Discovery of Bivalent GalNAc-Conjugated Betulin as a Potent ASGPR-Directed Agent against Hepatocellular Carcinoma

Bioconjug Chem. 2021 Apr 21;32(4):763-781. doi: 10.1021/acs.bioconjchem.1c00042. Epub 2021 Mar 10.

Abstract

Herein, we describe the design, synthesis, and biological evaluation of novel betulin and N-acetyl-d-galactosamine (GalNAc) glycoconjugates and suggest them as targeted agents against hepatocellular carcinoma. We prepared six conjugates derived via the C-3 and C-28 positions of betulin with one or two saccharide ligands. These molecules demonstrate high affinity to the asialoglycoprotein receptor (ASGPR) of hepatocytes assessed by in silico modeling and surface plasmon resonance tests. Cytotoxicity studies in vitro revealed a bivalent conjugate with moderate activity, selectivity of action, and cytostatic properties against hepatocellular carcinoma cells HepG2. An additional investigation confirmed the specific engagement with HepG2 cells by the enhanced generation of reactive oxygen species. Stability tests demonstrated its lability to acidic media and to intracellular enzymes. Therefore, the selected bivalent conjugate represents a new potential agent targeted against hepatocellular carcinoma. Further extensive studies of the cellular uptake in vitro and the real-time microdistribution in the murine liver in vivo for fluorescent dye-labeled analogue showed its selective internalization into hepatocytes due to the presence of GalNAc ligand in comparison with reference compounds. The betulin and GalNAc glycoconjugates can therefore be considered as a new strategy for developing therapeutic agents based on natural triterpenoids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylgalactosamine / chemistry*
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology*
  • Asialoglycoprotein Receptor / drug effects*
  • Carcinoma, Hepatocellular / pathology*
  • Cell Line, Tumor
  • Drug Delivery Systems
  • Drug Discovery
  • Drug Screening Assays, Antitumor
  • Fluorescent Dyes / chemistry
  • Humans
  • Hydrophobic and Hydrophilic Interactions
  • Liver Neoplasms / pathology*
  • Molecular Docking Simulation
  • Surface Plasmon Resonance
  • Triterpenes / chemistry*

Substances

  • Antineoplastic Agents
  • Asialoglycoprotein Receptor
  • Fluorescent Dyes
  • Triterpenes
  • betulin
  • Acetylgalactosamine