Reactive Oxygen Species (ROS)-Responsive Charge-Switchable Nanocarriers for Gene Therapy of Metastatic Cancer

ACS Appl Mater Interfaces. 2018 Dec 19;10(50):43352-43362. doi: 10.1021/acsami.8b13291. Epub 2018 Dec 4.

Abstract

The application of nonviral gene vectors has been limited by their insufficient transfection efficiency because of poor serum stability, high endosomal entrapment, limited intracellular release, and low accumulation in the targeted organelle. It is still challenging to design gene carriers with properties that can overcome all of the barriers. We previously developed a reactive oxygen species (ROS)-responsive cationic polymer, poly[(2-acryloyl)ethyl( p-boronic acid benzyl) diethylammonium bromide] (B-PDEAEA), which switches the charge at high concentrations of intracellular ROS to promote intracellular DNA release. However, its gene-delivery efficiency has been limited by serum instability and lysosomal trapping, and coating with an anionic PEGylated lipid only showed mild enhancement. Herein, we coated the ROS-responsive B-PDEAEA polymer with two cationic lipids to form ROS-responsive lipopolyplexes with integrated properties to overcome multiple delivery barriers. The surface cationic lipids endowed the nanocarrier with improved serum stability, effective cellular uptake, and lysosomal evasion. The interior B-PDEAEA/DNA polyplexes, which were highly stable in the extracellular environment, but quickly dissociated, released DNA, promoted nuclei localization, and achieved efficient transcription. The mechanisms of the ROS-responsive and charge-switchable properties of B-PDEAEA were quantitatively studied. The transfection efficiency and antitumor activity of lipopolyplexes were studied in vitro and in vivo. We found that the ROS-responsive lipopolyplexes effectively delivered therapeutic genes into cell nuclei and caused high tumor inhibition in mice bearing peritoneal or lung metastases.

Keywords: ROS-responsive; cationic lipids; charge-switchable; gene delivery; serum resistance.

MeSH terms

  • A549 Cells
  • Animals
  • Drug Carriers* / chemistry
  • Drug Carriers* / pharmacokinetics
  • Drug Carriers* / pharmacology
  • Female
  • Genetic Therapy / methods*
  • Genetic Vectors* / chemistry
  • Genetic Vectors* / genetics
  • Genetic Vectors* / pharmacokinetics
  • Genetic Vectors* / pharmacology
  • HeLa Cells
  • Humans
  • Mice
  • Mice, Inbred BALB C
  • Neoplasm Metastasis
  • Neoplasms, Experimental* / genetics
  • Neoplasms, Experimental* / metabolism
  • Neoplasms, Experimental* / pathology
  • Neoplasms, Experimental* / therapy
  • Reactive Oxygen Species / metabolism*
  • Transfection / methods*
  • Xenograft Model Antitumor Assays

Substances

  • Drug Carriers
  • Reactive Oxygen Species