization of asymmetric, chemically stabilized, cholesterol-modified siRNAs (sd-rxRNAs®) that efficiently enter cells and tissues without the need for formulation. We demonstrate that uptake is rapid with significant membrane association within minutes of exposure followed by the formation of vesicular structures and internalization. Furthermore, sd-rxRNAs are internalized by a specific class of early endosomes and show preferential association with epidermal growth factor (EGF) but not transferrin (Tf) trafficking pathways as shown by live cell TIRF and structured illumination microscopy (SIM). In fixed cells, we observe ∼25% of sd-rxRNA co-localizing with EGF and <5% with Tf, which is indicative of selective endosomal sorting. Likewise, preferential sd-rxRNA co-localization was demonstrated with EEA1 but not RBSN-containing endosomes, consistent with preferential EGF-like trafficking through EEA1-containing endosomes. sd-rxRNA cellular uptake is a two-step process, with rapid membrane association followed by internalization through a selective, saturable subset of the endocytic process. However, the mechanistic role of EEA1 is not yet known. This method of visualization can be used to better understand the kinetics and mechanisms of hydrophobic siRNA cellular uptake and will assist in further optimization of these types of compounds for therapeutic intervention.

MeSH terms

  • Animals
  • Biological Transport
  • COS Cells
  • Chlorocebus aethiops
  • Cholesterol / chemistry*
  • Cholesterol / metabolism
  • Cyclophilins / genetics
  • Cyclophilins / metabolism
  • Endocytosis
  • Endosomes / metabolism*
  • Epidermal Growth Factor / genetics
  • Epidermal Growth Factor / metabolism*
  • Gene Expression
  • HeLa Cells
  • Humans
  • Hydrophobic and Hydrophilic Interactions
  • Microscopy, Fluorescence
  • RNA, Small Interfering / chemistry
  • RNA, Small Interfering / metabolism*
  • Transferrin / genetics
  • Transferrin / metabolism
  • Vesicular Transport Proteins / genetics
  • Vesicular Transport Proteins / metabolism*

Substances

  • RBSN protein, human
  • RNA, Small Interfering
  • Transferrin
  • Vesicular Transport Proteins
  • early endosome antigen 1
  • cyclophilin B
  • Epidermal Growth Factor
  • Cholesterol
  • Cyclophilins