Myospreader improves gene editing in skeletal muscle by myonuclear propagation

Proc Natl Acad Sci U S A. 2024 May 7;121(19):e2321438121. doi: 10.1073/pnas.2321438121. Epub 2024 Apr 30.

Abstract

Successful CRISPR/Cas9-based gene editing in skeletal muscle is dependent on efficient propagation of Cas9 to all myonuclei in the myofiber. However, nuclear-targeted gene therapy cargos are strongly restricted to their myonuclear domain of origin. By screening nuclear localization signals and nuclear export signals, we identify "Myospreader," a combination of short peptide sequences that promotes myonuclear propagation. Appending Myospreader to Cas9 enhances protein stability and myonuclear propagation in myoblasts and myofibers. AAV-delivered Myospreader dCas9 better inhibits transcription of toxic RNA in a myotonic dystrophy mouse model. Furthermore, Myospreader Cas9 achieves higher rates of gene editing in CRISPR reporter and Duchenne muscular dystrophy mouse models. Myospreader reveals design principles relevant to all nuclear-targeted gene therapies and highlights the importance of the spatial dimension in therapeutic development.

Keywords: CRISPR; adeno-associated virus; gene therapy; myonuclear domains; spatial gene regulation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • CRISPR-Associated Protein 9 / genetics
  • CRISPR-Associated Protein 9 / metabolism
  • CRISPR-Cas Systems*
  • Cell Nucleus* / metabolism
  • Disease Models, Animal
  • Gene Editing* / methods
  • Genetic Therapy* / methods
  • Humans
  • Mice
  • Muscle, Skeletal* / metabolism
  • Muscular Dystrophy, Duchenne* / genetics
  • Muscular Dystrophy, Duchenne* / therapy
  • Myoblasts / metabolism
  • Nuclear Localization Signals / genetics

Substances

  • Nuclear Localization Signals
  • CRISPR-Associated Protein 9