Genome editing without nucleases confers proliferative advantage to edited hepatocytes and corrects Wilson disease

JCI Insight. 2023 Nov 8;8(21):e171281. doi: 10.1172/jci.insight.171281.

Abstract

Application of classic liver-directed gene replacement strategies is limited in genetic diseases characterized by liver injury due to hepatocyte proliferation, resulting in decline of therapeutic transgene expression and potential genotoxic risk. Wilson disease (WD) is a life-threatening autosomal disorder of copper homeostasis caused by pathogenic variants in copper transporter ATP7B and characterized by toxic copper accumulation, resulting in severe liver and brain diseases. Genome editing holds promise for the treatment of WD; nevertheless, to rescue copper homeostasis, ATP7B function must be restored in at least 25% of the hepatocytes, which surpasses by far genome-editing correction rates. We applied a liver-directed, nuclease-free genome editing approach, based on adeno-associated viral vector-mediated (AAV-mediated) targeted integration of a promoterless mini-ATP7B cDNA into the albumin (Alb) locus. Administration of AAV-Alb-mini-ATP7B in 2 WD mouse models resulted in extensive liver repopulation by genome-edited hepatocytes holding a proliferative advantage over nonedited ones, and ameliorated liver injury and copper metabolism. Furthermore, combination of genome editing with a copper chelator, currently used for WD treatment, achieved greater disease improvement compared with chelation therapy alone. Nuclease-free genome editing provided therapeutic efficacy and may represent a safer and longer-lasting alternative to classic gene replacement strategies for WD.

Keywords: Gene therapy; Genetics; Hepatology; Monogenic diseases.

MeSH terms

  • Animals
  • Copper / metabolism
  • Gene Editing
  • Hepatocytes / metabolism
  • Hepatolenticular Degeneration* / drug therapy
  • Hepatolenticular Degeneration* / therapy
  • Mice

Substances

  • Copper