Immortalized Canine Dystrophic Myoblast Cell Lines for Development of Peptide-Conjugated Splice-Switching Oligonucleotides

Nucleic Acid Ther. 2021 Apr;31(2):172-181. doi: 10.1089/nat.2020.0907. Epub 2021 Feb 9.

Abstract

Duchenne muscular dystrophy (DMD) is a severe muscle-wasting disease caused by frameshift or nonsense mutations in the DMD gene, resulting in the loss of dystrophin from muscle membranes. Exon skipping using splice-switching oligonucleotides (SSOs) restores the reading frame of DMD pre-mRNA by generating internally truncated but functional dystrophin protein. To potentiate effective tissue-specific targeting by functional SSOs, it is essential to perform accelerated and reliable in vitro screening-based assessment of novel oligonucleotides and drug delivery technologies, such as cell-penetrating peptides, before their in vivo pharmacokinetic and toxicity evaluation. We have established novel canine immortalized myoblast lines by transducing murine cyclin-dependent kinase-4 and human telomerase reverse transcriptase genes into myoblasts isolated from beagle-based wild-type or canine X-linked muscular dystrophy in Japan (CXMDJ) dogs. These myoblast lines exhibited improved myogenic differentiation and increased proliferation rates compared with passage-15 primary parental myoblasts, and their potential to differentiate into myotubes was maintained in later passages. Using these dystrophin-deficient immortalized myoblast lines, we demonstrate that a novel cell-penetrating peptide (Pip8b2)-conjugated SSO markedly improved multiexon skipping activity compared with the respective naked phosphorodiamidate morpholino oligomers. In vitro screening using immortalized canine cell lines will provide a basis for further pharmacological studies on drug delivery tools.

Keywords: Duchenne muscular dystrophy; canine X-linked muscular dystrophy in Japan (CXMDJ); cell-penetrating peptide; immortalized dystrophic canine myoblast; phosphorodiamidate morpholino oligomer; splice-switching oligonucleotides.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cyclin-Dependent Kinase 4 / genetics*
  • Dogs
  • Dystrophin / genetics*
  • Exons / genetics
  • Genetic Therapy
  • Humans
  • Mice
  • Morpholinos / genetics
  • Morpholinos / pharmacology*
  • Muscular Dystrophy, Duchenne / genetics
  • Muscular Dystrophy, Duchenne / pathology
  • Muscular Dystrophy, Duchenne / therapy*
  • Myoblasts / metabolism
  • Oligonucleotides, Antisense / genetics
  • Oligonucleotides, Antisense / pharmacology
  • Peptides / genetics
  • Peptides / pharmacology
  • RNA Splice Sites / genetics
  • Telomerase / genetics*

Substances

  • 140-kDa dystrophin
  • Dystrophin
  • Morpholinos
  • Oligonucleotides, Antisense
  • Peptides
  • RNA Splice Sites
  • Cyclin-Dependent Kinase 4
  • Telomerase